REVIEW
The amazing po en ial o ungi: 50 ways we can exploi ungi
indus ially
Ke in D. Hyde
1,2,3,4,5,9
·Jianchu Xu
1,10,21
·Syl ie Rapio
22
·Rajesh Jeewon
18
·Saisamo n Lumyong
9,13
·
Allen G ace T. Niego
2,3,20
·P anami D. Abeywick ama
2,3,7
·Jani h V. S. Alu hmuhandi am
2,3,7
·
Rashika S. B ahamanage
2,3,7
·Si ap apa B ooks
3
·Amo n a Chaiyasen
28
·K. W. Thilini Che hana
2,3,7
·
Pu a ak Chomnun i
2,3
·Cla a Chepki ui
12
·Boon iya Chuankid
2,3
·Nimali I. de Sil a
1,2,4,13
·
Mingkwan Doilom
1,4,13
·C aig Faulds
6
·Eleni Gen ekaki
3
·Venka Gopalan
14
·Pa ana Kakumyan
2,3
·
Dulanjalee Ha ishchand a
2,3,7
·H idya Hemachand an
24
·Sinang Hongsanan
26,27
·Anu uddha Ka una a hna
2,17
·
Saman ha C. Ka una a hna
1
·Seh oon Khan
10
·Ja u ong Kumla
13,9
·Ru ishika S. Jayawa dena
2,3
·
Jian-Kui Liu
11
·Ningguo Liu
2,3
·Tha sanee Luangha n
1,21,22,29
·Allan Pa ick G. Macabeo
12,23
·
Diana S. Ma asinghe
2,3
·Dan Meeks
19
·Pe e E. Mo ime
1,10
·Pe e Muelle
19
·Sadia Nadi
10,15,21
·
Ka aba N. Na a aja
16
·Su eepo n Non achaiyapoom
3
·Meghan O’B ien
19
·Wa sana Penkh ue
9,13
·
Chayana d Phukhamsakda
2,3
·Uma Shaanke Ramanan
16,25
·Achala R. Ra hnayaka
2,3
·Resu eccion B. Sadaba
29
·
Bi he Sanda go
12
·Binu C. Sama akoon
2,3
·Danushka S. Tennakoon
2,3
·Ramamoo hy Si a
24
·
Wasan S ip om
9,13
·T. S. Su yana ayanan
30
·Kanapo n Suja i
9,13
·Naka in Suwanna ach
9,13
·
Thi ipone Suwunwong
3,8
·Benja ong Thongbai
12
·Na i sada Thongklang
2
·Deping Wei
1,2,3,17
·
S. Nuwan hika Wijesinghe
2,3
·Jake Winiski
19
·Jiye Yan
7
·E andi Yasan hika
2,3
·Ma c S adle
12
Recei ed: 5 Ap il 2019 / Accep ed: 20 May 2019 / Published online: 3 July 2019
©The Au ho (s) 2019
Abs ac
Fungi a e an unde s udied, bio echnologically aluable g oup o o ganisms. Due o he immense ange o habi a s ha
ungi inhabi , and he consequen need o compe e agains a di e se a ay o o he ungi, bac e ia, and animals, ungi ha e
de eloped nume ous su i al mechanisms. The unique a ibu es o ungi hus he ald g ea p omise o hei applica ion in
bio echnology and indus y. Mo eo e , ungi can be g own wi h ela i e ease, making p oduc ion a scale iable. The
sea ch o ungal biodi e si y, and he cons uc ion o a li ing ungi collec ion, bo h ha e inc edible economic po en ial in
loca ing o ganisms wi h no el indus ial uses ha will lead o no el p oduc s. This manusc ip e iews i y ways in which
ungi can po en ially be u ilized as bio echnology. We p o ide no es and examples o each po en ial exploi a ion and gi e
examples om ou own wo k and he wo k o o he no able esea che s. We also p o ide a low cha ha can be used o
con ince unding bodies o he impo ance o ungi o bio echnological esea ch and as po en ial p oduc s. Fungi ha e
p o ided he wo ld wi h penicillin, lo as a in, and o he globally signi ican medicines, and hey emain an un apped
esou ce wi h eno mous indus ial po en ial.
Keywo ds Biocon ol · Biodi e si y · Bio echnology · Food · Fungi · Mush ooms
Table o con en s
F om basic o applied esea ch, p o o ypes and
p oduc s
con ibu ion by Bi he Sanda go, Ma c S adle
S a egies agains human disease
1. An ibac e ial an ibio ics
con ibu ion by Cla a Chepki ui, Benja ong Thong-
bai, Ma c S adle ,
2. An imyco ics
con ibu ion by Benja ong Thongbai, Ma c S adle
3. Bio ilm inhibi o s
con ibu ion by Benja ong Thongbai, Ma c S adle
&Jianchu Xu
[email p o ec ed]
Ex ended au ho in o ma ion a ailable on he las page o he a icle
123
Fungal Di e si y (2019) 97:1–136
h ps://doi.o g/10.1007/s13225-019-00430-9
4. An i-cance agen s
con ibu ion by Chayana d Phukhamsakda, Ma c
S adle
5. An i-diabe es
con ibu ion by Achala R. Ra hnayaka, Ma c S adle
6. Imp o ing ne e unc ioning
con ibu ion by Benja ong Thongbai, Ma c S adle
7. Fungi in T adi ional Chinese Medicine
con ibu ion by Tha sanee Luangha n, Ma c S adle
8. Ca dio ascula disease con ol by ungi
con ibu ion by Anu uddha Ka una a hna, Ma c
S adle
9. An i i al agen s
con ibu ion by Allan Pa ick G. Macabeo, Ma c
S adle
10. Immunosupp essi e and immunomodula o y agen s
om ungi
con ibu ion by Cla a Chepki ui, Ma c S adle
S a egies agains plan disease
11. Biocon ol o plan disease using endophy es
con ibu ion by Nimali I. de Sil a, Si ap apa B ooks
12. Biocon ol o insec s using ungi
con ibu ion by Allen G ace T. Niego
13. Biocon ol o nema odes and ungal nema izides
con ibu ion by Diana S. Ma asinghe, Cla a
Chepki ui
14. Biocon ol o weeds and he bicides om ungi
con ibu ion by P anami D. Abeywick ama, Jiye Yan
15. Fungal an agonis s used in pos -ha es disease
con ol
con ibu ion by Binu C. Sama akoon
16. Bio con ol o us s and smu s by an agonis ic ungi
con ibu ion by Rashika S. B ahmanage
Enhancing c ops and o es y
17. Bio e ilize s
con ibu ion by Mingkwan Doilom
18. A buscula myco hizae as bio e ilize s
con ibu ion by Amo n a Chaiyasen, Saisamo n
Lumyong
19. Applica ion o ec omyco hizal ungi in o es y
con ibu ion by Ja u ong Kumla, Saisamo n
Lumyong
20. Use o o chid myco hizae and endophy es in
bio echnology
con ibu ion by Nimali I. de Sil a, Su eepo n
Non achaiyapoom
21. G ow h p omo ing ho mones om ungi
con ibu ion by Saisamo n Lumyong
22. Mi iga ing abio ic s ess in plan s: he endophy e
me hod
con ibu ion by Ka aba N. Na a aja, Uma Shaanke
Ramanan
Food and be e ages om ungi
23. G owing mush ooms in compos
con ibu ion by Na i sada Thongklang
24. G owing mush ooms in bags
con ibu ion by Saman ha Ka una a hna
25. G owing mush ooms in he ield
con ibu ion by Pe e E. Mo ime , Saman ha C.
Ka una a hna
26. Mode n mush oom p oduc ion: an au oma ed ac o y
p ocess
con ibu ion by Jianchu Xu
27. New edible mush ooms
con ibu ion by Saman ha Ka una a hna
28. Aga icus sub u escens
con ibu ion by Na i sada Thongklang
29. Using ungi o enhance ood alue
con ibu ion by Danushka S. Tennakoon
30. Food colou ing om ilamen ous ungi
con ibu ion by Wasan S ip om and Saisamo n
Lumyong
31. Food la ou ing
con ibu ion by S. Nuwan hika Wijesinghe
32. Wha is mush oom s ock? P oduc s, p ocess and
la ou s con ibu ion by Deping Wei
33. Fungi in making ea
con ibu ion by Ningguo Liu, Jack JK Lui
34. Wine, bee and spi i s
con ibu ion by Sinang Hongsanan
35. Func ional oods and nu aceu icals
con ibu ion by Boon iya Chuankid
36. Ha es ing he un apped p obio ic po en ial o ungi
con ibu ion by Eleni Gen ekaki, Achala R.
Ra hnayaka
Sa ing he plane
37. Ag icul u al was e disposal
con ibu ion by Pu a ak Chomnun i, C aig Faulds
38. Myco emedia ion: Fungi o he escue
con ibu ion by Dulanjalee Ha ishchand a, Jiye Yan
39. Myco umiga ion using Muscodo
con ibu ion by Naka in Suwanna ach, Saisamo n
Lumyong
40. Biomass o bio uel: unmasking he po en ial o
lesse -known ungi
con ibu ion by Venka Gopalan, T.S.
Su yana ayanan
41. Packed-bed bio eac o o mycoma e ial p oduc ion
con ibu ion by Pe e Muelle , Dan Meeks, Meghan
O’B ien, Jake Winiski
2 Fungal Di e si y (2019) 97:1–136
123
42. Fungal deg ada ion o plas ics: A hidden easu e o
g een en i onmen
con ibu ion by Seh oon Khan, Sadia Nadi
43. Polycyclic a oma ic hyd oca bon deg ada ion by
basidiomyce es
con ibu ion by Allen G ace T. Niego, Resu eccion
B. Sadaba
44. Can ungi help modi y he sus ainable soil enhance
biocha ?
con ibu ion by Thi ipone Suwunwong, C aig Faulds
Commodi ies
45. Fungi and cosme ics
con ibu ion by E andi Yasan hika
46. Aga wood
con ibu ion by S. Nuwan hika Wijesinghe
47. Fungal enzymes
con ibu ion by Pa ana Kakumyan
48. P ese a i es
con ibu ion by Benja ong Thongbai
49. O ganic acids
con ibu ion by Jani h V.S. Alu hmuhandi am
50. Tex ile dyes
con ibu ion by Ru ishika S. Jayawa dena
The u u e
Func ional genomics and he sea ch o no el an i-
in ec i es
con ibu ion by K.W. Thilini Che hana, Jiye Yan and
Bi he Sanda go
F om basic o applied esea ch, p o o ypes
and p oduc s
Fungi ha e bo h good and bad ace s (Poin ing and Hyde
2001). They a e essen ial o nu ien cycling because o
hei abili y o deg ade cellulose and lignin (Poin ing e al.
2001). On he o he hand, hey cause se ious human, ani-
mal and plan diseases and ha e nume ous nega i e aspec s
on human li e (Hyde e al. 2018a). Fungi a e, howe e , also
ela i ely unde s udied, bu a e an essen ial, ascina ing
and bio echnologically use ul g oup o o ganisms wi h an
inc edible bio echnological po en ial o indus ial
exploi a ion. In his pape , we de ail 50 ways in which we
can po en ially exploi ungi. We p o ide no es and
examples o all po en ial exploi a ions and gi e examples
om ou own wo k and he wo k o o he s. We also p o-
ide a low cha ha can be used o con ince unding
bodies jus how impo an ungi a e and hei po en ial o
bio echnological esea ch and po en ial p oduc s.
While se e al o ou chap e s a e dealing wi h ma ke ed
p oduc s ha e en include blockbus e pha maceu icals,
such as he be a-lac am an ibio ics, he s a ins and cyclos-
po ine, o he s a e dedica ed o newly upcoming a eas ha
s ill emain o be explo ed. O he chap e s ea ela i ely
small ma ke segmen s ha may expand in he u u e. Fo
example, he consume s a ound he wo ld now inc easingly
p e e na u al compounds o e syn he ic chemicals and
e en in he indus ial sec o s ha p oduce commodi y
chemicals, he e is now an inc eased in e es in de elop-
men o sus ainable bio echnological p ocesses, in o de o
ob ain new na u al p oduc s ha can e en ually eplace
adi ional syn he ics. As compa ed o o he biological
sou ces, in pa icula plan s, ungi ha e he g ea ad an age
ha hey can be g own in la ge bio eac o s a an indus ial
scale, and sui able p ocesses o hei cos -e icien e -
men a ion ha e been a ailable o many decades, e.g. o
p oduc ion o ce ain o ganic acids, enzymes and an ibi-
o ics. As exempli ied by he ecen s udies o he Thai
mycobio a, mode n polyphasic axonomic app oaches a e
cons an ly e ealing a ple ho a o new and undesc ibed
species e en in he ai ly well-known gene a o ungi like
Aga icus (Hyde e al. 2018b). E en he majo i y o he
known species in he ungal kingdom a e i ually un ap-
ped wi h ega d o po en ial applica ions, also because hey
we e ne e cul u ed and s udied o hei g ow h cha ac-
e is ics and physiology. New me hods and p o ocols ha e
o be de eloped o his pu pose, and his implies ha
subs an ial basic esea ch mus be ca ied ou be o e he
exploi a ion o he no el o ganisms can be en isaged.
Al hough ungi ha e so many po en ial uses, esea ch on
hei po en ial applica ions is in gene al poo ly unded and
much o he esea ch ha is being ca ied ou in academia
is undamen al, e en in a eas ha belong o he ields o
bio echnology and applied mycology. Fo example,
sc eening ungi o p oduc ion o an ibio ics by an ago-
nis ic cul u e es ing has o en been epo ed, bu is unli-
kely o lead o indus ial p ojec s. O en, i will ake o e a
decade e en o b ing a gi en p ojec based on a no el
ungal me aboli e in o he p eclinics, and e en his is only
possible by join , in e disciplina y e o s o biologis s,
bio echnologis s, pha macis s and chemis s. Mo eo e , he
Big Pha ma indus y has ecen ly downsized hei capaci-
ies o in-house esea ch, meaning ha he academic
sec o (some imes suppo ed by smalle companies o
o ganisa ions like he Bill and Melinda Ga es Founda ion
and he Wellcome T us ) has become mo e and mo e
in ol ed in he p eclinical e alua ion o new compounds.
In es ing in basic esea ch may seem, a i s sigh , a
cos ly a ai . Howe e , he e a e nume ous examples o he
Fungal Di e si y (2019) 97:1–136 3
123
pas demons a ing why in es ing in basic esea ch pays o
in he long un, and e en mo e easons, why i is oday
mo e impo an han e e o enew an in e es in basic
esea ch on ungi. Bu how o con ince unde s, in pa -
icula om he p i a e sec o , o in es in o esea che s
doing basic esea ch on ungi?
The e a e, no doub , a eas o esea ch, which a e o
u mos impo ance o he en i e wo ld, ye a e conside ed
alueless o he pha maceu ical indus y. One o hese is
he sea ch o no el an i-in ec i es, as he wo ld is unning
ou o an ibio ics (Hes e kamp 2017; WHO epo 2017). I
has long been seen as a edious p ocess o ob ain no el
an ibio ics om li ing o ganisms.
Howe e , he ocus in he pas has been on he same
bac e ial and ungal gene a, such as S ep omyces in he
Ac inobac e ia and common soil moulds like Aspe gillus
and Penicillium in he ilamen ous ungi (Ka wehl and
S adle 2017). Since almos no no el ca bon skele ons ha e
been disco e ed om hese common soil mic obes in he
pas 20 yea s, i makes much mo e sense o s udy he
nume ous species ha a e cons an ly being disco e ed and
shown o belong o new phylogene ic g oups.
In ou e iew, we p esen ungi, in pa icula Basid-
iomyco a, as a s ill unde explo ed, highly p omising sou ce
o an i-in ec i es, immunosupp essan s, and o he pha -
maceu icals (see Badalyan e al. 2019; Sanda go e al.
2019a) ha is nowhe e nea d ied up. We gi e examples on
ecen de elopmen s o u ning ungal na u al p oduc s in o
comme cial d ugs and gi e an o e iew o he cu en s a e
o applied esea ch in his ield.
In he pas , ungal na u al p oduc s ha e also led o some
blockbus e s and a ious de elopmen al candida e com-
pounds o he ag ochemical indus y (Bills and Gloe
2016). Howe e , he uncon olled usage o such ungal
pes icides has led o he de elopmen o mo e and mo e
esis ances agains hese ag ochemicals (Lucas e al. 2015).
A mo e con olled app oach o c op p o ec ion is he e o e
ad isable. Mo e basic esea ch is needed o unde s and
na u al p ocesses, and he eby allow o he sea ch o
na u al con ol agen s. In he en ies dealing wi h “S a e-
gies agains plan disease”, we show he g ea po en ial o
ungi as biocon ol agen s. We gi e examples o how
ungal biocon ol agen s can help sa e he Ag o sec o
emendous amoun s o money, i companies a e gi en he
oppo uni y o p oduce cos e icien biocon ol agen s. In a
likewise manne , he pa on “Enhancing c ops and o -
es y” deals wi h he cu en esea ch on ec omyco hiza
and hei po en ial applica ion as na u al bio e ilize s.
Wi h he new end o a mo e sus ainable, heal h-o i-
en ed li ing, and cons an epo s o haza dous chemicals
ound in ood and cosme ics, he demand o mo e eco-
logical, mo e “na u al” al e na i es is high. This is again,
whe e ungi can s ep in. In he en ies on “Food and
be e ages om ungi” and “Commodi ies”, we p esen
examples o how basic esea ch on ungi has made i s way
in o he ood and be e age, bu also he ex ile and la ou
indus y. Finally, in he pa on “Sa ing he plane ” we
illus a e he g ea po en ial o ungi owa ds a mo e sus-
ainable li ing and how ungi can assis o cope wi h some
po en ial u u e challenges ha a e h ea ening human
ci ilisa ion. A diag am illus a ing all po en ial bene icial
uses o ungi ha a e ea ed he ein is gi en in Fig 1.
S a egies agains human disease
The scien i ic communi y ecen ly celeb a ed he 90
h
anni e sa y o Si Alexande Fleming’s disco e y o
penicillin, which ma ked he s a ing poin o he e a o
an ibio ic chemo he apy. As ou lined by Ka wehl and
S adle (2017), among he nume ous an ibio ics ha we e
disco e ed o e he nex 50 yea s, ela i ely ew compound
classes we e de i ed om ungi. The la e include he
cephalospo ins (New on and Ab aham 1955), which belong
o he same class as he penicillins, i.e. he be a glucan
an ibio ics, as well as usidic acid (God edsen e al. 1962)
and pleu omu ilin (No ak and Shlaes 2010; Sanda go e al.
2019a). Thei chemical s uc u es (1–4)
1
a e depic ed in
Fig. 2. Mos o he comme cial an ibio ics a e ac ually
de i ed om S ep omyces species and o he ac inobac e-
ia, o e en om o he p oka yo es. Fo de ails o he
his o y o esea ch on an ibio ics, we e e o he e iew by
Moh e al. (2017), as his does no all wi hin he scope o
he cu en pape . As we canno co e he en i e ield in his
pape , we will gi e a b ie o e iew on an ibac e ials,
an imyco ics and bio ilm inhibi o s and illus a e hei
usages wi h some examples o ma ke ed d ugs as well as
o he compounds ha ha e ecen ly been disco e ed.
1. An ibac e ial an ibio ics
The e m “an ibio ics” is used in he li e a u e wi h di -
e en de ini ions. The indus y mainly use i o an ibac-
e ial agen s, bu he de ini ion ha we p e e he e, which
was adap ed om he o iginal one coined by Waksman
(1947), i.e., an an ibio ic is “a chemical subs ance, p o-
duced by mic o-o ganisms (including ungi), which has he
capaci y o inhibi he g ow h o and e en o des oy bac-
e ia and o he mic o-o ganisms”. The na u al unc ions o
an ibio ics can easily be explained, esul ing om he high
compe i ion be ween ungi, bac e ia and o he o ganisms in
1
All chemical s uc u es o ungal seconda y me aboli es p esen ed
in his pape ha e been nume ed consecu i ely in bold ypese in
bo h, he igu es and he co esponding ex .
4 Fungal Di e si y (2019) 97:1–136
123
subs a es such as soil, dung and plan deb is. I a gi en
o ganism has acqui ed he abili y o p oduce a ce ain
seconda y me aboli e by which i can kill he compe ing
o ganisms ha dwell in he same habi a , i is conside ed o
possess a selec i e ad an age ha ul ima ely inc eases i s
i ness (Shea e 1995). The e o e i should come as no
su p ise ha one la ge expe imen al s udy concluded ha
he majo i y o ilamen ous ungi a e able o p oduce
an ibio ic compounds (Bills e al. 2009). Bills and Gloe
(2016) summa ized nume ous impo an ac s conce ning
he cu en s a e o he a in esea ch on ungal seconda y
me aboli es and concen a ed hea ily on he biochemical
and gene ic backg ound o hei biosyn hesis.
We a e cu en ly li ing in he “pos -an ibio ic” e a,
whe e bo h, he numbe s and pe cen ages o mul i- esis an
bac e ial and ungal pa hogens agains he es ablished
Fig. 1 Diag am showing he po en ial use o ungi in bio echnology.
The cycle s a s wi h basic biodi e si y esea ch, which in u n leads
o cul u es placed in he cen al cul u e collec ion. The cul u es a e
hen used o applied esea ch, which in u n leads o p oduc s in he
o m o he i ems discussed in he en ies o his pape
Fungal Di e si y (2019) 97:1–136 5
123

an ibio ics a e d as ically inc easing, while he numbe o
new he apeu ic agen s and de elopmen al candida es has
dec eased (Coope and Shlaes 2011). The easons o his
de elopmen a e mani old, bu he phenomenon is p i-
ma ily due o he ac ha he majo i y o pha maceu ical
companies ha e los in e es in Resea ch and De elopmen
on na u al p oduc s and/o gi en up hei ac i i ies in he
an i-in ec i es sec o . Expe s a ound he wo ld a e now
gi ing wa nings abou he se ious consequences ha he
lack o an ibio ics—in pa icula agains he mul i- esis an
G am nega i e human pa hogenic bac e ia—can ha e
(F iedman e al. 2016). A e wo decades o neglec ,
e o s o bo h he p i a e and he academic sec o on he
disco e y o new an ibio ics ha e subs an ially inc eased.
The pipeline o an ibac e ial an ibio ics (Hes e kamp
2017) shows ha he e a e s ill some compounds unde
de elopmen , bu he majo i y o hose ha e been op i-
mised om old compounds wi h known modes o ac ion, e.
g. by chemical modi ica ions. The e o e, i is likely ha he
esis an pa hogens will easily ind a way o cope wi h he
new p oduc s, once hey ha e eached he ma ke . The
a o emen ioned mu ilins, which a e de i ed om e men-
a ion o he basidiomyce e Cli opilus passecke ianus and
subsequen semisyn hesis, he e o e ep esen he “newes ”
compound class ha has been egis e ed as an an ibac e ial
d ug. A de i a i e, e apamulin (5), was launched o use
as a opical an ibio ic agains skin in ec ions, and se e al
u he de i a i es a e unde going clinical ials as sys-
emic an ibio ics. In gene al, basidiomyce e cul u es a e
much mo e di icul o handle wi h espec o la ge scale
p oduc ion o seconda y me aboli es, since hey g ow
a he slowly and o en ha e low yields. Fo he p oduc ion
o pleu omu ilin, howe e , Bailey e al. (2016) managed o
inc ease he yields subs an ially a e he ans e o he
biosyn he ic genes in o a as g owing he e ologous
Aspe gillus hos , which can mo e easily be handled in he
p oduc ion p ocess. This accomplishmen can gi e ise o
some hope ha in he u u e, mo e o he hi he o neglec-
ed, unique biologically ac i e me aboli es o basid-
iomyce es can be made accessible o p eclinical
de elopmen .
2. An imyco ics and ungicides
Whe eas mul i- esis an bac e ial pa hogens a e e y high
on he agenda o bo h he p ess and unding agencies,
ela i ely li le a en ion is p esen ly being paid o he ac
ha he numbe o esis an pa hogenic ungi is also on he
ise. This opic was ea ed by Hyde e al. (2018a), we e e
o i o he mos impo an an h ea ening human pa ho-
genic ungal o ganisms. In ac , he e a e only a hand ul o
e icien compound classes on he ma ke ha a e used in
an imyco ic chemo he apy, including g iseo ul in (6),
which was al eady disco e ed by G o e e al. (1952;
Fig. 3). The newes class o an imyco ics ha we e laun-
ched o he ma ke a e he echinocandins (e.g., pneumo-
candin B
0
(7) (Denning 2002). The biosyn hesis o hese
highly complex lipopep ides elies on PKS-NRPS hyb id
gene clus e s (Chen e al. 2013). They a e being p oduced
bio echnologically by la ge scale e men a ion using di -
e en ungi ha a e no phylogene ically ela ed and sub-
sequen semisyn hesis. The knowledge abou he molecula
mechanisms o hei biosyn hesis may in he u u e lead o
he concise manipula ion o he p oduc ion p ocess ha can
be di ec ed owa ds new na u al de i a i es. In e es ingly,
a compa a i e genomics s udy by Yue e al. (2015) has
e ealed a he high homologies among he biosyn hesis
gene clus e s o he p oduce o ganisms ha belong o h ee
di e en classes o Ascomyco a, namely Do hideomyce es,
Eu o iomyce es, and Leo iomyce es. Possibly, his has
O
NH
N
S
O
O
O
OH
OH O
O
ON
SNH O
NH
2
O
OHO
OH
H
OH
O
O
COOH
H
O
H
OH
O
O
OH
Pleu omu ilin (4)
Fusidic acid (3)
Cephalospo in C (2)
Penicillin V (1)
O
H
OH
O
O
S
N
Re apamulin (
5
)
Fig. 2 Chemical s uc u es o
ungal me aboli es ha we e
de eloped o an ibac e ial d ugs
6 Fungal Di e si y (2019) 97:1–136
123
been due o ho izon al gene ans e du ing he e olu ion-
a y his o y o hese o ganisms.
Recen e o s aimed a he disco e y o no el an i ungal
agen s ha e esul ed in a numbe o de elopmen al p o-
jec s, such as en uma ungin (8) om Ho monema spp.
(Pela
´ez e al. 2000). This compound class may soon yield
he i s pha maceu ical d ug o use in humans ha o ig-
ina ed om a ungal endophy e, o e 15 yea s a e hei
i s disco e y. E en he biosyn hesis genes encoding o
hese unique i e penoids (Fig. 3) has only ecen ly been
iden i ied (Kuhne e al. 2018).
The sea ch o no el an imyco ics and ungicides has
also esul ed in he edisco e y o “old” compounds ha
may become mo e in e es ing in he u u e because hey
ha e o iginally been ound in a sc eening o ag ochemical
ungicides and we e ne e e alua ed o hei e ec s on
human ungal pa hogens o hei mode o ac ion. While he
s obilu ins, which a e a e y comme cially success ul
an i ungal agen s in ag icul u e (Sau e e al. 1999), ha e
been ound ine icien o oo oxic o applica ion in
humans, many o he me aboli es wi h p onounced an i-
ungal e ec s we e appa en ly ne e es ed on hei e i-
cacy agains human pa hogens. A ecen example o such
edisco e ies is a olon (9), which is ac ually a co-
me aboli e o s obilu ins p oduced by he in asi e basid-
iomyce e Fa olaschia caloce a (Chepki ui e al. 2016) and
was o iginally isola ed by Anke e al. (1995). Like he
spo o h iolodes (10) om he xyla ialean ungus Hypoxy-
lon mon iculosum (Su up e al. 2014; Fig. 3; now classi ied
in he new genus Hypomon agnella as H. mon iculosa; c .
Lambe e al. 2019), his me aboli e shows e y s ong
an i ungal e ec s ha a e no accompanied by p ominen
cy o oxici y.
3. Bio ilm inhibi o s
Scien is s a e explo ing di e en a enues o comba
in ec ious diseases caused by bo h bac e ial and ungal
pa hogens, o which he inhibi ion o bio ilm o ma ion is
one o he mos p omising leads. Ab aham and Es ela
(2016) epo ed ha ungal me aboli es a e becoming
inc easingly explo ed o hei po en ial o inhibi he o -
ma ion o bio ilms, e.g. by in e e ing wi h quo um sensing,
and some compounds ha e al eady been disco e ed ha
can e en des oy p e- o med bio ilms. A ecen example is
cop inuslac one (11) (de Ca alho e al. 2016; Fig 3), a
small molecule de i ed om he edible mush oom Cop i-
nus coma us, which ac s agains Pseudomonas ae uginosa
bio ilms. O he examples include oussoellenic acid (12)
om a Roussoella sp. (Phukhamsakda e al. 2018), which is
ac i e agains bio ilm o ma ion in S aphylococcus au eus,
as well as mic opo enic acid A (13) om a Kenyan
basidiomyce e (Chepki ui e al. 2018; Fig. 4), which can
no only inhibi bio ilm o ma ion in bo h S aphlococcus
au eus and he human pa hogenic yeas , Candida albicans,
bu e en des oys p e- o med bio ilm in C. albicans a
a he low concen a ions. These compounds do no ha e
p ominen an imic obial ac i i ies and he e o e hei
applica ion is unlikely o aise esis ance. The bio ilm
inhibi o s a e e y p omising candida es o use in
O
NH
OH
OH
NH O
OH
N
O
NH
O
NH
O
OH
N
O
NH
O
OH
OH
OH
OH
OH
NH
2
O
HH
O
O
Cl
O
O
O
O
Pneumocandin B0 (7)
O
OH
H
H
H
O
O
OH
OH
O
O
O
Fa olon (9)
G iseo ul in (6)
OHO
H
O
OH
O
AcO
O
OH
OH
OH OH
En uma ungin (8)
O
O
O
O
H
H
Spo oh ioide (10)
Fig. 3 Chemical s uc u es o
ungal me aboli es wi h
an i ungal ac i i y agains
human pa hogens
Fungal Di e si y (2019) 97:1–136 7
123
combina ion he apy wi h an ibio ics. In se e al s udies,
bio ilm inhibi o s we e shown o enhance he ac i i y o he
an ibio ics by inc easing hei abili y o pene a e he
bio ilms.
These examples illus a e ha ungi a e unde -explo ed
wi h espec o no el an ibio ics and o he he apeu ic
agen s, and ha i is ce ainly wo hwhile o expend mo e
e o in his a ea o esea ch wi h an emphasis on hi he o
neglec ed species om egions and habi a s ha ha e no
ye been s udied sys ema ically. Fungi ha e much o o e
in e ms o no el chemis y: due o he ad en o e olu-
iona y echniques in genomics, ansc ip omics, bioin o -
ma ics, analy ical chemis y and bio echnological p ocess
de elopmen , we can now explo e he chemical di e si y o
he mycobio a much mo e concisely han e e be o e.
E idence is also accumula ing ha no el phylogene ic
lineages o hi he o neglec ed axonomic and ecological
g oups o ungi can now much mo e easily be ecognized
and subjec ed o he exploi a ion o hei seconda y me a-
bolome. Howe e , mo e public unding is needed o assu e
ha he subs an ial know-how ha has been acqui ed o e
many decades does no become o go en, and ha he nex
gene a ion o esea che s will also s ill be able o wo k on
no el, hi he o unexplo ed ungal g oups, a he han only
on model o ganisms.
4. An i-cance agen s
Cance is he second leading cause o mo ali y a e ca -
dio ascula disease, wi h an es ima ed 9.6 million cance -
ela ed dea hs in 2018 (GBD 2015). Cance is a mul i ac-
o ial disease cha ac e ized by he loss o g ow h ac o s
ha con ol he p oli e a ion and di ision o cells. These
abno mal malignan cells can e ade he umou supp esso
ac o s o he human immune sys em, hen de elop o
umou s and des oy adjacen issues (Saeidnia and
Abdollahi 2014). The e a e se e al ea men s o cance ,
adminis e ed acco ding o de elopmen al s a e o he dis-
ease. Chemo he apy, adia ion he apy, su ge y and
immuno he apy a e all impo an elemen s o cance
ea men . Howe e , while many cy o oxic agen s a e
known o Science (which could in p inciple se e as
chemo he apeu ic agen s), only ew o hem speci ically
a ge umou cells and a e less oxic o egula , heal hy
human issue (Pe elli e al. 2012; Cai e al. 2013; Zuga-
zagoi ia e al. 2016). Ta ge ed he apy, usually he conju-
ga ed elemen o cance ea men s, deli e s d ugs o
genes o p o eins ha a e speci ic o cance cells o he
en i onmen al issues ha p omo es he g ow h o cance
(Padma 2015). Fungi a e an impo ance sou ce o na u al
p oduc disco e y, albei mos an icance d ugs a e
e ie ed om plan s and bac e ia. In his en y, we
desc ibe se e al p omising na u al p oduc s de i ed om
ungi and highligh some o he chie compounds ha a e
cu en ly in he clinical and p eclinical de elopmen al
s age (Fig. 5).
I o ul en (14) is a semi-syn he ic de i a i e o illudin S
(15), a na u al oxin isola ed om Omphalo us illudens
(Jack O’Lan e n mush oom; c . Chin e al. 2006; Mo as-
saghi e al. 2006). I o ul en in e e es wi h DNA eplica-
ion-complexes and cell di ision in DNA syn hesis. The
abno mal cells in S-phase lead o apop o ic cell dea h
(Walse and Heins ein 1973; Jaspe s e al. 2002). The an i-
umou ac i i ies o i o ul en ha e been e alua ed in phase
I and II clinical ials wi h p omising esul s agains a
a ie y o cance s, including hose in he b ain and cen al
ne ous sys em, b eas , blood, colon, sa coma, p os a e,
lungs, o a ian and panc eas (Alexand e e al. 2004;
Miyamo o e al. 2018; Topka e al. 2018). Sanda go e al.
(2019a) ha e ecen ly desc ibed he s a e o he a ,
including some exci ing new illudin conjuga es ha show
supe io in i o ac i i ies han i u ul en and a e p esen ly
unde ea ly p eclinical de elopmen .
Aphidicolin (16) is a e acyclic di e pene wi h an i i al
and an imi o ic p ope ies. The compound was o iginally
isola ed om “Cephalospo ium aphidicola”(cu en ly
alid name: Akan homyces musca ius) and la e also
epo ed om Nig ospo a sphae ica (Bucknall e al. 1973;
S a a a and Loschia o 1974). Aphidicolin compe es o
he speci ic binding si e on DNA polyme ase α,δ, and ε
enzymes. I s mechanism o ac ion and e icacy ha e been
in ensi ely es ed in clinical ials (C ose o e al. 2013;
Ayob e al. 2017), bu so a i has no become a ma ke ed
d ug.
O he an icance lead compounds de i ed om ungi
include lep osins F (17) and C (18) isola ed om Lep-
oshae ia sp., which showed an i umo ac i i y in mouse
emb yos (Yanagiha a e al. 2005; Pejin e al. 2013); β-
glucans, he polysaccha ides ha a e na u ally ound on he
cell walls o ungi (Chan e al. 2009; Bashi and Choi
2017); as well as palma umycin (Powis e al. 2006) and
spi op eussione A (Chen e al. 2009). The la e
Fig. 4 Chemical s uc u es o ungal me aboli es wi h bio ilm
inhibi ion ac i i ies
8 Fungal Di e si y (2019) 97:1–136
123
compounds, howe e , ha e only demons a ed hese
ac i i ies in i o, and i is no clea whe he hey will
e en ually each he la e explo a o y s age o p eclinical
de elopmen .
5. An i-diabe es
Diabe es melli us, also known simply as diabe es, is a
ch onic me abolic diso de (De Sil a e al. 2012). People
who su e om diabe es canno p oduce o e ec i ely use
insulin in he body. Due o his insulin imbalance, hey
ha e high amoun s o glucose in hei blood. The e a e wo
common ypes o diabe es, i.e. ype 1 diabe es (insulin
dependen diabe es melli us) and ype 2 diabe es (nonin-
sulin-dependen diabe es melli us).
Pa ien s wi h ype 1 diabe es canno p oduce insulin, due
o he lack o unc ions o he insulin-sec e ing be a cells in
he panc eas (Meie e al. 2005). They mus ake insulin
con inuously e e y day o s ay ali e. Type 1 diabe es
mos ly a ec s child en and adolescen pa ien s, and i
ep esen s 5–10% o o al diabe es cases wo ldwide.
Pa ien s wi h ype 2 diabe es canno p oduce su icien
insulin o canno e ec i ely me abolize i . This o m o he
diso de commonly a ec s elde ly people and accoun s o
90–95% o all diabe es cases (Hameed e al. 2015). People
wo ldwide su e om diabe es melli us and 7% o he
wo ld’s adul popula ion is a ec ed by he disease (Phi-
lippe and Raccah 2009). In 2017, he la ges numbe o
diabe ic pa ien s, a ound 114 million, was eco ded in
China. Roughly 73 million diabe ic pa ien s we e eco ded
in India, and 30 million we e eco ded in he Uni ed S a es.
(h ps://www.s a is a.com/s a is ics/281082/coun ies-wi h-
highes -numbe -o diabe ics/).
The e a e many nega i e consequences o pa ien s i
diabe es emains un ea ed, such as blindness, kidney
ailu e, dep ession, ca dio ascula diseases, cance and
e en dea h (Ge s ein e al. 2011; Hansen e al. 2012; Huang
e al. 2018). Re inopa hy (damage o he e ina, leading o
blindness) and neu opa hy (damage o he ne ous sys em)
a e some o he mos se e e complica ions ha ha e been
a ibu ed o diabe es (De Sil a e al. 2012; Sobngwi e al.
2012).
Many Basidiomyco a, such as Aga icus bispo us,Cy-
clocybe aege i a, C. cylind acea and T emella uci o mis
a e used as medicine o he ea men o p ophylaxis o
ype 2 diabe es. These mush ooms help pa ien s a oid high
le els o glucose because hey con ain he leas amoun o
diges ible ca bohyd a es in he die (Pouche e e al. 2006).
Bioac i e me aboli es, which a e isola ed om medical
mush ooms and hei cul u ed mycelia, ac as biological
an ihype glycemic agen s in diabe es ea men (Table 1)
(De Sil a e al. 2012). Ex ac s o Inocu is le is (Hy-
menochae aceae) ha e been epo ed o possess u ili y as a
emedy o diabe es because hey inc ease insulin esis-
ance, insulin sensi i i y and glucose up ake in issues and
hence help o con ol blood glucose le els (Ehsani a d
OH
OH
H
H
H
OH
OH
Aphidicolin (16)
NH
NH N
N
H
O
O
S
4
OH
Lep osin F (17)
OH
O
OH
OH
O
OH
OH
Illudin S (15)
I o ul en (14)
NH N
N
H
O
O
S
2
OH
NH N
N
H
O
OH
O
S
2
OH
Lep osin C (
18
)
Fig. 5 Chemical s uc u es o
p omising na u al p oduc s
de i ed om ungi wi h
an icance ac i i y
Fungal Di e si y (2019) 97:1–136 9
123
lowe ing p ope ies a e mainly caused by he s uc u al
simila i y wi h choles e ol (Gil-Ramı
´ ez e al. 2016). Fu -
he , he biological ac i i y o β-glucans and chi in may be
due o hei binding abili ies o choles e ol ecep o s (Gil-
Ramı
´ ez e al. 2016).
F ancia e al. (1999) eco ded 16 species o edible
mush ooms wi h biological ac i i ies agains ca dio ascu-
la disease. Species o he gene a Au icula ia (Fan e al.
1989), Ganode ma (Kabi e al. 1988), G i ola (Kubo and
Namba 1997), Pleu o us (Bobeck e al. 1991) and T emella
(Cheung 1996) ha e been epo ed o con ain choles e ol-
lowe ing compounds. Ophioco dyceps sinensis has also
been shown o educe o al choles e ol le els, which has
been a ibu ed o he ac ha i con ains polysaccha ide
“CS-F30” composed o galac ose, glucose and mannose
(Kiho e al. 1996). Fo ins ance, low densi y lipop o ein
choles e ol le els we e epo ed o be educed by Au icu-
la ia au icula-judae (Fan e al. 1989) and T emella uci-
o mis (Cheung 1996), and iglyce ide le els we e
epo ed o be educed by G i ola ondosa (Kubo and
Namba 1997), Len inula edodes (Kabi and Kimu a 1989)
and Ophioco dyceps sinensis (Kiho e al. 1996).
9. An i i al agen s
Heal h and mo ali y-debili a ing diseases caused by i u-
ses con inue o cause se ious global epidemics, especially
in cases whe e accines and an i i al chemo he apies a e
insu icien o no a ailable. The cu en s a e o i us-
ela ed pandemics is also signi ican ly limi ing d ug e i-
cacy by he eme gence o d ug- esis an s ains. Hence,
he e is an u gen need o iden i y and de elop na u al
p oduc -inspi ed d ug leads ha could help con ol i al
in ec ions. A ple ho a o po en ially ac i e na u al p oduc s
ha e been isola ed om ungi and sc eened o an i i al
ac i i y, e en hough none o hem has eached he ma ke
ye . This en y ocuses on na u al p oduc s exhibi ing
po en ac i i y on selec ed human pa hogenic i uses, such
as he human immunode iciency i us (HIV), in luenza
i us, he pes simplex i us (HSV), hepa i is i us and o he
human pa hogenic i uses such as en e o i us-71, and
espi a o y syncy ial i us (RSV).
Human Immunode iciency Vi us (HIV) inhibi o y
na u al p oduc s om ungi
A comp ehensi e e iew o he li e a u e iden i ies h ee
main a ge s o an i-HIV d ug disco e y: i us en y,
e e se ansc ip ion and in eg a ion.
The en y o HIV in ol es in e ac ions wi h p o eins and
is a a ge o he disco e y o new i al en y blocke s.
Examples o a ew disco e ies a e p o ided. A bis-indolyl
quinone, hinnuliquinone (25) (Fig. 9) om an unknown
ungus isola ed om Que cus cocci e a, inhibi ed wild-
ype and clinically- esis an HIV-1 p o ease. HIV-1 p o-
ease is a key enzyme in ol ed in he eplica ion and
NH
O
OH
O
OH
NH
Hinnuliquinone (25)
O
O
OH
MeO
OH OH
OH
OMe
O
In eg as a in A (27)
OH
O
N
O
OH
H
O
S achybosin D (26)
OH
H
N
H
O
O
OH
O
O
O
OH
OH
OH
O
Vani a acin A (29)
S achy lin (28)
OH
OH
OH
O
O
OOH
OH
Cy ospo aquinone B (31)
OH
OH
OH
O
O
H
H
4-hyd oxypleu og isein (30)
O
OH
O
O
OH
OH
Rhoda in (32)
Fig. 9 Chemical s uc u es o
ungal me aboli es ha we e
epo ed o possess an i i al
ac i i ies
16 Fungal Di e si y (2019) 97:1–136
123

ma u a ion o he HIV-1 i us (Singh e al. 2004). Al e -
oxins I–III and V, oxidized pe ylenes om Al e na ia
enuissima, inhibi ed HIV-1 eplica ion a mic omola
concen a ions (Bashyal e al. 2014). The dime ic e ahy-
d oxan hone, penicillixan hone A om Aspe gillus umi-
ga us displayed s ong an i-HIV ac i i y by inhibi ing
CCR5- opic HIV-1 SF162 and CXCR4- opic HIV NL4-3
(Tan e al. 2017). A ma ine-de i ed A. nige p oduced
mal o min C, which exhibi ed a e y s ong an i-HIV-1
ac i i y (Zhou e al. 2015a). An endophy ic Aspe gillus sp.
CPCC 400735 p oduced h ee phenalone and cy ochalasin
de i a i es also showing an i-HIV ac i i y (Pang e al.
2017). Concen icolide om “Daldinia concen ica” ( ax-
onomy doub ul since his species does no occu in China
acco ding o he wo ld monog aph by S adle e al. 2014)
inhibi ed HIV-1 by induc ion o cy opa hic e ec s (Fang
and Liu 2009). No el sesqui e penoids om Pa aconio-
hy ium b asiliense showed mode a e an i-HIV-1 eplica-
ion in C8166 cells (Liu e al. 2010b). The pupukeanane
sesqui e penoid chlo opupukeannolide A om Pes alo-
iopsis ici showed signi ican an i-HIV-1 ac i i y (Liu e al.
2010c). The cy ochalasan pe coniasin J and he me o e -
penoid pe iconone B om Pe iconia sp. displayed mod-
e a e an i-HIV ac i i y (Liu e al. 2016,2017b). The
a nesyla ed isoindolinones s achybo ysams A–C and he
phenylspi od imane de i a i es s achbo ysin A and G
om S achybo ys cha a um displayed mode a e an i-HIV
ac i i y (Zhao e al. 2017a,b).
The h ee consecu i e unc ions con olled by HIV
e e se ansc ip ase a e: RNA e e se ansc ip ion o
DNA, deg ada ion o RNA empla e by RNase H, and
duplica ion o he emaining DNA s and. Inhibi ion o
hese p ocesses is impo an o he disco e y o an i-HIV
d ugs. S achybosin D (26) (Fig. 9), a phenylspi od imane
me aboli e om a sponge-de i ed isola e o S achybo ys
cha a um, showed inhibi o y e ec s on HIV-1 eplica ion
by a ge ing e e se ansc ip ase. I was able o inhibi
NNRTIs- esis an s ains and wild- ype HIV-1 (Ma e al.
2013).
In eg ase is he only p o ein encoded by HIV-1, aside
om he enzymes p o ease and e e se ansc ip ase. Singh
e al. (1998,2002a,b,2003a,b,c) desc ibed se e al
compounds wi h inhibi o y ac i i y agains in eg ase om
a ious ungal species. Acco dingly, equise in and pho-
mase in om Fusa ium he e ospo um and Phoma sp.,
espec i ely Singh e al. 1998); in eg acins (In eg as a in A
(27)) om Cy onaema sp. (Singh e al. 2002a); in eg as-
a ins ( om an uniden i ied ungus; c . Singh e al. 2002b);
epiphiobolins C and K om “Neosa o ya”; i.e., Aspe -
gillus sp.; 8-O-me hylan h agallol om Cylind oca pon
ian ho hele; hispidin and ca eic acid om Inono us
ama icis; 3-hyd oxy e phenyllin om Aspe gillus can-
didus (Singh e al. 2003a); naph ho-γ-py ones om
Fusa ium sp. (Singh e al. 2003b); and xan ho i idica ins
om Penicillium ch ysogenum (Singh e al. 2003c) all
showed low mic omola inhibi ion agains he clea age
eac ion o HIV in eg ase. Funalenone om Penicillium sp.
FKI-1463 also had he same e ec (Shiomi e al. 2005).
In luenza i us inhibi o y na u al p oduc s om ungi
The H1N1 and H3N2 i uses a e among he a ge s o
na u al p oduc s o ungal o igin wi h an i-in luenza
ac i i y. The e penoid s achy lin (28), isola ed om a
ma ine-de i ed isola e o S achybo ys showed modes
ac i i y agains he in luenza A i us (H1N1) wi h an IC
50
o 3 910
−3
µM (Minagawa e al. 2002). The γ-py one
isoas el oxin om Aspe gillus och aceope ali o mis
showed low mic omola ac i i y (IC
50
=0.23 µM) agains
bo h in luenza i uses (Wang e al. 2016). Ano he
Aspe gillus sp., s ain p oduced he γ-py one de i a i e
as el oxin E wi h IC
50
alues o 6.2 and 3.5 µM agains
H1N1 and H3N2, espec i ely (Tian e al. 2016). 3β-Hy-
d oxys e ol om Pes alo iopsis sp. (Sun e al. 2014) and
che mesinone om Nig ospo a sp. (Zhang e al. 2016b)
also had mode a e inhibi o y e ec s. Au eoni ol, a
me aboli e o Gliocladium spp. inhibi ed in luenza A and B
i us eplica ion wi h an EC
50
o 100 nM agains H3N2 ia
supp ession o in luenza hemagglu ina ion, while signi i-
can ly impai ing i al adso p ion (Sac amen o e al. 2015).
He pes Simplex i us (HSV) inhibi o y na u al p od-
uc s om ungi
The impo an human pa hogenic i uses HSV-1 and HSV-2
we e also subjec o sceening p og ams o ungal
me aboli e lib a ies, e en hough up o da e no d ug could
be disco e ed ha would ma ch he ac i i y o he ma ke
s anda d. Coccoquinone, an an h aquinone om Aspe gil-
lus e sicolo , demons a ed an IC
50
o 3 µM agains HSV-
1 (Huang e al. 2017a,b). Fi e lipopep ides om he
ma ine-de i ed ungus Scy alidium sp. showed mode a e
an i-HSV-1 and an i-HSV-2 ac i i ies in a dose- and ime-
dependen pa e n (Rowley e al. 2003). The diphenyl e he
glycoside co dyol C om Co dyceps sp. BCC 186 exhib-
i ed signi ican an i-HSV-1 ac i i y wi h an IC
50
alue o
1.3 μg/ml (Bunyapaiboons i e al. 2011).
Hepa i is i us inhibi o y na u al p oduc s om ungi
One no el icyclic polyke ide de i ed om a collec ion o
ungal-de i ed compounds, ani a acin A (29), was
epo ed o inhibi i al en y p ocess wi h an IC
50
alue o
0.6 µM and good selec i i y. I was obse ed o di ec ly
in e ac wi h he HBV en y ecep o co ela ed o hepa i is
D i us and impai ed i al bile acid anspo pa hway.
This compound also inhibi ed all HBV geno ypes (A–D)
(Kaneko e al. 2015). The an h aquinone me aboli e, 2′R-1-
hyd oxyiso hodop ilonme in, showed be e an i-hepa i is
B i us ac i i y as compa ed o he posi i e d ug con ol,
Fungal Di e si y (2019) 97:1–136 17
123
lami udine (Jin e al. 2018). The epipoly hiodioxopipe -
azine de i a i e, 11′-deoxy e icillin A, showed an i i al
ac i i y by dec easing HBV-X eplica ion h ough inhibi-
ion o Ak ac i i y o deple ion o he au ophagic genes,
LC3 and p62 (Wu e al. 2015a). Sanda go e al. (2018) and
Na mani e al. (2019) ha e ecen ly disco e ed addi ional
an i-HCV agen s like 4-hyd oxypleu og isein (30) om he
nema ode apping basidiomyce e Hohenbuehelia g isea
and cy ospo aquinone B (31) om an I anian phy-
opa hogen belonging o he genus Cy ospo a. Recen ly
Sanda go e al. (2019b) epo ed he me o e penoid ho-
da in (32) om cul u es o he a e basidiomyce e Rhodo-
us palma us and also ound signi ican an i-HCV ac i i ies
o his compound, which ea u es a new ca bon skele on.
In iew o he ac ha newly a ising i al diseases a e
s eadily being epo ed and hey can sp ead mo e easily due
o g lobaliza ion e ec s, he sea ch o no el an i i al
agen s is as o ecen ly gaining impo ance. Some o he
na u al p oduc s poin ed ou in his en y may po en ially
ind hei way o an i i al d ug de elopmen in he u u e.
Howe e , he disco e y o new chemical de i a i es wi h
nanomola ac i i y and high selec i i y indices is s ill
wa an ed.
10. Immunosupp essi e and immunomodula o y
agen s om ungi
Immunosupp ession is a o m o he apy ha p e en s he
immune sys em o pa ien s om ac ing agains ansplan ed
issues and o gans; wi hou he a ailabili y o
immunosupp essi e d ugs, he p og esses made in mode n
medicine, in pa icula ega ding kidney, hea and li e
ansplan s, would be un hinkable. Fu he mo e, immuno-
supp essan s a e used o con ol se e e mani es a ions o
alle gic and au oimmune ela ed diseases. Many o hese
d ugs speci ically add ess ce ain biochemical pa hways
ha a e c ucial o he unc ioning o human de ense
agains alien o ganisms, such as pa hogens, by selec i ely
inhibi ing he immunocompe en lymphocy es o signal
ansduc ion cascades ha egula e he ansc ip ion o
cy okines. Fo his eason, pa ien s ea ed wi h immuno-
supp essan s o en ha e o be hospi alized and ea ed in
pa allel wi h an ibio ics o p e en in ec ion.
Some o he mos impo an immunosupp essi e d ugs
a e na u al p oduc s ha a e being p oduced bio echno-
logically by e men a ion o bac e ia and ungi. While
ac olimus and si olimus a e de i ed om ac inobac e ia
and will acco dingly no be ea ed he e, cyclospo ine (35)
and mycophenola e mo e il (33) a e ungal me aboli es,
and he p esen en y is he e o e dedica ed o hese
impo an molecules (Fig. 10).
Mycophenolic acid (34) (Fig. 10) was he i s an ibio ic
disco e ed and isola ed in c ys alline o m om ungi,
con a y o wha is w i en elsewhe e in he li e a u e,
whe e he penicillins a e o en ega ded as he oldes na -
u al an ibio ics. Biogene ically, his compound is a
me o e penoid, p oduced by Penicillium species, including
P. b e icompac um and P. oque o ii, and i s biosyn hesis
has ecen ly been elucida ed in he la e species (Del-Cid
e al. 2016). Fo a ious easons, he compound ne e made
N
N
O
O
NH
ON
NH
O
NH O
N
O
O
N
N
O
N
O
NH
OH
O
O
Cyclospo in A (35)
O
OOH
OOH
O
Mycophenolic acid (34)
O
OOH
OO
O
N
O
Mycophenola e mo e il (33)
Fig. 10 Chemical s uc u es o
immunosupp essi e d ugs
de i ed om ungal
e men a ion
18 Fungal Di e si y (2019) 97:1–136
123
i in o clinical de elopmen as an an ibac e ial o an i ungal
agen (Ben ley 2000; Bills and Gloe 2016). Ul ima ely, i s
u ili y as an immunosupp essan became e iden , and i is
now he ac i e p inciple o se e al ma ke ed d ugs, such as
My o ic
®
and CellCep
®
. The compound selec i ely
inhibi s inosine monophospha e dehyd ogenase (IMPDH),
an enzyme ha is c ucial o he biosyn hesis o guanosine
nucleo ides in mammalian cells. As his enzyme is mo e
essen ial in he T- and B-lymphocy es han in o he cell
ypes, and i s iso o m in he lymphocy es is mo e sensi i e
o mycophenolic acid, he d ug has a mo e po en cy os a ic
e ec on lymphocy es han on o he cell ypes, and he eby
supp esses he immune sys em (Allison and Eugui 2000).
Ano he seconda y bene icial e ec o mycophenolı
´c acid
is he deple ion o e ahyd obiop e in, which is a co- ac o
o he inducible ni ic oxide syn hase (iNOS). Conse-
quen ly, he adminis a ion o mycophenolic acid p e en s
damage o issues media ed by pe oxyni i e. The d ug is
mainly being used o p e en o gan ejec ion ollowing
ansplan s, as well as in he he apy o pso iasis (Epine e
e al. 1987) and o he immunological diso de s.
Cyclospo ine A (35) (Fig. 10) was i s disco e ed as a
mildy ac i e an i ungal an ibio ic by D ey uss e al. (1996),
who also ga e he i s hin s as o i s immunomodula o y
ac i i y. The compound is a non ibosomally biosyn hesized
pep ide de i ed om e men a ion o he ascomyce e
Tolypocladium in la um, and i s biosyn he ic gene clus e
was ecen ly elucida ed by Bushley e al. (2013). A e
yea s o in ensi e esea ch, i was ound ha his
cyclopep ide has a highly speci ic biochemical mode o
ac ion as i selec i ely binds o cyclophilin A. This p o ein
is an inhibi o o calcineu in, which is esponsible o
ac i a ion o ansc ip ion o he cy okine, in e leukine 2. I
in e leukine 2 is deple ed, he immune esponse o he
human body will be supp essed and ejec ion o ansplan s
can be p e en ed (G een e al. 1981; Wiesinge and Bo el
1980). The e o e, cyclospo ine A has become he ac i e
ing edien o blockbus e d ugs, such as Sandimmune
®
,
Neo al
®
and Res asis
®
). In addi ion o o gan ansplan s,
such immunosupp essan s can be e y use ul in he he apy
o o he diseases, including alle gies and neu odegene a-
ion. An example o he la e indica ion is he syn he ic
d ug, ingolimod (Gilenya
®
;21 in Fig. 6), which is
desc ibed u he abo e in chap e 6.
In his con ex , i is wo hwhile o no e ha many ungal
me aboli es a e highly use ul in he apy because hey show
he opposi e ac i i ies in biological sys ems, i.e., hey boos
he immune sys em and he e o e inc ease he esis ance
agains pa hogens o e en help o p e en cance . S iking
examples o such molecules a e he β-glucanes and p o-
ein–polysaccha ide complexes ha a e being ea ed
elsewhe e he ein.
S a egies agains plan disease
Fungi a e impo an agen s in comba ing a ious ungal
pes s and plan diseases ound in g eenhouses, he ield,
and e en pos -ha es . Fungi also ha e he po en ial o be
used agains ce ain animal pa asi es, such as nema odes. In
his sec ion, we discuss how ungi a e being used o con ol
plan disease, pes s, nema odes, and he bicides, as well as
hei possible u u e applica ions.
11. Biocon ol o plan disease using endophy es
Fungal pa hogens a e he chie agen o plan disease,
e ec ing se e e ag icul u al losses wo ldwide (Hyde e al.
2014; Punja and Raj 2003; S ange and Sco 2005; Ho -
bach e al. 2011). Ag ochemicals play a signi ican ole in
plan disease managemen and ensu e sus ainable and
p oduc i e ag icul u e sys ems. Howe e , he in ensi e use
o chemicals (de e mined by equen and high dose o
pes icides) has ad e se e ec s on human heal h, ecosys em
unc ioning, and ag icul u al sus ainabili y (Ande son e al.
2004; Vinale e al. 2008; Su yana ayanan e al. 2016).
Biocon ol is a s a egy used o con ol plan pa hogens,
esul ing in minimal impac o he en i onmen (De Waa d
e al. 1993; Vinale e al. 2008).
Endophy es eside asymp oma ically wi hin a plan o
a leas pa o hei li e cycle (Ca ol 1998; Huang e al.
2009; Sun e al. 2011; Clay e al. 2016). Fungal endophy es
can be b oadly classi ied in o wo g oups, he cla icipi a-
ceous (C) and he non-cla icipi aceous (NC). These
endophy es a e classi ied based on e olu iona y ela ed-
ness, axonomy, hos plan ange and ecological unc ion
(Hyde and Soy ong 2008; Rod iguez e al. 2009; O’Hanlon
e al. 2012; San angelo e al. 2015). Cla icipi aceous
endophy es, including A kinsonella,Balansia,Balansiop-
sis,Echinodo his,EpichloS
ˇ,My iogenospo a and Pa a-
epichloS
ˇspecies a e commonly associa ed wi h g asses in
he amily Poaceae and ely on hei hos h oughou hei
li e cycle as mu ualis species (Rod iguez e al. 2009;
Pu ahong and Hyde 2011; O’Hanlon e al. 2012; De Sil a
e al. 2016). Non-cla icipi aceous endophy es, such as
Fusa ium sp., Colle o ichum sp., Phomopsis sp. and Xy-
la ia sp. a e ound in mos e es ial plan s, and migh no
inhabi he hos plan s o hei en i e li e cycle (Rod iguez
e al. 2009; Delaye e al. 2013; De Sil a e al. 2016;
Jayawa dena e al. 2016).
Endophy es a e neu al o bene icial o hei plan hos s
(Backman and Siko a 2008). They boos hos plan g ow h,
i ness, s ess ole ance, and al e in e ac ions wi h pes s
and pa hogens (Oono e al. 2015; Clay e al. 2016).
Endophy es also p o ide p o ec ion agains he bi o y
(O’Hanlon e al. 2012; San angelo e al. 2015). Mo e
Fungal Di e si y (2019) 97:1–136 19
123
impo an ly, endophy es ha e po en ial as an unexplo ed
sou ce o candida e s ains o po en ial biocon ol appli-
ca ions (Ek-Ramos e al. 2013; Oono e al. 2015). Fo
example, endophy ic Ampelomyces species pa asi ize
powde y mildews (Busby e al. 2016). Since powde y
mildews a e bio ophs, hei an agonis s ac mainly h ough
an ibiosis and mycopa asi ism (Busby e al. 2016).
Biocon ol s a egies u ilize an agonis ic mechanisms o
dis up he li e cycle o pa hogens (c . Fig. 11), leading o
he p e en ion o in ec ion, educ ion in coloniza ion o
hos issues, educ ions in spo ula ion, and a ec ing he
pa hogen’s abili y o su i e (Punja and Raj 2003; Busby
e al. 2016). The hype pa asi ic an agonism may be medi-
a ed by ac o s such as include he as p oduc ion o ly ic
enzymes and/o an ibio ics, while o he biocon ol agen s
may induce he hos plan ’s de ense o jus compe e wi h
he pa hogen o nu ien s and ecological niches (Yan e al.
2015; Busby e al. 2016; Lecom e e al. 2016; Schlegel
e al. 2016).
Mejı
´a e al. (2008) s udied endophy es wi hin he heal-
hy lea es o Theob oma cacao, as well as hei an agonism
agains he pa hogenic Basidiomyco a species Monilioph-
ho a pe niciosa (wi ches b oom), Monilioph ho a o e i
( os y pod o ) and he oomyce e Phy oph ho a palmi o a
(black pod o ). The esul s showed ha wo endophy es,
iden ied as Colle o ichum gloeospo ioides and Clonos-
achys osea, espec i ely, dec eased pod loss due o black
pod o , and educed spo ula ing lesions in cacao pods
caused by Monilioph ho a o e i.
Endophy ic ungi om a ious hos plan s ha e been
shown o be e ec i e biocon ol agen s, including Al-
e na ia sp. and Cladospo ium sp., isola ed om whea
(Huang e al. 2016), and Al e na ia al e na a, isola ed om
g ape ine lea es (Zhang e al. 2017b). The use o an ag-
onis ic endophy es as biocon ol agen s, such as T icho-
de ma and Chae omium, p esen an a ac i e op ion o
managemen o ce ain plan diseases. I is impo an o
sc een po en ial endophy es h ough in- i o expe imen s
ollowing ield expe imen s unde di e en en i onmen
condi ions. In u u e esea ch using molecula echnologies
(e.g., me agenomics), ecological dynamics a e essen ial o
de eloping comme cial biocon ol agen s, as hese con-
ibu e o sus ainable ag icul u e. I is c i ical o no e ha
he species isola ed as endophy es om a ce ain hos plan
may be pa hogenic o o he plan s. Mo eo e , a ca e ul isk
assessmen ha excludes he possibili y o he o e p o-
duc ion o myco oxins is a manda o y p e equisi e o
egis a ions o new biocon ol agen s, ega dless o whe-
he he p oduce o ganisms a e endophy es.
12. Biocon ol o insec s using ungi
The loss in p oduc i i y due o c op damage om insec s
ep esen s a se ious h ea o he ag icul u al sec o . The
global c op loss due o insec s con ibu ed o losses o
almos $470 billion each yea (Culliney 2014), wi h he
global expendi u es on pes icides being in he ange o $56
billion in 2012. S ikingly, o he $56 billion, only $2–3
billion was spen on biopes icides (Ma one 2014). In he
USA, insec icides con ibu ed o almos 14% o all pes i-
cide expendi u es (Saba wal e al. 2018).
The mos common s a egy o con olling insec in a-
sions is he use o syn he ic chemical pes icides, such as
Chlo py i os, Acepha e and Bi en h in (Dai e al. 2019a).
Howe e , insec icidal esis ance has become an undeniable
phenomenon, and has led o he disas ous collapse o he
pes con ol in many coun ies (Naqqash e al. 2016). The e
a e also o he conce ns a ising ega ding he use o hese
syn he ic chemicals, namely wi h ood sa e y, ad e se
e ec s o non- a ge o ganisms—especially hose
Endophy es we e isola ed om heal hy lea es and pods o
Theob oma cacao plan
Dual cul u e assays
An agonis ic ac i i y o endophy es agains h ee
pa hogens; Monilioph ho a pe niciosa, M. o e i and
Phy oph ho a palmi o a
Used 3 me hods – an ibiosis, compe i ion o subs a e and
mycopa asi ism
G eenhouse expe imen
Spo e suspension o endophy es we e inocula ed o
cacao lea es and he pe cen o ungal coloniza ion
pe lea assessed pla ing on cul u e media
Field ials
Spo e suspension was sp ayed o cocoa pods and
measu e he pe cen age o each pod had been
colonized by he inocula ed ungus
Fig. 11 Me hodology used o assess biocon ol ac i i y o endophy es
agains pa hogens in cocoa plan s
20 Fungal Di e si y (2019) 97:1–136
123
bene icial an agonis s o insec s—and he en i onmen al
impac associa ed wi h he use o ha m ul chemical com-
pounds (Sandhu e al. 2017). The d awbacks o con en-
ional insec icides spu ed he sea ch o po en and eco-
iendly biocon ol agen s.
Biological con ol agen s o e mo e ad an ages han
hei chemical coun e pa s, since hey a e sa e o o he
non- a ge o ganisms and in ec only speci ic species, wi h
long- e m esul s on a ge pes s (Sanda and Sunusi 2016).
In pa icula , he en omopa hogenic ungi, ha e he
capaci y o educe o e adica e insec popula ions. Mos
ungi used o he con ol o insec pes s a e ascomyce es,
which a e usually ound in he soil and can cause na u al
ou b eaks on hei own when en i onmen al condi ions a e
a o able. Some ungal s ains ha e been de eloped in o
comme cial p oduc s because o hei abili y o be mass
p oduced (e.g. Beau e ia bassiana, Lecanicillium mus-
ca ium, Me a hizium anisopliae). These can in ec a wide
ange o insec hos s. (c . Fig. 12). Speci ic ungal s ains in
comme cial p oduc s a ge insec g oups such as Coleop-
e a, Dip e a, Hemip e a, Hymenop e a, Lepidop e a and
O hop e a (Dauda e al. 2018).
Some en omopa hogenic ungi can also exis as plan
endophy es in a a ie y o hos s. They can exhibi dual
unc ions, ac ing agains insec s and plan pa hogens, hus
gi ing p o ec ion o plan hos s. Mo eo e , hey can ha e
addi ional oles in endophy ism, plan disease an agonism,
g ow h p omo ion and hizosphe e coloniza ion (Yun e al.
2017; Jabe and Ownley 2018).
Gene ally, he i s mode o ac ion o en omopa hogenic
ungi is o p oduce s icky spo es o insu e adhesion o he
body o he hos . The non-speci ic adhesion mechanism o
he conidia is due o hei hyd ophobic p ope ies, which
has p o ein in e ac ions wi h he hyd ophobic exoskele on
o he suscep ible hos . The spo es ge mina e quickly and
ini ia e pene a ion o he insec exoskele on. The ungal
cells mul iply in he hemocoel o he hos ’s body,
inc easing he u go p essu e and e en ually killing he
insec . The en omopa hogen g ows in he hos ’s cada e o
op imize spo e p oduc ion and dispe sal unde a o able
en i onmen al condi ions (Roy e al. 2006). High numbe s
o spo es a e equi ed o insu e in ec ion, wi h a minimum
o 1910
8
o 1910
9
conidia/ml (Inglis e al. 2012).
En omopa hogenic ungi also p oduce seconda y
me aboli es ha can ac as oxins wi h insec icidal e ec s.
P oli e a ing p o oplas s p oduce hese compounds o
weaken he hos ’s de ense mechanisms, causing apid
dea h (Hussain e al. 2014). The en omopa hogens ha
p oduce oxins a e mo e e ec i e a killing he insec hos s
as compa ed wi h hose s ains ha do no p oduce such
me aboli es (Ke shaw e al. 1999). The e a e a a ie y o
ac i e compounds p oduced by en omopa hogenic ungi
ha exhibi insec icidal p ope ies, as lis ed in Table 4.
Beau e icin (36 in Fig. 13) is a well-known ac i e com-
pound p oduced by en omopa hogenic ungi. I plays a key
Fig. 12 En omopa hogens
in ec ing insec hos s.
aAc odon ium c a e i o me,
bCo dyceps mili a is,
cOphioco dyceps nu ans
Fungal Di e si y (2019) 97:1–136 21
123

ole in he i ulence o ungi ha in ec a h opods (Rohl s
and Chu chill 2011). I is a cyclic hexadepsipep ide, con-
aining h ee D-hyd oxyiso ale yl and h ee
N-me hylphenylalanyl esidues in al e na ing sequence,
and belongs o he ennia in an ibio ic amily. I is s uc-
u ally simila o ennia ins; howe e , i di e s in he na u e
o i s N-me hylamino acid (Wang and Xu 2012). I was i s
isola ed om Beau e ia bassiana (Hamill e al. 1969) and
la e om Fusa ium species (Liuzzi e al. 2017). Beau-
e icin has a s ong insec icidal unc ion agains a b oad
spec um o insec s. Since he a ge insec s a e mo ing
o ganisms, he en omopa hogenic ungi p oducing beau-
e icin a e mo e e ec i e insec icidal agen s han he
di ec use o he compound. Beau e icin was i s disco -
e ed o ha e insec icidal ac i i y by Hamill e al. (1969).
O he s udies p o ed he e icacy o beau e icin in killing
o he insec s, such as Callipho a e y h ocephala,Lygus
spp. (Leland e al. 2005), Aedes aegyp ii (G o e and Pople
1980), Spodop e a ugipe da and Schizaphis g aminum
(Ganassi e al. 2002); howe e , i can also be oxic o bees,
hus posing a h ea o o he bene icial insec s when applied
in he ield.
Bassianolide (37) a cyclic depsipep ide om Lecani-
cilium lecanii, exhibi s mode a e cy o oxici y and an
immunosupp essi e e ec o insec hos s. I can cause
signi ican maximum mo ali y o Plu ella xylos ella a
0.5 mg/ml concen a ions (Keppanan e al. 2018). As in
o he g oups o ungal cyclopep ides, se e al a ian s i
bassianolies a e known (Ma suda e al. 2004).
Des uxins (38–40), he cyclic hexadepsipep ide
myco oxins a e p oduced by Me a hizium anisopliae. They
can kill a a ie y o insec pes s. The pu i ied des uxins
can cause oxic e ec s on he la al de elopmen al s age o
mosqui oes (Aedes aegyp ii) wi h high mo ali y a es
(Ra ind an e al. 2016). The s udy o Dong e al. (2016)
also e ealed posi i e co ela ions be ween des uxin p o-
duc ion and blas ospo e o ma ion, and he p oduce s ain
has he po en ial o be de eloped in o a mycoinsec icide.
Ennia ins (41–44) a e only p oduced by Fusa ium
species. They ac as ionopho es ha bind wi h ammonium
in he anspo o ions in he lipid bilaye memb ane o he
cell. This ionopho ic p ope y o ennia ins leads o he
oxic ac ion in he cell h ough he dis u bance o he
no mal physiological concen a ion. Thei bes s udied
de i a i e, Ennia in B was p e iously shown o exhibi
insec icidal ac i i y agains blow ly (Callipho a e y h o-
cephala) and mosqui o la ae (Aedes aegyp i) (G o e and
Pople 1980).
The success ul applica ion o en omopa hogenic ungal
s ains elies on se e al ac o s, such as le el o i ulence,
p oduc ion e iciency and le el o sa e y o humans and
o he non- a ge species. Vi ulence depends on a complex
o ac o s, such as spo e hyd ophobici y, which is in ol ed
in he conidial adhesion, ge mina ion pola i y o he spo es
whe ein unidi ec ional spo es a e mo e i ulen han mul i-
Table 4 Some insec icidal compounds p oduced by en omopa hogenic ungi
En omopa hogen Insec icidal compounds Re e ences
Beau e ia bassiana Bassiac idin
Bassianin
Bassianolide
Beau e icins (36)
Beau e olides
Ma suda e al. (2004), Quesada-Mo aga e al.
(2004), Ohshi o e al. (2006), Heneghan e al.
(2011), Fisch e al. (2011), Su
¨ssmu h e al. (2011)
Beau e ia enella Beau e olides,
Beau e icins (36)
Bassianolide (37)
Ohshi o e al. (2006), Nama ame e al. (1999),
Su
¨ssmu h e al. (2011)
Lecanicillium lecanii Hel olic acid Kildgaa d e al. (2014), Liang e al. (2016)
Fusa ium spp.;“Paecilomyces”(Isa ia)
umoso oseus, Paecilomyces (Isa ia)
enuipes
Beau e icins (36)
Isa ia sp. Beau e olides B iggs and A kins (1966), Isogai e al. (1978),
Elswo h and G o e (1980), G o e (1980)
Me a hizium anisopliae Des uxins (38–40) Wang e al. (2012), Yoshida e al. (2014)
22 Fungal Di e si y (2019) 97:1–136
123
di ec ional ones, p esence o hyd oly ic enzymes o b each
he hos ’s de ense wall, and sensi i i y o abio ic ac o s
like empe a u e and humidi y. Mo eo e , en o-
mopa hogenic ungi should only be conside ed o com-
me cializa ion i hey demons a e high p oduc ion
e iciency, whe ein he s ains ha e minimum equi emen s
o g ow h and can be g own and mass p oduced in solid
subs a e (Hussain e al. 2014), hus educing p oduc ion
cos s.
Ce ain echniques should be conside ed in o de o
inc ease he e ec i eness o mycoinsec icides. Since insec
la ae usually embed hemsel es in o plan issues o soil
and do no eed on c ops (Hall 1998), hey do no ypically
s ay in a speci ic loca ion and he e o e a e e y di icul o
a ge . Sp ay applica ion can be ine icien a his s age and
deposi ing mycoinsec ides o e a ield o c op may no be
e ec i e. The e o e, g anula o mula ions which coa d y
spo es on o b an o g ains, o he d ying and agmen a ion
o mycelium o hold spo es in s a ch, can bo h be e ec i e
me hods o ea insec s in he ield (Hall 1998). Adding he
g anula subs ances o mycoinsec icides inc eases he
accu acy and e iciency o he sp ay.
Se e al ac ics ha e been iden i ied by Lacey and Kaya
(2007) o inc ease he e ec i eness o mycoinsec icides.
P e en i e applica ions could be ine icien because he
esidues a e no long-las ing, and he e o e hey should be
applied only when he a ge pes is seen. Mycoinsec icides
should be applied be o e he pes popula ion eaches peak
numbe s, and he e o e ea ly applica ion is essen ial.
Timing is also impo an : iden i ying he li e cycle o he
hos , which has a highe p obabili y o being in con ac
wi h he spo es, could also inc ease he e ec i eness o he
mycoinsec icide. Fo example, Beau e ia bassiana is mo e
e icien in in ec ing ac i e nymphs han winged adul s.
Mo eo e , mycoinsec icides should no be applied du ing
N
O
O
O
O
NO
O
O
O
N
O
O
O
N
O
Bassianolide (37)
NH
O
N
N
O
NHO
O
O
H
O
O
N
H
NH
O
N
N
O
NHO
O
O
H
O
R
O
N
H
Des uxin A (39)
Des uxin B, R= CH-(CH (38)
3
)
2
Des uxin E, R= (40)
O
O
NN
OO
N
O
O
O
O
O
O
Ennia in A (41)
O
NN
OO
N
O
O
O
O
O
O
Ennia in A1 (42)
O
NN
OO
N
O
O
O
R
O
O
O
Ennia in B, R=CH (43)
3
Ennia in B1, R=-CH (44)
2
CH
3
O
N
O
N
O
O
O
N
O
O
O
O
Beau e icin (
36
)
Fig. 13 Chemical s uc u es o
insec icidal compounds om
ungi
Fungal Di e si y (2019) 97:1–136 23
123
d ough s because he en i onmen al condi ions a e no
a o able o he ge mina ion o he spo es.
App oxima ely 750 ungal species ha e been iden i ied
as insec pa hogens; howe e , in 1998 only 12 species we e
u ilized as mycoinsec icides in insec sp ays (W aigh and
Ca u he s 1998). By 2007 he numbe o mycoinsec icides
had inc eased o abou 110 comme cially a ailable p od-
uc s in he ma ke (de Fa ia and W aigh 2007). The
numbe has con inued o inc ease, wi h almos 2700
a h opod pes icides in oduced wo ldwide (Cock e al.
2010), in which abou 230 species o biological con ol
agen s ha e been ma ke ed and a ailable o comme cial
use ( an Len e en 2012). The demand and comme cial
applica ion o mic obial pes icides ha e inc eased
emendously. O 82 mic obial biopes icides egis e ed in
B azil, nea ly 46% a e mycoinsec icides (Masca in e al.
2018). Fungal biopes icides con ibu ed o a la ge po ion
o his inc eased demand and popula i y in pes manage-
men in he pas wo decades (Ja onski and Masca in 2017).
Se e al p oduc s ha e al eady disappea ed om he in e -
na ional ma ke place because hey we e no comme ically
success ul, bu a subs an ial numbe o ungal species ha e
been exploi ed (Kabaluk e al. 2010; Lacey e al. 2015)
(Fig. 12).
De Fa ia and W aigh (2007) and Masca in e al. (2018)
lis ed ep esen a i es o mycoinsec icides de i ed om
Beau e ia, Isa ia, Lecanicillium, and Me a hizium species
ound in he ma ke . Mos de eloped mycoinsec icdes we e
made o Eu opean and Ame ican ma ke s, whe eas only a
ew we e aimed a he A ican and Asian ma ke s
(Table 5).
The e ha e been con inual obs acles and challenges o
he de elopmen and comme cializa ion o ungal biolog-
ical con ol agen s o use in con olling insec popula ions,
anging om gaps in unde s anding he basic biological
knowledge o hei po en ial socio-economic impac .
P oblems ega ding he e ec i eness o insec icides a e
linked o economic p oduc ion. The inc ease in pes - e-
sis ance o chemical o mulas has led o d as ic en i on-
men al p oblems. New chemical insec icides a e no being
de eloped quickly enough, and he e o e he e is oom o
mic obial insec icides, which a e g owing a he apid pace
o 10–25% pe yea (S a nes e al. 1993), wi hin he ma -
ke . Enhancing he i ulence o po en ial ungal species is
essen ial o mycoinsec icides o de elop and each hei
ma ke po en ial.
The u u e o mycoinsec icides is p omising, wi h con-
inued esea ch o inc ease pa hogenic i ulence o en o-
mopa hogenic ungi in o de o achie e comme cial
success wi h gene ic and physiological enginee ing. Fu -
he s udies should be conduc ed o de e mine he ungal
ai s esponsible o he e ec i eness o mycoinsec icides,
enhancemen o hei i ulence, and de elopmen o eco-
iendly and e ec i e pes managemen s a egies.
13. Biocon ol o nema odes and ungal
nema icides
Plan -pa asi ic nema odes a e pa asi es which cause se e e
damage o many economically impo an c ops such as
oma oes, po a oes and whea . Fo example, a ound US $80
billion o yield losses a e caused annually by damage om
plan oo –kno nema odes, such as M. ja anica and M.
incogni a (Li e al. 2007). Nema icidal chemicals ha we e
once a he e ec i e, such as me hyl b omide, ha e ul i-
ma ely been banned because hey a e b oad-spec um
biocides ha kill all li e in he soil and con ibu e o he
deple ion o he ozone laye , he eby causing g a e p ob-
lems o he en i onmen . The e o e, in ecen yea s he e
ha e been g ea e o s in bo h academia and indus y o
ind ecologically iable al e na i es.
Nema ophagous ungi a e capable o con olling plan
pa asi ic nema odes h ough an agonis ic beha iou (Zaki
and Siddiqui 1996). The e a e mo e han 700 species o
nema ophagous ungi, which a e ound in ungal axa
including Muco omyco a, Basidiomyco a, Ascomyco a and
Chy idiomyco a (Li e al. 2005; Degenkolb and Vilcinskas
2016). These nema ophagous ungi a e ca ego ized in o
ou g oups acco ding o hei mode o pa asi ism: nema-
ode- apping (o he wise known as p edacious); nema ode
egg and emale pa asi es; endopa asi ic; and oxin-p o-
ducing ungi (Li e al. 2005; Degenkolb and Vilcinskas
2016). Nema ode– apping ungi o m speci ic apping
s uc u es on hypha, such as adhesi e knobs, cons ic ing
ings and adhesi e ne wo ks; hese h ee apping de ices
can be ca ego ized u he in o se en ypes: simple adhe-
si e b anches, uns alked adhesi e knobs, s alked adhesi e
knobs, non-cons ic ing ings, cons ic ing ings, wo
dimensional ne wo ks and h ee-dimensional ne wo ks
(Rubne 1996).
The cons ic ing ing ap is he mos sophis ica ed
mo phological adap a ion, which can be ound in ungi ha
a e no accommoda ed in he genus D echsle ella (Ba al
e al. 2018). When a nema ode en e s he ing, he h ee
cells swell, o ming h ee sphae ical s uc u es ha ap and
immobilize he nema ode (Jansson and Lopez-Llo ca
2004). Endopa asi ic ungi a ack nema odes o ally o by
pene a ion o spo es o zoospo es h ough he cu icles o
he nema ode hos (Moosa i e al. 2011). A e in ec ion,
he hyphae de elop inside he nema ode and diges s i s
con en . Fo example, he spo es o Ca ena ia anguillulae
a e inges ed by seden a y nema odes such as He e ode a
spp. The spo es ge mina e in he esophagus and he
mycelia hen diges he nema odes; 10–12 h a e he
in ec ion, zoospo angia de elop o elease new zoospo es
24 Fungal Di e si y (2019) 97:1–136
123
Table 5 Rep esen a i e mycoinsec icides in he ma ke (de Fa ia and W aigh 2007; Masca in e al. 2018)
Fungal species Ma ke ed
ade name
Coun y egis e ed Pes s a ge ed Manu ac u e
Me a hizium
anisopliae
A izium B azil Mahana a imb iola a, No ozulia (Zulia)
en e iana
TecniCon ol
BioMe ha GR
Plus
B azil M. imb iola a, No ozulia sp., Deois sp. Bio ech
Bioninsec B azil M. imb iola a, N. en e iana, D. la opic a Koppe do B asil
GR-INN B azil M. imb iola a, N. en e iana, D. la opic a Ag i alle
Me amax
Lı
´quido
B azil M. imb iola a Bio Soja
Me ap emium B azil M. imb iola a, N. en e iana, D. la opic a Biop emium
Me a i o B azil M. imb iola a, N. en e iana Fi oag o Con ole
Biolo
´gico
Me a hizium
JCO WP
B azil M. imb iola a, N. en e iana, D. la opic a JCO
Me a hizium
Oligos
B azil M. imb iola a, N. en e iana, D. la opic a Oligos Bio ecnologia
Me a hizium
P obio
B azil M. imb iola a, N. en e iana, D. la opic a P obio
Me haCon ol B azil M. imb iola a, N. en e iana, D. la opic a Simbiose
Me hamax EC B azil M. imb iola a No ozymes
Me ie B azil N. en e iana Ballag o
Opala B azil M. imb iola a, N. en e iana Lab. Biocon ole
Fa oupilha
Real
Me a hizium
Kenya, Sou h A ica,
E hiopia, Ghana
Mealybugs, h ips, whi e lies Real IPM (Kenya)
Me a hizium
b unneum
Me 52 EC USA Whi e lies, h ips, wee ils No ozymes Biologicals
(USA)
Me 52
G anula
USA, Eu ope Wee ils, h ips No ozymes Biologicals
(USA)
Bio1020 Ne he lands Wee ils No ozymes Biologicals
F ance
Beau e ia
bassiana
Ad al Colombia Aphids Bio-C op (Colombia)
Ag i alle
AUIN
B azil Bemisia abaci,Cosmopoli es so didus, Dalbulus
maidis, Te anychus u icae
Ag i alle
Ball e
´ ia B azil B. abaci Ballag o
Bassico e SC Colombia Whi e lies Co e Bio echnology
(Colombia)
Beau eCon ol B azil B. abaci, D. maidis, T. u icae Simbiose
Beau e ia
JCO
B azil B. abaci, C. so didus, D. maidis, T. u icae JCO
BioExpe Colombia Whi e lies, h ips Li e Sys ems
Technology
(Colombia)
Bio e ia WP B azil B. abaci, C. so didus, D. maidis, T. u icae Bioene gia do B asil SA
Bo emax EC B azil H. hampei, Diapho ina ci i, Hedypa hes
be ulinus
No ozymes
Bo e il WP B azil B. abaci, Hypo henemus hampei, Gonip e us
scu ella us, T. u icae
Koppe do B asil
B oadband Sou h A ica Whi e lies, h ips BASF Sou h A ica
Cade e SC Colombia Whi e lies, h ips Myc os In e nacional
(Colombia)
Ecobass B azil B. abaci, C. so didus, D. maidis, T. u icae Toyobo do B asil
Fungal Di e si y (2019) 97:1–136 25
123
in i o applica ion o Pichia anomala has educed c own
o disease in banana (Lassois e al. 2008). Saccha omyces
boula dii can induce phy oalexin o ma ion on so ghum
and soybean (S anga lin e al. 2010). Saccha omyces
ce e isiae inhibi ed he ac i i y o Bo y is cine ea (in
g apes) by p oducing ola ile compounds (Pa a a i e al.
2015). In i o applica ion o Me schnikowia pulche ima
agains pos -ha es o o g apes (Ble e e al. 2006, Pa -
a a i e al. 2015) was also no ably success ul.
O he Ascomyco a:Au eobasidium pullulans has been
used o con ol bunch o in able g apes caused by Bo y is
cine ea (Pa a a i e al. 2015). In addi ion, pos -ha es o
o able g apes caused by Monilinia laxa (Schena e al.
2003) we e also con olled success ully by his ungus.
Penicillium equen ans has been shown o e ec i ely
inhibi he g ow h o Monilinia sp., which causes b own o
in peaches (Guija o e al. 2007).
Basidiomyco a:C yp ococcus magnus can inhibi he
mycelial g ow h o Colle o ichum gloeospo ioides
in i o, and con olled pos -ha es an h acnose in papaya
(de Capde ille e al. 2007). An aqueous ex ac s om he
basidiomes o Len inula edodes has con olled he g ow h
o Puccinia econdi a . sp. i ici (Fio i-Tu ida e al. 2007).
In addi ion, he in i o applica ion o Pycnopo us san-
guineus has con olled he angula lea spo in beans caused
by Pseudoce cospo a g iseola (Viecelli e al. 2009).
Aqueous ex ac s o he basidiomes o Aga icus sub-
u escens ha e also shown an an agonism agains Puccinia
econdi a . sp. i ici. (Fio i-Tu ida e al. 2007). Howe e ,
hese basidiomyce es and hei ex ac s ha e no been
p o en o be e ec i e in ield ials, and he de elopmen
o me hods o e ec i e mass p oduc ion o a ain a o -
able cos s o goods will cons i u e a se ious p oblem.
16. Biocon ol o us s and smu s by an agonis ic
ungi
Rus ungi (U edinales) a e one o he la ges g oups in he
Basidiomyco a, comp ising abou 5000–6000 species
ound on a wide ange o hos s, including e ns, gym-
nospe ms, and mono- and dico yledonous angiospe ms
(Alexopoulos e al. 1996). Diseases such as co ee lea us ,
Hemileia as a ix, whea s em us , Puccinia g aminis,
Melampso a lea us s o Salicaceae (Populus and Salix)
and C ona ium s em us s o ha d pines a e causing
eno mous losses and o en making i necessa y o eplace
suscep ible c ops en i ely wi h non-hos species (Li le ield
1981).
Smu s p ima ily a ec g asses iz co n (maize), whea ,
suga cane, ba ley, oa s, o age g asses and so ghum
(Feldb u
¨gge e al. 2013). A smu is cha ac e ized by spo es
ha accumula e in soo -like masses called so i, which a e
o med wi hin blis e s in seeds, lea es, s ems, lowe pa s,
and bulbs (Lau ie e al. 2012). The so i usually b eak up
in o a black powde ha is eadily dispe sed by he wind.
Many smu ungi en e emb yos o seedling plan s, hen
de elop sys emically, and appea ex e nally only when he
plan s a e nea ing ma u i y (Liu e al. 2017a). Cu en ly,
he mos widely used con ol me hod o suga cane smu
disease is he b eeding o esis an cul i a s (Shen 2002;
Wada 2003; C o e al. 2008; Lwin e al. 2012; Shen e al.
2014). Howe e , i s de elopmen is cons ained by long
b eeding p ocesses, high cos s, and he a ailabili y o smu -
esis an pa en al lines. Disease a ibu ed o smu ungi
could also be con olled by soaking seed canes wi h
chemical ungicides (Olu olaji 1993; Bhuiyan e al. 2012).
Ano he app oach is using plan o ungal ex ac s ha
inhibi smu pa hogen ge mina ion and g ow h (Lal e al.
2009). A la ge numbe o ungi ha e been iden i ied as
hype pa asi es o us and smu ungi, which a e being used
as biocon ol agen s wo ldwide (Gowdu and Balasub a-
manian 1988; K anz 1981; Feldb u
¨gge e al. 2013).
Va ious s udies suppo he abili y o ce ain ungi o
con ol he g ow h o smu s and us s. The mechanisms
h ough which biocon ol agen s ac a e an ibiosis, sec e-
ion o me aboli es ha a e oxic, ly ic enzymes, pa asi ism
and compe i ion o nu ien s. Figu e 3shows he di e en
mechanisms o an agonis ic ungal species ac ion. Bio-
logical app oaches a e gaining popula i y, including he use
o mic obial an agonis s (Ecke and Ogawa 1988). Cla-
dospo ium species co-exis wi h us so i, and some a e
belie ed o be in a iably hype pa asi es o U edinales
(Mo icca e al. 1999). Cladospo ium u edinicola is a
common nec o ophic hype pa asi e ha can des oy us
hyphae and causes coagula ion and disin eg a ion o he
cell cy oplasm o Puccinia ces i (Spegazzini 1912), Puc-
cinia (Ellis 1976), C ona ium que cuum (Mo gan-Jones
and McKemy 1990), Puccinia iolae (T aquai e al. 1984)
and Puccinia ho iana (S i as a a e al. 1985). Mo eo e ,
C. u edinophilum was also epo ed o colonize and des oy
U edo cyclo auma p opagules in Pa aguay (Spegazzini
1912). S eyae (1930) also desc ibed C. hemileiae as an
e ec i e hype pa asi e o co ee us ungus, Hemileia
as a ix, in Zai e (Democ a ic Republic o Congo). Powell
(1971) epo ed ha C. gallicola in galls o C ona ium
comand ae on Pinus con o a a . la i olia is pa asi ic on
aeciospo es. Hyphae o C. gallicola pene a e in o he
aeciospo es o pine gall us , Endoc ona ium ha knessii
(Su on 1973). Tsuneda and Hi a suka (1979) in es iga ed
C. gallicola and ound ha i pa asi ized E. ha knessii by
bo h simple con ac —disin eg a ing he cell walls o he
spo es—and by ac ual pene a ion o he spo e walls, wi h
o wi hou he o ma ion o app esso ia, causing he
coagula ion and disappea ance o he hos cy oplasm.
32 Fungal Di e si y (2019) 97:1–136
123

Hulea (1939) and Rayss (1943) documen ed a simila
phenomenon whe e C. aecidiicola, a common hype pa a-
si e o us s in Eu ope and in he Medi e anean a ea,
pa asi ized E. ha knessii on Pinus spp. in Cali o nia (Byle
e al. 1972). Keene (1954) s a ed ha his hype pa asi e
also d as ically pa asi ized aecia o Puccinia conspicua in
A izona and u ediniospo es o Melampso a medusae unde
s o age condi ions (Sha ma and Hea he 1980). Mo eo e ,
S i as a a e al. (1985) also documen ed ha Puccinia
ho iana was o en egula ed by Cladospo ium sphae os-
pe mum and C. enuissimum. They we e also de ec ed om
aeciospo es o he wo-needle pine s em us C ona ium
laccidum (Mo icca e al. 1999). O he g oups o ungi
aside om Cladospo ium we e also epo ed o ac as
biocon ol agen s. The en omopa hogenic and mycopa a-
si ic ungus Lecanicillium lecanii is also known o a ack
co ee lea us , Hemileia as a ix (Jackson e al. 1997).
No many comme cial bio ungicides o us and smu s
based on an agonis ic ungi a e cu en ly a ailable. Mah-
mud and Hossain (2016) showed ha he BAU-bio ungi-
cide (2%) (T ichode ma based p epa a ion) signi ican ly
a ec ed he mycelial g ow h o Us ilaginoidea i ens in an
in- i o es , bu his obse a ion emains o be con i med
in g eenhouse and ield ials.
K anz (1981) documen ed mo e han 80 species o ungi
om o e 50 gene a epo ed as hype pa asi es o us s.
Howe e , his numbe migh be an o e es ima e due o
some axa being synonyms. E en hough his la ge numbe
o an agonis ic ungi on us s and smu s has been epo ed,
ew comme cially, imp o ed bio ungicides a e a ailable
o p ac ical applica ion. As in o he applica ions o bio-
con ol agen s (see he abo e chap e s), p oduc o mula-
ion is he mos c i ical s ep o he en i e de elopmen
p ocess (Janisiewicz and Je e s 1997). The nex ew yea s
will likely see he inc eased applica ion o biocon ol
agen s in ag icul u e, wi h pa icula emphasis on he use o
mix u es o an agonis s on he same plan o gan. This
app oach may lead o a wide spec um o ac i i y o he
biological ea men o an inc ease in ei he he e icacy o
consis ency o he biological ea men . Fu he mo e, col-
labo a i e wo k o academic, ede al and p i a e sec o
scien is s is necessa y o de elop mo e e ec i e and con-
sis en bio ungicides.
Enhancing c ops and o es y
In his sec ion, we epo on he ways in which ungi a e
being used o may be used in he u u e in enhancing plan
de elopmen wi hin ag icul u e, o es y and ho icul u e.
17. Bio e ilize s
Bio e ilize s a e p oduced om o ganic ma e o ag o-
indus ial was es, which ac as subs a e o p opaga ion o
inoculum o selec ed mic oo ganisms (Kaewchai e al.
2009). The e a e wo app oaches o de eloping po en ial
bio e ilzie s: ei he he applica ion o a single supe io
species wi h mul i unc ions, o g oups o mic oo ganisms
(conso ia) bene icial o plan s (Vassile e al. 2015).
Bio e ilize s ha e been used in ag icul u e, ho icul u e,
landscape es o a ion, and soil emedia ion since he la e
1980s (Ha and T e o s 2005). The long- e m use o
bio e ilize s is economical and also eco- iendly o plan ,
animal and human heal h, and bio e ilize s a e enewable
and low-cos esou ces which a e accessible o ma ginal
and small a me s (Dubey and Maheshwa i 2008; Pal e al.
2015). Thus, he use o bio e ilize s is ecommended o e
chemical e ilize s. De ails ega ding bio e ilize s such as
e m, ole, ypes and ad an ages ha e been desc ibed by
Kaewchai e al. (2009), Pal e al. (2015), Vassile e al.
(2015) and I elima e al. (2018).
Se e al s udies ha e applied ungal inocula as bio e -
ilize s in g eenhouse and/o ield ials (G ige a e al.
2007; Rahi e al. 2009; Goe en e al. 2016; Zhang e al.
2016a; Wang e al. 2018c). Myco hizal ungi a e widely
used in ag icul u e, as hey o m oo symbio ic ela ion-
ships and p o ide many bene i s o plan s, such as
imp o ed plan g ow h and de elopmen , inc eased nu i-
en up ake and enhanced plan ole ance o disease (Whipps
2004; Liu and Chen 2007; El-Shaikh and Mohammed
2009; Smi h e al. 2010; He na
´ndez-Mon iel e al. 2013;
Goe en e al. 2016; Janous
ˇko a
´e al. 2017). S ains o he
gene a, such as Al e na ia,Aspe gillus,Chae omium,
Fusa ium,Penicillium,Se endipi a (Pi i o mospo a),
Phoma, and T ichode ma ha e been epo ed as plan
g ow h p omo ing ungi (Soy ong e al. 2001; Muhammad
e al. 2009; Salas-Ma ina e al. 2011; Va ma e al. 2012;
Bi as e al. 2015; Mu ali and Am u hesh 2015; Zhang e al.
2016a; Zhou e al. 2018). Examples o he use o ungal
inocula ea men s on plan s a e p o ided in Table 8. These
po en ial plan g ow h-p omo ing ungi can be u he
esea ched and de eloped as po en ungal bio e ilize s.
Nume ous comme cial ungal bio e ilize p oduc s
ha e been manu ac u ed globally and a e a ailable on he
ma ke oday. The e a e a ious o mula ion ypes, such as
g anules, we able powde , pelle s and liquids, which
comp ise one o mul iple ungal inocula. Aspe gillus,
Chae omium,Penicillium and T ichode ma species ha e
been used in bio e ilize p oduc s. Fo example,
Ke omium
®
has been de eloped and imp o ed om s ains
o Chae omium spp. in pelle and powde o m. The p o-
duc was used in g eenhouse and ield ials o oma o,
Fungal Di e si y (2019) 97:1–136 33
123
co n, ice, peppe , ci us, du ian, bi d o pa adise and
ca na ion plan s in Thailand (Soy ong e al. 2001). Plan s
ea ed wi h Ke omium
®
showed be e plan g ow h and
highe yield han non- ea ed con ol plan s. In addi ion,
Ke omium
®
had he abili y o con ol Phy oph ho a sp.,
causing ci us oo o in he ield. O he examples o
ungal bio e ilize p oduc s a e gi en in Table 8.
Bio e ilize s inc ease he up ake o nu ien s om he
soil o a mosphe e, and p oduce bioac i e compounds,
enzymes and ho mones which s imula e plan g ow h and
enhance oo g ow h (Chi e al. 2010; Abdel-Fa ah e al.
2013; Pal e al. 2015). Fungal bio e ilize s a e able o
solubilize and mobilize una ailable o ganic and ino ganic
o ms o phospho us in o soluble o ms, making hem
a ailable o plan s. Fo example, Aspe gillus nige was
mixed wi h Bacillus mega e ium o o m phospha e solu-
bilizing mic oo ganisms. These mic oo ganisms we e
applied as bio e ilize s in India (Pal e al. 2015). A bus-
cula myco hizae ha e been used as phospha e mobilizing
bio e ilize s (Zhang e al. 2018). Bio e ilize s play an
impo an ole in he ecycling o plan nu ien s and in
enhancing he a e o compos deg ada ion (Pal e al. 2015).
Some bio e ilize s ac as an agonis s and supp ess he
incidence o soil bo ne plan pa hogens while helping in he
biocon ol o plan diseases (Thame e al. 2011; Pal e al.
2015).
Table 8 Examples o he use o ungal (and oomyce e) inocula ea ed on plan s
Fungal inoculum T ea ed plan Resul Re e ences
A buscula myco hiza Zea mays Ac i e du ing he ep oduc i e g ow h s ages and may
bene i high p oduc i i y o maize c ops by acili a ing P
up ake
G ige a e al. (2007)
A buscula myco hiza Ci ullus lana us Reduced eplan p oblems h ough e ec i e modi ica ion
o he soil mic obo a s uc u e, and by inc easing he soil
enzyme ac i i ies
Zhao e al. (2010)
A buscula myco hiza
(Rhizophagus cla us and
Cla oideoglomus e unica um)
Woody plan
seedlings o
a ious plan s
- Inc eased oo coloniza ion o all woody plan seedlings
- Inc eased plan heigh and s em diame e o L. di a ica a,
C. obus um and C. issilis
- Inc eased shoo biomass g ow h o L. di a ica a,C.
obus um,G. ga dne iana and C. issilis
- Inc eased shoo phospho us o C. obus um,S.
e ebin hi olius and G. ga dne iana
Goe en e al. (2016)
Aspe gillus nige (CS-1) Whea P omo ed plan g ow h by inc easing he esh and d y
mass o whea pe plan in po expe imen s
Wang e al. (2018c)
Discosia sp. (HKUCC 6626) Zea mays,Pisum
sa i um,Cice
a ie inum
Inc eased oo leng h, shoo leng h and d y ma e in he
es plan s o e he uninocula ed con ol unde he
con olled en i onmen
Rahi e al. (2009)
Endophy ic s ains o Fusa ium
icinc um (RSF-4L) and
Al e na ia al e na a (RSF-6L)
Rice plan s Enhanced g ow h a ibu es, including inc eased oo -shoo
leng hs, chlo ophyll con en s, and biomass
Khan e al. (2015a)
Penicillium sp., T ichode ma sp.,
(Py hium sp. (Oomyce e)
Pea l mille seeds - Penicillium sp. a 5% (w/w) concen a ion eco ded
highes seed ge mina ion o 92% and 1701.9 seedling
igo
-Penicillium sp. a 5% (w/w) and Py hium sp. a 10% (w/
w) showed maximum disease p o ec ion o 67% and 61%
espec i ely agains downy mildew disease o pea l mille
-Penicillium sp. and T ichode ma sp. eco ded highes
disease p o ec ion o 71% and 66%, espec i ely unde
g eenhouse condi ions
Mu ali e al. (2012)
Pu pu eocillium lilacinum Toma o seeds Inc eased o he pe cen age o oma o seed ge mina ion
om 71 o 85% a e 48 h
Ca ello e al. (2015)
T ichode ma longib achia um Whea seeds Inc eased whea seedling heigh and oo leng h, compa ed
o he NaCl s ess ea men
Zhang e al. (2016a)
34 Fungal Di e si y (2019) 97:1–136
123
Fungal de i ed s imulan s, o elici o s, a e ungi o
ungal compounds ha enhance he p oduc ion o sec-
onda y me aboli es, o elici g ow h o immune esponse in
a a ge plan species upon applica ion. Plan esponses
include he up egula ion o genes in ol ed in plan de ense,
as well as he inc eased p oduc ion o an imic obial com-
pounds, lignin, seconda y me aboli es, and ce ain p o eins
(Vassile e al. 2015). Po en ial uses o such elici o s
include he enhanced p oduc ion o comme cially aluable
compounds/me aboli es, o he a i icial enhancemen o
plan de enses when pa hogens a e de ec ed (Radman e al.
2003). A no el app oach o he use o elici o s is o
inco po a e hem wi h immobilized s imulan s, such as
wi h a buscula myco hizal inoculum. Addi ionally, plan -
de i ed elici o s, which enhance he g ow h and de elop-
men o bene icial ungi such as a buscula myco hizae,
also show p omise in ad ancing his ield o s udy
(Akiyama e al. 2005; Besse e e al. 2006). Elici o s ha e a
high po en ial o enhancing plan p oduc i i y and
imp o ing plan de enses agains pa hogens, and gi en ha
elici o s can be used in combina ion wi h o he ypes o
bio e ilize s, hey hold much po en ial o wide scale
applica ion in he u u e.
Fungal bio e ilize s a e applied on a e y small scale in
ag icul u e as compa ed o chemical e ilize s due o hei
limi ed shel li e and slowe a e o e ec . Oli ian e al.
(2004) epo ed using s e ilized pea as solid suppo o
Fusa ium oxyspo um inocula ion, s o ing his admix u e a
oom empe a u e wi hou loss o ac i i y. G ow h and
o mula ions based on ecycling ag o-indus ial was es can
be expec ed o employ ni ogen- ixing and o he mic oo -
ganisms wi h di e en cha ac e is ics, such as biocon ol,
P-solubiliza ion, lignocelluloly ic ac i i y. Fo example,
combina ions be ween T ichode ma spp. and P-solubilizing
ungi can be cul u ed based on ag oindus ial-was es,
leading o mine aliza ion o he ma ix/subs a e by he
combined enzyme ac ions. We could apply immobiliza ion
o ungal cells oge he wi h enhanced bio echnology and
in combina ion wi h elici o s. Immobilized cell echnolo-
gies pe mi he use o wo and mo e mic oo ganisms,
which esul in highly e ec i e syne gies bene i ing all he
o ganisms in ol ed, including he plan s (Vassile e al.
2015). In o de o e ec i ely implemen he use and gain
he ull bene i s o bio e ilize s, an in eg a ed app oach
engaging a a ie y o mechanisms should be conside ed.
Such an app oach could be ailo ed o sui speci ic indus y
needs and a ge de ined ou comes, such as imp o ed
g ow h, up egula ion o key me aboli es, o enhanced plan
de enses.
18. A buscula myco hizae as bio e ilize s
Ec omyco hizal associa ion desc ibes a s uc u e ha
esul s om a mu ualis ic symbiosis be ween he oo s o
highe plan s and oo -inhabi ing ungi. Wi hin his sym-
bio ic ela ionship, he ole o he ungi is o help he hos
plan s ake up wa e and nu ien s, ecei ing plan -de i ed
ca bohyd a es om pho osyn hesis in e u n. Abou 6000
plan species in 145 gene a and 26 amilies (app oxima ely
5600 angiospe ms and 285 gymnospe ms) ha e been es i-
ma ed o possess ec omyco hizal symbio ic ungal pa -
ne s (B und e 2009; Tede soo e al. 2010).
Ec omyco hizal associa ion helps bo h he ungi and hei
hos plan s o o e come en i onmen al s esses caused by
low nu ien s, d ough , disease, ex eme empe a u es and
hea y me al con amina ion (Smi h and Read 2008; Cou y
e al. 2010; Kip e e al. 2012; Heilmann-Clausen e al.
2014). Mo eo e , ec omyco hizae can imp o e soil
s uc u e and nu ien s; p o ec he plan s agains oo
pa hogens; p omo e plan g ow h by p oducing phy oho -
mones; and inc ease he pho osyn he ic a e o he plan s
(Spli allo e al. 2009; Ramachela and The on 2010; Maki a
e al. 2012). Ec omyco hizae a e domina ed by membe s
o he Basidiomyco a, some Ascomyco a, and, a ely,
Muco omyco a (Taylo and Alexande 2005; Rinaldi e al.
2008; Tede soo e al. 2010). Gene ally, ec omyco hizae
p oduce ep oduc i e ui ing bodies appea ing abo e- o
below-g ound ha a e essen ial o he ood webs o o es
ecosys ems and hei spo e dispe sal (Rinaldi e al. 2008;
Wilson e al. 2011).
Plan seedling egene a ion and es o a ion a e o pi o al
in e es o o es y, bu he su i al o seedlings is o en
poo bo h in nu se ies and na u al plan a ion a eas, espe-
cially in mine spoils, pollu ed a eas, and o he eeless
a eas. The e o e, he main pu pose o he applica ion o
ec omyco hizae is o imp o e he su i al and g ow h o
seedlings. The po en ial ad an ages o ec omyco hizal
associa ion in nu se ies a e no only he posi i e g ow h
esponses o he seedlings, bu also a educ ion o e il-
iza ion cos s in an en i onmen ally iendly manne . The
ole o ec omyco hizae in o es es ablishmen and
eco e y has been well-es ablished. Nume ous s udies on
he ec omyco hizae inocula ion o seedlings ha e shown
inc eases in plan g ow h and p oduc i i y, he iabili y o
seedlings, and seedling es ablishmen on a o es es o a-
ion p og ams (Tes e e al. 2009; Dalong e al. 2011;
B ea ley e al. 2016; Velmala e al. 2018). Ec omyco -
hizae a e pa icula ly impo an o he g ow h o eco-
nomically impo an ees, including species o beech
(Fagus), dip e oca ps (Dip e oca pus and Sho ea), euca-
lyp us (Eucalyp us), oak (Que cus and Cas anopsis), pine
Fungal Di e si y (2019) 97:1–136 35
123
(Pinus) and sp uce (Picea) (Tennakoon e al. 2005; Flyk
e al. 2008; Dalong e al. 2011; Kayama and Yamanaka
2016). Cenocococum,Pisoli hus,Lacca ia, Rhizopogon,
Russula, Scle ode ma and Thelepho a species ha e been
shown o inc ease he a e o su i al and g ow h o
eucalyp us, pine and oak seedlings in bo h plan a ion and
e o es a ion p og ams (Fig. 16) (Chen e al. 2006; Jha
e al. 2008; C am and Dum oese 2012; Kip e e al. 2012;
Zong e al. 2015).
Gene ally, h ee main ypes o ec omyco hizal inocu-
lan s—soil, ui ing body/spo e and ege a i e mycelium—
ha e been used in nu se ies. Fo es soil was used as a sou ce
o indigenous ec omyco hizal ungi in an inocula ion
expe imen mixed wi h plan ing subs a es (Kaewg ajang
e al. 2013; Dulme e al. 2014; Res ep-Liano e al. 2014;
Li ne-Luzon e al. 2017). This me hod is s ill used in many
pa s o he wo ld, pa icula ly in de eloping coun ies.
Howe e , he use o o es soil inoculan s has he majo
disad an age ha he ec omyco hizal composi ion is
unknown. Mo eo e , i equi es la ge amoun s o soil and
hence isks in oducing plan pa hogens and weeds exi s.
F ui ing bodies/spo es o a ious ec omyco hizae a e easily
ob ained om na u al o es s and can be easily applied o
plan seedlings as inoculan s. The a ie y o applica ion
me hods include mixing wi h sand, clay, o e miculi e
ca ie be o e being added o plan ing subs a e o soil, sus-
pension in wa e and d enching o i iga ing, sp aying, and
encapsula ion o coa ing on o seeds. Ec omyco hizae ha
a e “gas e omyce es” (pu ball ungi) wi h conspicuous
basidomes a e be e sou ces han he gilled ungi i la ge
numbe s o spo es a e equi ed, as hey a e easie o collec
and use. Fo ins ance, species o he gene a Pisoli hus,Rhi-
zopogon and Scle ode ma p oduce a la ge quan i y o spo es,
and he app oxima e spo e concen a ion in a seedling
inocula ion may ange om 10
5
–10
7
spo es/ml (Chen e al.
2006; B uns e al. 2009; Rai and Va ma 2011; Aggangan
e al. 2013). Mos p e ious s udies esul ed in accep -
able le els o ec omyco hizal associa ion, imp o ed seed-
ling g ow h o pines in he nu se y, and imp o ed ou plan ing
success ollowing inocula ion wi h Pisoli hus and Rhizo-
pogon spo es (B uns e al. 2009; Dalong e al. 2011).
The e a e o cou se limi a ions o ui ing body/spo e
inoculan s: only hose ec omyco hizal species able o
p oduce la ge numbe s o ui ing bodies and spo es can be
used, and he e may be a conce n abou he compa ibili y
and e iciency o ec omyco hizae o he plan species o be
cul i a ed. As an al e na i e, ege a i e mycelial inocu-
lan s ob ained om pu e cul u es o ec omyco hizae may
be p epa ed om a pu e cul u e using di e en me hods, e.
g. using mycelial suspensions and subs a e ca ie s such as
o es li e , ce eal g ains, pea moss, e miculi e, and
algina e-beads (de Oli ei a e al. 2006; Rossi e al. 2007;
Lee e al. 2008a,b; Res ep-Liano e al. 2014; Kayama and
Yamanaka 2016; Kumla e al. 2016). This inoculan ype
Fig. 16 A buscula myco hizae
inoculum p oduc ion. aPo
cul u e o so ghum and maize,
bon- a m inoculum p oduc ion
using lea li e compos and
ag icul u al was es; cIn i o
p oduc ion wi h oo o gan
cul u e; dnewly p oduced
Funneli o mis mosseae spo es
a ached o Ri T-DNA
ans o med ca o oo s
36 Fungal Di e si y (2019) 97:1–136
123
has p o en o be he mos sui able me hod because o hei
e iciency in p omo ing plan g ow h by selec ed ungal
isola es. Howe e , op imal condi ions, including nu i ion,
empe a u e and subs a e ca ie , mus always be es ab-
lished empi ically o la ge-scale p oduc ion.
Se e al comme cial ec omyco hizal p oduc s ha e been
de eloped. Fo ins ance, he comme cial mycelial inocu-
lan s o MycoRhiz
®
, Ec omyco hiza Spawn
®
, Somycel
PV and Mycobead
®
a e a ailable. BioG ow Blend
®
,
MycoApply
®
-Ec o, Ec o i
®
and Myco T ee
®
Ec o-In-
jec able a e comme cially a ailable p oduc s wi h ec o-
myco hizae spo es. The comme cial p oduc s p oduced by
mixing endomyco hizae and ec omyco hizae spo es a e
MycoApply
®
-Endo/Ec o, BioO ganic
TM
Myco hizal
Landscape Inoculan and Mycoke
®
P o ARBOR·WP. In
o de o apply ec omyco hizae in o es y, i is necessa y
o selec ec omyco hizal isola es o high compa ibili y and
e iciency in he coloniza ion o he a ge plan species.
Inoculan ypes, as well as inocula ion p o ocols and skills
in nu se y p ac ices, lead o he success o an inocula ion
p og am unde he p ope en i onmen al condi ions in he
plan a ion si e.
The po en ial o a buscula myco hizae o inc ease
c op yields has been known o decades, bu he e a e ew
published s udies demons a ing he e ec i eness o he
la ge-scale inocula ion o globally impo an c ops, espe-
cially in he opics whe e popula ion g ow h is high (Ro-
d iguez and Sande s 2015). The e o e, esea che s need o
s udy la ge-scale a buscula myco hizae applica ion o
c ops in he opics whe e phospha e bioa ailabili y is low
and he applica ion o a buscula myco hizae has he
s onges po en ial o inc ease ood p oduc ion and educe
he need o apply phospha e e ilize s (Ceballos e al.
2013). Manu ac u e s should ensu e hei a buscula myc-
o hizae p oduc s a e ee om o he mic oo ganisms and
ensu e p oduc quali y and su icien weigh o cheap
anspo . Fa me s should ha e easy access o a buscula
myco hizae p oduc s, co ec ly apply hem o he c ops,
and know how o p oduce on- a m a buscula myco hizae
inoculum o sus ainable ag icul u e.
19. Applica ion o ec omyco hizal ungi
in o es y
Ec omyco hizal associa ion desc ibes a s uc u e ha
esul s om a mu ualis ic symbiosis be ween he oo s o
highe plan s and oo -inhabi ing ungi. Wi hin his sym-
bio ic ela ionship, he ole o he ungi is o help he hos
plan s ake up wa e and nu ien s, ecei ing plan -de i ed
ca bohyd a es om pho osyn hesis in e u n. Abou 6000
plan species in 145 gene a and 26 amilies (app oxima ely
5600 angiospe ms and 285 gymnospe ms) ha e been es i-
ma ed o possess ec omyco hizal symbio ic ungal
pa ne s (B und e 2009; Tede soo e al. 2010). Ec omy-
co hizal associa ion helps bo h he ungi and hei hos
plan s o o e come en i onmen al s esses caused by low
nu ien s, d ough , disease, ex eme empe a u es and
hea y me al con amina ion (Smi h and Read 2008; Cou y
e al. 2010; Kip e e al. 2012; Heilmann-Clausen e al.
2014). Mo eo e , ec omyco hizae can imp o e soil
s uc u e and nu ien s; p o ec he plan s agains oo
pa hogens; p omo e plan g ow h by p oducing phy oho -
mones; and inc ease he pho osyn he ic a e o he plan s
(Spli allo e al. 2009; Ramachela and The on 2010; Maki a
e al. 2012). Ec omyco hizae a e domina ed by membe s
o he Basidiomyco a, some Ascomyco a, and, a ely,
Muco omyco a (Taylo and Alexande 2005; Rinaldi e al.
2008; Tede soo e al. 2010). Gene ally, ec omyco hizae
p oduce ep oduc i e ui ing bodies appea ing abo e- o
below-g ound ha a e essen ial o he ood webs o o es
ecosys ems and hei spo e dispe sal (Rinaldi e al. 2008;
Wilson e al. 2011).
Plan seedling egene a ion and es o a ion a e o pi o al
in e es o o es y, bu he su i al o seedlings is o en
poo bo h in nu se ies and na u al plan a ion a eas, espe-
cially in mine spoils, pollu ed a eas, and o he eeless
a eas. The e o e, he main pu pose o he applica ion o
ec omyco hizae is o imp o e he su i al and g ow h o
seedlings. The po en ial ad an ages o ec omyco hizal
associa ion in nu se ies a e no only he posi i e g ow h
esponses o he seedlings, bu also a educ ion o e il-
iza ion cos s in an en i onmen ally iendly manne . The
ole o ec omyco hizae in o es es ablishmen and
eco e y has been well-es ablished. Nume ous s udies on
he ec omyco hizae inocula ion o seedlings ha e shown
inc eases in plan g ow h and p oduc i i y, he iabili y o
seedlings, and seedling es ablishmen on a o es es o a-
ion p og ams (Tes e e al. 2009; Dalong e al. 2011;
B ea ley e al. 2016; Velmala e al. 2018). Ec omyco -
hizae a e pa icula ly impo an o he g ow h o eco-
nomically impo an ees, including species o beech
(Fagus), dip e oca ps (Dip e oca pus and Sho ea), euca-
lyp us (Eucalyp us), oak (Que cus and Cas anopsis), pine
(Pinus) and sp uce (Picea) (Tennakoon e al. 2005; Flyk
e al. 2008; Dalong e al. 2011; Kayama and Yamanaka
2016). Cenocococum,Pisoli hus,Lacca ia, Rhizopogon,
Russula, Scle ode ma and Thelepho a species ha e been
shown o inc ease he a e o su i al and g ow h o
eucalyp us, pine and oak seedlings in bo h plan a ion and
e o es a ion p og ams (Fig. 17) (Chen e al. 2006; Jha
e al. 2008; C am and Dum oese 2012; Kip e e al. 2012;
Zong e al. 2015).
Gene ally, h ee main ypes o ec omyco hizal inocu-
lan s—soil, ui ing body/spo e and ege a i e mycelium—
ha e been used in nu se ies (Fig. 18a). Fo es soil was used
as a sou ce o indigenous ec omyco hizal ungi in an
Fungal Di e si y (2019) 97:1–136 37
123

inocula ion expe imen mixed wi h plan ing subs a es
(Kaewg ajang e al. 2013; Dulme e al. 2014; Res ep-
Liano e al. 2014; Li ne-Luzon e al. 2017). This me hod is
s ill used in many pa s o he wo ld, pa icula ly in
de eloping coun ies. Howe e , he use o o es soil
inoculan s has he majo disad an age ha he
ec omyco hizal composi ion is unknown. Mo eo e , i
equi es la ge amoun s o soil and hence isks in oducing
plan pa hogens and weeds exi s. F ui ing bodies/spo es o
a ious ec omyco hizae a e easily ob ained om na u al
o es s and can be easily applied o plan seedlings as
inoculan s. The a ie y o applica ion me hods include
mixing wi h sand, clay, o e miculi e ca ie be o e being
added o plan ing subs a e o soil, suspension in wa e and
d enching o i iga ing, sp aying, and encapsula ion o
coa ing on o seeds. Ec omyco hizae ha a e “gas-
e omyce es” (pu ball ungi) wi h conspicuous basidomes
a e be e sou ces han he gilled ungi i la ge numbe s o
spo es a e equi ed, as hey a e easie o collec and use.
Fo ins ance, species o he gene a Pisoli hus,Rhizopogon
and Scle ode ma p oduce a la ge quan i y o spo es, and
he app oxima e spo e concen a ion in a seedling inocu-
la ion may ange om 10
5
–10
7
spo es/ml (Chen e al.
2006; B uns e al. 2009; Rai and Va ma 2011; Aggangan
e al. 2013). Mos p e ious s udies esul ed in accep -
able le els o ec omyco hizal associa ion, imp o ed
seedling g ow h o pines in he nu se y, and imp o ed
ou plan ing success ollowing inocula ion wi h Pisoli hus
and Rhizopogon spo es (B uns e al. 2009; Dalong e al.
2011).
The e a e o cou se limi a ions o ui ing body/spo e
inoculan s: only hose ec omyco hizal species able o
p oduce la ge numbe s o ui ing bodies and spo es can be
used, and he e may be a conce n abou he compa ibili y
and e iciency o ec omyco hizae o he plan species o be
cul i a ed. As an al e na i e, ege a i e mycelial inocu-
lan s ob ained om pu e cul u es o ec omyco hizae may
be p epa ed om a pu e cul u e using di e en me hods, e.
Fig. 17 Applica ion o
Pisoli hus albus in eucalyp us
(Eucalyp us camaldulensis)
seedlings a e 3 mon hs o
inocula ion (a). T1 Pisoli hus
inocula ion expe imen . T2
Nu ien solu ion expe imen .
T3 Uninocula ed expe imen .
Ec omyco hizal oo ip o
Pisoli hus albus (b). C oss
sec ion o ec omyco hizal oo
ip o E.camaldulensis showed
man le shea h (M) and Ha ig
ne (a owed). Scale ba
B=1 mm, C =20 μm
Fig. 18 Inoculan ypes o ec omyco hizae (Pisoli hus o ien alis).
aSoil inoculan , bspo e suspension inoculan , c,d ege a i e
mycelial inoculan s
38 Fungal Di e si y (2019) 97:1–136
123
g. using mycelial suspensions and subs a e ca ie s such as
o es li e , ce eal g ains, pea moss, e miculi e, and
algina e-beads (de Oli ei a e al. 2006; Rossi e al. 2007;
Lee e al. 2008a,b; Res ep-Liano e al. 2014; Kayama and
Yamanaka 2016; Kumla e al. 2016). This inoculan ype
has p o en o be he mos sui able me hod because o hei
e iciency in p omo ing plan g ow h by selec ed ungal
isola es. Howe e , op imal condi ions, including nu i ion,
empe a u e and subs a e ca ie , mus always be es ab-
lished empi ically o la ge-scale p oduc ion.
Se e al comme cial ec omyco hizal p oduc s ha e been
de eloped In o de o apply ec omyco hizae in o es y, i
is necessa y o selec ec omyco hizal isola es o high
compa ibili y and e iciency in he coloniza ion o he
a ge plan species. Inoculan ypes, as well as inocula ion
p o ocols and skills in nu se y p ac ices, lead o he success
o an inocula ion p og am unde he p ope en i onmen al
condi ions in he plan a ion si e.
20. Use o o chid myco hizae and endophy es
in bio echnology
O chidaceae is one o he la ges amilies o lowe ing
plan s wi h o e 700 gene a and 25,000 species (Dea naley
2007; Sa hiyadash e al. 2012). O chids a e ound in a wide
ange o habi a s and may g ow au o ophically o
he e o ophically (Sa hiyadash e al. 2012; Tan e al. 2014;
Fochi e al. 2017). O chids a e economically e y impo -
an and hei sales ep esen a ound 8% o he wo ld
lo icul u e ade. The economically mos impo an gene a
a e Cymbidium,Dend obium, and Phalaenopsis (Dea na-
ley 2007, 2016; Chugh e al. 2009; Emsa-a e al. 2018).
Some o chids, such as Gas odia (G iesbach 2002; Dea -
naley 2007), Dend obium o icinale and D. nobile a e used
as na u al medicines (Li e al. 2009). Fu he mo e, he
economically mos impo an o chid p oduc s a e he la-
ou s de i ed om some species o he genus Vanilla,
which a e g own a a la ge scale and used in ood and
d inks (Dea naley 2007; Gonzalez-Cha ez e al. 2018).
Mos o chids ely on myco hizal ungi o su i al, as
hey a e essen ial o seed ge mina ion and ea ly plan
g ow h (Sa hiyadash e al. 2012; Fochi e al. 2017). Di -
e en ungal symbio ic myco hizae ha e been eco ded
om o chids (Table 9). O chid associa ed non-myco hizal
endophy ic ungi ha e been in es iga ed ia heal hy plan
o gans including lea es, oo s and s ems (Ma e al. 2015a),
whe eas myco hizal ungi a e gene ally isola ed om oo
issues (Tan e al. 2014; Ma e al. 2015a,b). Non-myco -
hizal endophy ic ungi ep esen o e 110 gene a,
including So da iomyce es (Neonec ia,T ichode ma,Ni-
g ospo a,Pes alo iopsis) and Do hideomyce es (Ce -
cospo a,Lasiodiplodia,Phyllos ic a) (Ma e al. 2015a,b).
Da k sep a e endophy es isola ed om Dend obium and
Lep odon idium sp. enhanced seedling de elopmen o
Dend obium nobile by o ming pelo on-like s uc u es in
he co ical cells o he o chid (Hou and Guo 2009;Ma
e al. 2015a,b). Fusa ium species p omo ed seed ge mi-
na ion o Cyp ipedium and Pla an he a o chids (Ma e al.
2015a,b). The endophy e Umbelopsis nana isola ed om
Cymbidium spp., p omo ed g ow h o Cymbidium hyb i-
dum (Ma e al. 2015a,b).
Many epiphy ic and e es ial o chids p oduce minu e
seeds wi h minimal nu ien ese es, and lack nu ien s o
seed ge mina ion and de elopmen in he ea ly g ow h
s age (Came on e al. 2006, Sa hiyadash e al. 2012; Tan
e al. 2014). A e ge mina ion, o chid seeds p oduce a
p o oco m (a p eseedling s age/ ea ly s age o he plan )
ha lacks chlo ophyll (Leake 2004; Sa hiyadash e al.
2012; Fochi e al. 2017). P o oco ms g ow in comple e
dependence on ungal symbion s o nu ien s and o ganic
ca bon supply (Came on e al. 2006; Dea naley 2007).
O chid seedlings de elop pho osyn he ic lea es la e and
hen ma u e oo s a e colonized by myco hizal ungi
(Came on e al. 2006; Smi h and Read 2008; Fochi e al.
2017). The p o oco m and ma u e oo s cells a e colonized
by in acellula ungal coils (pelo ons) (Fig. 19) (Dea naley
2007; Dea naley e al. 2016; Fochi e al. 2017).
O chid myco hizal associa ions a e use ul in he lo i-
cul u e ade, as hey s imula e seed ge mina ion and
Table 9 Fungal symbion s associa ed wi h di e en o chid species
Fungal symbion s
(Basidiomyco a)
O chid species Locali y Re e ences
Rhizoc onia Gas ochilus acaulis,Ne ilia p ainiana and Polys chya
conc e a
India Sen hilkuma (2003) Sa hiyadash e al.
(2012)
Ce a obasidium Zeuxine s a euma ica India Kuma and Kaushik (2004)
Tulasnella Ame o chis o undi olia
Dac ylo hiza majalis
Neuwiedia e a i olia
Wo ldwide Zelme e al. (1996)
K is iansen e al. (2001)
K is iansen e al. (2004)
Fungal Di e si y (2019) 97:1–136 39
123
p opaga e o chids (Tan e al. 2014). A b ie me hodology
o he inocula ion o myco hizal ungus (Tulasnella sp.)
o o chids acco ding o Non achaiyapoom e al. (2010) and
Tan e al. (2014) is ep esen ed in a low cha (Fig. 20). A
Tulasnella sp. isola ed om oo s o Dend obium nobile
acili a es signi ican ly highe seed ge mina ion o D.o -
icinale han ha o he con ol (wi hou inocula ion o
Tulasnella sp.) (Tan e al. 2014). In addi ion, Tulasnella sp.
Fig. 19 a,bMycelial coils
(pelo ons, seen as b own a eas)
in he oo sec ion o
Cymbidium lowianum collec ed
om he o chid nu se y a
Queen Si iki Bo anical Ga den
in Chiang Mai, Thailand, in
No embe 2008
Seed ge mina ion and
p o oco m de elopmen a e
assessed.
Small sec ions o oo a e placed on he po a o dex ose aga
(PDA), and hyphal ips o ungi a e ans e ed o esh PDA.
PDA aga plugs wi h ungi a e
inocula ed o oa meal aga
wi h n
y
lon clo hes.
Axenic seeds a e sown on o plan
issue cul u e media. A e 60 days,
seedlings a e ans e ed o esh
media.
Iden i ica ion o pelo ons om o chid oo s –
using mic oscope
Su ace s e iliza ion o oo
- 70% ( / ) e hanol, 2.5% ( / )
2 mon hs old seedlings and aga
plugs wi h ungi a e g own on PDA.
Seedlings a e ans e ed o s e ile
cylind ical glass bo le a e 10
d
Axenic o chid seeds a e sown on
he su ace o nylon clo hes and
placed in issue cul u e chambe .
F esh weigh and d y weigh
a e assessed a e 7 weeks.
B
A
Fig. 20 Scheme illus a ing he
me hodology o o chid seed
p opaga ion using myco hizal ungi
(in- i o condi ions)
(Non achaiyapoom e al. 2010; Tan
e al. 2014). aE ec o myco hizal
ungi on ge mina ion o o chid seeds.
bE ec o myco hizal ungi on
g ow h o o chid seedlings
40 Fungal Di e si y (2019) 97:1–136
123
p omo es seed de elopmen up o s age 5 (Table 10), while
he con ol wi hou he ungus de eloped only o s age 2
(Table 10) (Tan e al. 2014). Howe e , ungi isola ed om
o chid plan oo s do no always exhibi unc ional sym-
bio ic associa ions wi h he o chid plan (Dea naley 2007).
Mic oscopic obse a ions o o chid oo sec ions migh be
use ul o con i m he p esence o in acellula ungal
mycelium (Non achaiyapoom e al. 2010; Emsa-a e al.
2018). Fu he mo e, i is impo an o e alua e seedling
g ow h o myco hizal inocula ed o chids unde na u al
condi ions (Tan e al. 2014).
O chid myco hizal ungi a e also impo an o con-
olling disease in lo icul u e ade (Yode e al. 2000;
Emsa-a e al. 2018). Inocula ion o o chid myco hizal
ungi may enhance plan immuni y agains pa hogenic
diseases (Wu e al. 2011; Emsa-a e al. 2018). Fo
example, so o disease is one o he mos de as a ing
diseases caused by Dickeya spp., which kills o chids o
causes spo s/sca s on lea es and lowe s (Liau e al. 2003;
Emsa-a e al. 2018). One ecen s udy showed ha so o
de elopmen in myco hizal ungi inocula ed o chids was
signi ican ly educed compa ed o ha o non-myco hizal
ungi inocula ed o chids in g eenhouse condi ions. Pha-
laenopsis is a popula po ed plan species ha was used o
he s udy by Emsa-a e al. (2018). A b ie o e iew o he
me hodology o inocula ion o myco hizal ungi (Tulas-
nella deliquescens) oPhalaenopsis o con ol pa hogenic
Dickeya is p esen ed in Fig. 21.
Se e al comme cial p oduc s con aining myco hizal
inoculan s exis . These inoculan s a e a ailable o sale in
liquid and powde o m o easy and e ec i e usage. Mos
o hese p oduc s a e o ganic e ilize s inocula ed wi h
myco hizae spo es and wi h i amins, mine als, and
nu ien s o help bols e he e ili y and biological ac i i y
o he soil (see Table 11). Myco hizal ungi a e use ul in
o chid conse a ion (Tan e al. 2014). O chids a e a highly
di e se plan amily and many species may ace ex inc ion
h ea s (Rei e e al. 2016) because o habi a loss and o e -
exploi a ion o a ac i e species (Dea naley 2007). Wi h
his decline o o chid di e si y, i is now an u gen
equi emen o encou age esea ch on he ein oduc ion o
endange ed species o na u al habi a s (Rei e e al. 2016).
21. G ow h p omo ing ho mones om ungi
Fungi li e in di e se habi a s and ha e adap ed o eco-
logical niches, including plan sys ems. Plan s and ungi
ha e es ablished complex mu ualis ic ela ionships, and
wild plan s a e almos always colonized by endophy ic,
pa asi ic and myco hizal ungi (Rod iguez e al. 2009;
Pa ka and Naq i 2017). Fungi p oduce a a ie y o
bioac i e compounds ha play an impo an ole in he
physiological ac i i ies o he hos plan , in luencing he
g ow h o he hos s. This can e en lead o an inc eased
ole ance o abio ic and bio ic s esses o he plan s (Pineda
e al. 2010). Many s udies ha e shown ha ungi enhance
plan g ow h h ough he solubiliza ion o insoluble min-
e als in soil and sec e ion o plan g ow h egula o s (Bilal
e al. 2018; Chanclud and Mo el 2016;Ju
´nio e al. 2017;
Khan e al. 2012). G ow h p omo ion by plan g ow h
egula o s o phy oho mones p oduc ion, a e signal mole-
cules ac ing as chemical messenge s and play a unda-
men al ole in plan s. Plan g ow h ho mones p oduced by
symbio ic ungi may g ea ly in luence p ocesses including
Plan le s o Phalaenopsis sp. and Tulasnella
deliquescens, ungal myco hizal isola es we e
selec ed o he expe imen .
Fungal inoculum p epa a ion - coconu dus was soaked in
ap wa e o e nigh and d ied. PDA pieces con aining he
ungal mycelium we e placed on coconu dus .
Plan le s o Phalaenopsis we e asep ically placed on
coconu dus and incuba ed a 25oC o 30 days. Randomly
selec ed oo samples we e checked he p esence o
pelo ons.
Plan le s we e po ed o small plas ic po s
con aining sphagnum moss.
Bac e ial suspension was applied and
checked o de elopmen so o a eas
on lea es.
Fig. 21 Scheme illus a ing he me hodology o he inocula ion o
myco hizal ungi, Tulasnella deliquescens o he o chid Phalaenop-
sis o con ol pa hogenic bac e ia (Emsa-a e al. 2018)
Table 10 Di e en s ages o o chid seed ge mina ion (Tan e al.
2014)
S age Desc ip ion
0 No ge mina ion, iable emb yo
1 Enla ged emb yo, p oduc ion o hizoid(s) (=ge mina ion)
2 Con inued emb yo enla gemen , up u e o es a, u he
p oduc ion o hizoids
3 Appea ance o p o ome is em
4 Eme gence o i s lea
5 Elonga ion o i s lea
Fungal Di e si y (2019) 97:1–136 41
123
24. G owing mush ooms in bags
Wood-inhabi ing mush ooms can be cul i a ed in any ype
o lignocellulosic ma e ial, such as s aw, sawdus o ice
hulls (Vic o and Ola omiwa 2013). Pa hmashini e al.
(2008) showed ha he cul i a ion o he oys e mush oom
(Pleu o us os ea us) on a ious sawdus ypes p oduces
di e en ui ing yields. Sawdus is he mos commonly
used ma e ial o he cul i a ion o oys e mush ooms and
is he p e e ed medium o comme cial p oduc ion (Oei
2005). Maximum biological e iciency o oys e mush oom
cul i a ion is gained om g ow h on he sawdus o ubbe
ees (Pa hmashini e al. 2008). I has also been shown ha
so wood sawdus such as coconu , cashew, mango and
ubbe a e mo e sui able han ha dwood sawdus (Cus odio
and C is ophe 2004). The a ailabili y o aw ma e ials
such as sawdus , ice s aw, suga cane was es a e key
ac o s in he choice o ag icul u al was e o g owing
mush ooms (Pa hmashini e al. 2008). The mos commonly
and easily cul i a ed mush ooms in Sou h Eas Asian
coun ies a e oys e mush ooms (Pleu o us), ea mush-
ooms (Au icula ia), and s aw mush ooms (Vol a iella),
Len inula edodes (shii ake), as well as Len inus (e.g.
Len inus squa osulus), Ganode ma, Mac olepio a and
“Ag ocybe” (i.e., Cyclocybe) spp. (Kwon and Tha i ha -
goon 2004).
Di e en ypes o sawdus a e used as he g owing
medium in opical a eas, depending on he cha ac e is ics
o he a ea and he ees a ailable. Rubbe ee sawdus is
he mos popula (Kwon and Tha i ha goon 2004; Klomk-
lung e al. 2012; Nguyen 2004), ollowed by Acacia
au iculi o mis (Tapingkae 2005), Mangi e a indica (Tong
and Rajend a 1992) and Tama indus indica. Fo e e y 1 kg
saw dus bag, addi ions a e made o 10 g o calcium ca -
bona e, 50 g o iceb an, 10 g o pumice, 10 ml o
molasses, 10 g o lou and 10 g o b ewe ’s was e. These
componen s a e hen mixed wi h wa e o ob ain a wa e
con en o 65–70%. Each 800 g o subs a e is hen igh ly
packed in a 25.8 cm polyp opylene bag and capped wi h a
plas ic ing o bo le neck, lea ing space o la e inocula e
wi h mycelium (Kwon and Tha i ha goon 2004; S ame s
2000; Klomklung e al. 2012; Yamamaka 1997). Each
sawdus bag is sealed wi h a co on wool plug, co e ed
wi h newspape , and ied wi h a ubbe band. The sawdus
bags a e s e ilized a 121 °C o 15 min o a 90–100 °C o
3 h. A e he empe a u e d ops o 25 °C, he bags a e
inocula ed wi h spawn (Fig. 25c) ha comp ises 10% o he
weigh o he sawdus bag. Sawdus bags a e kep a oom
empe a u e (25 °C) a 70–80% humidi y o p oduce
ui ing bodies (Klomklung e al. 2012).
When new wild mush ooms a e in oduced o he ma -
ke , i is impo an o conduc ui ing es s. Depending on
he ype o mush oom, a choice can be made be ween
compos o sawdus media. As a ule o humb, o wood-
inhabi ing mush ooms (e.g. Len inula,Au icula ia)i is
be e o use sawdus media in bags (Fig. 25a, b), while o
soil-inhabi ing mush ooms (e.g. Aga icus,Mac olepio a)i
is be e o use s aw compos .
Fo wood-inhabi ing mush ooms, p o ocols adap ed
om Klomklung e al. (2012) a e ollowed. The su ace o
sawdus g owing bags is inocula ed wi h spawn. The bags
a e kep in a da k incuba ion oom a he op imum em-
pe a u e and ela i e humidi y o he pa icula mush oom.
Bags a e opened when he mycelium has comple ely col-
onized he subs a e. The su ace o he subs a e is sc aped
sligh ly wi h a s e ile easpoon o emo e he hin whi ish
Fig. 25 aAu icula ia hailandica g owing on sawdus subs a e bags; bAu icula ia co nea whi e a ie y g owing on sawdus subs a e bags;
cmush oom spawn bo les
48 Fungal Di e si y (2019) 97:1–136
123

mycelia. The subs a e bags a e hen placed on a shel and
co e ed wi h black clo h o allow app op ia e en ila ion.
They a e main ained in a g owing house a 80–85% ela i e
humidi y, and sp ayed daily wi h wa e un il pin heads
appea and e en ually de elop in o ui ing bodies. The
ui ing bodies a e manually ha es ed, coun ed and
weighed (Klomklung e al. 2012).
25. G owing mush ooms in he ield
Wi h he inc ease in consume awa eness and subsequen
demand o cul i a ed mush ooms, he e now exis s a need
o al e na i e, cos -e ec i e s a egies o mush oom cul-
i a ion. The global mush oom indus y is o ecas o g ow
om a alue o abou $35 billion USD in 2015 o nea ly
$60 billion USD in 2021, hus cla i ying he need o a
di e se ange o p oduc ion s yles in o de o de elop he
indus y in a sus ainable manne (Resea ch and Ma ke s
2018). Al e na i es o mo e adi ional high- olume p o-
duc ion echniques include he inocula ion o logs, cul i-
a ion in o es unde s o ies, and use o managed o es s, as
well as ield-g own mush ooms.
Field-g own mush ooms o e an e ec i e use o space,
allowing o he p oduc ion o mush ooms in ag icul u al
ields, alongside c ops, o be ween c opping cycles
(Fig. 26). O e ing addi ional income o a me s, his
p ac ice has become popula wi h u al de elopmen p o-
g ams (Zhang e al. 2014a,b; B um and B um 2017).
Addi ionally, ield cul i a ion allows o imp o ed soil
sys ems in ag icul u al ields due he inc eased a es o
nu ien cycling and p o ision o o ganic ma e in o he
soils (Phan and Saba a nam 2012; Zhang e al. 2012).
In his sec ion, we ou line some o he basic p inciples
and conside a ions o ield cul i a ion while lis ing some
Table 12 Examples o mush oom species sui able o ield cul i a ion, including soil cha ac e is ics, subs a es, and clima ic equi emen s o he
lis ed species
Species Soil ype Soil
pH
Subs a e Tempe a u e
(°C)
Humidi y
(%)
Re e ences
Cop inus coma us Sandy 7 Co onseed meal 16–22 85–95 Chen (2000)
Dic yopho a
indusia a
Loam 6.5–7 Bamboo li e , s aw,
sawdus
22–30 60–65 Chen (2000)
a
Ganode ma sp. Sandy 4.2–
5.3
Sawdus 23–34 80–90 Mayzumi e al. (1997), Cha and
Yoo (1997)
Len inula edodes Clay loam 4.5–6 Sawdus , whea / ice
b an
5–20 80–90
a
Mo chella spp. Sandy loam 7–7.5 Sawdus , whea b an,
humus
20 50–70 Liu e al. (2018a)
a
Oudemansiella
adica a
Clay loam 6.5–
7.2
Wood chips/co n cobs 20–30 60–80 Hao e al. (2016)
Phlebopus
po en osus
Clay loam,
humus
4–6 Sawdus 27–37 55–80 Ji e al. (2011), Kumla e al.
(2011,2015)
a
Polypo us umbella us Sandy loam,
humus
5.5–7 Lea es, humus, 18–24 60–80 Banda a e al. (2015)
a
S opha ia
ugosoannula a
Humus ich
sandy
5–6 Wood chips/ ice s aw 22–28 70–75
a
Vol a iella ol acea Clay 7.5–8 Rice s aw 22–40 90
a
a
Rows include unpublished indings/da a
Fig. 26 Field p epa a ion o cul i a ion o S opha ia ugosoannula a in Honghe Coun y, China
Fungal Di e si y (2019) 97:1–136 49
123
o he key species ha can be success ully cul i a ed in a
ield en i onmen (Table 12). We will limi ou discussion
o he cul i a ion o mush ooms in ag icul u al ields and
soils, no he b oade p ac ices o ou doo cul i a ion using
bags o inocula ed logs.
The e a e a ange o mush ooms ha can be cul i a ed
ou doo s, and app op ia e species can be selec ed acco ding
o local g owing condi ions (Table 12). Fo example, Co-
p inus coma us o S opha ia ugosoannula a can be
g own du ing he au umn and win e mon hs when em-
pe a u es a e milde , and Vol a iella ol acea should be
g own du ing he wa me summe mon hs. Conside a ion
o soil pH, ex u e and heal h is also c i ical. The pH and
ex u e will pa ially de e mine which species o mush oom
will be g own, and also he deg ee o i iga ion equi ed o
main ain desi ed soil wa e le els (Table 12). Soil heal h is
c ucial o he inal p oduc , as many species o ungi can
hype accumula e hea y me als (Cocchi e al. 2006;Tu -
kekul e al. 2004).
A e he selec ion o an app op ia e g owing a ea, a ew
basic s eps a e equi ed o he p epa a ion o he ield and
subsequen cul i a ion. A e ligh illing o he ield,
compos is applied, ollowed by he applica ion o he
ungal ma e ial (spawn o colonized bags), his is hen
co e ed in compos and a inal laye o soil o e ha (a
mulch o s aw o shade clo h could u he p o ec agains
desicca ion and d ying ou ) (Fig. 26).
The e a e a wide ange o applica ions o he ield
cul i a ion o mush ooms, bu mos ela e o he in ensi i-
ca ion o land use sys ems, gene a ion o addi ional sou ces
o income, and appeal o low income g oups ha canno
a o d he cos s o es ablishing g ow houses. This me hod
o p oduc ion has become popula in many pa s o Asia
whe e clima es a e sui able and smallholde a me s need
al e na i e sou ces o income. Fo example, in Cambodia,
a me s ha e adop ed he p ac ice o sp eading spawn
p oduced om Len inus o Vol a iella species o e ice
s aw was e in he paddies (wi h supplemen ed wa e ing).
This p o ides an addi ional ha es o mush ooms om he
paddies du ing he o season. Ano he p og am un in
Honghe Coun y, Yunnan P o ince, China, assis s local
a me s wi h he cul i a ion o S opha ia ugosoannula a
in hei ields; his is a seasonal mush oom c op p oduced
mos ly in au umn and sp ing when he empe a u es a e
sui able (Fig. 27, Table 12).
The na u e o g owing mush ooms ou doo s means ha
he mush oom c op is subjec o ambien en i onmen al
condi ions, wi h no clima e con ols in place, o example,
empe a u e and humidi y luc ua e wi h no eal mecha-
nisms in place o con ol hese pa ame e s. In addi ion o
clima ic a iabili y, ou doo cul i a ion exposes he
mush ooms o non-s e ile condi ions, allowing easy access
o seconda y in ec ion by slime molds, p eda o y ungi,
and insec s (Table 12).
Field cul i a ion o mush ooms is applicable o a wide
ange o habi a s and condi ions, depending on he desi ed
species o be g own. By o e ing no el and exci ing
al e na i es o plan -based ag icul u e, and p o iding
addi ional income o a me s, ield cul i a ion o mush-
ooms is becoming popula in p og ams aimed a imp o -
ing he li elihoods o smallholde a me s and o
inco po a ion in o p ojec s looking o di e si y he ag i-
cul u al ou pu o a uni o land. Howe e , g owing
mush ooms ou doo s is no wi hou challenges and equi es
ca e ul species selec ion and aining o p ac i ione s
be o e any such p og ams can commence.
26. Mode n mush oom p oduc ion:
an au oma ed ac o y p ocess
Limi ed ha es s du ing unp oduc i e seasons and he isk
o mush oom poisoning p e en wild mush ooms om
en e ing he ood ma ke alue chain in a majo way.
Domes ica ion and indus y p oduc ion has he e o e
Fig. 27 S opha ia
ugosoannula a eme ging om
soil subs a e mix and ma u e
c op shown. Shade clo h is
pulled back o e eal ha es
50 Fungal Di e si y (2019) 97:1–136
123
become essen ial o inco po a ing mush ooms in o die a y
di e si y and nu i ional secu i y. The global p oduc ion
has inc eased om 30.2 million ons in 2010 o 48 million
in 2017 (FAO). As a leading p oduce , China inc eased
om 22.6 million ons in 2010 o 38.4 million in 2017,
accoun ing o 75% o global p oduc ion (CIRI 2017). O
he 16,000 known mush oom species (Hawkswo h 2012),
abou 7000 species ha e a ying deg ees o edibili y, mo e
han 3000 species a e majo edible mush ooms, and 700 a e
ega ded as sa e medicinal mush ooms (Chang and Wasse
2017).
Global demand o mush ooms has apidly inc eased
and hus la ge-scale g owe s ha e been es ablished, wi h
yea - ound ma ke ing domina ing comme cial mush oom
p oduc ion. In China, he e a e six g oups o mush ooms
each wi h a p oduc ion capaci y o o e one million ons
pe yea (Zhang e al. 2015): 8.2 million ons o Au icu-
la ia species; 7.7 million ons o Len inula edodes (Shi-
i ake mush oom); 5.9 million ons o Pleu o us species;
3.4 million ons o Aga icus bispo us; 2.6 million ons o
Flammulina spp.; and 1.4 million ons o Pleu o us
e yngii. The g ow h o he comme cial mush oom indus y
depends on p oduc i i y, e iciency, and compe i i eness
wi hin he en i e ma ke alue chain. Mos o he mo e
ecen ly domes ica ed species can ecycle was e subs a es
Fig. 28 Di e en mush oom species cul i a ed wo ldwide. a,bHy-
menopellis sp., c,ePleu o us sp. (Oys e mush ooms), Ganode ma
sp. (Lingzhi). Pho o c edi : T. Luangha n
Fig. 29 Equipmen o manu ac u e s o mush oom cul i a ion. aSubs a e media mixe , bmush oom bag illing machine, c anspo e and
con eyo s ca y ou subs a e bags, ds eam s e iliza ion machine, einocula ion, au o- anspo a ion, gincuba ion. Pho o c edi : F. Huang
Fungal Di e si y (2019) 97:1–136 51
123
and he e o e sui smallholde s in ag oecosys ems (Dai
e al. 2010b) (Fig. 28).
In he las decade, he e ha e been ema kable ad ances
in mush oom g owing echnology. No only ha e s ains
been imp o ed, bu he whole mush oom p oduc ion p o-
cess has changed om manual o au oma ed sys ems. The
mixing o subs a es, illing o bags, g owing o liquid
spawn, inocula ion o bags, mo ing o bags, empe a u e
and humidi y con ol, and packing a e all au oma ed p o-
cesses (Fig. 29).
Reliable subs a e sou ces and machine y a e wo o he
ac o s ha de e mine he scale o ope a ion and p oduc-
i i y. Subs a es can be ha es ed om nea by o es s
h ough sus ainable o es managemen , om ecycled
ag icul u al esidue, suga cane ac o ies, li es ock eed and
was e, and he mulbe y indus y (Fig. 29) (Zhou e al.
2012). Al hough mush ooms can be cul i a ed using di -
e en me hods, such as sawdus bags, bo les, shel es, and
logs (see p eceding chap e s) he e is an inc easing demand
o he es ablishmen o mode n mush oom acili ies,
which p o ides a ange o 1*10 million bags annually
wi h well-equipped enclosed cooling and s e ilized build-
ings. This enables p ope g owing condi ions o be main-
ained. The mos sui able condi ions o mush oom
p oduc ion mus be es ablish and a e empe a u e, humid-
i y, uni o m en ila ion, subs a e mois u e le els and o
ligh o p omo e he o ma ion o ui bodies. Fo example,
blue ligh -emi ing diodes impac he quali y o Len inus
sajo -caju (Huang e al. 2017a). Howe e , main aining and
unning such g owing houses equi es high olumes o
elec ici y and wa e , making he p oduc ion p ocess cos ly
and ha ing a la ge impac on he elease o g eenhouse
gases. Fu u e ends should ocus on he use o enewable
ene gy sou ces.
The de elopmen o new echnologies, such as pho o-
ol aics o hea ing and cooling, a i icial in elligen and
echnology o con olling he en i onmen o op imize
empe a u es and mois u e and e en ligh o mula by LED,
will maximize he p oduc ion season, enhance he p o-
duc i i y and quali y o mush ooms, and educe ene gy
cos s (Fig. 30). A i icial in elligence o au oma ion
includes subs a e bag illing, inocula ion, cul i a ion,
scanning and picking up con amina ed bags, and obo s o
packing and anspo a ion. Bo h small- and la ge-scale
p oduc ion lines should emb ace in eg a ed sys ems, o
example inco po a ing he use o ecycled ma e ials, such
as ag icul u al was e, o making use o a sus ainable supply
Fig. 30 Mush oom indus y zone wi h con olled en i onmen o u al employmen and u al de elopmen
52 Fungal Di e si y (2019) 97:1–136
123
o woody subs a es om managed plan a ions, coupled
wi h he in eg a ion o enewable ene gies.
Edible mush ooms ha e been cul i a ed o many cen-
u ies, and i is expec ed ha hei p oduc ion will inc ease
u he due o ma ke demand. The imp o emen and
de elopmen o mode n echnologies, such as compu e -
ized con ol sys ems o con ol en i onmen al pa ame e s,
au oma ed ha es ing, echniques o he p oduc ion o
mush ooms in a non-compos ed subs a e, and new me h-
ods o subs a e s e iliza ion and spawn p epa a ion, will
inc ease he p oduc i i y o mush ooms (Sa
´nchez 2004).
Howe e , he mode n au oma ed ac o y p ocesses o
mush oom p oduc ion equi e a signi ican ini ial in es -
men o ixed asse s. Typically, his la ge capi al ou lay o
ixed asse s equi es a eco e y pe iod o a leas 5 yea s
(Li and Hu 2014). I is un easonable o a me s in low-
and middle-income coun ies o own au oma ed equipmen ,
since he up on capi al in es men equi ed o hese
i ems is economically unsus ainable, e en in he long e m
(Higgins e al. 2017). A mo e iable, long- e m solu ion is
he g an ing o unds o a me s ia ei he public o p i-
a ely unded o ganiza ions (Zied and Pa do-Gime
´nez
2017).
27. New edible mush ooms
Due o hei culina y, nu i ional, and heal h bene i s, he
global ma ke o mush ooms con inues o g ow, om US
$34.1 billion in 2015 o US$69.3 billion by he end o 2024
(Val e de e al. 2015; Bal 2018). Mush ooms also show
po en ial o use in was e managemen , as discussed else-
whe e. Howe e , mush ooms ha e li e cycles e y di e -
en om hose o g een plan s. The choice o mush oom
species o cul i a ion depends bo h on he g ow h media
a ailable and on ma ke conside a ions (Bee z and G ee
1999; Rosmiza e al. 2016;Sa
´nchez 2004). Oys e mush-
ooms, which g ow on many subs a es, a e easies (Pa il
e al. 1989). Shii ake mush ooms ha e al eady ga ne ed
conside able consume demand (Teng 2008). To da e, only
wo myco hizal mush ooms, mo els (Mo chella spp.) and
u les (Tube spp.), ha e been comme cially cul i a ed
(Selosse e al. 2017).
Se e al new species o wild edible mush ooms ha e
been success ully domes ica ed o e he las ew yea s,
especially in opical a eas (Klomklung e al. 2012;
Thongklang e al. 2014a,b,2016; Rizal e al. 2016; Ban-
da a e al. 2017) (Fig. 31A). Luangha n e al. (2017),
Thongbai e al. (2017) and Klomklung e al. (2012) ha e
shown ha i is possible o domes ica e local s ains o
Pleu o us gigan eus ha can g ow a empe a u es
Fig. 31 AAu icula ia hailandica;BHyb id om Thai and F ench
s ains o Aga icus sub u escens;CWhi e Au icula ia co nea;
DLepis a so dida;EAga icus locculosipes;FAga icus sub ilipes;
GF ui ing bodies o Mac olepio a dolichaula s ain MFLUCC-13-
0579. adi e en s ages o ui ing body de elopmen , bpileus wi h
annulus, csquamules on pileus, dand ebud s ages o ui ing bodies;
ma u e ui ing bodies. a =25 cm, b =10 cm, c, d, e, =5cm
Fungal Di e si y (2019) 97:1–136 53
123

consis en wi h Thai a m p oduc ion. A new hyb id
de eloped om Thai and F ench s ains o Aga icus sub-
u escens was de eloped success ully be ween INRA,
F ance and Mae Fah Luang Uni e si y, which uc i ies in
opical clima es (Thongklang e al. 2014b, Fig. 31B). Fo
he i s ime, a new whi e s ain o Au icula ia co nea was
success ully domes ica ed a he Kunming Ins i u e o
Bo any, Chinese Academy o Sciences (Fig. 31C). In
Thailand, s ains o Au icula ia hailandica (Fig. 35),
Lepis a so dida (Fig. 31D), Aga icus locculosipes
(Fig. 31E), A. sub ilipes (Fig. 31F) and Mac olepio a
dolichaula (Fig. 31G) ha e success ully been cul i a ed.
Mush ooms a e no only used in adi ional medicines, bu
a e known o con ain a ious bioac i e componen s which
can be used in cosme ics (Kwon and Tha i ha goon 2004;
Hyde e al. 2010) and in medicine (De Sil a 2013; Wisi-
assameewong e al. 2012b). People in mos pa s o he
wo ld enjoy ea ing mush ooms, and he e o e he e is
eno mous po en ial o in oducing new opical mush-
ooms o he global ma ke .
The numbe o ungi wo ldwide is es ima ed o be
be ween 2.2 o 3.8 million, bu only 120,000 species ha e
been desc ibed, so i appea s ha abou 92% o ungi ha e ye
o be desc ibed (Hawkswo h and Lu
¨cking 2017). O e he
pas 5 yea s, nume ous new ungi ha e been desc ibed,
especially wi hin opical a eas (A iyawansa e al. 2015; Liu
e al. 2015; Li e al. 2016; Hyde e al. 2016; Tibp omma e al.
2017,2018; Hyde e al. 2017; Wanasinghe e al. 2018). One
ecen pape published by Hyde e al. (2018a,b,c) showed
ha up o 96% o ungi in no he n Thailand may be new o
science. On he o he hand, he S a e o he Wo ld’s Fungi
epo 2018 (Willis 2018) s a es ha abou 350 species o
edible ungi a e collec ed and ea en wo ldwide annually, bu
his igu e should be highe . To add ess his knowledge gap,
he Cen e o Excellence in Fungal Resea ch in Mae Fah
Luang Uni e si y and he Soil Biology g oup o he Kunming
Ins i u e o Bo any a e wo king on upda ing he global lis o
edible and medicinal ungi. The e a e many easons o being
op imis ic abou he u u e o wild edible ungi: hey help
main ain he heal h o o es s and a e a aluable sou ce o
nu i ion and income.
28. Aga icus sub u escens
Aga icus sub u escens is an impo an medicinal mush-
oom (Wisi assameewong e al. 2012a; De Sil a e al.
2013), which belongs o sec ion A enses (subgenus
Fla oaga icus)o Aga icus. The main synonyms o A.
sub u escens a e A. blazei sensu Heinemann (misapplied),
A. b asiliensis (illegi ima e), and A. u o egulis. This spe-
cies has a b oad clima ic and geog aphical dis ibu ion
ange in Asia, Eu ope, Oceania and A ica (Thongklang
e al. 2016). Aga icus sub u escens was disco e ed in
Ame ica in he la e nine een h cen u y and la e in Sao
Paolo, B azil; i was called Piedade mush oom. One
mush oom (named A.blazei Mu ill) was in oduced in
Asia in 1965 by T. Fu omo o, who sen i o Japan o
medicinal in es iga ion bu u ned ou o be conspeci ic
wi h A. sub u escens (Ke igan 2005). The common name
o A.sub u escens is he almond mush oom. In addi ion,
o he common names a e Himema su ake in Japan, Cogu-
melo do Sol in B azil, and Royal Sun Aga icus in se e al
o he coun ies (Wisi assameewong e al. 2012a,b). The
main cha ac e s o A. sub u escens a e a eddish-b own cap
co e ed wi h silk-like ib es, a wo-laye ed and loccose
annulus, he odou o almond, yellow s aining, and a pos-
i i e Scha
¨ e ’s eac ion (Thongklang e al. 2014b).
Aga icus sub u escens has been comme cially cul i a ed
in B azil, Japan, China, Ko ea and Taiwan (Ke igan 2005;
G ego i e al. 2008). In B azil, he mush oom is a pa ic-
ula ly impo an expo mush oom wi h a highe p ice han
o he comme cial mush ooms (Souza Dias e al. 2004).
Bu on mush oom compos is no mally used o cul i a e
A.sub u escens comme cial s ains. O he o ms o ag i-
cul u al was e a e also used as al e na i e subs a es o
g ow his mush oom. Gonza
´lez Ma u e e al. (2011) p o-
duced A.sub u escens based on spen oys e mush oom
subs a e mixed wi h sun lowe seed hulls, e micompos
and supplemen s. Wild s ains o A. sub u escens ha e been
s udied o cul i a ion. Zied e al. (2011) epo ed he
success o whea s aw wi h chicken manu e and black
pea ?soil (4:1) as casing o cul i a e a B azilian/F ench
A.sub u escens s ain and hei hyb ids. Thongklang e al.
(2014b) isola ed a wild Thai A.sub u escens s ain and
success ully cul i a ed i in whea s aw/ho se manu e
based compos a 25 °C and 95% humidi y (Fig. 26a).
Thongklang e al. (2014b) epo ed ha samples om
B azil, F ance and Thailand a e in e e ile. Hyb id s ains
o Thai 9B azilian and Thai 9F ench showed highe
yields han Thai pa en al s ains.
The mush oom is bo h nu i ious and medicinal. Zied e al.
(2017) e alua ed he chemical composi ion o A. sub-
u escens, and epo ed ha he s ipe o he mush oom con-
ained 69.56% o o al ca bohyd a es, 63.89% o a ailable
ca bohyd a es, and an ene gy alue o 363.97 kcal 100 g
−1
DM). The pilei comp ised 33.96% p o ein, 7.75% ni ogen,
8.24 and 2.44% ash and c ude a . Medicinal bene i s ha e
also been epo ed o his mush oom, o example in cance
ca e, as an i umo agen s, and in choles e ol educ ion
(Wisi assameewong e al. 2012a,b; De Sil a e al. 2013;
S adle and Ho meis e 2015). Aga icus sub u escens p o-
duces se e al bioac i e compounds, such as lec in, iboglu-
can, glucomannan, aga i ine and blazien, all o which we e
shown o educe umo g ow h. In addi ion, spi o i e -
penoids o he blazeispi ol ype a e p oduced in mycelial
cul u es o his mush oom (Hi o ani e al.
54 Fungal Di e si y (2019) 97:1–136
123
1999,2000,2001,2002). Ex ac s we e ound o be highly
selec i e an agonis s o Li e X ecep o s (LXR) alpha
(G o he e al. 2011). Thongklang e al. (2017) epo ed ha
Thai–B azilian and Thai–F ench hyb id s ains p oduce
highe yields o blazeispi ol A in cul u e han hei Thai
pa en al s ain. Howe e , blazeispi ols ha e ne e been
ound in he basidiomes o A. sub u escens (Thongklang
e al. 2017). This is impo an , as i s ains could be ound
wi h blazeispi ols in he basidiomes, hen ea ing he mush-
oom would ha e impo an medicinal bene i s.
Mush ooms ha e been used as ood and heal h p oduc s
o millions yea s o hei pe cei ed medicinal p ope ies.
Aga icus sub u escens is widely cul i a ed in B azil (Souza
Dias e al. 2004; Mendonc¸a e al. 2005), and he mush oom is
expo ed om B azil o a ious coun ies such as Aus alia,
Boli ia, Ge many, Ko ea, India, Japan, Sou h A ica, Thai-
land, and he USA (Mendonc¸a e al. 2005). The mush oom
no mally equi es compos o cul i a ion (Thaw hong e al.
2014). Aga icus sub u escens is consumed wo ldwide in
esh, d ied and powde o m om mycelium/ ui ing bod-
ies. F esh mush ooms ha e been consumed as ood because
o hei po en ial medicinal p ope y and pleasan almond
la ou . Mo eo e , d ied o powde ed mycelium/ ui ing
bodies a e used as nu ien supplemen s. In Japan, 100,000–
300,000 kg o d ied almond mush ooms is p oduced e e y
yea (Takaku e al. 2001).
The mush ooms ha e been used as complemen a y and
al e na i e medicine o cance ca e. P i a e companies
such as King Aga icus 100, Sen-Sei-Ro Gold, and ABMK
sell p oduc s om A. sub u escens, and hese p oduc s a e
cu en ly being used by a ound 500,000 people o cance
ea men and p ophylaxis (Hyodo e al. 2005).
29. Using ungi o enhance ood alue
Fo housands o yea s, human socie ies ha e been u ilizing
ungi as ood sou ces (Chang 1980; Moon and Lo 2014;
Siddiq e al. 2018). In pa icula , edible mush ooms a e
ideal o ege a ians, because hey a e excellen sou ces o
p o ein ( ypically 20–30% c ude p o eins as a pe cen age o
d y ma e ), ha e a low- a con en , a e ee o choles e ol,
and con ain mos o he amino acids essen ial o human and
animal nu i ion (Kau e al. 2018). Fungal axa a e u ilized
in he ood indus y aking ad an age o hei me abolism
and me aboli es (Gilbe and Robinson 1957; Moo e and
Chiu 2001; Ad io and Demain 2003; Gho ai e al. 2009). In
pa icula , ungal species a e used in he p oduc ion o
e men ed oods and be e ages in many adi ional and
indigenous cul u es a ound he wo ld (Abe e al. 2008;
Dupon e al. 2016). Fo ins ance, he yeas Saccha omyces
ce e isae is he oldes and bes known ungal species used
o wine and b ead making, in d ug p oduc ion, as bio-
con ol agen s, in enzyme bio echnology, as well as o
esea ch and de elopmen (Gho ai e al. 2009; Sha ma
e al. 2018). A b ie desc ip ion o some o he mos
impo an e men ed ood indus ies is p o ided below.
Mold- ipened cheese
Cheese is a solid o semi-solid p o ein ood p oduc man-
u ac u ed om milk. Fungal species a e impo an o he
manu ac u e and ipening o wo ypes o cheese, he
Camembe and Blue- eined a ie ies (Fox e al. 2017).
The name “blue- eined cheese” de i es om he blue–
g een mold g owing h oughou he p oduc (Ma ı
´n and
Co on 2016). The e a e a ious kinds o blue- eined cheese
p oduc s, iz. Roque o , Go gonzola, S il on, Danish Blue,
and Blue Cheshi e. Mos Blue cheese is p oduced om
unpas eu ized milk, and Penicillium oque o i is added o
he cheese p io o s o age a con olled empe a u e and
humidi y. Penicillium oque o i g ows h oughou he
cheese and p oduces p o eoly ic and lipoly ic enzymes ( iz.
p o eases, lipase and be a-ke oacid deca boxylase) and
me hyl ke ones, pa icula ly 2-hep anone, as he majo
la ou and odou compounds (Kinsella e al. 1976; Dupon
e al. 2016; Ropa s e al. 2017). Penicillium oque o i
g ows a a low oxygen ension and low pH alues, while
ha ing he abili y o use bo h pen oses and hexoses as
subs a e. These cha ac e is ics make he ungus ideally
sui ed o he indus ial Roque o - ype cheese p oduc ion
(Babel 1953; Kinsella e al. 1976, Ga cı
´a-Es ada and
Ma ı
´n2016). Camembe cheese is a he di e en om
blue- eined cheese, as i cha ac e ized by a whi e mold
g ow h on he su ace and a so ex u e. Penicillium can-
didum and P.camembe i a e used o he camembe
cheese p oduc ion (Bou dichon e al. 2012).
Fe men ed p oduc s
Soy sauce (Shoyu) and Miso
Soy sauce is one o wo ld’s oldes la o ing edien s;
made om e men ed soybeans/whea . I is a da k b own
liquid ha is s able a ambien empe a u e and does no
equi e e ige a ion du ing s o age due o i s low wa e
ac i i y and high sal con en . Soy sauce has been used in
cooking o o e 1000 yea s, in pa icula in China, Japan,
Ko ea and o he Asian coun ies (Luh 1995; Hong e al.
2015; Liu 2017). The soy sauce p oduc ion p ocess com-
p ises h ee majo s eps, which a e Koji p oduc ion, b ine
e men a ion and e ining. In he i s s ep, soaked, cooked,
mashed soy beans a e mixed wi h an equal amoun o
oas ed, ligh ly c ushed whea , and inocula ed wi h 0.1–
0.2% s a e mold (Aspe gillus o yzae o A.sojae)in
wooden ays. The e men ed mix u e (Koji) hen unde -
goes b ine e men a ion using he lac ic acid bac e ium,
Pediococcus halophiIus, and yeas s including Zygosac-
cha omyces ouxii and Candida species (Liu 2017). The
inal s ep o soy sauce e men a ion ( e ining), includes
p essing, il a ion, pas eu iza ion and packaging. The
Fungal Di e si y (2019) 97:1–136 55
123
e men ed soybean pas e is called miso, has a simila
a oma and la o o soy sauce.
Indonesian empeh
Tempeh is a mould- e men ed p oduc p epa ed om
e men ed soy beans and is consumed mos ly in Indonesia
(Babu e al. 2009). Tempeh possesses some unique cha -
ac e is ics, including i s la o , sliceable mea -like ex u e,
and nu i ional p ope ies (As u i e al. 2000; Nou and
Kie s 2005). Rhizopus oligospo us is he dominan ungal
species used in he soy bean e men a ion p ocess. Ini ially,
husk- ee, soaked and p essed soybeans a e inocula ed wi h
R. oligospo us and e men ed o 1–2 days. Du ing he
e men a ion p ocess, he whi e mycelia o R. oligospo us
in ade and co e he subs a e mass o bind he soy bean
(Shu le and Aoyagi 1979; S eink aus 1995; Nou and
Kie s 2005; Babu e al. 2009; Shah and Pa el 2017).
Tempeh p o ides many heal h bene i s, in pa icula o
hea diseases, s okes, os eopo osis, cance and diges i e
diso de s, loss o excess weigh ), as i con ains essen ial
a y acids, nume ous i amins, ibe and mine als.
Quo n
Quo n is made om myco-p o eins, which a e p oduced by
a e men a ion p ocess using he ilamen ous ungus
Fusa ium enena um (Finnigan e al. 2017; Kozubal e al.
2019). Quo n mycop o ein s ains we e p e iously
misiden i ied as Fusa ium g aminea um, bu we e la e
ound o ep esen F. enena um (Wheelock 1993; T inci
1994; Wiebe 2004; Finnigan e al. 2017). Wi h a low a
con en and being ee o choles e ol, quo n p o ides an
al e na i e p o ein op ion ha is mea - ee and nu i ious
(Ga odia e al. 2017). In addi ion, i is high in die a y ib e,
which has been ound o lowe blood choles e ol (Denny
e al. 2008; Rux on and McMillan 2010; Ga odia e al.
2017; Kozubal e al. 2019). The p oduc ion p ocess o
Quo n is simila o ha o bee , equi ing less whea and
wa e o p oduc ion, as well as esul ing in lowe ca bon
emissions, compa ed wi h mea sou ced p o eins (Finnigan
2011). Du ing he p oduc ion p ocess, mycop o ein is
mixed wi h ege able la o ings and a small amoun o egg
albumen. To ob ain i s cha ac e is ic ex u e, a se ies o
s eaming, chilling and eezing p ocesses a e used o ob ain
he mea -like ex u e o Quo n p oduc s (Wiebe 2004;
Finnigan 2011). Ini ially, Quo n p oduc s o igina ed in he
UK, bu cu en ly a e a ailable wo ldwide (Apos olidis and
McLeay 2016).
Renne
Renne is used by ood companies o he milk clo ing
p ocess wi hin cheese p oduc ion (Ogel 2018). Cal enne
was adi ionally used o cheese-making wo ldwide
(Thaku e al. 1990; Mamo and Balasub amanian 2018).
Subsequen ly, he global inc ease in cheese p oduc ion,
along wi h a dec ease in animal enne p oduc ion, aised
he p ice o adi ional enne . The e o e, ood esea che s
ied o ind al e na i es o he milk clo ing p ocess wi hin
cheese p oduc ion (Moschopoulou 2017; Ogel 2018). As a
consequence, mic obial enne was p oduced using Rhi-
zomuco miehei and R. pusilus (Thaku e al. 1990; Sil ei a
e al. 2005; De Lima e al. 2008). Mic obial enne is
cheape han he enne p oduced by animals, and he bes
op ion o ege a ians.
O he han hose e men ed ood p oduc s, he e a e
many comme cial ood indus ies in he wo ld. Some ood
p oduc s which use ungal species a e lis ed in Table 13.
30. Food colou ing om ilamen ous ungi
Syn he ic colo an s a e widely used in ood p oduc ion o
enhance he appea ance o ood colo s. Al hough syn he ic
colo an s a e s able and inexpensi e, he demand o hese
p oduc s has dec eased due o hei po en ial o pe cei ed
ha m ul e ec s on human heal h (Ba eman e al. 2004).
Today, many syn he ic colo an s ha e been eplaced wi h
sa e na u al colo an s. Pigmen s om plan s a e o en used
as ood colo an s (Shamina e al. 2007; Amba i e al. 2014;
Leong e al. 2018; Upadhyay 2018). Al hough hese pig-
men s can gene a e a ious colo s, p oduc ion p ocesses
a e limi ed due o plan g ow h needs. Filamen ous ungi
can be g own in e men e s, and a e also being in es iga ed
as impo an sou ces o pigmen s (Table 14, Fig. 32). Some
examples a e gi en below.
Red mold ice, also known as ed yeas ice, is an Asian
adi ional e men a ion p oduc o s eamed ice e men ed
wi h ilamen ous ungi belonging o he genus Monascus
(Fig. 33). Red mold ice has been widely used in Eas
Asian coun ies wi h a e y long his o y as bo h ood
colo ing and medicine. The ed colou om ed mold ice
is used in a a ie y o Chinese, Ko ean and Japanese oods,
such as e men ed bean cu d, p ese ed d y ish, po k s ew,
oas duck, and oas po k (Chen e al. 2015). Red mold
ice is also used as subs a e o he p oduc ion o “Hong
Qu glu inous ice wine,” which gi es i a b igh - ed colou
and ine swee la o (Liu e al. 2018b; Pa k e al. 2016).
A e he op imiza ion o bio echnological p oduc ion
p ocesses, some species can easily p oduce pigmen s a a
la ge scale in bio eac o s, elying on ela i ely sho e -
men a ion imes, and esul ing in accep able cos s-o -
goods. Fo example, he op imiza ion o ed pigmen p o-
duc ion in a subme ged cul u e by Monascus ube in
complex cul u e media esul ed in he de elopmen o a
medium con aining 10 g/l glucose, 5 g/l co n s eep liquo
and 7.6 g/l monosodium glu ama e, gene a ing he highes
amoun o ed pigmen a 20.7 U (Hamano and Kilikian
2006).
56 Fungal Di e si y (2019) 97:1–136
123
Red mold ice also gene a es o ange pigmen . Pigmen
p oduc ion is pa ially associa ed wi h cell g ow h and a
dissol ed oxygen concen a ion o be ween 0.894 and
1.388 mg O
2
/l a 30 °C. Limi ing condi ions o dissol ed
oxygen dec eases he p oduc ion o o ange pigmen s
(Vend uscolo e al. 2017). An induced mu a ion o M.
pu pu eus led o p oduc ion o yellow pigmen s, which can
be added o Chinese esh noodles, p o iding a yellow
shade wi h no discolo a ion (Yongsmi h e al. 2013).
Klinsupa e al. (2016) in es iga ed using in aspeci ic
p o oplas s o a yellow mu an o Monascus spp. wi h a
whi e p o o oph, and a s ain wi h high yellow pigmen
p oduc ion was p oduced. Ano he mu an s ain o M.
ube 10910, gene a ed h ough UV mu agenesis,
imp o ed he p oduc ion o ex acellula hyd ophilic yel-
low pigmen en old (Wu e al. 2015b).
Un o una ely, he myco oxin ci inin is o en ound in
ed mold ice, and has a nega i e impac on heal h. This
myco oxin has been in es iga ed as neph o oxic and hep-
a o oxic o human cells (Bilg ami e al. 1988). The egu-
la ion o ci inin concen a ion in comme cial ed mold ice
occu s in many coun ies, such as Commission Regula ion
(EU), Taiwan, US FAD, and Japan (Le Bloc’h e al. 2015;
Eu opean Commission 2014). The e o e, he p oduc ion o
ed mold ice wi h low ci inin is impo an o inc easing i s
alue and sa e y. Pengnoi e al. (2017) e alua ed he e ec s
o a ious pu ple ice a ie ies on he p oduc ion o ci inin
and ed pigmen s by M. pu pu eus CMU002U (UV-mu an
s ain). The lowes alue o ci inin concen a ion
(132 ppb) was ound in he Na a ie y, which passed he
s anda ds o Japan, Taiwan, and he Eu opean Union. The
highes ed pigmen yield was ob ained om he e men ed
Doi Muse a ie y. These esul s demons a e ha e -
men ed pu ple ice has a high po en ial o be de eloped as a
sa e ood colo an .
Table 13 Fungal species used in
he ood and be e age indus ies Applica ion P oduc Fungal species
Be e ages Bee , Rum, Wine Saccha omyces ce e isae
Sake Aspe gillus o yzae
Cheeses Roque o , Blue cheese Penicillium oque o i
Camembe , B ie, so ipened Penicillium camembe i
O ien al ood e men a ions Ang-kak Monascus pu pu eus
Doenjang Aspe gillus o yzae
Hamana o Aspe gillus o yzae
Miso Aspe gillus o yzae,A.sojae
On jom Neu ospo a in e media
Renne Rhizomuco miehei
Rhizomuco pusilus
Shoyu (soy sauce) Aspe gillus o yzae,A.sojae
Tempeh (Indonesian) Rhizopus oligospo us
Quo n Fusa ium enena um
Table 14 Examples o pigmen s p oduced by ilamen ous ungi
Colo Pigmen s Fungal p oduce s Re e ences
Blue Sanguinone A Mycena sanguinolen a Pe e s and Spi elle (2007)
G een Xylindein Chlo ocibo ia ae uginosa Saikawa e al. (2000)
O ange Monasco ub in
Rub opunc a in
Monascus sp. Vend uscolo e al. (2017)
β-Ca o ene Muco ci cinelloides Neu ospo a in e media To es e al. (2016)
Red Rub opunc amine
Monasco ub amine
Monascus sp. Hamano and Kilikian (2006), Dikshi and Tallap agada (2013)
Lycopene Blakeslea ispo a Feo ilo a e al. (2006)
Yellow Anka la in
Monascin
Monascus sp. Yongsmi h e al. (2013), Klinsupa e al. (2016)
Fungal Di e si y (2019) 97:1–136 57
123
essel. The liquids dis illed a e cooled in a condense and
o en be e-boiled o ensu e hei pu i y (Fo bes 1970;
Lembeck 1983; Bi ch and Lindley 1985; Thomas and
Shipman 2016). The aw ma e ials esul in a a ie y o
la ou s and a omas in he spi i s, bu he aging p ocesses
and pe iods a e also impo an (Ch is oph and Baue -
Ch is oph 2007; Rosso e al. 2009; Robe 2010). The
a ie y o spi i s is showed in Table 17; howe e , he e a e
many sub-ca ego ies wi hin each ype o spi i as well.
The b ewed alcoholic be e age indus y has g own
apidly o e ecen decades, and i is inc easingly p o-
ducing compe i i e p oduc s heigh ened by consume
equi emen s wo ldwide. C ea ing unique expe iences o
bee consume s is one o he mos impo an goals o
alcoholic be e age manu ac o ies. B ewe s ha e es ab-
lished nume ous new echniques and p ocesses o
imp o ing he la ou s, colou s, and nu ien s in wines,
bee s, and spi i s. Nume ous new ma e ials and p ocesses
in b ewing ha can a ec la ou s and a omas a e being
de eloped, and he e will likely be hund eds o di e en
kinds o alcoholic be e ages in he u u e. The de elop-
men o bio echnology and new disco e ies will be he
mos impo an ools o each he goals o u u e b ewing.
35. Func ional oods and nu aceu icals
The a e age age o he global popula ion is inc easing, and
socie y is becoming mo e awa e o he po en ial side
e ec s o p esc ip ion medicines, and he e o e a e seeking
al e na i e he apeu ics (Eko 2014; Rowe e al. 2016;
WHO 2004a,b,2015). Va ious new nu i ional concep s,
such as unc ional oods and nu aceu icals ha e been
de eloped o e ecen decades. By de ini ion, unc ional
oods a e con en ional o e e yday oods consumed as pa
o he no mal daily die , a ge ing he enhancemen o he
well-being and quali y o li e and hus educing he isk o
Fig. 36 Global ma ke sha e o bee consump ion in 2016 by egions
( ep duced wi h kind pe mission om Ki in Holdings Company,
Limi ed)
Table 16 The majo di e ences be ween ales and lage s
Bee s
ypes
B ewing
p ocess
Types o yeas
(Saccha omyces)
Fe men a ion
empe a u e
B ewing
imes
Colou Example
Ale Top- e men ing S. ce e isiae Wa m (15.5 o
25.5 °C)
7 days B own o da k Goose Island
Bou bon Coun y S ou
Samuel Smi h’s Taddy
Po e
Sie a Ne ada
Th ee Floyds Da k Lo d
Lage s Bo om-
e men ing
S. pas o ianus Cool (7.2 o 12.8 °C) Se e al
mon hs
Bligh gold o
yellow
Ca lsbe g
Co ona
Dunkel
Heineken
Ki in
Mille
Pilsne U quell
Schwa zbie
Singha
Tsing ao
64 Fungal Di e si y (2019) 97:1–136
123

disease (El Sohaimy 2012). The e m “nu aceu icals” is
de ined as ood cons i uen s ha p o ide medical o heal h
bene i s, including he p e en ion and ea men o disease
(Kal a 2003). Nu aceu icals can be ood in he o m o
ex ac s, single, pu e na u al compounds, o nu ien s ha
ha e been u ned in o a pha maceu ical o mula ion (e.g.
pills o able s), and hey can be applied as die a y sup-
plemen s o as pa o a speci ic die (Gia asis 2014;Reis
e al. 2017). The e o e, he ole o unc ional oods is
mainly ela ed o educing he isk o disease, while
nu aceu icals a e usually consumed o p omo e well-being
h ough he p e en ion o ea men o diseases and diso -
de s (Bagchi e al. 2014).
Fungi, and especially edible mush ooms, a e well
known o hei nu i ional alue and heal h-p omo ing
p ope ies. Mush ooms a e ideal die a y supplemen s
because hey a e ela i ely ich in p o eins, con ain almos
no a , and possess a a ie y o ibe s and i amins (Val-
e de e al. 2015). Many s udies ha e been conduc ed o
p o e he bene i s o unc ional oods and nu aceu icals
de i ed om ungi in a ious pa hological complica ions,
such as diabe es, a he oscle osis, ca dio ascula diseases,
cance , in ec ion, enal, and gas oin es inal and neu o-
logical diso de s (Banik e al. 2015).
Polysaccha ides such as be a-glucanes a e one o he
mos widely s udied and ecognized g oups o bioac i e
molecules de i ed om mush ooms. Fo ins ance, he
glucanes om Len inula edodes (shii ake, Fig. 37) we e
success ully used as a pa ial eplacemen o whea lou
in baked oods o p oduce a low calo ie, ibe - ich,
unc ional ood (Guillamo
´n e al. 2010). Among all
s udied mush ooms species, L. edodes is also known o
ha e an ibac e ial ac i i ies agains bo h G am-posi i e
and G am-nega i e bac e ia (Al es e al. 2012a,b). In
ano he s udy, he be a glucane len inan (65, Fig. 38)o L.
edodes was added o noodles as a pa ial whea lou
eplacemen , and i was claimed ha hei an i-oxidan
and hypocholes e olemic e ec s in i o would imp o e
he quali y o he noodles (Kalac
ˇ2013). Ex ac s om
Ganode ma glucans, on he o he hand, ha e been
epo ed o ac as ee adical sca enge s, he eby p e-
en ing lipid pe oxida ion, and o s imula e in e e on
syn hesis in human blood cells a e consump ion
(Koza ski e al. 2011).
In o he s udies, glucans om a ious edible mush ooms
including Aga icus bispo us,Au icula ia au icula-judae,
and he Asian “Flammulina elu ipes”(Enoki ake: cu en
name: F. ili o mis; c . Wang e al. 2018a), we e shown o
possess no able an ioxidan capaci ies and ee adical
sca enging po en ial in i o, and hence we e p oposed as
na u al an ioxidan s in ood applica ions. O he snack oods
en iched wi h a powde om ex ac s o he Ches nu
Mush oom (Cyclocybe aege i a) as a pa ial s a ch
eplacemen exhibi ed a low glycemic esponse a e con-
sump ion, which was co ela ed o he die a y ibe con en
(B ennan e al. 2012). Aga icus sub u escens (synonyms:
A. blazei; A. b asiliensis) is ano he mush oom which has
been sugges ed as a sa e immunos imulan and o ame-
lio a ing obesi y o diabe es (Yamanaka e al. 2013).
Las ly, Japanese esea che s managed o p oduce a unc-
ional cheese-like ood con aining Schizophyllum com-
mune. The inal p oduc con ains a be a-glucan, which was
claimed o ha e a signi ican an i h ombo ic unc ion
(Okamu a-Ma sui e al. 2001).
The e m “mush oom nu aceu icals” was coined by
Chang and Buswell (1996) o desc ibe hose compounds
ha ha e conside able po en ial as die a y supplemen s and
a e used o he enhancemen o heal h and p e en ion o
Table 17 Di e ences o majo ypes o spi i s
Spi i s Raw ma e ials Mashing Fe men a ion Dis illing Aging Mos % ABV
B andy G apes and ui s e c. ✓✓ ✓(dis illed
wine)
In oak 40% (80 p oo )
Gin Vodka?junipe be ies ✓✓ ✓ 940–47% (80–94
p oo )
Liqueu Spi i s?suga ? la o ( ui , c eam,
he bs, spices, lowe s o nu s)
✓✓ ✓ 9/✓15–55%
Rum Suga cane o Molasses ✓✓ ✓ 9(ligh um)
✔in oak ba els (o he ums)
40% (80 p oo ), up o
75% (150 p oo )
Tequila Juices om blue Aga e plan ✓✓ ✓(dis illed
Aga e)
9(whi e/sil e equila)
✓in oak ba els (gold
equila-blended)
40–50% (80–100
p oo )
Vodka G ains, ye, co n, whea , po a oes e c. ✓✓ ✓ 940–50% (80–100
p oo )
Whisky G ains (co n, ye, whea , ba ley, e c.) ✓✓ ✓(dis illed
bee )
✓in cha ed oak, o used
whiskey o wine ba els
40–50% (80–100
p oo )
Summa ized om G aham (h ps://www. hesp uceea s.com/quick-guide- o-dis illed-spi i s-760713)
Fungal Di e si y (2019) 97:1–136 65
123
Fig. 37 Len inula edodes
(shii ake)
ONH
OH
N
NH N
O
OH
OH OH
OH
Ganode iol A (62), Ganode ma sp.
(Sa o e al. 1986)
Hispidin (63), Phellinus
lin eus (Shao e al. 2015)
OH
O
O
OH
OH O
O
OH
MeO
O
He icenone A (64), He icium e inaceus
(Thongbai e al. 2015)
O
OH
OH
OH
OH
O
OH
OH
OH
OO
OH
O
OH
O
OH
OH
H
OO
OH
O
OH
OH O
O
O
OH
OH
OH
OH
O
O
OH
OH
OH
OH
n
len inan (65), Len inula edodes
(Eaele e al.2015)
Didanosine (61), Sy he ic
compound (based on he
Co yceps spp compound)
(Alapi EM and Fische J 2006)
Fig. 38 Examples o
biologically ac i e compounds
om ungi used in unc ional
oods and nu aceu icals. 61:
Syn he ic compound inspi ed
om co dycepin (Alapi and
Fische 2006); 62: T i e penoid
om Ganode ma sp. (Sa o e al.
1986); 63: Main ac i e p inciple
o “Phellinus” (i.e.
T opicopo us)lin eus (Shao
e al. 2015); 64: Blazeispi ols
( i e penoid om cul u es o
Aga icus sub u escens
(Thongklang e al. 2017); 65:
Len inan, a be a-glucane om
Len inula edodes (Ina e al.
2013)
66 Fungal Di e si y (2019) 97:1–136
123
a ious human diseases (Tao iq e al. 2016). The impo an
edible mush ooms wi h ema kable nu aceu icals p ope -
ies include he species o Au icula ia,G i ola,He icium,
Lac a ius,Pisoli hus,Pleu o us and T emella. Some s ud-
ies sugges mush ooms as inhibi o s o myco oxin p o-
duc ion (Re e be i e al. 2005). The bioac i e glycop o ein
(SX- ac ion) ex ac ed om G i ola ondosa, o mai ake
mush ooms, ha e been in es iga ed in animal and clinical
ials. I is pa icula ly encou aging ha he glycemic
con ol o se e al diabe ic pa ien s unde o al medica ions
was signi ican ly imp o ed wi h a SX- ac ion egimen ha
may p ima ily a ge o ac on he insulin signal ansduc-
ion pa hway, o e coming insulin esis ance (IR and IRS-1)
(Konno e al. 2013). O he o mula ions exis on he ma -
ke , such as a new p oduc o demen ia, pa icula ly Alz-
heime ’s disease, based on a p op ie a y s anda dized
ex ac ha con ains he icenones (e.g. 64) and amyloban
(bo h om H. e inaceus) (Thongbai e al. 2015). The
popula culina y oys e mush oom Pleu o us os ea us and
o he species o his genus syn hesize bioac i e pleu an,
which is ano he po en ial candida e o he de elopmen o
nu aceu icals (Gia asis and Biliade is 2006; Zhang e al.
2001). Some examples o biologically ac i e compounds
om ungi used in unc ional oods and nu aceu icals a e
gi en in Fig. 38.
Today, i is e y easy o ind unc ional oods and
nu aceu icals de i ed om mush ooms in he ma ke .
Many o hese p oduc s can e en be pu chased ia he
In e ne . Howe e , i mus be kep in mind ha hese
s udies do o en no ely on s anda dized ma e ial and ha
he “heal h claims” de i ed om hem a e o en no sub-
s an ially jus i ied, e.g. because he s udies we e conduc ed
wi h oden s o e en only in i o (cell-based o enzyme
based assays), and we e ne e alida ed by ea men on
humans in a simila manne as he clinical ials ha a e
manda o y in de elopmen o e hical d ugs. Se ious dis-
eases should he e o e no be ea ed be sel -medica ion
and pa ien s should by all means seek ad ice om a
medical doc o . Among he a ious side e ec s epo ed o
pa ien s ha ha e used such p epa a ions om TCM
mush ooms as sel -medica ions, pancy openia (i.e. a
dec ease in he numbe o all blood cells) has ecen ly been
equen ly eco ded (Yoon e al. 2011; Jung e al. 2013).
E en hough he symp oms disappea ed a e he con-
sump ion o he mush oom p oduc s opped, hese cases
should gi e a wa ning o e e ybody who uses mush oom
nu aceu icals no o o e dose hem.
36. Ha es ing he un apped p obio ic po en ial
o ungi
Gas oin es inal diso de s and diseases cons i u e a majo
cause o mo bidi y and mo ali y wo ldwide (Kaplan 2015;
Ki k e al. 2015; Pee y e al. 2015). Diseases o he gas-
oin es inal ac may o may no be con agious. In he case
o non-communicable gas oin es inal ac diseases, he e
is no ansmissible o ganism in ol ed. These include
in lamma o y bowel disease, i i able bowel synd ome,
colon cance , C ohn’s disease and coli is. In he case o
communicable gas oin es inal ac diseases, he ae iolog-
ical agen is an in ec ious o ganism. Su e e s may exhibi
one o se e al o a b oad a ay o gas oin es inal ac
dis u bances and pe u ba ions, including la ulence,
abdominal pain, omi ing, nausea, gas oin es inal ac
bleeding, cons ipa ion, and dia hoea (Wadswo h e al.
2011).
Se e al gas oin es inal ac diso de s a e becoming
inc easingly di icul o ea due o ambiguous o e all
symp oma ology o inc eased esis ance o pa hogens o
adminis e ed pha maceu ical d ugs, mainly an ibio ics
(P es inaci e al. 2015). Gi en hese issues, he e is a
c i ical need o he apeu ics ha will complemen / eplace
exis ing s a egies. In ha ligh , p obio ics p esen an
a ac i e op ion. The Food and Ag icul u e O ganiza ion
o he Uni ed Na ions and he Wo ld Heal h O ganiza ion
along wi h he In e na ional Scien i ic Associa ion o
P obio ics and P ebio ics de ine p obio ics as “li e
mic oo ganisms, which when adminis e ed in adequa e
amoun s, con e a heal h bene i on he hos ” (FAO/WHO
2001; Hill e al. 2014).
P obio ics can be deli e ed as die a y supplemen s (e.g.
capsules, able s, and powde ) o ood ing edien s (e.g.
yogu s and ke i s) (Szajewska e al. 2016). The heal h
bene i s o p obio ics include s eng hening o he gu
mucosal ba ie ollowed by gu pa hogen coloniza ion
esis ance, eplenishing o bene icial gu mic obes a e
dia he ic episodes, and enhancing o e all heal h o he
diges i e ac (Hill e al. 2014). P obio ics ha e been used
o a limi ed ex en o he ea men /p e en ion o gas-
oen e i is, in lamma o y bowel disease, i i able bowel
synd ome, colo ec al cance , and coli is (B own and
Valie e 2004; Hill e al. 2014).
Mos p obio ics cu en ly in use a e limi ed o bac e ial
s ains wi h membe s o he gene a Bacillus, Bi idobac-
e ium, En e ococcus, Lac obacillus, P opionibac e ium
and S ep ococcus being he mos common (Ouwehand
e al. 2002; B own and Valie e 2004; Szajewska e al.
2016). A no able excep ion is he yeas Saccha omyces
boula dii, which was ini ially isola ed o comba chole a-
associa ed dia hoea, and is now being used o ea dia -
hoea o a ying ae iology (McFa land and Be nasconi
1993). The heal h bene i s o S. boula dii ha e been well-
documen ed in se e al andomized clinical ials
(Table 18). None heless, he p obio ic po en ial o a ious
o he ungal species is also well known. Fo ins ance,
membe s o he gene a Kluy e omyces and Ya owia a e
Fungal Di e si y (2019) 97:1–136 67
123
p omising candida es due o hei s ong ac i i y agains
bac e ial pa hogens and hei abili y o ole a e he inhos-
pi able en i onmen o he gu (Kumu a e al. 2004; Chen
e al. 2010). Howe e , his a enue o esea ch emains
la gely unexplo ed (Huseyin e al. 2017).
A la gely un apped sou ce o po en ial ungal p obio ics
is he human gu mycobiome, he collec ion o ungi
esiding in he gu . Membe s o he gene a Candida and
Saccha omyces a e consis en ly p e alen ac oss s udies,
bu Cladospo ium, Malassezia and Penicillium seem o be
also abundan depending on he popula ion unde s udy
(Ho mann e al. 2013; Rod iguez e al. 2015; Nash e al.
2017). Fu u e esea ch should ocus on iden i ying and
p ecisely cha ac e izing app op ia e ungal p obio ic
s ains. Ou comes o each p obio ic ungal s ain should be
de e mined explici ly and op imal doses de ined acco ding
o age g oup and disease s a e. Resea ch e o s should also
expand o examine he use o ungal p obio ics in he
aquacul u e and animal husband y indus ies.
Sa ing he plane
Was e is a common and majo global p oblem. An h o-
pogenic ac i i ies esul in he gene a ion o millions o
ons o plas ic was e each yea . Ex ensi e ag icul u al
p ac ices ha e also con ibu ed o he gene a ion o eno -
mous quan i ies o was e, which a e being disposed o in
non-cos -e ec i e and en i onmen ally un iendly ways.
The e a e a ious ways in which ungi can help dec ease
was e and educe pollu ion. The e is he e o e an u gen
need o ap in o he powe o ungal o ganisms and de ise
sma s a egies ega ding how hey can educe he nega-
i e e ec s ha pollu an s ha e on he en i onmen . The
sec ion below ou lines how ungi con ibu e o he heal h o
ou plane and ha e he abili y o cu b a numbe o en i-
onmen al p oblems, mos no ably pollu ion. Examples a e
gi en as o how ag icul u al was e (which was p e iously
disposed o o bu n , esul ing in ai pollu ion) can be
con e ed in o use ul subs a es on which o g ow edible
mush ooms a an indus ial scale. Mycologis s ha e also
conduc ed esea ch on esilien ungal mic oo ganisms and
explo ed hei abili y o deg ade plas ics, ex ile e luen s,
and hyd oca bons, all o which a e pollu ing ou en i on-
men a an ala ming a e.
37. Ag icul u al was e disposal
Ag icul u al was e, he esidue om plan ing un il ha es ,
gene ally con ains a mix u e o plan was e, animal/insec
was e, and oxic esidues om he chemicals used as pes-
icides, insec icides, and he bicides. Asia is one o he
wo ld’s mos ag icul u e-in ensi e a eas: om 2010 o
2016, 46.9% o emissions in Asia came om c op esidue,
compa ed o 28.2% and 16.2% om Ame ica and Eu ope,
espec i ely. Acco ding o he FAOSTAT
2
emissions
da abase, 90.6% o ice p oduced wi hin Asia gene a ed
mo e han a hund ed million ons o esidual ma e ial. This
ag icul u al was e accoun ed o o e 50% o he ni ous
oxide gene a ed om he decomposi ion o c op esidue on
cul i a ed soils, one o he main con ibu o s o he
g eenhouse gas e ec and a cause o global wa ming. In
he Sac amen o Valley o Cali o nia, ice and whea s aw
a e also majo con ibu o s o gene a ed ag icul u al was e,
wi h 1.5 ons o ice s aw was e p oduced annually (Zhang
e al. 2002). In Thailand, he main c ops a e suga cane,
ce eal, ice, cassa a and oil palm, and hese con ibu e 80%
o he o al solid was e gene a ed om c op cul i a ion.
A numbe o p ocesses ha e been de eloped o p o-
posed o ag icul u al was e managemen (such as com-
pos ing, which is a sus ainable p ocess), while he common
p ac ice o bu ning he ice s aw, husk, s alks, co n cobs,
s ubble and g asses is conside ed a cheap and easy means
o he disposal o excess esidues (Obi e al. 2016; Walia
e al. 1999). Un o una ely, bu ning ag icul u al was e
gene a es many poisonous and ha m ul oxides and hyd o-
ca bona es in o he a mosphe e (Shaban and Omaima
Table 18 Fungal p obio ics and hei heal h bene i s
Fungi Heal h bene i s Re e ences
Saccha omyces
boula dii
Conside able educ ion o du a ion o dia hoea-RCT Szajewska e al. (2016) and e e ences
he ein
Risk educ ion o an ibio ic-associa ed dia hoea-RCT
Risk educ ion o dia hoea associa ed wi h Clos idium di icile in
child en-RCT
Reduc ion o dia hoea associa ed wi h Helicobac e pylo i in ec ion-
RCT
Amelio a ion o abdominal pain in IBS su e e s-RCT
Saccha omyces
ce e isiae
Abso p ion o myco oxins Moslehi-Jenabian e al. (2010)
RCT andomized clinical ials
2
h p://www. ao.o g/ aos a /en/?#da a/GA.
68 Fungal Di e si y (2019) 97:1–136
123
2010), which in u n inc eases ai pollu ion and causes
espi a o y p oblems, which hen impac he economy
h ough highe medical cos s and employee absences.
The e o e, he e is an inc easing demand o sus ainable
p ocesses ha u ilize ag icul u al was e in mo e eco-
iendly ways.
Biological p ocesses a e conside ed bo h na u al and
sus ainable, and a e also impo an in ca bon ecycling.
Fungi a e some o he mos e ec i e decompose s in an
ecosys em and a e ex emely e icien in he deg ada ion o
plan -based ag icul u al was e such as ice s aw, whea
s aw, maize s o es and suga cane esidue (Dinis e al.
2009). Mush oom cul i a ion using ag icul u al was e, e.g.
whea , ice, paddy s aw, ice b an, co ee s aw, ea lea es,
co on s aw sawdus , p o ide p o i able ag i-business
oppo uni ies o small a me s and o e s an eco- iendly
al e na i e o disposing o was e, which is no mally bu n
(Zhang e al. 2002). Va ious comme cial mush ooms a e
cul i a ed wo ldwide, and ag icul u al esidues a e used as
cheap and enewable subs a es, and a selec ion is gi en in
Table 19.
Ag icul u al was e consis s o la ge quan i ies o ligno-
cellulosic was e, and is composed o app oxima ely 60–
70% e men able suga s and 20–30% a oma ic compounds.
Lignocellulosic was e is a enewable and impo an sou ce
o biomass/e hanol p oduc ion (Kim and Dale 2004).
Whea s aw, co n s o e , suga cane bagasse, and ice
s aw a e he mos common subs a es o bio uel p oduc-
ion, and ilamen ous ungi a e key componen s o he
e men a ion p ocess. Pichia s ipi es (s ain NRRL
Y-7124) is used in he e men a ion p ocess o p oduce
e hanol om whea s aw and ice s aw (Moni uzzaman
1995), and Fusa ium oxyspo um, Neu ospo a c assa, and
Paecilomyces sp. a e ypically used o e men cellulose
di ec ly o e hanol (Szczod ak and Fiedu ek 1996).
The e o e, a ious ungi ha e he po en ial o p oduce
lignocellulosic enzymes and play impo an oles in eco-
ag icul u al was e p ac ice. Whi e- o ungi can also be
used o p e- ea he ag icul u al was e o enhance he
enzyma ic saccha i ica ion p ocess due o he selec i e
emo al o lignin (Miyauchi e al. 2018; Rouches e al.
2018; Zhou e al. 2015b,2018). The sc eening o he
sec e ed enzymes om ungi can also be used o enhance
he saccha i ica ion o ag icul u al was e by comme cial
enzyme cock ails, and his app oach has led o he dis-
co e y o new ac i i ies such as ly ic polysaccha ide oxi-
dases which open up he lignocellulose s uc u es o
acili a e u he access o celluloly ic enzymes (Be in
e al. 2012; Cou u ie e al. (2012,2018). Al e na i ely,
ungi can be used o ans o m compounds in ag icul u al
was e in o highe alue comme cial molecules such as
anillin (Tai a e al. 2018) and cannolo (Odino e al.
2017).
In mos coun ies, some was e, such as ce eal esidue, is
uni e sal, whe eas o he o ms o ag icul u al was e a e
mo e egion-speci ic. In he F ench egion o P o ence, o
example, la ende is g own on a la ge scale o he p o-
duc ion o essen ial oils. Globally, hese oils a e among
hose mos commonly used o indus ial pu poses,
including in pe umes, pha maceu icals and cosme ics.
Table 19 Ag icul u al was e use as subs a e o mush oom cul i a ion
Fungal axa Ag icul u al was e Re e ences
Aga icus
bispo us
Bu on
mush oom
Whea s aw Kam han and Tiwa i
(2017)
Ganode ma
sp.
Chinese
mush oom
Sawdus Shashi ha e al. (2016)
Len inula
edodes
Shii ake
mush oom
B ac s o pineapple c own, suga cane bagasse, suga cane lea es, whea s aw, co n-
cobs, oak-wood sawdus
Salmones e al. (1999)
Philippoussis e al.
(2007)
Pleu o us
e yngii
King oys e
mush oom
Supplemen a ion o whea b an wi h wood chips. Ba ley s aw and suga bee pulp wi h
ice b an
Jeznabadi e al. (2016)
Pleu o us
djamo
Pink oys e
mush oom
Supplemen a ion o whea b an wi h suga cane bagasse Hasan e al. (2015)
Pleu o us
os ea us
Oys e
mush oom
Paddy s aw, ice s aw whea s aw, da e-palm lea es emp y ui bunch, oli e cake,
oma o u , banana lea es, pine needles, suga cane bagasse
Alananbeh e al.
(2014)
Ananbeh and
Almomany
(2005,2008)
Ali e al. (2010)
Ma lina e al. (2015)
Rezania e al. (2017)
Yang e al. (2013a)
Fungal Di e si y (2019) 97:1–136 69
123

A e s eam dis illa ion, he esidual s aw is conside ed o
be ag icul u al was e, hough i can also be used as a sou ce
o e pene de i a i es (e.g. τ-cadinol, β-ca yophyllene),
lac ones (e.g. couma in, he nia in), and phenolic com-
pounds o indus ial in e es , including osma inic acid
( h ough ungal ea men s) (Lesage-Meessen e al. 2018).
Fungal-de i ed enzymes ep esen o e 60% o he wo ld
ma ke in indus ial enzymes. La ende esidues, like mos
ag icul u al was e esidues, a e bo h sui able ca alys s o
he sec e ion o a wide panel o lignocellulose-ac ing
enzymes, such as cellulases, laccases and xylanases, and
he e o e can p o ide a local and cheap sou ce o
deg ada i e and ans o ming bioca alys s. E en plan
pa hogens like Phyllos ic a capi alensis p oduce a abinase,
cellulase, laccase, pec inase and xylanase, especially when
cul i a ed on la ende esidues. The ini ial g ow h o P.
capi alensis on la ende was e was highe in compa ison o
i s g ow h on o he ag icul u al was e ma e ials, such as
miscan hus, ice s aw, ice husk, so ghum, and whea
s aw, sugges ing u he s imula ion o g ow h by a com-
pound emaining wi hin he la ende esidue (Wikee e al.
2017). This opens up u he a enues o in es iga e he
p esence o mic obial g ow h enhance s wi hin ag icul u al
was e o u iliza ion in bio echnology. The e o e, he aims
o his p esen e iew a e o e eal he capaci y o ungi o
ag icul u al was e managemen and o explo e he a ie ies
o ungi and hei lignocelluloly ic p oduc ion, aking ull
ad an age o a ious ag icul u al was e p oduc s as
subs a e.
38. Myco emedia ion: Fungi o he escue
Man-made ac i i ies ha e esul ed in ex eme en i on-
men al pollu ion, and he e o e en i onmen ally iendly
emedia ion echniques a e mo e necessa y han e e be o e
(Rhodes 2013). Fungi, he mos igo ous decompose s
ound in na u e, a e a po en ial solu ion o his p oblem
(Singh 2006). Bio emedia ion wi h ungi, known as
myco emedia ion, is an inno a i e bio echnological
app oach which uses li e ungi o clean up con amina ion
h ough o al mine aliza ion using enzymes, o h ough he
o al emo al o he con aminan ia abso p ion (S ame s
2005). Pollu an s eleased in o he en i onmen due o man-
made ac i i ies pose a signi ican h ea o he sus ainabili y
o he en i onmen and o human heal h. The bu ning o
wood and ossil uels, as well as coal mining and oil d illing
all elease ecalci an pollu an s such as polycyclic a o-
ma ic hyd oca bons (PAH), which a e no easy o emo e
once hey ha e been eleased. In addi ion, pes icides ha
leak in o na u al wa e ways and indus ial e luen s con-
aining hea y me als, ha ha e been eleased in o he
en i onmen wi hou p ope ea men can be e ec i ely
emo ed i ungi a e u ilized as a emedia ion ool.
The ege a i e pa o he ungi, called mycelium, has
he abili y o exude powe ul ex acellula enzymes and
acids ha a e able o decompose many o ganic subs a es,
including lignin and cellulose (Poin ing e al. 2001; Buche
e al. 2004). Wi h a simple sc eening p ocedu e, he mos
sui able ungal species o he a ge pollu an can be
iden i ied (Ma suba a e al. 2006). Many species o ungi,
such as Aspe gillus nige , A. e eus, Cladospo ium oxys-
po um, Fusa ium en icosum, Rhizopus o yzae, T icho-
de ma ha zianum as well as he model whi e o ungus,
Phane ochae e ch ysospo ium, ha e been es ed o hei
abili y o deg ade pes icides (Bhale ao and Pu anik 2007;
Leo
´n-San ies eban e al. 2016). Polychlo ina ed biphenyls,
which a e highly oxic chemicals p e iously used in many
indus ies and one o he mo e pe sis en o ganopollu an s,
can be deg aded by non-ligninoly ic enzymes om ungi
such as Fusa ium solani, Penicillium ch ysogenum and
Scedospo ium apiospe mum (Tigini e al. 2009).
Di e en species o basidomyce e whi e o ungi a e
bes sui ed o myco emedia ion, as hei ex acellula
lignin modi ying enzymes ha e low subs a e speci ici y
(Lang e al. 1995). No only do hey a ge lignin, bu hey
also a e capable o a ge ing many o ganic pollu an s ha
a e simila in s uc u e o lignin, like DDT, lindane,
chlo odane and PCBs (A isoy 1998; Poin ing 2001; Man-
su e al. 2017). Enzymes like lignin pe oxidases (LiP),
manganese pe oxidases (MnP) and laccases (LAC) sec e-
ed by whi e o ungi a e excellen a deg ading
o ganopollu an s held oge he by hyd oca bon bonds
(Ku
¨es 2015). Whi e o ungi such as Len inus subnudus,
Phlebia acan hocys is and Pleu o us os ea us, and many
o he s ha e been success ully used sepa a ely as well as in
mix u es o ea si es con amina ed wi h pes icides and
he bicides (Kamei e al. 2011; Nyakundi e al. 2011; Xiao
e al. 2011). Since whi e o ungi g ow by hyphal ex en-
sion, hey can be e each he pollu an s in con amina ed
si es, unlike o he o ganisms wi h a low colonizing
capaci y (Reddy and Ma hew 2001). Fu he mo e, he lig-
nin deg ading enzymes used by whi e o ungi a e ex a-
cellula (No o ny
´e al. 2004). These ungi can ole a e
high concen a ions o he pollu an , as he pollu an does
no need o be in e nalized in o de o s a he deg ada ion
p ocess.
Lama and Whi e (2001) ecommend a ou -s ep s a -
egy o he p ac ical implemen a ion o ungi o he
myco emedia ion o con amina ed si es. The s eps include
labo a o y scale expe imen s o es ablish p epa a ion
me hods; on-si e pilo es ing o unde s and sound echnical
and enginee ing echniques; and he p oduc ion o inocu-
lum o i ied wi h nu ien s o ensu e g ow h and inally
ull-scale applica ion (Fig. 39).
Because o hei ole ance o ex eme pH condi ions,
empe a u es, and nu ien a ailabili y, ungal species such
70 Fungal Di e si y (2019) 97:1–136
123
as Aspe gillus sp. and S e igma omyces halophilus ha e
been es ed o hei abili y o abso b hea y me als om
con amina ed si es (Bano e al. 2018). The cell walls o
hese ungi ha e excellen me al binding capabili ies, and
can abso b con aminan s which hen can be physically
emo ed by ha es ing he ungus (Bald ian 2003). The
u iliza ion o he biosu ac an s o ungal species has been a
success o he emo al o hea y me als such as Fe, Zn and
Pb (Igi i e al. 2018). Fo example, an anionic biosu ac an
om Candida sphae ica was es ed on cleaning soil col-
lec ed om an au omo i e ba e y indus y, and he hea y
me al emo al success a e was 95%, 90% and 79% o Fe,
Zn and Pb, espec i ely (Luna e al. 2016).
The ex ile indus y is one o he p ima y con ibu o s o
en i onmen al pollu ion. Un ea ed ex ile e luen s, ine -
iciency in he dyeing p ocess, and he poo handling o
spen dye s u e luen s a e he main causes o su ounding
na u al wa e and land con amina ion, bo h o which
ad e sely a ec plan , human and animal li e. Tex ile dyes,
such as azo dyes (acid ed) o an h aquinonic dyes (basic
blue) a e highly oxic and mu agenic in na u e (Delclos
e al. 1984). Biological ea men o hese ha m ul pollu-
an s h ough mic obial decolou iza ion and deg ada ion
ha e a ac ed a en ion as he con en ional ea men
me hods p oduce haza dous by-p oduc s and a e no e y
cos e ec i e. T ichode ma ha zianum (Singh and Singh
2011) has been success ully bench es ed o he decon-
amina ion o a ious ex ile dyes.
Apa om he abso bance p ocess, enzyma ic deg a-
da ion o was e is ano he easible app oach ha can be
used o he emo al o slow-deg ading was e. Va ious
ypes o cellulose-based u ban solid was e a e p ima ily
disposed o ia incine a ion. One s udy conduc ed by
Espinosa-Valdema e al. (2011) used Pleu o us os ea us
(Oys e mush oom) o educe he mass and olume o used
disposable diape s ia cellulose deg ading enzymes sec e-
ed by he ungi, which simul aneously p oduced a pa ho-
gen- ee, high-p o ein ood sou ce in he o m o a
mush oom ui ing body ha could be used o human
consump ion o as a ood supplemen o animals.
Fig. 39 The p ocess o
myco emedia ion
Fungal Di e si y (2019) 97:1–136 71
123
O he con en ional s a egies o he decon amina ion o
pollu ed si es, such as he use o chemicals o h ough
incine a ion, a e compa a i ely less e ec i e han
myco emedia ion. The washing and ex ac ing used in he
chemical me hod only shi s he con aminan om one
place o ano he (Valen ı
´n e al. 2013); likewise, incine -
a ion can be highly ene gy in ensi e, no cos e ec i e, and
has he po en ial o cause ha m h ough he o ma ion o
dioxides (Shibamo o e al. 2007).
The e a e ongoing s udies o es whe he edible mush-
ooms could be used i s o myco emedia ion and hen o
human consump ion. In one s udy, o example, Pleu o us
pulmona ius was success ully es ed o cleaning c ude oil
(Olusola and Anslem 2010); in ano he s udy, Aga icus
bispo us and Lac a ius pipe a us we e success ully used
o he bioso p ion o Cd
2?
unde labo a o y condi ions
(Nagy e al. 2013). Howe e , hese myco emedia ion p o-
cesses emain imp ac ical due o he ac ha he abso p-
ion o pollu an s, such as hea y me als migh ende he
edible pa o he mush ooms highly con amina ed (Kul-
sh esh ha e al. 2014). Howe e , i means o u ilizing
mush ooms wi h an i-mu agenic and an i-geno oxic abili-
ies could be de eloped (Mendez-Espinoza e al. 2013),
hen i would be possible o simul aneously educe he
oxici y o he pollu an s, clean he lands deemed un i o
ag icul u e, and p oduce c ops o animal eed.
Some ungi no being able o g ow in he p esence o he
na u al mic obio a o he con amina ed si e and he need o
ha e p ecise unde s anding he nu ien equi emen s o he
ungus o i o h i e in he con amina ed si e migh be
some small se backs o his echnology. In compa ison o
he al e na i e me hods, hese p oblems a e negligible. And
hey can be eadily sol ed wi h imp o ed in-si u and ex-
si u ails.
The lack o mo e comp ehensi e in o ma ion abou
deg ada ion mechanisms and he enzymes in ol ed in he
pollu an deg ada ion by di e en ungal species hinde s
he possible use o hem in myco emedia ion in a mo e
speci ic manne . Mo e in dep h s udies should be done o
ecognize he oxida i e enzymes, o ganic acids and
chela o s exc e ed by ungi du ing he mine aliza ion and
deg ada ion p ocess. Ano he way o inc ease e iciency o
myco emedia ion is using la ge scale s udies o e i y he
esul s o he bench scale s udies ha would p o ide
insigh s in o e icien use o he exis ing species o ungi
and iden i ying new species sui able o bio emedia ion.
Mo e esilien ungal species adap ed o ha sh en i on-
men al condi ions should be es ed o hei adap abili y as
bio emedia e s as hey a e mo e physiologically ac i e. Fo
example in some a eas o he wo ld, he soil is high in sal
concen a ion due o ine icien d ainage and his makes he
ecosys ems in hese a eas e y simple and agile. To make
hese a eas mo e ag icul u ally easible, halophilic o
halo ole an ungi can be used use o clean up he soil o
he excessi e sal . Up un il now mos o he s udies done
ega ding halophilic ungi only ocus on he cha ac e iza-
ion. Fungi such as Aspe gillus penicillioides,Gymnascella
ma ismo ui,Cladospo ium cladospo ioides and Penicil-
lium wes lingii a e well cha ac e ized as halophilic bu hei
po en ial use as soil myco emedia o s should be done wi h
mo e ocused s udies speci ically designed o check hei
sal emedia ion abili y (Zhang and Wei 2017).
By s udying he genes ela ed o enzyme deg ada ion,
mine aliza ion, abso bance and adap abili y o ex eme
en i onmen al condi ions, ansgenic ungi can be p o-
duced wi h supe io myco emedia ion capabili ies. How-
e e , since he emedia ion capaci y o na u ally occu ing
ungi is s ill e y much unde s udied, isola ing and
sc eening sui able ungi om hei na u al habi a s should
ca ied ou in o de o eclaim pollu ed si es and o sus ain
a be e en i onmen o u u e gene a ions.
39. Myco umiga ion using he genus Muscodo
Myco umiga ion is he use o an imic obial ola iles p o-
duced by ungi o he con ol o o he o ganisms (S inson
e al. 2003). The p o o ypes o he myco umigan agen s
belong o s ains o he genus Muscodo , on which mos o
he ac i i ies in esea ch and de elopmen in his a ea ha e
so a been ocused. Muscodo species a e endophy es ha
belong o he o de Xyla iales (Ez a e al. 2004; Gonza
´lez
e al. 2009; Kudalka e al. 2012; Suwanna ach e al.
2013a; Wijayawa dene e al. 2018; Chen e al. 2019), bu
he axonomic and phylogene ic posi ion o he genus
emains unse led (Da anagama e al. 2018; Wend e al.
2018). Muscodo cul u es do no spo ula e, hei sexual
s a e is as ye unknown, and hei mos salien common
ea u e is hei abili y o p oduce ola ile o ganic com-
pounds. All s ains o his genus can inhibi and kill o he
ungi, including human and plan pa hogenic species, as
well as bac e ia and insec s, h ough he p oduc ion o a
mix u e o ola ile o ganic compounds. These mix u es a e
p ima ily composed o a ious small molecula weigh
alcohols, o ganic acids, es e s, ke ones, and se e al a o-
ma ic hyd oca bons as de e mined by gas ch oma og aphy-
mass spec ome y. The mix u e o VOCs p oduced om
Muscodo species has been epo ed o be an imic obial
ola iles ( o a selec ion see compounds 66–72 in Fig. 40;
o o iginal li e a u e see, A mosuka o e al. 2005;
Kudalka e al. 2012; Me cie and Jime
´nez 2004; Mi chell
e al. 2008; Ramin e al. 2005; Si i-Udom e al. 2017;
Suwanna ach e al. 2013a,2015a,2017; Wo apong e al.
2001; Zhang e al. 2010b). S udies by Alpha e al. (2015)
and Hu chings e al. (2017) sugges ed ha VOC p oduced
by Muscodo may ac in he bac e ial DNA damage
h ough inducing DNA alkyla ion and DNA me hyla ion
72 Fungal Di e si y (2019) 97:1–136
123
p ocesses; howe e , he ac i e ing edien s ye emain o be
iden i ied. I such biological ac i i ies would also be
obse ed in euka yo es, including mammalian cells, his
migh cons i u e a u u e challenge o he egis a ion o
p oduc s based on he espec i e s ains because o hei
mu agenic po en ial.
The mos ad anced p ojec o his kind has ocused on
Muscodo albus (s ain 620), o iginally isola ed om
Cinnamomum zeylanicum. This s ain was shown o be an
e ec i e bio umigan capable o con olling lemon decay
caused by Penicillium digi a um; lemon sou o caused by
Geo ichum ci i-au an ii; apple decay caused by Penicil-
lium expansum and Bo y is cine ea; as well as peach
b own o caused by Monilinia uc icola (Me cie and
Jime
´nez 2004; Me cie and Smilanick 2005). The s ain
also can con ol g ain smu ungi (Goa es and Me cie
2009) and ac as an insec icide agains po a o ube mo hs
(Lacey and Ne en 2006). Ano he s ain, Muscodo
su hepensis (Fig. 41a), isola ed om Cinnamomum bejol-
gho a in Thailand, has po en ial applica ion as a bio umi-
gan o con olling blue mold (Penicillium digi a um)
decay o he ange ine ui (Fig. 42a) (Suwanna ach e al.
2015a,b).
Muscodo inoculum also has he po en ial o eplace
me hyl b omide (a oxic chemical umigan and pes icide)
umiga ion in con olling soil-bo ne plan diseases. Mus-
codo albus (s ain MFC2), isola ed om My is ica
ag ans, has he po en ial o con ol kale oo o disease
caused by Py hium ul imum (Wo apong and S obel 2009).
Muscodo albus (s ain 620) and M. oseus (isola ed om
G e illea p e idi olia) showed he abili y o con ol disease
se e i y caused by a a ie y o ungal and oomyce e plan
pa hogens, e.g. Aphanomyces cochlioides, Rhizoc onia
solani,Py hium ul imum and Ve icillium dahliae (S inson
e al. 2003; Me cie and Jime
´nez 2009). Muscodo oseus
also has nema icidal and nema os a ic applica ion agains
ou plan -pa asi ic nema ode species (Meloidogyne chi -
woodi,M. hapla,Pa a ichodo us allius, and P.pene ans)
ound on economically impo an ege able c ops (Riga
e al. 2008). Muscodo cinnamomi (Fig. 41b) comple ely
con olled damping-o symp oms on plan seedlings and
Rhizoc onia- oo o in oma o plan s, (Fig. 42c) (Suwan-
na ach e al. 2012,2015b). Muscodo he eae isola ed om
ubbe ees (He ea b asiliensis) is e ec i e a con olling
whi e oo o disease in ubbe ees caused by Rigido-
po us mic opo us (Si i-Udom e al. 2017).
The applica ion o Muscodo in he con ol o soil-bo ne
disease migh be o conce n due o he phy o oxic ac i i y
which depends on he mix u e o ola ile o ganic com-
pounds and ype o plan (Suwanna ach e al. 2012; Si i-
Udom e al. 2017). Suwanna ach e al. (2017) sugges ed
ha M.cinnamomi could be used in umiga ion wi h an
ac i e cul u e o a biological con ol agen o educe he
numbe o mic oo ganisms p esen on eggshell su aces
O
O
3-Me hylbu yl ace a e (66)
OH
2-Me hylbu an-1-ol (67)
OH
3-Me hylbu an-1-ol (68)
O
2-Me hyl u an (69)
O
Te ahyd o u an (70)
O
2-Bu anone (71)
OH
O
2-Me hylp opanoic cid (72)
Fig. 40 Bioac i e compounds
epo ed om Muscodo species
Fig. 41 Colonies o Muscodo
su hepensis (a) and M.
cinnamomi (b) on po a o
dex ose aga a 25°C a e
12 days. Scale ba =1cm
Fungal Di e si y (2019) 97:1–136 73
123
manu ac u ing p ocess and biodeg adabili y a he p o-
duc ’s end-o -li e s age, i was ound ha op imum pe -
o mance occu ed a he c i ical au omo i e oad noise
equency o 1000 Hz. Subsequen ly, es ing was pe -
o med wi h panels p oduced wi hin he bulk bin eac o
pa adigm wi h h ee subs a e blends (Table 20), acco ding
o ASTM C423 using an IBM HVAL wi h a No sonics
NE840 eal ime analyse . The highes sound abso p ion
was ound wi h he aspen sha ing blend, which boas ed an
NRC a ing o 0.9, hus demons a ing a Class A abso p ion
coe icien and sugges ing po en ial applica ion o manu-
ac u e o low VOC, biodeg adable, acous ic panels. S a e-
o - he-a acous ic panels a e p oduced wi h polyu e hane
oam, wi h mine al wool and ibe glass p o iding low-
VOC op ions, bu he e is a g owing in e es in de elop-
men o na u al al e na i es due o human heal h and p o-
duc end-o -li e conce ns (Kaamin 2017).
A c i ical p ope y o acous ic panels o indoo
applica ions is i e a ing. Jones e al. (2017) epo ed
meaning ully lowe CO2 and CO elease, along wi h
educed smoke densi y, o mycelium- ice hull composi es,
as compa ed o XPS by cone calo ime e . Addi ionally, i e
pe o mance can be imp o ed by amendmen wi h glass
ines (Jones e al. 2018).
Cons uc ed loa ing we land panels ep esen ano he
applica ion oppo uni y o he mechanical and end-o -li e
p ope ies o mycelium composi es. Cons uc ed loa ing
we lands a e p ima ily u ilized o imp o e we land wa e o
was ewa e quali y, hough hey a e also used o a a ie y
o o he objec i es, including habi a c ea ion, sho eline
p o ec ion, and landscape imp o emen . Floa ing we lands
a e ypically cons uc ed om a a ie y o ma e ials,
including non-biodeg adable ma e ials such as ex uded
polys y ene, PVC pipes, and high-densi y polye hylene
(Pa line i e al. 2017). In his conside a ion, mycelium
composi e panels may p o ide a biodeg adable op ion wi h
he equi ed mechanical and hyd ophobic p ope ies (Ha-
nee e al. 2017). This applica ion is being es ed by he
G een Fu u es Resea ch and Design Lab a he Uni e si y
o Washing on (Sea le, WA, USA), wi h mycelium com-
posi e panels cu en ly in ield deploymen .
42. Fungal deg ada ion o plas ics: A hidden
easu e o a g eene en i onmen
In he mode n plas ic e a, p ima y plas ic p oduc ion has
inc eased o 335 million onnes pe yea , wi h Asia
accoun ing o 50% o he o al wo ldwide p oduc ion
(Plas icsEu ope 2017). Acco ding o a ecen es ima e,
om 1950 o 2015 abou 9150 million onnes o p ima y
plas ics we e p oduced, esul ing in he accumula ion o
abou 6945 million onnes o plas ic was e on he su ace o
he ea h. O he o al was e gene a ed, only a small pe -
cen age was ecycled (9%) and incine a ed (12%), while
79% amassed in land ills and o he e es ial and ma ine
en i onmen s (Geye e al. 2017).
The majo i y o pe oleum-based plas ics, such as
polye hylene (PE), poly(e hylene e eph hala e) (PET),
polys y enes (PS), polyu e hanes (PUs), and poly inyl
chlo ide (PVC), a e esis an o biodeg ada ion, and
he e o e pe sis in he en i onmen wi h a ious conse-
quences (Wei and Zimme mann 2017). Biodeg adable
plas ics a e conside ed eco- iendly al e na i es o pe o-
leum-based non-biodeg adable polyme s. Howe e , limi ed
in o ma ion is a ailable ega ding he exac mechanisms
unde lying he biodeg ada ion p ocess, he ime scale o
biodeg ada ion, and he op imal en i onmen al condi ions
equi ed o hei biodeg ada ion (Yang e al. 2014a). Thus,
he ca eless disposal and deg ada ion o bo h biodeg adable
and syn he ic plas ics esul in he accumula ion o was e in
e es ial land ills and ma ine en i onmen s, and pose a
se ious h ea o su ounding ecosys ems (And ady 2015).
None heless, nume ous s udies ha e epo ed ha plas ics
a e ulne able o mic obial a ack (Ba a e al. 2003;
K asowska e al. 2012; Ma hu and P asad 2012; Za a
e al. 2013,2014; Res epo-Flo
´ ez e al. 2014; Khan e al.
2017).
The conse a ional and ecological oles o ungi a e no
only limi ed o ene gy o elemen al cycling, bu can also be
used in he biodeg ada ion o a ious ypes o plas ics.
Nume ous s udies ha e men ioned ungi as he p edomi-
nan mic oo ganisms esponsible o he biodeg ada ion o
bo h bio- and syn he ic- plas ics (Ba a e al. 2003; Khan
e al. 2017). Acco ding o he indings o one su ey, he
majo i y o plas ic deg ading ungi belong o he gene a
Aspe gillus, Fusa ium, Paecilomyces and Penicillium (Kim
and Rhee 2003). The mechanical o ces exe ed by he
ungi du ing g ow h, hyphal pene a ion in o he plas ic
laye , as well as he simul aneous sec e ion o a ious
enzymes and adicals, a e all cha ac e ized as he ungal
deg ada ion o plas ics (Moo e e al. 2000). The mecha-
nism o ungal deg ada ion begins wi h he a achmen o
hyphal ilamen s o he su ace o a plas ic subs a e. The
hyphal ips hen ex end, using mechanical o ce o sec e e
enzymes and adicles ha allow he pene a ion o he
ungus in o he subs a e (see Fig. 45).
The nex s ep is he abso p ion o small molecules,
polyme s, adicles, o a oms h ough he po ous ips o he
hyphae, ollowed by hei anspo a ion h ough he
unde lying plasma memb ane (Moo e e al. 2000; Khan
e al. 2017). The enzymes a e known o hyd olyze he
polyme ic subs a e and in u n p o ide nu ien s, which
acili a es he g ow h o ungi o o he mic oo ganisms
(San e e e al. 1994; Lucas e al. 2008; Bane jee e al.
80 Fungal Di e si y (2019) 97:1–136
123

2014). The a ious ungal species and he associa ed
enzymes epo ed o deg ade a ious ypes o plas ics a e
lis ed in Table 21.
Mos o he enzymes known o he deg ada ion o plan
polyme s a e able o depolyme ize syn he ic polyme s,
such as PE and PU, by hyd olyzing he es e bonds p esen
in he polyme backbone. The su ace a ea o polyme s
exposed o ungal enzyme a ack has an ad ancing e ec
on biodeg ada ion. The e o e, plas ic pa icles in he ange
o 0.5 o 0.25 mm a e mos sui able o enzyme
biodeg ada ion. Al hough pu i ied enzymes a e known o
b eakdown he C–C bond in poly inyl chlo ide (PVC), he
use o mic oo ganisms is a o ed o he biodeg ada ion o
polyme s. Mo eo e , he mixed cul i a ion o se e al
s ains is known o ha e a g ea e impac on biodeg ada ion
e iciencies han he use o single s ains (Wei and Zim-
me mann 2017).
The o e all p ocess o plas ic biodeg ada ion is depen-
den on he p esence o op imal en i onmen al condi ions
o acili a e he g ow h o ungi and maximize he ac i i ies
o he enzymes o depolyme ize he polyme ic ma e ials.
The biodeg ada ion p ocess is also a ec ed by he physio-
chemical p ope ies o he plas ics, such as su ace
opology, molecula weigh , hyd ophobici y, and he
deg ee o c ys allini y (Manzu e al. 2004; B ueckne e al.
2008; Jenkins and Ha ison 2008; Ronk is e al. 2009;
Res epo-Flo
´ ez e al. 2014; Wei and Zimme mann 2017).
Highe deg ees o c ys allini y s ongly educed he
biodeg ada ion o speci ic plas ics. Alipha ic ca bon chains
a e mo e easily biodeg adable han a oma ic polyme s. The
hyd ophobici y o plas ics makes he su ace wa e epel-
lan , educing he success o he a achmen , g ow h, and
p opaga ion o ungal hyphae, and he eby educing he
deg ee o plas ic biodeg ada ion. Simila ly, abio ic ac o s
such as en i onmen al empe a u e; a ailabili y o oxygen;
exposu e o ligh o UV; and a ailabili y o adicles in he
en i onmen all a ec he mechanisms o plas ic
biodeg ada ion (Wei and Zimme mann 2017).
The di e si y, zonal dis ibu ion, and niche pa i ioning
o ungal s ains in he en i onmen also a ec he
biodeg ada ion p ocess. Fu he mo e, he amoun and ype
o enzymes sec e ed by he ungal s ain o diges he
polyme also s ongly a ec he biodeg ada ion p ocess
(Fig. 10). The sec e ion o speci ic ypes o enzymes o
a ious ypes o enzymes by ungi o deg ade polyme s
Fig. 45 Fungal deg ada ion o
polyes e polyu e hane (PEU)
ilms. aPEU ilm no exposed o
ungal deg ada ion (con ol); b–
dPEU ilms exposed o
di e en Aspe gillus spp. on
mal ex ac aga medium
incuba ed o 28 days in da k a
30 °C. The ex en o
biodeg ada ion di e ed o each
s ain. Fungal hyphal g ow h is
obse ed on he PEU su ace
and some po ions o he PEU
ilms a e deg aded due o ungal
ac i i ies
Fungal Di e si y (2019) 97:1–136 81
123
Fig. 46 Polyes e polyu e hane
(PEU) ilms wi h ungal g ow h
and signs o biodeg ada ion on
he su ace. aPEU ilm no
exposed o Aspe gillus species;
b ungal g ow h on he su ace
o PEU; c,dPEU ilms a e he
washing o ungal hyphae om
he su ace o he ilms
Table 21 Lis o ungal species wi h hei enzymes esponsible o biodeg ada ion and ypes o plas ics used
Fungal s ain Enzyme Plas ic
ype
Re e ences
Aspe gillus la us Glucosidases PCL Tokiwa e al. (2009)
Aspe gillus nige Ca alase, p o ease PCL Tokiwa e al. (2009)
Aspe gillus e eus Es e ase, u e hane hyd olase PU Boubendi (1993)
Aspe gillus ubingensis Es e ase, lipase PU Khan e al. (2017)
Bipola is (Cochliobolus) sp. Laccase PVC Suma hi e al. (2016)
Chae omium globosum Es e ase, u e hane hyd olase PU Boubendi (1993)
Cu ula ia senegalensis Polyu e hanase PU C abbe e al. (1994)
Fusa ium sp. Cu inase PCL Shimao (2001)
Pes alo iopsis mic ospo a Se ine hyd olase PU Russell e al. (2011)
Phane ochae e ch ysospo ium Manganese pe oxidase PE Shimao (2001)
Tala omyces uniculosus ( o me ly Penicillium
uniculosum)
Glucosidases PHB Tokiwa e al. (2009)
Tala omyces pinophilus ( o me ly Penicillium pinophilum) PHB-depolyme as PHB Panagio idou e al. (2014)
T ichode ma sp. U ease, p o ease, es e ase and
laccase
PU Lo edo-T e in
˜o e al.
(2011)
Disclaime : Some o he ungal species in he able a e pa hogenic and i is ou o ques ion o use hem in bio echnological p ocesses
PCL polycap olac one, PE polye hylene, PHB polyhyd oxybu y a e, PU polyu e hane, PVC poly inyl chlo ide
82 Fungal Di e si y (2019) 97:1–136
123
a y om one species o ano he , o e en wi hin he same
species (Doi 1990; Howa d 2012).
Cu en ly, mo e han 100 ungal species a e known o
deg ade di e en ypes o plas ics, and many mo e a e s ill
in he p ocess o being isola ed and iden i ied (Howa d
2012). Mos o he ungal s ains disco e ed we e s udied
o hei enzyme biodeg ada ion abili ies a he labo a o y
scale. No e o s ha e ye been made o de elop la ge scale
o indus ial scale bio eac o s o speci ic ypes o plas ic
deg ading ungi. The e o e, his esea ch is o g ea
impo ance o indus ial de elopmen , as well as o u u e
esea ch pu poses. Collabo a ions be ween chemis s, biol-
ogis s, enginee s and physicis s could esul in he de el-
opmen o a la ge-scale bio eac o o plas ic
biodeg ada ion u ilizing ungi. A p esen , such p ocesses
a e oo expensi e o be applied a la ge scale, and col-
lec ing and bu ning plas ics unde high hea emains mo e
economical. Howe e , once such bio eac o s a e success-
ully de eloped, new indus ies will eme ge o bo h he
deg ada ion o a ious plas ics as well as o he u iliza ion
o he deg aded compounds in he manu ac u ing o new
p oduc s. The e is a need o p ope ly collec disposed
plas ics and de elop sophis ica ed la ge-scale bio eac o s
in which ungi could be used o deg ade a ious ypes o
plas ics sepa a ely in con olled condi ions using mode n
bio echnological echniques. A en ion should be gi en o
esea ch and de elopmen on immobilized enzyme ech-
nologies wi h ega d o ungal-deg ada ion o plas ics
h ough enzymes. Mo e knowledge is needed conce ning
he connec ion be ween speci ic-plas ic ypes and speci ic
ungal species, o de e mine he ac ual ood web o a ious
ungi. In eg a ion o low-cos and easily deg adable bio-
plas ics in ma ke s a ound he globe is impo an . The
mechanisms o ungal deg ada ion o plas ics need o be
cla i ied using iso opic ma king o plas ics. The s uc u e
and ac i e si es o biodeg ading enzymes o a ious ungi
need o be de e mined, and me hods o inc ease he ca -
aly ic deg ada ion o polyme s need o be de eloped.
43. Polycyclic a oma ic hyd oca bon deg ada ion
by basidiomyce es
Polycyclic a oma ic hyd oca bons a e ubiqui ous con am-
inan s widely dis ibu ed in he en i onmen , wi h sus-
pec ed ca cinogenic and mu agenic e ec s. The clean-up o
polycyclic a oma ic hyd oca bon con amina ed si es is o
g ea impo ance o p o ec ing human heal h. Polycyclic
a oma ic hyd oca bons a e o ganic compounds composed
o wo o mo e used benzene ings which a e o med
du ing he combus ion o o ganic molecules and hei
subsequen ecombina ion (Ha i ash and Kaushik 2009).
Low molecula weigh polycyclic a oma ic hyd oca -
bons a e composed o 2–3 a oma ic ings. They a e
commonly ound in pe ogenic sou ces (e.g. gasoline,
ke osene) and can be in oduced o he aqua ic en i onmen
h ough oil spillage and discha ge om ships, anke s,
mo o boa s, e c. Con amina ion can also come om
municipal and u ban uno (Viei a e al. 2018). Polycyclic
a oma ic hyd oca bons o high molecula weigh , com-
posed o 4–6 a oma ic ings (e.g. py ene and benzo[a]
py ene), a e o en eleased in o he en i onmen h ough
py ogenic sou ces (Souza e al. 2015). Such polycyclic
a oma ic hyd oca bons a e conside ed p io i y pollu an s
because hey a e ecalci an in he soil, due o hei high
a ini y and low wa e solubili y (Ro he mich e al. 2002).
The biodeg ada ion o polycyclic a oma ic hyd oca bon
(Fig. 46) con aminan s is a complex p ocess which is
highly dependen on he numbe o con aminan s, na u al
condi ions (e.g. empe a u e, humidi y and clima e), and
p esence o o ganisms consuming he a ailable hyd oca -
bons. Polycyclic a oma ic hyd oca bons end o bind o soil
componen s, hus becoming di icul o emo e and
deg ade (Pandey e al. 2016). Hyd oca bons di e in hei
suscep ibili y o mic obial a ack, in which some o he
high molecula weigh polycyclic a oma ic hyd oca bons
may only be pa ially deg aded o no deg aded a all (A las
and B agg 2009).
Fungi can u n hyd oca bon con aminan s in o an ene gy
sou ce. In he hyd oca bon con amina ed en i onmen ,
hose ungi capable o deg ading hyd oca bon ha e be e
chance o su i ing by u ilizing his ca bon sou ce o
g ow h (Fe nandez-Luqueno e al. 2010). Some ungi, and
in pa icula basidiomyce es, a e e icien deg ade s o high
molecula weigh polycyclic a oma ic hyd oca bons. In his
way, ungi a e unlike bac e ia, which a e be e equipped
o deg ading smalle molecules (Peng e al. 2008).
The biodeg ada ion o polycyclic a oma ic hyd oca -
bons can be enhanced h ough ex acellula oxida ion.
Whi e o ungi a e he mos e icien p oduce s o oxida-
i e ex acellula enzymes. Whi e- o ungi a e wood
deg ading basidiomyce es which p oduce special oxidases
o enzymes ha help in he deg ada ion o lignin and o he
plan polyme s. These enzymes can also deg ade a a ie y
o chemicals, including en i onmen al pollu an s (C aw-
o d 2006) such as polycyclic a oma ic hyd oca bon.
Success ul polycyclic a oma ic hyd oca bon biodeg a-
da ion is b ough abou by di e en ca abolic ac i i ies,
such as me abolic capabili ies, he induc ion o speci ic
enzymes, and he p esence o a ou able o ganisms cap-
able o deg ada ion (Al-Hawash e al. 2018) unde
a ou able condi ions.
The deg ada ion o polycyclic a oma ic hyd oca bons
can be a ec ed by condi ions such as empe a u e, oxygen,
pH, and nu ien a ailabili y. Tempe a u es can a ec he
physical and chemical composi ion o polycyclic a oma ic
hyd oca bons: a low empe a u es, he deg ada ion a e is
Fungal Di e si y (2019) 97:1–136 83
123
slow due o he dec eased enzyma ic ac i i ies (Bish e al.
2015). Polycyclic a oma ic hyd oca bon deg ada ion can
ac ually occu a a wide ange o empe a u es acco ding o
medium: he maximum deg ada ion was documen ed o be
in he ange o 30 o 40 °C in soil en i onmen s, 20 o 30 °
C in ma ine en i onmen s, and 15 o 20 °C in esh wa e
en i onmen s (Al-Hawash e al. 2018). Oxygen concen-
a ion is also impo an in he biodeg ada ion p ocess.
Biodeg ada ion can be a i s bes in highly oxygena ed
en i onmen s. Though he deg ada ion o polycyclic a o-
ma ic hyd oca bons can also occu a negligible a es unde
anae obic en i onmen s (Ha i ash and Kaushik 2009), he
p ocess is no as apid as unde ae obic condi ions (G -
ishchenko e al. 2000). The pH alue should also be aken
in o accoun in he success ul deg ada ion o polycyclic
a oma ic hyd oca bons, as i egula es he passage o small
molecules and ions in he biological memb ane and a ec s
he ca aly ic eac ion balance. In gene al, ungi would
p e e nea ly neu al pH o maximize hei deg ada ion
ac i i y, al hough hey can also ole a e acidic condi ions
(Bonomo e al. 2001). Nu ien s can also become a limi ing
ac o in he p ocess o biodeg ada ion. The concen a ion
as well as he a io o ce ain nu ien s such as ca bon,
ni ogen, i on and phospho ous can a ec he g ow h and
spo ula ion o hyd oca bon-deg ading ungi (Za a and
Co e
´s-Espinosa 2015). The chemical composi ion o
polycyclic a oma ic hyd oca bons is ye ano he ac o ha
can g ea ly a ec he success o polycyclic a oma ic
hyd oca bon deg ada ion. The highe he molecula weigh ,
he mo e ecalci an polycyclic a oma ic hyd oca bons a e
in he en i onmen , hus aking much longe o be deg aded
(Fedo ak and Wes lake 1981).
Basidiomyce es use a a ie y o mechanisms o com-
ple ely deg ade o ganic compounds such as hyd oca bons.
In gene al, bo h oxida i e and educ i e eac ions a e
equi ed o he comple e me abolism o hyd oca bon
compounds. The i s s ep in deg ada ion occu s a he
in a-cellula le el in he o m o oxida ion and he in e-
g a ion o oxygen wi h he aid o he enzyma ic ca alys s
pe oxidases and oxygena es (Al-Hawash e al. 2018).
Basidiomyce es sec e e hese enzymes o ca alyse bo h he
di ec and indi ec oxida ion o chemicals. The enzymes,
which a e oxido educ ases, aid in he de oxi ica ion o oxic
o ganic compounds h ough biochemical eac ions, which
in u n ans o m polycyclic a oma ic hyd oca bons s ep by
s ep in o in e media es o he cen al in e media y me a-
bolisms (such as he ica boxylic acid cycle). The ac ion o
oxido educ ases ende s he con aminan s and xenobio ics
in o ha mless compounds ha can be easily deg aded u -
he (ITRC 2002). Fo ins ance, he ligninoly ic ungus,
Pleu o us os ea us, can deg ade phenan h ene in o less
ha m ul compounds, including 2,2′-diphenic acid (Fig. 47).
Whi e- o basidiomyce es p oduced non-speci ic ex a-
cellula ligninoly ic enzymes consis ing o h ee g oups:
lignin pe oxidase (LiP), manganese-dependen pe oxidases
(MnP), and laccase (Ho ich e e al. 2001), all o which
a e essen ial o he ans o ma ion and mine aliza ion o
o ganic pollu an s (Wang e al. 2009) such as polycyclic
a oma ic hyd oca bons. The gene a Ganode ma (Ag awal
e al. 2018), A milla ia (Hadiba a a and K is an i 2013),
Cop inus (Li e al. 2009), Ma asmiellus (Viei a e al.
2018), Pleu o us (Hadiba a a and Teh 2014; Li e al. 2009),
Pycnopo us (Munusamy e al. 2008) and Phane ochae e
(Wang e al. 2009) we e able o deg ade polycyclic a o-
ma ic hyd oca bon moie ies such as an h acene, py ene,
phenan h ene and benzo[a]py ene (Table 22).
Many ungal species, and in pa icula whi e- o basid-
iomyce es, ha e demons a ed he abili y o deg ade poly-
cyclic a oma ic hyd oca bons unde labo a o y condi ions;
howe e , hese p ocesses equi e u he in es iga ion in
he ield, and o da e a limi ed numbe o s udies ha e
es ed he e icacy o hese ungi in he deg ada ion o
polycyclic a oma ic hyd oca bons wi hin ypical en i on-
men al condi ions. The placemen o ungi in o he en i-
onmen equi es u he s udies o e alua e hei impac on
o he o ganisms. In ensi e s udies should also be con-
duc ed in o analy ical chemis y and gene ic enginee ing
ools which could help in success ul bio emedia ion o
inc ease ungal e iciency in deg ading hyd oca bons and
o he ecalci an con aminan s. Fu he mo e, h ough he
op imiza ion o adso p ion, bioa ailabili y and mass
ans e o polycyclic a oma ic hyd oca bons, scien is s
could enhance he a e o bio emedia ion. This could p o-
ide one e ec i e means o mi iga ing en i onmen al
pollu ion.
44. Can ungi help modi y he sus ainable soil
enhance biocha ?
Biocha has achie ed popula i y as a sus ainable soil
enhance . Biocha is de i ed om biomass such as lea es,
o es y and ag icul u al esidue, and animal manu e
(Spokas 2010; Shackley e al. 2012). This biomass is
con e ed in o a highly po ous, ca bonaceous p oduc
h ough a con olled py olysis p ocess, namely he mo-
chemical decomposi ion in he absence o oxygen (p e-
en ing combus ion). In his way, i is di e en om
cha coal. While cha coal p oduces ene gy, biocha is used
in ca bon seques a ion, en i onmen al managemen , and
soil amendmen s (Lehmann and Joseph 2009; Wa nock
e al. 2007).
Biocha is added o poo ly pe o ming o con amina ed
soil as a means o inc easing he ecalci ance o o ganic
soil ma e in a sus ainable manne . Due o i s polycon-
densed a oma ic s uc u es, he added biocha can emain
84 Fungal Di e si y (2019) 97:1–136
123
in he soil o cen u ies o millennia, hus con ibu ing
highe le els o a oma ic compounds o he soil o e long
pe iods o ime. Impo an physicochemical p ope ies o
he e alua ion o biocha u ilized in soil ha e been de ined:
pH, ola ile compounds con en , ash con en , bulk densi y,
wa e -holding capaci y, po e diame e and olume, and
speci ic su ace a ea (Sohi e al. 2010). The o igin o he
biomass o eeds ock and he py olysis condi ions, he e-
o e, a e he key ac o s go e ning he physicochemical
p ope ies o biocha . Wi hin he py olysis p ocess, em-
pe a u es be ween 400 and 500 °C p oduce highe amoun s
o biocha (Gaun and Lehmann 2008; Qamb ani e al.
2017). While py olysis occu s mo e apidly a high em-
pe a u es, a slowed py olysis p ocess can p oduce a sub-
s an ially highe quan i y o biocha p oduc . The yields o
ash- ee biocha we e posi i ely co ela ed wi h he cellu-
lose, hemicellulose and lignin con en s o eeds ock; he
biomass samples possessing highe lignin con en p oduced
highe amoun s o biocha , and he samples o high ash
con en hampe ed biocha p oduc ion (Sun e al. 2017).
When inco po a ed in o soils, biocha exhibi s a na u al
oxida ion h ough he o ma ion o unc ional g oups.
These g oups a e dependen on he empe a u e employed
o p oduce he biocha . Thus, biocha s a e edox ac i e and
as such con ibu e o he educ i e ans o ma ion o
o ganic con aminan s in soil by acili a ing elec on ans-
e om bulk chemical elec on dono s (e.g. phenolic
moie ies a ising om he lignin in he o iginal biomass) o
he ecei ing o ganic compounds (e.g. quinone–hyd o-
quinone moie ies) and edox-ac i e me als (e.g. i on,
manganese, coppe ), e e sibly dona ing and ecei ing up
o 2 mmol elec ons pe g am o biocha (Klu
¨p el e al.
2014). Biocha -media ed mic obial elec on shu ling has
also been conside ed as an impo an p ocess in soil
O
OH
OH
OH
OSO
3
OH
OH
O
O
COOH
COOH
PHENANTHRENE
s ep 1. OXIDATION
(CYTOCHROME P450
MONOXYGENASE)
PHENANTHRENE 9,10-OXIDE
S ep 2. HYDROLYSIS
(EPOXIDE HYDROLYSIS)
ans-9,10-
PHENANTHRENE
DIHYDRODIOL 9-O-(HYDROXY- aNs-9,10-
DIHYDROPHENANTRYL)
SULFATE
s ep 3.
CONJUGATION
WITH SULFATE
9,10-DIHYDROPHENANTHRENE
S ep4
S ep 5B
9,10-PHENANTHRENEQUINONE
2, 2'-DIPHENIC ACID
CO
2
S ep 5A
LIGNINOLYTIC RING
CLEAVAGE ENZYMESS
S ep6
Fig. 47 P oposed pa hway o
he deg ada ion o phenan h ene
by he ligninoly ic ungus
Pleu o us os ea us (Bezalel
e al. 1996; Aus e al. 2003;
Gup e e al. 2016)
Fungal Di e si y (2019) 97:1–136 85
123

emedia ion and o he biogeochemical eac ions (Yu e al.
2016), leading o an inc ease in mic obial g ow h while
educing Fe(III) mine als in he soil (Kapple e al. 2014).
The e ec s o biocha on soil e ili y ha e been
demons a ed h ough he pH inc ease o he acid ound in
soils (Van Zwie en e al. 2010), and he bene i s in high
nu ien le els and e en ion h ough he ions abso p ion
(Liang e al. 2006). Howe e , biocha has also been shown
o bo h s abilize and change soil biological communi y
composi ion and abundance, depending on he biomass
sou ce and he empe a u e used in he py olysis eac ion
(Kim e al. 2012; Lo enz and Lai 2014). Such changes may
a ec soil s uc u e and nu ien cycles (Gaskin e al. 2010;
Rillig and Mummey 2006; S eine e al. 2008), he eby
indi ec ly a ec ing plan g ow h (Wa nock e al. 2007).
Rhizosphe e bac e ia and ungi may also di ec ly p omo e
he g ow h o plan s (Compan e al. 2010). Soil ungi (e.g.
sap o ophs, pa hogens and myco hizae) espond di e -
en ly o biocha applica ions. Sap o ophic ungi ha e he
po en ial o modi y biocha in he soil h ough he colo-
niza ion o he po es p esen in he s uc u e, and his can
lead o decomposi ion (A kinson e al. 2010; Lipczynska-
Kochany 2018). Ce ain a buscula myco hizae a e able o
inc ease hei oo coloniza ion si es in he p esence o
biocha , enhancing he a ailabili y o phospha e o he
plan , and he eby nega ing he need o add a i icial
e ilize s.
Fungal ex acellula enzymes a e he agen s o bo h
coloniza ion and decomposi ion, and a e becoming
inc easingly common ools o examining soil mic obial
esponse in clima e change expe imen s (Weedon e al.
2011). Sap o ophic ungi a e conside ed o be e icien
Table 22 Deg ada ion o polycyclic a oma ic hyd oca bons by enzymes om basidiomyce es
Enzyme Basidiomyce e s ain Polycyclic a oma ic hyd oca bon
moi ies
Pe cen age o deg ada ion
(%)
Re e ences
Laccase “Ganode ma lucidum”
a
Phenan h ene 99.65 Ag awal e al. (2018)
Py ene 99.58
Pycnopo us sanguineus Phenan h ene 90.00 Munusamy e al. (2008)
Py ene 96.00
An h acene 37.00
A milla ia sp. Py ene 63.00 Hadiba a a and K is an i
(2013)
Pleu o us e yngii An h acene 99.90 Li e al. (2009)
Benzo[a]py ene 87.50
Aga icus bispo us An h acene 89.80
Benzo[a]py ene 48.60
Pleu o us os ea us An h acene 38.00
Benzo[a]py ene 31.00
Cop inus coma us An h acene 9.80
Benzo[a]py ene 9.30
Lignin pe oxidase “Ganode ma lucidum” Phenan h ene 99.65 Ag awal e al. (2018)
Py ene 99.58
Phane ochae e
ch ysospo ium
Phenan h ene 72.77 Wang e al. (2009)
Py ene 51.16
Benzo[a]py ene 25.50
Ma asmiellus sp. Py ene 100.00 Viei a e al. (2018)
Manganese
pe oxidase
“Ganode ma lucidum” Phenan h ene 99.65 Ag awal e al. (2018)
Py ene 99.58
Phane ochae e
ch ysospo ium
Phenan h ene 72.77 Wang e al. (2009)
Py ene 51.16
Benzo[a]py ene 25.50
a
The axonomy o “Ganode ma lucidum” gi en in he pape by Ag awal e al. (2018) is doub ul since his species has ne e been sa ely eco ded
om India
86 Fungal Di e si y (2019) 97:1–136
123
deg ade s o lignocellulosic biomass due o he wide
spec um o ex acellula enzymes hey p oduce. Thei
p oduc ion and ac i i ies a e s ongly a ec ed by empe -
a u e, mois u e and pH. Many s udies ha e been pe o med
on he in luence o empe a u e and mois u e on he
mic obial ecosys em o soils and he concomi an e ec on
global enzyme pool composi ion and size (Schimel e al.
2007; Sowe by e al. 2005). Enzyme pool size is con olled
by he a e a which enzymes a e p oduced by mic obes
ela i e o he a e a which hey a e deg aded by he
en i onmen . The p oduc ion o hese ex acellula
enzymes incu s a cos o he mic oo ganism in e ms o
ene gy and nu ien s, and so mic obes p oduce ce ain
enzymes a ge ing speci ic compounds ich in ca bon,
ni ogen o phospho ous. Mois u e le els in luence he
di usion o subs a es, he hyd a ion s a e o he indi idual
enzymes, and he a e o wa e eac i i y.
Due o he chemical na u e o biocha , i may be pos-
sible o use ungi di ec ly a ached o he biosou ced
ma e ial o o use ungi in solid-s a e e men a ion condi-
ions o p e ea he biocha p io o soil addi ion (a ype o
compos ing). Figu e 48 p o ides a scanning elec on
mic oscopy (SEM) image o ield-aged biocha bu ied in
ag icul u al soil in which hyphal agmen s o ungi we e
ixed on he biocha su ace. I is also possible, h ough a
mo e bio echnologically sophis ica ed app oach, o ha ness
he powe o hese sec e ed enzymes o modi y he
physicochemical p ope ies o he exposed hyd oxyl and
ca bonyl g oups on he su ace o he biocha . This will
make hem mo e unc ionally ac i e as a soil amendmen
o he s imula ion o he exis ing mic obial communi ies.
The s uc u e o biocha is simila o lignin, and so he
edox- esponsi e enzymes, such as laccases and heme-
pe oxidases p oduced by Basidiomyce es, Ascomyce es
and so - o ungi such as Chae omium globosum,Phialo-
pho a malo um, and P. mu abilis a e designed o modi y
hese s uc u es, and o gene a e hyd oxyl adicals (Gao
e al. 2018). These ungi also con ol he a ailabili y o
me al ions in he sys em, ei he h ough hei inco po a ion
in o he p o ein s uc u e as co- ac o s, o chela ed in
o ganic acids. While his ex acellula p ocess is designed
o aid he ungus in he lignin deg ada ion p ocess, hese
enzymes and chela o s could also be a way o con ol he
elease o cap i a ion o me als in soils. A modi ied bio-
cha , wi h inc eased su ace-ac i e g oups, would enhance
he soil e en u he , mos no ably he ac i i y o he na -
u al soil mic obiome, including myco hizal ungi. This in
u n would u he imp o e he wa e dynamics, nu ien
cycling, and supp ession o c op diseases, he eby
enhancing he p oduc i i y o he soil and he c ops ha a e
cul i a ed in i , while a he same ime con ibu ing o
ca bon seques a ion and educed ai con amina ion in u al
a eas o he wo ld.
Commodi ies
Fungi ha e been exploi ed bo h indus ially and comme -
cially in many ways especially when aluable commodi ies
a e in ol ed. These o ganisms o e unique ad an ages in
bio echnology as hey can be easily cul u ed, ep oduce
quickly and ha e sho li e cycles. In his sec ion we
Fig. 48 The scanning elec on
mic og aphs o ield-aged
biocha bu ied in ag icul u al
soil, showing he ou e su ace
o biocha soil in e ace
(Quilliam e al. 2013; wi h
pe mission), wi h he a ow
indica ing an example o po e
blockage (a); spa ial
he e ogenei y and spa si y o
in e nal mic obial colonisa ion
(b); in e nal colonisa ion by
hyphal and single-celled
mic obes (a ows) (c,d)
Fungal Di e si y (2019) 97:1–136 87
123
discuss some o he many non- ood commodi ies de i ed
om ungi.
45. Fungi and cosme ics
Fungi a e used as ing edien s in nume ous cosme ic p od-
uc s, including in some o he e y expensi e b ands. The
bene icial claims a e all-encompassing, bu many ha e ye
o be p o en. As he uses o ungi in cosme ics was
e iewed by Hyde e al. (2010), which includinges, skin
whi ene s, mois u ize s, an i-aging, shampoos and many
o he s we e e iewed by Hyde e al. (2010), we b ie ly
summa ize he opic he e. The demand o cosme ic
p oduc s has apidly inc eased, and; hence cosme ics has
ha e become a wo ldwide indus y (Hyde e al. 2010).
Cosme ics a e mainly classi ied as cosmeceu icals, applied
ex e nally o he skin, such as c eams, lo ions o oin men s,
and nu icosme ics, which a e consumed as die a y sup-
plemen s (Hyde e al. 2010). Apa om makeup, cosme-
ceu icals a e ca ego ized as an i-aging, an i-w inklinge,
skin e i alizinga ion, skin whi ening, an i-oxidan and
mois u izing p oduc s. To a oid any ca cinogenic e ec s,
he e has been a ecen end owa ds na u al cosme ics,
such as ungi-based p oduc s (Hyde e al. 2010; Imho
e al. 2011; Mohd-Nasi and Mohd-Se apa 2018). Fu -
he mo e, he po en ial o ungi o be u ilized as “bio ac-
o ies” o p oduce nanopa icles in he cosme ic indus y is
cu en ly being explo ed (El Enshasy e al. 2018).
Ascomyco a and Basidiomyco a a e ex ensi ely used in
he cosme ic indus y (Hyde e al. 2010). Seconda y
me aboli es ex ac ed om he mycelia o ui ing bodies
and ing edien s om ungal e men a ion a e used as cos-
me ic ing edien s. Aspe gillus species (Hyde e al. 2010)
and Rhizopus species (Muco omyco a) a e used in he
p oduc ion o lac ic acid, which is a main ing edien in bo h
an i-aging and skin whi ening cosme ics. Lac ic acid is
mainly used o hyd a e and make he skin smoo h. Addi-
ionally, in peeling lo ions, lac ic acid is con ained in
highe concen a ions and helps o emo e he ou e laye
o he skin (Zhang e al. 2007). Fungi a e u ilized in he
p oduc ion o an i-oxidan s, a y acids and polysaccha ides
in an i-aging p oduc s, such as he chi in-glucan complexes
o Aspe gillus nige and some mush oom species (Syny -
sya e al. 2009; Vyso skaya e al. 2009).
Eicosapen aenoic acid is a a e omega a y acid used in
an i-aging p oduc s. I is ex ac ed om Mo ie ella species
(Wang e al. 2007). Mo ie ella and Rhizopus species
p oduce γ-linolenic acid. This compound is used as an an i-
in lamma o y agen and acili a es heal hy skin (K is
ˇ o ı
´-
ko a
´e al. 1991). Spo o ichum p uinosum is used o
p oduce melanocy ic enzymes h ough a subme ged ae o-
bic e men a ion p ocess. Melanocy ic enzyme is used in
some skin whi ening cosme ics o ac i a e he
depigmen a ion o he skin (Moho c
ˇic
ˇe al. 2007). To ea
neu ode ma i is and scle ode ma i is, an ex ac ob ained
om T emella sp. is used. Ex ac s o Ophioco dyceps
sinensis and T emella uci o mis a e u ilized o inc ease he
mois u ising e ec in ce ain cosme ic p oduc s (Hyde
e al. 2010) (Fig. 49).
46. Aga wood
Aga wood is an economically aluable esinous hea wood
p oduc de i ed om wounded ees o he amily Thy-
malaeaceae (No iyan i e al. 2010; Subasinghe e al. 2012;
Peng e al. 2015a; Chowdhu y e al. 2016; Chen e al.
2018b). Aga wood incenses a e used o ag ance in soaps
and shampoos and ha e a pleasan a oma and gene al
pe ume and a e an elemen o impo an eligious i uals in
Ayu edic, Tibe an and adi ional Eas Asian medicine
(Subasinghe e al. 2012; Rhind 2013; Chowdhu y e al.
2016; Lee and Mohamed 2016;Lo
´pez-Sampson and Page
2018) and as a oma ic ood ing edien s (Liu e al. 2013;
Tan e al. 2019). India as well as he Sou heas Asian
coun ies a e he main manu ac u es o aga wood p oduc s,
while China, India, he Middle Eas and Japan a e he
p ima y consume coun ies. Species o Aquila ia (Adams
e al. 2014; Mohamed e al. 2014; Sel an e al. 2014: Az en
e al. 2019), Gy inops, Ae oxylon and Gonys ylus a e used
o he p oduc ion o aga wood (Subasinghe e al. 2012;
Mohamed e al. 2014; Mohamed and Rasool 2016). Cu -
en ly, aga wood p oducing Aquila ia species a e cul i-
a ed om he home ga den le el o la ge scale plan a ions
in Sou heas Asia, India and sou he n China (Lee and
Mohamed 2016; Az en e al. 2019).
Na u ally, aga wood o ma ion occu s h ough wounds.
The in ec ed issues p oduce oleo esin which is con e ed
o odo i e ous a oma ic aga wood esin (Peng e al. 2015a;
Chowdhu y e al. 2016). When mic obial pa hogens en e
Fig. 49 The King’s Co dy Se um con ains Co dyceps mili a is
ex ac . The ex ac is claimed o acili a e an i-w inkle e ec s and
add mois u e and an ioxidan s o he skin. I is p oduced in he Cen e
o Excellence in Fungal Resea ch in Mae Fah Lung Uni e si y,
Chiang Rai, Thailand
88 Fungal Di e si y (2019) 97:1–136
123
he wound, he de ense mechanism o he ees is igge ed
(Mohamed e al. 2014; Chowdhu y e al. 2016; Az en e al.
2019). Sesqui e penes and 2-(2-phenyle hyl) ch omone
de i a i es a e he key ac i e compounds in aga wood
(Chen e al. 2011; Nae 2011; Mohamed e al. 2014;Li
e al. 2019; Tan e al. 2019).
Aga wood causal agen s a e di ided in o chemical,
physical, and biological agen s. Fungi a e he biological
agen s (No iyan i e al. 2010; Chhipa e al. 2017).
Depending on he s ess, he ee o ms ei he physical o
chemical de ense mechanisms (Mohamed and Rasool
2016; Chhipa e al. 2017). The de ense subs ances p o-
duced ac as biochemical o biological de ense agen s
(Mohamed and Rasool 2016). The wounded o in ec ed
ee s em u ns da k b ownish o black (Fig. 50, Adams
e al. 2014). A e in ec ion aga wood esin is sec e ed by
he ee and deposi ed a ound he wound o numbe o
yea s. Resinous aga wood o m pe umed compounds and
is a a e na u al mechanism which is poo ly unde s ood
(Sen e al. 2015). Vola ile compounds e en ually esul in
aga wood (Tan e al. 2019). O he han na u al aga wood
o ma ion, a i icial aga wood inducing me hods ha e been
de eloped. Biological inocula such as mic obes and ungi
a e key agen s o non-con en ional a i icial aga wood
o ma ion (Az en e al. 2019).
Resea ch has been ca ied ou o de e mine which ungi
a e esponsible o aga wood p oduc ion and some o he
isola ed axa a e lis ed in Table 23. Howe e , he ole o
indi idual ungi needs ex ensi e esea ch o es ablish
which species a e impo an in he p ocess.
47. Fungal enzymes
Enzymes a e bioca alys s ha a e in ol ed in ca alysis
eac ions wi hou needing ex eme condi ions, such as e y
high empe a u es, high p essu es o co osi e en i on-
men s, all o which a e o en equi ed in chemical p o-
cesses. Enzymes o en o e a compe i i e ad an age when
compa ed o chemical ca alys s. The enzyma ic app oach is
en i onmen ally iendly, as i equi es mild condi ions and
does no no mally esul in he p oduc ion o oxic by-
p oduc s (Chapla e al. 2012). Enzymes a e used o ca alyze
eac ions in p oduc ion p ocesses o se e al sec o s
including indus ial biocon e sion (bioca alys ), en i on-
men al bio emedia ion, ag icul u al sec o s and also bio-
ans o ma ions o nume ous compounds such as
la onoids (Das and Rosazza 2006; Wohlgemu h 2010;
Choi e al. 2015). The e a e se e al sou ces o enzymes
including animals, plan s and mic oo ganisms (bac e ia,
ungi and p o is s). Mic obial enzymes ha e gene ally been
used because o hei easie isola ion in high amoun s, low-
cos p oduc ion, s abili y a a ious ex eme condi ions,
and hei co-compounds, which a e also mo e con ollable
and less ha m ul. Mic obial enzymes sec e ed in o he
media a e highly eliable o indus ial p ocesses and
applica ions. Mic obes isola ed om di e en sou ces e en
among species and s ains o he same genus may p oduce
a ying le els o enzymes o di e ing p ope ies.
Fungal enzymes ha e a ac ed a en ion o se e al
applica ions because ungi can g ow on low cos ma e ials
and sec e e la ge amoun s o enzymes in o he cul u e
medium, which eases downs eam p ocessing (Ani ha and
Palani elu 2013). Se e al ungal enzymes a e a ailable
comme cially including amylases, cellulases, lipases,
phy ases, p o eases, and xylanases (Saxena e al. 2005;
S ilakshmi e al. 2015). The posi i e en i onmen al impac
o he p oduc ion p ocesses is o gene al in e es and he
use o enzyma ic eac ions ins ead o o ganic sol en s o
chemical eac ions is highly alued. Figu e 51 and
Table 24 show examples o impo an ungal enzymes and
he enzyme sou ces ha a e used in many applica ions, bu
only a ew ungal s ains mee he c i e ia o comme cial
p oduc ion.
Mos applica ions o enzymes in he ood indus y ha e
ocused on hyd oly ic eac ions (Akoh e al. 2008; Choi
e al. 2015). Glycoside hyd olases and β-galac osidase a e
Fig. 50 Ba ks o Gy inops
walla Gae n. (Thymelaeaceae)
in Sba agmuwa Uni e si y
p emises, S i Lanka 2018
aHeal hy ba k, b,cdamaged
ba k (Pho o c edi : H.A.T.
Chin haka)
Fungal Di e si y (2019) 97:1–136 89
123
g ade uma ic acid is adminis e ed in he managemen o
pso iasis in humans (Balak 2015) and has shown o sig-
ni ican ly educe me hane emission by ca le, when added
as a supplemen in ca le eed (Roa Engel e al. 2008). I
also has applica ions in ood and be e age indus y as an
acidulan and la o enhancing agen . Fuma ic acid can
Table 25 O ganic acids p oduced by ungi and di e si y o hei applica ions
O ganic acids O ganisms Applica ions Chemical o mula Molecula s uc u e
Ci ic acid Aspe gillus awamo i
Aspe gillus la us
Aspe gillus onsecaeus
Aspe gillus nidulans
Aspe gillus nige
Aspe gillus phoenicis
Aspe gillus sai oi
Aspe gillus wen ii
Ya owia lipoly ica
Cosme ics
Food and be e ages
Me al cleaning
Pha maceu icals
Toile ies
C
6
H
8
O
7
OH
OH
O
OH
OH
O
OH
Fuma ic acid Rhizopus a hizus
Rhizopus o mosa
Rhizopus nig icans
Rhizopus o yzae
Bio-polyme s
Ca le eed
Food and be e ages
Pha maceu icals
C
4
H
4
O
4
O
OH
OH
O
Gluconic acid Aspe gillus nige De i a iza ion eac ions
Food and be e ages
C
6
H
12
O
7
OH
OH
OH
OH
OH
OOH
I aconic acid Aspe gillus e eus
Saccha omyces ce e isiae
Us ilago maydis
Coa ings
De e gen s
Polyme s (poly-MMA)
Rubbe indus y
Supe -abso ben s
C
5
H
6
O
4
OH
O
O
OH
Lac ic acid Recombinan yeas s ains
Rhizopus o yzae
Biodeg adable polyme s
Cosme ics
Food indus y
O al hygiene p oduc s
Bio-polyme s
De i a iza ion eac ions
C
3
H
6
O
3
OH
OH
O
Succinic acid Rhizopus sp. C
4
H
6
O
4
OOH
OOH
96 Fungal Di e si y (2019) 97:1–136
123

unde go de i a iza ion eac ions o p oduce malic acid and
L-aspa ic acid (Goldbe g e al. 2006; Roa Engel e al.
2008). Bio-based uma ic acid is p oduced by he e -
men a ion o di e en subs a es such as glucose by Rhi-
zopus a hizus, R. nig icans, and R. o yzae, molasses by R.
a hizus and cassa a bagasse by R. o mosa (Table 25)
(Roa Engel e al. 2008; Xu e al. 2012).
Gluconic acid
Since he chemical s uc u e o gluconic acid combines
bo h, ca boxylic and alcohol unc ional g oups, i can
unde go a ious de i a iza ion eac ions including in a
molecula es e i ica ion. Gluconic acid has applica ions in
he ood and be e age indus y as a senso y p ope y
enhance , acidi y egula o and p ese a i e o pickled
ood and p ocessed mea p oduc s (Cane e-Rod iguez e al.
2016). Gluconic acid is p oduced by su ace o subme ged
e men a ion p ocedu es wi h a ious ypes o inpu
ma e ials such as s a ch, lignocellulosic biomass, suga -
cane molasses, whey, was e pape , igs, banana mus and
g ape mus as ca bon sou ce using Aspe gillus nige s ains
(Table 25) (Cane e-Rod iguez e al. 2016). Du ing he
e men a ion p ocess, glucose in he medium is con e ed
ex acellula ly by he enzyma ic eac ion o glucose oxi-
dase by A. nige (Magnuson and Lasu e 2004).
I aconic acid
I aconic acid has applica ions in de e gen s, coa ings and
in he ubbe indus y. Poly(ac ylamide-co-i aconic acid) a
supe abso ben polyme which is used o abso b aqueous
solu ions is also de i ed om i aconic acid (Choi e al.
2015). The mos on demand indus ial scale applica ion is
he con e sion o i aconic acid o me hyl me hac yla e
(MMA) and he p oduc ion o poly MMA, commonly
known as Plexiglass (Becke e al. 2015; Choi e al. 2015).
The acid is gene ally p oduced ia e men a ion o glucose
using Aspe gillus e eus. Fu he mo e, Us ilago maydis
and Saccha omyces ce e isiae a e also capable o p o-
ducing i aconic acid by glucose e men a ion (Table 25)
(Becke e al. 2015).
Lac ic acid
Lac ic acid is widely used in ood indus y in yoghu
and cheese p oduc ion, cosme ic indus y in skin ca e
p oduc s, and o al hygiene p oduc s (Ma inez e al. 2013).
One o he mos impo an uses o lac ic acid is he man-
u ac u ing o polylac ic acid which has applica ions in he
ex ile indus y and ood packaging u ensils (Saue e al.
2008; Bozell and Pe e sen 2010; Ma inez e al. 2013).
Lac ic acid is mos ly p oduced by e men a ion wi h
lac ic acid bac e ia (Saue e al. 2008); howe e , he
exploi a ion o Rhizopus o yzae has shown p omising
ou comes by p oducing highe i e s o lac ic acid o 280 g/
L as anhyd ous calcium lac a e wi h 0.92 g/g p oduc i i y
o glucose inpu unde ed-ba ch cul u es (Yamane and
Tanaka 2013). Xylose, a pen ose suga de i ed om lig-
nocellulosic biomass hyd olysis, can also be u ilized as an
inpu ca bon sou ce o lac ic acid biosyn hesis. Xylose
e men a ion is ca ied ou by employing ecombinan
yeas s ains (Saue e al. 2010) and R. o yzae, g own in
mine al medium (Magnuson and Lasu e 2004; Maas e al.
2006) (Table 25). The ex acellula elease o amylases by
ungi is an added ad an age o he e men a ion p ocess in
hyd olyzing s a ch om a ious inpu sou ces, especially
by he species o Rhizopus (Ma inez e al. 2013).
Fig. 53 Schema ic ep esen a ion o gene al o ganic acid p oduc ion p ocedu e using ungi
Fungal Di e si y (2019) 97:1–136 97
123
Succinic acid
Succinic acid ac s as a building block componen o he
syn hesis o aluable chemicals, such as 1,4-bu anediol,
e ahyd o u an, γ-bu y olac one, N-me hylpy olidone,
and e en in he syn hesis o bio-based polyme s such as
polybu ylene succina e and polyes e polyols, which may
e en ually eplace con en ional pe ol-de i ed polyme s in
he u u e (Choi e al. 2015). An imp o ed e men a ion
p ocess o Rhizopus species was pa en ed by DuPon o
inc ease he TCA cycle based ca boxylic acid p oduc ion
by limi ing he dissol ed oxygen le els in e men e s
be ween 30 and 80%. Du ing his e men a ion p ocess
uma ic acid, succinic acid and L-malic acid a e p oduced
(Ling and Ng 1989). In a ecen s udy 209.7 g/L succinic
acid i e was ob ained unde ed ba ch e men a ion con-
di ions using Ya owia lipoly ica ed wi h c ude glyce ol as
he ca bon sou ce (Li e al. 2018).
Comme cial scale p oduc ion o o ganic acids is highly
dependen on s ain pe o mance. Since mos o he wild
ype s ains do no p oduce comme cially accep -
able yields, e men a ion condi ions need o be modi ied
acco ding o he equi emen and s ain (Xu e al. 2012). To
mee indus ial scale equi emen s, he wild ype s ains a e
being gene ically modi ied o subjec ed o classical mu a-
genesis wi h he goal o inc ease p oduc ion. Recen ly, i
was epo ed ha he dele ion o he mi ochond ial
uma ase gene and in oduc ion o succina e/ uma a e
anspo e inc eased uma ic acid p oduc ion in Saccha-
omyces ce e isiae (Yin e al. 2015). A high yielding
uma ic acid p oducing Rhizopus o yzae RUR709 s ain
was de eloped by UV and γ- ay mu agenesis and inally
p oduced 32.1 g/L uma ic acid—a concen a ion 1.9- old
highe han he wild ype s ain (Huang e al. 2010). Glu-
cose oxidase de icien mu an s o Aspe gillus ca bona ius
ha e shown inc eased ci ic acid p oduc ion by educing
by-p oduc (gluconic acid) o ma ion h ough an inc ease
o he ca bon lux owa ds he educ i e ica boxylic acid
pa hway (Yang e al. 2014b).
These me abolic enginee ing echniques ha e led o he
indus ial scale p oduc ion o na u al p oduc s by modi y-
ing na u al biosyn he ic pa hways o inc ease p oduc i i y
o syn hesize no el de i a i es o mee he global demand
o o ganic acids.
50. Tex ile dyes
Fungi a e impo an as na u al dye p oduce s in ex ile
indus ies (Mapa i e al. 2010; Chadni e al. 2017). The
ex ile indus y is he la ges consume o o ganic pigmen s
and syn he ic dyes (Mapa i e al. 2010). Tons o dyes a e
los as e luen s and can esul in en i onmen al pollu ion
and se ious human heal h p oblems, especially i hei
elease is no p ope ly ea ed. Colou as ness o washing
and c ocking a e essen ial quali ies o any dye/ ab ic
combina ion. Fungal species ha a e used in ex ile dyeing
a e lis ed in Table 26.
He na
´ndez e al. (2018a) epo ed ha wood o ing
ungi can be used in ex ile dyeing. Sucia mih (2002)
s udied he e ec o colou ing pH and mo dan on ungal
dyes quali y using woolen ya n (Fig. 54). In hei s udy,
h ee isola es o Aspe gillus, h ee isola es o Penicillium,
wo isola es o Paecilomyces, one isola e o Monascus
pu pu eus and one isola e o T ichode ma ha zianum we e
used wi h wo di e en mo dan s (alum and FeSO
4
)by
h ee di e en dying pH (3, 6, and 9). The esul s indica ed
ha low pH alue exhibi ed a s ong colou as well as he
mo dan FeSO
4
p oduced almos da ke colou .
When used in manu ac u ed p oduc s, conce ns ela ed
o he p esence o oxic me aboli es in pigmen s and dyes
p oduced by ungi a e commonly aised. In his ega d, he
co ec iden i ica ion o ungal s ains and he implemen-
a ion o oxici y es s a e key ac o s o ensu e a sa e
en i onmen o wo ke s and ha mless p oduc s o end
use s (He na
´ndez e al. 2018a). Rega ding he b oad
spec um o he ungal pigmen s, ungi including edible
and non-edible mush ooms a e a esou ce o na u al dyes.
The u u e
Func ional genomics and he sea ch o no el
an i-in ec i es
Func ional genomics is he app oach used o s udy unc-
ions and in e ac ions o genes and hei p oduc s in a
speci ic con ex (Liu e al. 2010a; Buza and McCa hy
2013). This equi es sequencing o he en i e genome.
Sequencing echniques ha e come a long way, since he
elease o he i s whole ungal genome o Saccha omyces
ce e isiae (Go eau e al. 1996). Today he combining o
newly a ising echniques like PacBio wi h Illumina o
p o ide ully closed genomes has led o nume ous ungal
genome da abases, such as he ungal genome ini ia i e
(Haas e al. 2011), comp ising o e 100 ungal genomes, o
FungiDB (S ajich e al. 2012) and Ensembl Fungi (Ke sey
e al. 2010) wi h o e 1000 ungal genomes. Ou o many
examples ha a ge a ious p oduc ca ego ies, we will
he e only gi e some examples on wha is easible now o
he seconda y me aboli e biosyn hesis due o he employ-
men o —OMICS and bioin o ma ics ools and syn he ic
bio echnology.
The genomes o he Fungi con ain many genes and gene
clus e s ha encode o po en ially bene icial p oduc s,
including indus ially impo an enzymes as well as sec-
onda y me aboli es. Also he bioin o ma ics ools o he
98 Fungal Di e si y (2019) 97:1–136
123
Table 26 Examples o pigmen s p oduced by ungi
Fungal p oduce Pigmen name/colou Applica ion Re e ences
Ac os alagmus sp. B own and eddish b own A alla e al. (2011)
Aga icus xan hode mus Yellow Hanson (2008)
Al e na ia al e na a Dyeing o wool and silk Sha ma e al. (2012)
B own and eddish b own A alla e al. (2011)
Amani a musca ia Be ains(O ange- ed Li and Obe lies (2005)
Aspe gillus nige B own and eddish b own A alla e al. (2011)
Aspe gillus sp. Yellow Dyeing o co on, silk and silk co on Anchana de i (2014), Kuma e al.
(2017), Sa ka e al. (2017)
Bole ales (Gomphidiaceae
and Suillaceae)
Yellow pul inic acid de i a i es Knigh and Pa enden (1976)
Bispo omyces sp. B own and eddish b own A alla e al. (2011)
Chlo ocibo ia ae uginosa Xylindein/G een Colou as dyeing o co on,
polyamide, polyes e and wool
Webe e al. (2014), Hinsch and
Robinson (2016)
Co ina ius cinnaba inus
(Eu opean oads ool)
Fallacinol/ Da k o ange Gill (1994)
Co ina ius iolaceus S iking deep iole colou Von Nussbaum e al. (1998)
Co ina ius sp. Dime ic an h aquinone de i a i e/
B igh yellow
Velis
ˇek and Cejpek (2011)
Cunninghamella sp. B own and eddish b own A alla e al. (2011)
Cu ula ia luna a Dyeing o wool and silk Sha ma e al. (2012)
De mocybe sanguinea An h aquinone compounds as
aglycones
Hynninen e al. (2000), Ra
¨isa
¨nen
e al. (2000)
De mocybe sp. Dime ic an h aquinone de i a i e/
B igh yellow
Velis
ˇek and Cejpek (2011)
Fusa ium oxyspo um An h aquinone/Pu ple Dyeing o wool Nagia and El-Mohamedy (2007),
He na
´ndez e al. (2018a)
Gymnopilus sp. Yellow-b own s y ylpy one
pigmen s bis-no yangonin and
hispidin
Gill (1994)
Hymenochae aceae
(Inono us,Onnia and
Phellinus)
Yellow pigmen hispolon Lee and Yun (2006)
Hypholoma sp. Yellow-b own s y ylpy one
pigmen s bis-no yangonin and
hispidin
Gill (1994)
Hyg ocybe sp. (wi chs’ ha ) Musca la in/yellow Li and Obe lies (2005)
Penicillium ch ysogenum B own and eddish b own A alla e al. (2011)
Penicillium i alicum B own and eddish b own A alla e al. (2011)
Penicillium miniolu eum Dyeing o web blue goa nappa skin Gup a and Agga wal (2016)
Penicillium mu cianum Yellow Dyeing o wool He na
´ndez e al. (2018a,b)
Penicillium oxalicum B own and eddish b own A alla e al. (2011)
Penicillium egulosum B own and eddish b own A alla e al. (2011)
Penicillium sp. Dyeing o co on and silk Sa ka e al. (2017)
Pholio a sp. Yellow-b own s y ylpy one
pigmen s bis-no yangonin and
hispidin
Gill (1994)
Phyma o ichum sp. B own and eddish b own A alla e al. (2011) es ed
Scy alidium cuboideum D aconin ed Colou as dyeing o co on,
polyamide, polyes e and wool
Colou as en
Webe e al. (2014), Hinsch and
Robinson (2016)
Scy alidium
ganode moph ho um
Yellow Colou as dyeing o co on,
polyamide, polyes e and wool
Webe e al. (2014), Hinsch and
Robinson (2016)
Fungal Di e si y (2019) 97:1–136 99
123
anno a ion o genomes ha e signi ican ly imp o ed and
oday, nex o he long es ablished an iSMASH (Blin e al.
2017), ungi-speci ic algo i hms o iden i ying biosyn-
he ic gene clus e s, like he FunGeneClus e S (Ves h e al.
2016) exis . These ools ha e enabled esea che s o
he e ologously exp ess such gene clus e s in well-known
hos s, such as Aspe gillus nige (Boecke e al. 2018). This
s a egy can be used no only o acili a e an easie p o-
duc ion o a known me aboli e a indus ial scale, bu also
o exp ess p e iously silen gene clus e s, which we e
ound while analysing he genome—a echnique o en
e e ed o as ‘genome mining’, o e ing a whole new
sou ce o he disco e y o no el an i-in ec i es. He e ol-
ogous exp ession o speci ic gene clus e s in a di e en
hos now also allows o he elucida ion o biosyn heses o
known an ibio ics/na u al p oduc s. One o he i s ungal
biosyn hesis s udied in such manne , was his o he
myco oxin icho hecene (Tokai e al. 2007). O e he
Fig. 54 aColou a ia ion on woolen ya n dyed wi h Pu pu eocillium
lilacinum dye wi h di e en mo dan s and dyeing pH. bColou
a ia ion on woolen ya n dyed wi h Penicillium sp. dye wi h di e en
mo dan s and dyeing pH (Fe =FeSO
4
·7H
2
O, A =alum and K =pH
con ol) (cou esy o Sucia mih)
Table 26 con inued
Fungal p oduce Pigmen name/colou Applica ion Re e ences
Suillus g e illei Con ains a leas 11 yellow, o ange
and ed pigmen s
Besl and B esinsky (1997)
Tala omyces aus alis Red Dyeing o wool He na
´ndez e al. (2018a,b)
Tala omyces sp. O ange Mo ales-Oye ides e al. (2017),
He na
´ndez e al. (2018a)
Tala omyces e uculosus Red Adequa e colou one o co on
ab ic wi hou any cy o oxic e ec
Chadni e al. (2017)
The momyces sp. Yellow Dyeing o silk (Poo niammal e al. 2013)
T ichode ma spi ale Yellow He na
´ndez e al. (2018a)
T ichode ma i ens Dyeing o wool and silk and ha e
an i ungal p ope ies
Sha ma e al. (2012)
T ichode ma sp. Dyeing o co on, silk and silk co on Anchana de i (2014)
T icholoma sp. Dime ic an h aquinone de i a i e/
B igh yellow
Velis
ˇek and Cejpek (2011)
Xyla ia polymo pha Blackish b own Kuma e al. (2017)
100 Fungal Di e si y (2019) 97:1–136
123
yea s, many o he s udies on Ascomyco a ha e ollowed,
bu as o ecen ly e en he Basidiomyco a ha e been a -
ge ed o elucida ion o he biosyn hesis o hei seconda y
me aboli es (Lin e al. 2019). Mos ecen ly, he biosyn-
hesis o he an i ungal s obilu ins (see en y on an imy-
co ics and ungicides), has been elucida ed, h ough
exp ession in Aspe gillus o yzae (No iani e al. 2018). In
he u u e, modi ying he biosyn hesis o a ungal
me aboli e in o de o enhance i s p oduc ion a comme cial
scale o o achie e adjus ed, be e bioa ailable d ugs, may
well become he no m. S udies on he egula ion o sec-
onda y me aboli e biosyn hesis (B akhage and Sch oeckh
2010) ha e also been de eloped in model o ganisms and
a e now a ailable o b oad applica ions ac oss he ungal
kingdom. This may soon lead o he disco e y o o ally
no el classes o me aboli es, using genome mining, which
was al eady demons a ed o enzymes (e.g. Dilokpimol
e al. 2018). Figu e 55 illus a es he p oduc ion and iso-
la ion p ocedu e o a bioac i e me aboli e om a basidi-
myce e cul u e, which was ob ained in e y high yields in a
ela i ely sho ime, owing o he ac ha mode n bio-
p ocess echnology and me hods o sys ems biology we e
employed.
Acknowledgemen s This wo k was suppo ed by he S a egic P i-
o i y Resea ch P og am o he Chinese Academy o Sciences, G an
No. XDB31000000. Na i sada Thongklang would like o hank
Thailand esea ch und g an s “S udy o sap obic Aga icales in
Thailand o ind new indus ial mush oom p oduc s” (G an No.
DBG6180015) and Mae Fah Luang Uni e si y g an “Op imal
condi ions o domes ica ion and biological ac i i ies o selec ed
species o Ganode ma” (G an No. 621C1535). K.D. Hyde and
Na i sada Thongklang would like o hanks o Thailand esea ch und
g an s “Domes ica ion and bioac i e e alua ion o Thai Hymenopel-
lis,Oudemansiella,Xe ula and Vol a iella species (basidiomyce es)”
(G an No. DBG6180033). K.D. Hyde hanks he inancial suppo
om he Visi ing P o esso g an a Chiang Mai Uni e si y, Thailand
and KIB. The au ho s acknowledge he con ibu ion o M.M. Vas-
an hakuma i, K.M. Manasa and P. Rajani, in a ious s ages o
p epa a ion o he manusc ip . Saman ha C. Ka una a hna hanks CAS
P esiden ’s In e na ional Fellowship Ini ia i e (PIFI) o unding his
pos doc o al esea ch (Numbe 2018PC0006), and he Na ional Sci-
ence Founda ion. Associa e P o esso R Jeewon hanks Uni e si y o
Mau i ius o suppo . Binu C. Sama akoon o e s he since e g a i-
ude o he “Na ional Resea ch Council o Thailand” (NRCT G an
No. 256108A3070006) o he inancial suppo . Pe e E Mo ime
would like o hank he Na ional Science Founda ion o China and he
Chinese Academy o Sciences o inancial suppo unde he ol-
lowing G an s: 41761144055, 41771063, Y4ZK111B01. M. Doilom
would like o hank Chiang Mai Uni e si y, he 5 h ba ch o Pos -
doc o al O ien a ion T aining Pe sonnel in Yunnan P o ince and he
64 h ba ch o China Pos doc o al Science Founda ion. T.S. Su ya-
na ayanan hanks he Uni ed S a es-India Educa ional Founda ion
(USIEF), New Delhi and he Fulb igh Schola P og am (USA) o he
awa d o a Fulb igh -Neh u Senio Resea che g an o conduc
esea ch in he Depa men o Chemis y and Biochemis y, The Ohio
S a e Uni e si y, USA. Thanks o Resea ch and Resea che s o
Indus ies G an (PHD57I0015) o inancial suppo o Boon iya
Chuankid. Bi he Sanda go is g a e ul o he Deu sche Fo schungs-
gemeinscha (DFG) o a PhD g an . Cla a Chepki ui is indeb ed o a
PhD s ipend om he Ge man Academic Exchange Se ice (DAAD)
and he Kenya Na ional Council o Science and Technology
(NACOSTI). Ke in D Hyde would also like o hank he Na ional
Resea ch Council o Thailand g an s Thailands’ Fungal Di e si y,
Sol ing P oblems and C ea ing Bio echnological P oduc s (G an No.
61201321016). This wo k is pa ly suppo ed by he Depa men o
Fig. 55 S ages o he p oduc ion and isola on o a biologically ac i e
me aboli e om he cul u es o a basidiomyce e (Omphalo us
nidi o mis).aSubme ged cul i a ion in shake lasks. bS i ed ank
e men a ion in a pa allel 1.5 L Bio eac o sys ems. C. Bench-Scale
10 L s i ed ank. D. Column ch oma og aphy o ac iona ion and
compound eco e y using he polyme ic adso ben XAD. E. Elu ed
ac ions om compound pu i ica ion. F. C ys als o pu e compound.
Images by Te esa B iem and Lillibe h Cha e a-Mun
˜oz, HZI,
B aunschweig, Ge many
Fungal Di e si y (2019) 97:1–136 101
123

Bio echnology, Go e nmen o India, New Delhi (Chemical Ecology
o he No h Eas Region (NER) o India: A collabo a i e p og amme
Linking NER and Bangalo e Resea che s; DBT-NER/Ag i/24/2013)
and Indian Council o Ag icul u al Resea ch (ICAR-CAAST-P ojec
F.No./NAHEP/CAAST/2018-19), Go e nmen o India, New Delhi.
Open Access This a icle is dis ibu ed unde he e ms o he
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made.
Re e ences
Abdel-Fa ah GM, Ib ahim AH, Al-Am i SM, Shoke AE (2013)
Syne gis ic e ec o a buscula myco hizal ungi and spe mine
on amelio a ion o salini y s ess o whea (“‘T i icum aes i um
L.” c . 9). Aus J C op Sci 7:1525
Abdelaziz ME, Kim D, Ali S, Fedo o NV, Al-Babili S (2017) The
endophy ic ungus Pi i o mospo a indica enhances A abidopsis
haliana g ow h and modula es Na
?
/K
?
homeos asis unde sal
s ess condi ions. Plan Sci 263:107–115
Abe M, Takaoka N, Idemo o Y, Takagi C e al (2008) Cha ac e is ic
ungi obse ed in he e men a ion p ocess o Pue ea. In J
Food Mic obiol 124:199–203
Ab aham WR, Es ela AB (2016) Fungal me aboli es o he con ol
o bio ilm in ec ions. Ag icul u e 6:37
Adams SJ, Manoha a T, K ishnamu hy K, Kuma TS (2014)
His ochemical s udies on ungal-induced aga wood. Indian J
Plan Sci 5:102–110
Adekunle AE, Guo C, Liu CZ (2016) Lignin-enhanced laccase
p oduc ion om T ame es e sicolo . Was e Biomass Valo i
8:1061–1066
Ad io JL, Demain AL (2003) Fungal bio echnology. In Mic obiol
6:191–199
Aggangan NS, Pollisco MA, B uzon JB, Gilbe o JS (2013) G ow h o
Sho ea con o a Vid. inocula ed wi h eucalyp us ec omyco hiza
ungi in he nu se y and in a logged-o e dip e oca p o es in
Su igao, Philippines. Am J Plan Sci 4:896–904
Ag awal N, Ve ma P, Shahi SK (2018) Deg ada ion o polycyclic
a oma ic hyd oca bons (phenan h ene and py ene) by he
ligninoly ic ungi Ganode ma lucidum isola ed om he ha d-
wood s ump. Bio esou Biop ocess 5:11
Ahmed ME, Rahman A (2014) De ec ion o he pe ec condi ion o
p oduce he annase om Aspe gillus nige a di e en medium.
J Babylon Uni Pu e Appl Sci 22:1363–1371
Aka in MY (2013) Cha ac e iza ion o a β-glucosidase om an edible
mush oom, Lycope don py i o me. In J Food P op 16:1565–
1577
Akihisa T, Uchiyama E, Kikuchi T, Tokuda H e al (2009) An i-
umo -p omo ing e ec s o 25-me hoxypo icoic acid A and o he
i e pene acids om Po ia cocos. J Na P od 72:1786–1792
Akiyama K, Ma suzaki K, Hayashi H (2005) Plan sesqui e penes
induce hyphal b anching in a buscula myco hizal ungi. Na u e
435:824–827
Akoh CC, Chang SW, Lee GC, Shaw JF (2008) Bioca alysis o he
p oduc ion o indus ial p oduc s and unc ional oods om ice.
J Ag ic Food Chem 56:10445–10451
Al-Hawash AB, Alkoo anee JT, Abbood HA, Zhang J e al (2018)
Isola ion and cha ac e iza ion o wo c ude oil-deg ading ungi
s ains om Rumaila oil ield, I aq. Bio echnol Rep 17:104–109
Al-Hazmi AS, Schmi DP, Sasse JN (1982) The e ec o
A h obo ys conoides on Meloidogyne incogni a popula ion
densi ies in co n as in luenced by empe a u e, ungus inoculum
densi y, and ime o ungus in oduc ion in he soil. J Nema ol
14:168
Alananbeh KM, Bouqellah NA, Al Ka NS (2014) Cul i a ion o
oys e mush oom Pleu o us os ea us on da e-palm lea es mixed
wi h o he ag o-was es in Saudi A abia. Saudi J Biol Sci 21:616–
625
Alapi EM, Fische J (2006) Table o selec ed analogue classes. In:
Fische J, Ganellin CR (eds) Analogue-based d ug disco e y.
Wiley-VCH, Weinheim, pp 441–552
Albe mann S, El e T, Teubne A, K ischke W, Hi h T, Tudzynski B
(2013) Cha ac e iza ion o no el mu an s wi h an al e ed
gibbe ellin spec um in compa ison o di e en wild- ype s ains
o Fusa ium ujiku oi. Appl Mic obiol Bio echnol 97(17):7779–
7790
Albe s AW, Chen J, Ku on G, Hun V e al (1980) Me inolin: a
highly po en compe i i e inhibi o o hyd oxyme hylglu a yl-
coenzyme A educ ase and a choles e ol-lowe ing agen . P oc
Na l Acad Sci USA 77:3957–3961
Alexand e J, Raymond E, Kaci MO, B ain EC e al (2004) Phase I and
pha macokine ic s udy o i o ul en adminis e ed weekly o
biweekly in ad anced solid umo pa ien s. Clin Cance Res
10:3377–3385
Alexopoulos CJ, Mims CW, Blackwell M (1996) In oduc o y
mycology, 4 h edn. Wiley, New Yo k
Ali MR, Hoque MS, Ahmed KU, Rahman MH (2010) E ec o whea
b an supplemen s wi h suga cane bagasse on he yield and
p oxima e composi ion o Pleu o us os ea us. Bangladesh J
Mush oom 4:21–26
Allison AC, Eugui EM (2000) Mycophenola e mo e il and i s
mechanisms o ac ion. Immunopha macology 47:85–118
Almeida JR, Be ilsson M, Go wa-G auslund MF, Go sich S, Lide
´nG
(2009) Me abolic e ec s o u aldehydes and impac s on
bio echnological p ocesses. Appl Mic obiol Bio echnol
82:625–638
Alpha CJ, Campos M, Jacobs-Wagne C, S obel SA (2015)
Myco umiga ion by he ola ile o ganic compound-p oducing
ungus Muscodo albus induces bac e ial cell dea h h ough
DNA damage. Appl En i on Mic obiol 81:1147–1156
Al es MJ, Fe ei a IC, Dias JF, Teixei a V, Ma ins A, Pin ado M
(2012a) A e iew on an imic obial ac i i y o mush oom
(Basidiomyce es) ex ac s and isola ed compounds. Plan a Med
78:1707–1718
Al es MJ, Fe ei a IC, Ma ins A, Pin ado M (2012b) An imic obial
ac i i y o wild mush oom ex ac s agains clinical isola es
esis an o di e en an ibio ics. J Appl Mic obiol 113:466–475
Amba i RR, Phang SM, Ra i S, Aswa hana ayana RG (2014)
As axan hin: sou ces, ex ac ion, s abili y, biological ac i i ies
and i s comme cial applica ions—a e iew. Ma D ugs 12:128–
152
Ananbeh KM, Almomany AR (2005) P oduc ion o oys e mush oom
Pleu o us os ea us on oli e cake ag o was e. Di asa Ag ic Sci
32:64–70
Ananbeh KM, Almomany AR (2008) P oduc ion o Oys e mush oom
(Pleu o us os ea us) on oma o u ag o–was e. Di asa Ag ic
Sci 35:133–138
Anchana De i A (2014) Ex ac ion o na u al dyes om ungus—an
al e na e o ex ile dyeing. J Na Sci Res 4:1–7
Ande son PK, Cunningham AA, Pa el NG, Mo ales FJ e al (2004)
Eme ging in ec ious diseases o plan s: pa hogen pollu ion,
clima e change and ag o echnology d i e s. T ends Ecol E ol
19:535–544
102 Fungal Di e si y (2019) 97:1–136
123
And ady AL (2015) Pe sis ence o plas ic li e in he oceans. In:
Be gmann M, Gu ow L, Klages M (eds) Ma ine an h opogenic
li e . Sp inge , Cham, pp 57–72
Ani ha TS, Palani elu P (2013) Pu i ica ion and cha ac e iza ion o an
ex acellula ke a inoly ic p o ease om a new isola e o
Aspe gillus pa asi icus. P o ein Exp Pu i 88:214–220
Anke H, S adle M, Maye A, S e ne O (1995) Seconda y
me aboli es wi h nema icidal and an imic obial ac i i y om
nema ophaous ungi and Ascomyce es. Can J Bo 73:932–939
Ao T, Deb CR, Kh uomo N (2016) Wild edible mush ooms o
Nagaland, India: a po en ial ood esou ce. J Exp Biol Ag ic Sci
4:59–65
Apos olidis C, McLeay F (2016) I ’s no ege a ian, i ’s mea - ee!
Mea ea e s, mea educe s and ege a ians and he case o
Quo n in he UK. Soc Bus 6:267–290
A i Y, Che e D, Hen issa B, Be in JG e al (2013) Cha ac e -
iza ion o sal -adap ed sec e ed lignocelluloly ic enzymes om
he mang o e ungus Pes alo iopsis sp. Na Commun 4:1810
A isoy M (1998) Biodeg ada ion o chlo ina ed o ganic compounds
by whi e- o ungi. Bull En i on Con am Toxicol 60:872–876
A iyawansa HA, Hyde KD, Jayasi i SC, Buyck B e al (2015) Fungal
di e si y no es 111–252 axonomic and phylogene ic con ibu-
ions o ungal axa. Fungal Di e s 75:1–248
A ms ong DW, B own LA (1994) Alipha ic, a oma ic, and lac one
compounds. Biop ocess p oduc ion o la o , ag ance, and
colo ing edien s. Wiley, Hoboken, pp 41–94
A o a DK (2003) Handbook o ungal bio echnology, 2nd edn.
Ma cel Dekke Inc., New Yo k, p 573
A o a DS, Chande M, Gill PK (2002) In ol emen o lignin
pe oxidase manganese pe oxidase and laccase in deg ada ion and
selec i e ligninolysis o whea s aw. In Biode e Biodeg
15:115–120
Ash a i S, Helaly S, Sch oe s HJ, S adle M e al (2017a) Ijuhya
i ellina sp. no ., a no el sou ce o chae oglobosin A, is a
des uc i e pa asi e o he ce eal cys nema ode He e ode a
ilipje i. PLoS ONE 12:e0180032
Ash a i S, S adle M, Dababa AA, Riche - Poeggele KR e al
(2017b) Monocillium gamsii sp. no . and Monocillium bulbil-
losum: wo nema ode-associa ed ungi pa asi ising he eggs o
He e ode a ilipje i. MycoKeys 27:21
Ash a i S, Knapp DG, Blaudez D, Chalo M e al (2018) Inhabi ing
plan oo s, nema odes, and u les—Polyphilus, a new helo-
ialean genus wi h wo globally dis ibu ed species. Mycologia
110:286–299
Asmelash F, Bekele T, Bi hane E (2016) The po en ial ole o
a buscula myco hizal ungi in he es o a ion o deg aded
lands. F on Mic obiol 7:1095
As u i M, Meliala A, Dalais FS, Wahlq is ML (2000) Tempe, a
nu i ious and heal hy ood om Indonesia. Asia Pac J Clin Nu
9:322–325
A alla MM, El-kh isy EAM, Yousse YA, Mohamed AA (2011)
P oduc ion o ex ile eddish b own dyes by ungi. Mal J Mic ob
7:33–40
A kinson CJ, Fi zge ald JD, Hipps NA (2010) Po en ial mechanisms
o achie ing ag icul u al bene i s om biocha applica ion o
empe a e soils: a e iew. Plan Soil 337:1–18
A las R, B agg J (2009) Bio emedia ion o ma ine oil spills: when and
when no — he Exxon Valdez expe ience. Mic ob Bio echnol
2:213–221
A mosuka o I, Cas illo U, Hess WM, Sea s J, S obel G (2005)
Isola ion and cha ac e iza ion o Muscodo albus I-41.3 s, a
ola ile an ibio ic p oducing ungus. Plan Sci 169:854–861
Auld BA (1993) Vege able oil suspension emulsions educe dew
dependence o a mycohe bicide. C op P o 12:477–479
Auld BA (1997) Biohe bicides in biological con ol o weeds. Theo y
and p ac ical applica ion. Aus alian Cen e o In e na ional
Ag icul u al Resea ch, Canbe a, pp 129–134
Aus SD, Swane PR, S ahl JD (2003) De oxi ica ion and me abolism
o chemicals by whi e- o ungi. In: Zhu JJPC, Asu SD, Lemley-
Gan AT (eds) Pes icide decon amian ion and de oxi ica ion.
Ox o d Uni e si y P ess, Washing on, DC, pp 3–14
Ayob FW, Sima ani K, Zainal Abidin N, Mohamad J (2017) Fi s
epo on a no el Nig ospo a sphae ica isola ed om Ca ha-
an hus oseus plan wi h an ica cinogenic p ope ies. Mic ob
Bio echnol 10:926–932
Az en PD, Lee SY, Emang D, Mohamed R (2019) His o y and
pe spec i es o induc ion echnology o aga wood p oduc ion
om cul i a ed Aquila ia in Asia: a e iew. J Fo Res 30:1–11
Babel FJ (1953) The ole o ungi in cheese ipening. Econ Bo 7:27–
42
Babu PD, Bhakya aj R, Vidhyalakshmi R (2009) A low cos
nu i ious ood “ empeh”—a e iew. Wo ld J Dai y Food Sci
4:22–27
Backman PA, Siko a RA (2008) Endophy es: an eme ging ool o
biological con ol. Biol Con ol 46:1–3
Badalyan SM, Ba khuda yan A, Rapio S (2019) Recen p og ess in
esea ch on he pha macological po en ial o mush ooms and
p ospec s o hei clinical applica ion. In: Ag awal DC,
Dhanseka an M (eds) Medicinal mush ooms: ecen p og ess in
esea ch and de elopmen . Publishe Sp inge Na u e Singapo e,
pp 1–70. h ps://doi.o g/10.1007/978-981-13-6382-5_1
Bagchi D, Ghosh D, Konishi T (2014) Clinical aspec s o unc ional
oods and nu aceu icals, 1s edn. CRC P ess, Boca Ra on,
pp 51–76
Bagga J, P amanik SK, Pandey V (2015) P oduc ion and pu i ica ion
o annase om Aspe gillus aculea us using plan de i ed aw
annin. In J Sci Eng Technol 4:50–55
Bai R, Zhang CC, Yin X, Wei J, Gao JM (2015) S ia oids A-F,
cya hane di e penoids wi h neu o ophic ac i i y om cul u es o
he ungus Cya hus s ia us. J Na P od 78:783–788
Bailey KL, Boye chko SM, Langle T (2010) Social and economic
d i e s shaping he u u e o biological con ol: a Canadian
pe spec i e on he ac o s a ec ing he de elopmen and use o
mic obial biopes icides. Biol Con ol 52:221–229
Bailey KL, Pi WM, Falk S, De by J (2011) The e ec s o Phoma
mac os oma on non- a ge plan and a ge weed species. Biol
Con ol 58:379–386
Bailey KL, Falk S, De by JA e al (2013) The e ec o e ilize s on
he e icacy o he biohe bicide, Phoma mac os oma, o con ol
dandelions in u g ass. Biol Con ol 65:147–151
Bailey AM, Albe i F, Kila u S, Collins CM e al (2016) Iden i ica ion
and manipula ion o he pleu omu ilin gene clus e om
Cli opilus passecke ianus o inc eased apid an ibio ic p oduc-
ion. Sci Rep 6:25202
Bajaj R, Huang Y, Geb ech is os S, Mikolajczyk B e al (2018)
T ansc ip ional esponses o soybean oo s o coloniza ion wi h
he oo endophy ic ungus Pi i o mospo a indica e eals al e ed
phenylp opanoid and seconda y me abolism. Sci Rep 8(1):10227
Bakshi M, She ame i I, Meichsne D, Thu
¨ ich J e al (2017)
Pi i o mospo a indica ep og ams gene exp ession in A abidop-
sis phospha e me abolism mu an s bu does no compensa e o
phospha e limi a ion. F on Mic obiol 8:1262
Bal C (2018) Bene i s and uses o mush oom. J Bac e iol Mycol
6:155–156
Balak DMW (2015) Fuma ic acid es e s in he managemen o
pso iasis. Pso iasis 5:9–23
Balak ishnan B, Ka ki S, Chiu SH, Kim HJ e al (2013) Gene ic
localiza ion and in i o cha ac e iza ion o a Monascus
azaphilone pigmen biosyn he ic gene clus e . Appl Mic obiol
Bio echnol 97:6337–6345
Fungal Di e si y (2019) 97:1–136 103
123
Bald ian P (2003) In e ac ions o hea y me als wi h whi e- o ungi.
Enzyme Mic ob 32(1):78–91
Banda a AR, Rapio S, Bha DJ, Kakumyan P e al (2015) Polypo us
umbella us, an edible–medicinal cul i a ed mush oom wi h
mul iple de eloped heal h-ca e p oduc s as ood, medicine and
cosme ics: a e iew. C yp ogamie Mycol 36(1):3–42
Banda a AR, Ka una a hna SC, Mo ime PE, Hyde KD e al (2017)
Fi s success ul domes ica ion and de e mina ion o nu i ional
and an ioxidan p ope ies o he ed ea mush oom Au icula ia
hailandica (Au icula iales, Basidiomyco a). Mycol P og 16(11–
12):1029–1039
Bane jee A, Cha e jee K, Mad as G (2014) Enzyma ic deg ada ion o
polyme s: a b ie e iew. J Ma e Sci Technol 30:567–573
Banik SP, Khowala S, Pal C, Mukhe jee S (2015) P o eomic
app oaches o iden i y no el he apeu ics and nu aceu icals
om ilamen ous ungi. In: Bagchi D, Swa oop A, Bagchi M
(eds) Genomics, p o eomics and me abolomics in nu aceu icals
and unc ional oods, 2nd edn. Wiley, New Yo k, pp 265–295
Bano A, Hussain J, Akba A, Mehmood K e al (2018) Bioso p ion o
hea y me als by obliga e halophilic ungi. Chemosphe e
199:218–222
Banu AR, De i MK, Gnanap abhal GR, P adeep BV e al (2010)
P oduc ion and cha ac e iza ion o pec inase enzyme om
Penicillium ch ysogenum. Indian J Sci Technol 3:377–381
Ba al HO, Webe E, Gams W, Hagedo n G, Liu B, Liu X, Ma son G,
Ma ano a
´L, S adle M, Weiß M (2018) Recommenda ions
abou gene ic names o be p o ec ed o supp essed in he
O biliaceae (O biliomyce es). Mycol P og 17:5–31
Ba oni TJ (2017) Mush ooms o he No heas e n Uni ed S a es and
Eas e n Canada. Timbe P ess, Po land
Ba a SR, Ennos AR, G eenhalgh M, Robson GD e al (2003) Fungi
a e he p edominan mic o-o ganisms esponsible o deg ada-
ion o soil-bu ied polyes e polyu e hane o e a ange o soil
wa e holding capaci ies. J Appl Mic obiol 95:78–85
Ba y D, Williams G, Chan C (2015) Au oma ed analysis o
ilamen ous mic obial mo phology wi h AnaMo . Bio echnol
P og 31:849–852
Bashi KM, Choi JS (2017) Clinical and physiological pe spec i es o
β-glucans: he pas , p esen , and u u e. In J Mol Sci 18:1906
Bashyal B, Wellensiek B, Ramak ishnan R, Fae h SH, Ahmad N,
Guna ilaka AA (2014) Al e oxins wi h po en an i-HIV ac i i y
om Al e na ia enuissima QUE1Se, a ungal endophy e o
Que cus emo yi. Bioo g Med Chem 22:6112–6116
Ba eman B, Wa ne JO, Hu chinson E, Dean T e al (2004) The
e ec s o a double blind, placebo con olled, a i icial ood
colou ings and benzoa e p ese a i e challenge on hype ac i i y
in a gene al popula ion sample o p eschool child en. A ch Dis
Child 89:506–511
Ba a A, Saxena RK (2005) Po en ial annase p oduce s om he
gene a Aspe gillus and Penicillium. P ocess Biochem 40:1553–
1557
Becke J, Lange A, Faba ius J, Wi mann C (2015) Top alue
pla o m chemicals: bio-based p oduc ion o o ganic acids. Cu
Opin Bio echnol 36:168–175
Bee z AE, G ee L (1999) Mush oom cul i a ion and ma ke ing.
ATTRA, Melbou ne
Bei J, Chen Z, Fu J, Jiang Z e al (2009) S uc u e-based agmen
shu ling o wo ungal phy ases o combina ion o desi able
p ope ies. J Bio echnol 139:186–193
Belma es R, Con e as-Esqui el JC, Rod iguez-He e a R, Co onel
AR e al (2004) Mic obial p oduc ion o annase: an enzyme
wi h po en ial use in ood indus y. Lebensm Wiss Technol
37:857–864
Benjamins R, Sche es B (2008) Auxin: he looping s a in plan
de elopmen . Annu Re Plan Biol 59:443–465
Benocci T, Aguila -Pon es MV, Zhou M, Seibo h B, V ies RP (2017)
Regula o s o plan biomass deg ada ion in ascomyce ous ungi.
Bio echnol Bio uels 10:152
Ben ley R (2000) Mycophenolic acid: a one hund ed yea odyssey
om an ibio ic o immunosupp essan . Chem Re 100:380–3826
Be in JG, Na a o D, Cou u ie M, Oli e
´C e al (2012) Explo ing
he na u al ungal biodi e si y o opical and empe a e o es s
owa d imp o emen o biomass con e sion. Appl En i on
Mic obiol 78(18):6483–6490
Besl H, B esinsky A (1997) Chemosys ema ics o Suillaceae and
Gomphidiaceae (subo de Suillineae). Plan Sys E ol 206:223–
242
Besse e A, Puech-Pages V, Kie e P, Gomez-Roldan V e al (2006)
S igolac ones s imula e a buscula myco hizal ungi by ac i-
a ing mi ochond ia. PLoS Biol 4:e226
Beye DM (2003) Basic p ocedu es o Aga icus mush oom g owing.
Pennsyl ania S a e Uni e si y, Uni e si y Pa k, pp 1–16
Bezalel L, Hada Y, Fu PP, F eeman JP e al (1996) Ini ialoxida ion
p oduc s in he me abolism o py ene, an h acene, luo ene, and
dibenzo hiophene by he whi e o ungus Pleu o us os ea us.
Appl En i on Mic obiol 62:2554–2559
Bhale ao TS, Pu anik P (2007) Biodeg ada ion o o ganochlo ine
pes icide, endosul an, by a ungal soil isola e, Aspe gillus nige .
In Biode e io Biodeg ad 59:315–321
Bha MK (2000) Cellulases and ela ed enzymes in bio echnology.
Bio echnol Ad 18:355–383
Bhuiyan SA, C o BJ, James RS, Cox MC (2012) Labo a o y and
ield e alua ion o ungicides o he managemen o suga cane
smu caused by Spo iso ium sci amineum in seedcane. Aus alas
Plan Pa hol 41:591–599
Bilal L, Asa S, Hamayun M, Gul H (2018) Plan g ow h p omo ing
endophy ic ungi Aspe gillus umiga us TS1 and Fusa ium
p oli e a um BRL1 p oduce gibbe ellins and egula es plan
endogenous ho mones. Symbiosis 76:117–127
Bilg ami KS, Sinha SP, Jeswal P (1988) Neph o oxic and hepa o oxic
e ec s o ci inin in mice (Mus musculus). P oc Na l Acad Sci
India B 54(1):35–37
Bills GF, Gloe JB (2016) Biologically ac i e seconda y me aboli es
om he Fungi. Mic obiol Spec 4:VE-0001-2014
Bills GF, Ma ı
´n J, Collado J, Pla as G e al (2009) Measu ing he
dis ibu ion and di e si y o an ibiosis and seconda y me aboli es
in he ilamen ous ungi. SIM News 59:133–147
Bi ch GG, Lindley MG (1985) Alcoholic be e ages. Else ie , London
Bish S, Pandey P, Bha ga a B, Sha ma S e al (2015) Bio emedia ion
o polya oma ic hyd oca bons (PAHs) using hizosphe e ech-
nology. B az J Mic obiol 46:7–21
Bi as V, McCa ney N, Li N, Deme s J (2015) Fusa ium oxyspo um
ola iles enhance plan g ow h ia a ec ing auxin anspo and
signaling. F on Mic obiol 6:1248
Bi ze J, Henkel T, Niki o o AI, Rihne MO, Hende son KA (2017a)
A 90-day o al oxici y s udy o glycolipids om Dac yopinax
spa hula ia in Beagle dogs. Food Chem Toxicol 109:544–551
Bi ze J, Henkel T, Niki o o AI, Rihne MO, Leuschne J (2017b) A
90-day o al oxici y s udy o glycolipids om Dac yopinax
spa hula ia in CD
®
a s. Food Chem Toxicol 109:569–584
Bi ze J, Henkel T, Niki o o AI, Rihne MO, Thomas JA (2017c)
Pha macokine ics, exc e ion balance, and issue dis ibu ion o
[14C]-labeled glycolipids and long chain a y acids om
Dac yopinax spa hula ia in a s. Food Chem Toxicol 109:552–
568
Bi ze J, Henkel T, Niki o o AI, Rihne MO, He be h MT (2018)
De elopmen al and ep oduc ion oxici y s udies o glycolipids
om Dac yopinax spa hula ia. Food Chem Toxicol 120:430–
438
Biz A, Finkle ATJ, Pi ol LO, Medina BS e al (2016) P oduc ion o
pec inases by solid-s a e e men a ion o a mix u e o ci us
104 Fungal Di e si y (2019) 97:1–136
123
was e and suga cane bagasse in a pilo -scale packed-bed
bio eac o . Biochem Eng J 111:54–62
Bjawa AA (2014) Sus ainable weed managemen in conse a ion
ag icul u e. C op P o 65:105–113
Ble e G, G ieco F, Cozzi G, Log ieco A, Viscon i A (2006) Isola ion
o epiphy ic yeas s wi h po en ial o biocon ol o Aspe gillus
ca bona ius and A. nige on g ape. In J Food Mic obiol
108:204–209
Blin K, Wol T, Che e e MG, Lu X e al (2017) an iSMASH
40-imp o emen s in chemis y p edic ion and gene clus e
bounda y iden i ica ion. Nucl Acids Res 45(W1):W36–W41
Blomq is J (2011) Dekke a b uxellensis—a compe i i e yeas o
e hanol p oduc ion om con en ional and non-con en ional
subs a es. Doc o al hesis, Facul y o Na u al Resou ces and
Ag icul u al Sciences Depa men o Mic obiology. Swedish
Uni e si y o Ag icul u al Sciences, Uppsala
Bluemke W, Sch ade J (2001) In eg a ed biop ocess o enhanced
p oduc ion o na u al la o s and ag ances by Ce a ocys is
monili o mis. Biomol Eng 17:137–142
Boa E (2004) Wild edible ungi: a global o e iew o hei use and
impo ance o people (non-wood o es p oduc s). Food &
Ag icul u e O ganiza ion o he Uni ed Na ions, Rome
Bobeck P, Gin e E, Ju co ico a M, Kuniak L (1991) Choles e ol-
lowe ing e ec o he mush oom Pleu o us os ea us in he ed-
i a y hype choles e olemic a s. Ann Nu Me ab 35:191–195
Boecke S, G a
¨ z S, Ke wa D, Adam L e al (2018) Aspe gillus nige
is a supe io exp ession hos o he p oduc ion o bioac i e
ungal cyclodepsipep ides. Fungal Biol Bio echnol 5:7
Bonomo L, Sola i E, Scopelli i R, Flo iani C (2001) The π
complexa ion o alkali and alkaline ea h ions by he use o m
meso-Oc aalkylpo phy inogen and a oma ic hyd oca bons.
Chem Eu J 7:1322–1332
Bonugli-San os RC, Du an LR, Sil a M, Se e LD (2010) P oduc-
ion o laccase manganese pe oxidase and lignin pe oxidase by
B azilian ma ine-de i ed ungi. Enzyme Mic ob Technol 46:32–
37
Boubendi A (1993) Pu i ica ion and biochemical e alua ion o
polyu e hane deg ading enzymes o ungal o igin. Diss Abs In
53:4632
Bou dichon F, Casa egola S, Fa okh C, F is ad JC e al (2012) Food
e men a ions: mic oo ganisms wi h echnological bene icial
use. In J Food Mic obiol 154:87–97
Boye chko SM, Pede sen E, Punja ZK, Reddy MS (1999) Fo mula-
ions o biopes icides. In: Hall FR, Ba y JW (eds) Bio
pes icides: use and deli e y. Me hods in bio echnology, ol 5.
Humana P ess, To owa, pp 487–508
Boye e CD, Temple on GE, Smi h RJ J (1979) Con ol o winged
wa e p im ose (Jussiaea decu ens) and No he n join e ch
(Aeschynomene i ginica) wi h ungal pa hogens. Weed Sci
27:497–501
Bozell JJ, Pe e sen GR (2010) Technology de elopmen o he
p oduc ion o biobased p oduc s om bio e ine y ca bohyd a es-
he US Depa men o Ene gy’s “Top10” e isi ed. G een Chem
12:539–554
B akhage AA, Sch oeckh V (2010) Fungal seconda y me aboli es—
s a egies o ac i a e silen gene clus e s. Fungal Gene Biol
48:15–22
B ea ley FQ, Sane P, Uchida A, Bu slem DFRP e al (2016) Tes ing
he impo ance o a common ec omyco hizal ne wo k o
dip e oca p seedling g ow h and su i al in opical o es s o
Bo neo. Plan Ecol Di e s 9:563–576
B ennan MA, De byshi e E, Tiwa i BK, B ennan CS (2012)
En ichmen o ex uded snack p oduc s wi h cop oduc s om
ches nu mush oom (Ag ocybe aege i a) p oduc ion: in e ac ions
be ween die a y ibe , physicochemical cha ac e is ics, and
glycemic load. J Ag ic Food Chem 60:4396–4401
B iggs RS, A kins E (1966) S udies in c yp ococcal e e . I. Re-
sponses o in ac o ganisms and o a soluble agen de i ed om
c yp ococci. Yale J Biol Med 38:431–448
B own AC, Valie e A (2004) P obio ics and medical nu i ion
he apy. Nu Clin Ca e 7:56
B own AG, Smale TC, King TJ, Hasenkamp R, Thompson RH (1976)
C ys al and molecula s uc u e o compac in, a new an i ungal
me aboli e om Penicillium b e icompac um. J Chem Soc
11:1165–1170
B own MS, Faus JR, Golds ein JL (1978) Induc ion o 3-hyd oxy-3-
me hylglu a yl coenzyme A educ ase ac i i y in human ib ob-
las s incuba ed wi h compac in (ML-236B), a compe i i e
inhibi o o he educ ase. J Biol Chem 253:1121–1128
B ueckne T, Ebe l A, Heumann S, Rabe M, Guebi z GM (2008)
Enzyma ic and chemical hyd olysis o poly(e hylene e eph ha-
la e) ab ics. J Polym Sci A 46:6435–6443
B ugge R, Nunes CS, Hug D, Vogel K e al (2004) Cha ac e is ics o
ungal phy ases om Aspe gillus umiga us and Sa o ya
umiga e. Appl Mic obiol Bio echnol 63:383–389
B um AN, B um AA (2017) Mush oom cul i a ion as an al e na i e
o u al de elopmen in sou h B azil. J Nu Food Sci 7:57
B und e MC (2009) Myco hizal associa ions and o he means o
nu i ion o ascula plan s: unde s anding he global di e si y o
hos plan s by esol ing con lic ing in o ma ion and de eloping
eliable means o diagnosis. Plan Soil 320:37–77
B uns TD, Peay KG, Boyn on P, G ubisha LC e al (2009) Inoculum
po en ial o Rhizopogon spo es inc eases wi h ime o e he i s
4-y o a 99-y spo e bu ial expe imen . New Phy ol 181:463–
470
Buche VVC, Poin ing SB, Hyde KD, Reddy CA (2004) P oduc ion
o wood decay enzymes, loss o mass, and lignin solubiliza ion
in wood by di e se opical esh wa e ungi. Mic ob Ecol
48:331–337
Bucknall RA, Moo es H, Simms R, Hesp B (1973) An i i al e ec s o
aphidicolin, a new an ibio ic p oduced by Cephalospo ium
aphidicola. An imic ob Agen s Chemo he 4:294–298
Budi S, San oso E, Wahyudi A (2010) Iden i ica ion o po en ial ypes
o ungi on es ablishmen aga wood s em o Aquila ia spp.
Ju nal Sil ikul u T opika 1:1–5
Bunyapaiboons i T, Yoip omma a S, S isanoh U, Choowong W e al
(2011) Isa io ins G-J om cul u es o he Lepidop e a pa ho-
genic ungus Isa ia enuipes. Phy ochem Le 4:283–286
Busby PE, Ridou M, Newcombe G (2016) Fungal endophy es:
modi ie s o plan disease. Plan Mol Biol 90:645–655
Bushley KE, Raja R, Jaiswal P, Cumbie JS e al (2013) The genome
o Tolypocladium in la um: e olu ion, o ganiza ion, and exp es-
sion o he cyclospo in biosyn he ic gene clus e . PLoS Gene 9:
e1003496
Buza T, Mcca hy FM (2013) Func ional genomics: applica ions o
p oduc ion ag icul u e. CAB Re 8:1–21
Byle JW, Cobb FW, Pa men e JR (1972) Occu ence and signi -
icance o ungi inhabi ing galls caused by Pe ide mium ha k-
nessii. Can J Bo 50:1275–1282
CPL Business Consul an s (2010) The 2010 wo ldwide biopes icides
ma ke summa y. CAB In e na ional, Walling o d
Cai J, Ma H, Huang F, Zhu D, Bi J, Ke Y, Zhang T (2013) Co ela ion
o be acizumab-induced hype ension and ou comes o me a-
s a ic colo ec al cance pa ien s ea ed wi h be acizumab: a
sys ema ic e iew and me a-analysis. Wo ld J Su g Oncol
11:306
Cambell I (1996) Wild yeas in b ewing and dis illing. In: P ies FG,
Campbell I (eds) B ewing mic obiology, 2nd edn. Chapman &
Hall, London, pp 193–208
Came on DD, Leake JR, Read DJ (2006) Mu ualis ic myco hiza in
o chids: e idence om plan – ungus ca bon and ni ogen
Fungal Di e si y (2019) 97:1–136 105
123
Gue ini L, Angeloni G, Baldi F, Pa en i A (2017) The mal e ec s o
pump-o e s du ing ed wine e men a ion. Appl The m Eng
112:621–626
Guija o B, Melga ejo P, To es R, Lama ca N e al (2007) E ec s o
di e en biological o mula ions o Penicillium equen ans on
b own o o peaches. Biol Con ol 42:86–96
Guillamo
´n E, Ga cı
´a-La uen e A, Lozano M, Ros agno MA, Villa es
A, Ma ı
´nez JA (2010) Edible mush ooms: ole in he p e en ion
o ca dio ascula diseases. Fi o e apia 81:715–723
Guo YX, Qin JZ, Chen JZ, Yang YC (2011) S udy on he p oduc ion
o Ag icus bispo us seasoning by enzyme me hod. J Shanxi Uni
Sci Technol 29:53–57 In Chinese
Gup a S, Agga wal S (2016) Dyeing we blue goa nappa skin wi h a
mic obial colo an ob ained om Penicillium miniolu eum.
J Clean P od 127:585–590
Gup a C, P akash D, Gup a S (2015) Bio echnological app oach o
mic obial based pe umes and la o s. J Mic obiol Exp 2:34–41
Gup e A, T ipa hi A, Pa el H, Rudakiya D, Gup e S (2016)
Bio emedia ion o polycyclic a oma ic hyd oca bon (PAHs): a
pe spec i e. Open Bio echnol J 10:363–378
Gup a S, Summuna B, Gup a M, Annepu SK (2018) Edible
mush ooms: cul i a ion, bioac i e molecules, and heal h bene-
i s. In: Me
´ illon JM, Ramawa K (eds) Bioac i e molecules in
ood. Sp inge , Be lin, pp 1–33
Gu
¨lse C, Peks¸en A (2003) Using ea was e as a new casing ma e ial
in mush oom Aga icus bispo us (L.) Sing. cul i a ion. Bio esou
Technol 88:153–156
Gu
¨n he M, Zibek S, Rupp S (2017) Fungal glycolipids as biosu -
ac an s. Cu Bio echnol 6:205–218
Gu
¨ enc¸ A, Kapucu N, Mehme og
˘lu U
¨(2002) The p oduc ion o
isoamyl ace a e using immobilized lipases in a sol en - ee
sys em. P ocess Biochem 38:379–386
Haas BJ, Zeng Q, Pea son MD, Cuomo CA, Wo man JR (2011)
App oaches o ungal genome anno a ion. Mycology 2:118–141
Hadiba a a T, K is an i RA (2013) Biodeg ada ion and me aboli e
ans o ma ion o py ene by basidiomyce es ungal isola e
A milla ia sp. F022 36: 461. Biop ocess Biosys Eng 36:461–
468
Hadiba a a T, Teh ZC (2014) Op imiza ion o py ene deg ada ion by
whi e- o ungus Pleu o us pulmona ius F043 and cha ac e iza-
ion o i s me aboli es. Biop ocess Biosys Eng 37:1679–1684
Hagedo n S, Kaphamme B (1994) Mic obial bioca alysis in he
gene a ion o la o and ag ance chemicals. Annu Re
Mic obiol 48:773–800
Hai jema CH, Gilmo e SP, Henske JK, Solomon KV e al (2017) A
pa s lis o ungal cellulosomes e ealed by compa a i e
genomics. Na Mic obiol 2:17087
Hall FR (1998) Biopes icides: use and deli e y. Humana P ess,
To owa, pp 233–270
Hamano PS, Kilikian BV (2006) P oduc ion o ed pigmen s by
Monascus ube in cul u e media con aining co n s eep liquo .
B az J Chem Eng 23:443–449
Hameed I, Masoodi SR, Mi SA, Nabi M e al (2015) Type 2 diabe es
melli us: om a me abolic diso de o an in lamma o y condi-
ion. Wo ld J Diabe es 6:598–612
Hameed A, Hussain SA, Yang J, Ijaz MU e al (2017) An ioxidan s
po en ial o he ilamen ous ungi (Muco ci cinelloides).
Nu ien s 9:1101
Hamill RL, Higgens CE, Boaz HE, Go man M (1969) The s uc u e
o beau e icin, a new depsipep ide an ibio ic oxic o A emia
salina. Te ahed on Le 10:4255–4258
Han SY, Hong ZY, Xie YH, Zhao Y, Xu X (2017) The apeu ic e ec
o Chinese he bal medicines o pos s oke eco e y: a
adi ional and ne wo k me a-analysis. Medicine 96:1–13
Hanee M, Cese acciu L, Canale C, Ilke B e al (2017) Ad anced
ma e ials om ungal mycelium: ab ica ion and uning o
physical p ope ies. Sci Rep 7:41292
Hansen MB, Jensen ML, Ca s ensen B (2012) Causes o dea h among
diabe ic pa ien s in Denma k. Diabe ologia 55:294–302
Hanson JR (2008) Fungal me aboli es de i ed om amino acids. In:
Hanson JR (ed) The chemis y o Fungi. The Royal Socie y o
Chemis y, Camb idge, pp 32–46
Hao YJ, Zhao Q, Wang SX, Yang ZL (2016) Wha is he adica e
Oudemansiella cul i a ed in China? Phy o axa 286:1–12
Hapua achchi KK, Wen TC, Jeewon R, Wu XL, Kang JC (2014)
Mycosphe e essays 7. Ganode ma lucidum—a e he bene icial
an i-cance p ope ies subs an ia ed? Mycosphe e 7:305–332
Hapua achchi KK, Ka una a hna SC, Phengsin ham P, Kakumyan P,
Hyde KD, Wen TC (2018) Amau ode ma (Ganode ma aceae,
Polypo ales)—bioac i e compounds, bene icial p ope ies and
wo new eco ds om Laos. Asian J Mycol 1:121–136
Hapua achchi KK, Ka una a hna SC, McKenzie EHC, Wu XL,
Kakumyan P, Hyde KD, Wen TC (2019) High pheno ypic
plas ici y o Ganode ma sinense (Ganode ma aceae, Polypo-
ales) in China. Asian J Mycol 2:1–47
Ha i ash AK, Kaushik CP (2009) Biodeg ada ion aspec s o poly-
cyclic a oma ic hyd oca bons (PAHs): a e iew. J Haza d Ma e
169:1–15
Ha MM, T e o s JT (2005) Mic obe managemen : applica ion o
myco hizal ungi in sus ainable ag icul u e. F on Ecol En i on
3:533–539
Hasan HA (2002) Gibbe ellin and auxin-indole p oduc ion by plan
oo - ungi and hei biosyn hesis unde salini y-calcium in e ac-
ion. Ac a Mic obiol Immunol Hung 49:105–118
Hasan S, Ay es PG (1990) The con ol o weeds h ough ungi:
p inciples and p ospec s. New Phy ol 115:201–222
Hasan MT, Kha un MHA, Sajib MAM, Rahman MM e al (2015)
E ec o whea b an supplemen wi h suga cane bagasse on
g ow h, yield and p oxima e composi ion o pink oys e mush-
oom Pleu o us djamo . Am J Food Sci Technol 3:150–157
Hawkswo h DL (2012) Global species numbe s o ungi: a e opical
s udies and molecula app oaches con ibu ing o a mo e obus
es ima e. Biodi e s Conse 21:2425–2433
Hawkswo h DL, Lu
¨cking R (2017) Fungal di e si y e isi ed: 2.2 o
3.8 million species. Mic obiol Spec um 5:1–17
He W, Zhao W, Yang R (2019) E ec s o whea glu en modi ied by
deamida ion-hea ing wi h h ee di e en acids on he mic os uc-
u e o model oil-in-wa e emulsion and heological–physical
p ope y o ice c eam. Food Hyd ocoll 87:679–690
Hecque L, Sancelme M, Bol e J, Demuynck C (1996) Biosyn hesis o
4-hyd oxy-2,5-dime hyl-3(2H)- u anone by Zygosaccha omyces
ouxii. J Ag ic Food Chem 44:1357–1360
Hedden P, Sponsel V (2015) A cen u y o gibbe ellin esea ch. J Plan
G ow h Regul 34:740–760
Heilmann-Clausen J, Ba on ES, Boddy L, Dahlbe g A e al (2014) A
ungal pe spec i e on conse a ion biology. Conse Biol 29:61–
68
Helaly SE, Ash a i S, Teponno RB, Be necke S e al (2018a)
Nema icidal cyclic lipodepsipep ides and a xan hocillin de i a-
i e om a phaeospha iaceous ungus pa asi izing eggs o he
plan pa asi ic nema ode He e ode a ilipje i. J Na P od
81:2228–2234
Helaly SE, Thongbai B, S adle M (2018b) Di e si y o biologically
ac i e seconda y me aboli es om endophy ic and sap o ophic
ungi o he ascomyce e o de Xyla iales. Na P od Rep 35:992–
1014
Heneghan MN, Yakasai A, Williams K, Kadi KA e al (2011) The
p og amming ole o ans-ac ing enoyl educ ases du ing he
biosyn hesis o highly educed ungal polyke ides. Chem Sci
2:972–980
112 Fungal Di e si y (2019) 97:1–136
123

He na
´ndez VA, Galleguillos F, Thibau R, Mu
¨lle A (2018a) Fungal
dyes o ex ile applica ions: es ing o indus ial condi ions o
wool ab ic dyeing. J Tex ile Ins . h ps://doi.o g/10.1080/
00405000.2018.1460037
He na
´ndez VA, Galleguillos FA, Sag edo N, Machuca A
´(2018b) A
no e on he dyeing o wool ab ics using na u al dyes ex ac ed
om o en wood-inhabi ing ungi. Coa ings 8:77–83
He na
´ndez-Mon iel LG, Rueda-Puen e EO, Co doba-Ma son MV,
Holguı
´n-Pen
˜a JR, Zulue a-Rod ı
´guez R (2013) Mu ualis ic
in e ac ion o izobac e ia wi h a buscula myco hizal ungi
and i s an agonis ic e ec on Fusa ium oxyspo um in Ca ica
papaya seedlings. C op P o 47:61–66
Hes e kamp T (2017) An ibio ics clinical de elopmen and pipeline.
In How o o e come he an ibio ic c isis— ac s, challenges,
echnologies & u u e pe spec i e (S adle , M, De sch P, eds.).
Cu Top Mic obiol Immunol 398:447–474
Hibbe DS, Vilgalys R (1993) Phylogene ic ela ionships o Len inus
(Basidiomyco ina) in e ed om molecula and mo phological
cha ac e s. Sys Bo 18:409–433
Hicks W (2011) Wal e Hicks wine lis 2011, p 92
Higgins C, Ma go H, Wa nquis S, Obeyseka e E, Meh a K (2017)
Mush oom cul i a ion in he de eloping wo ld: a compa ison o
cul i a ion echnologies. In: Global Humani a ian Technology
Con e ence (GHTC), pp 1–7
Hill C, Gua ne F, Reid G, Gibson GR e al (2014) The In e na ional
Scien i ic Associa ion o P obio ics and P ebio ics consensus
s a emen on he scope and app op ia e use o he e m p obio ic.
Na Re Gas oen e ol Hepa ol 11:506–514
Himmel ME, Ding SY, Johnson DK, Adney WS e al (2007) Biomass
ecalci ance: enginee ing plan s and enzymes o bio uels
p oduc ion. Science 315:804–807
Hinsch E, Robinson S (2016) Mechanical colou eading o wood-
s aining ungal pigmen ex ile dyes: an al e na i e me hod o
de e mining colou as ness. Coa ings 6:1–12
Hi o ani M, Hi o ani S, Takayanagi H, Yoshikawa T (1999)
Blazeispi ol A, an unp eceden ed skele on om he cul u ed
mycelia o he ungus Aga icus blazei. Te ahed on Le 40:329–
332
Hi o ani M, Hi o ani S, Yoshikawa T (2000) Blazeispi ol X and Y,
wo no el ca bon skele al s e ols om he cul u ed mycelia o
he ungus Aga icus blazei. Te ahed on Le 41:5107–5110
Hi o ani M, Hi o ani S, Yoshikawa T (2001) Blazeispi ol D and Z, as
he ac ual in e media es o blazeispi ol A biosyn hesis om he
cul u ed mycelia o he ungus Aga icus blazei. Te ahed on Le
42:5261–5264
Hi o ani M, Sai K, Hi o ani S, Yoshikawa T (2002) Blazeispi ols B,
C, E and F, des-A-e gos ane- ype compounds, om he cul u ed
mycelia o he ungus Aga icus blazei. Phy ochemis y 59:571–
577
Ho mann C, Dolli e S, G unbe g S, Chen J e al (2013) A chaea and
ungi o he human gu mic obiome: co ela ions wi h die and
bac e ial esiden s. PLoS ONE 8:1–12
Ho mann T, K au wu s D, Schiebe le P (2018) Cu en s a us and
u u e pe spec i es in la o esea ch: highligh s o he 11 h
Wa bu g Symposium on la o chemis y & biology. J Ag ic
Food Chem 66:2197–2203
Ho ich e M, Lundell T, Ha akka A (2011) Con e sion o milled
pine wood by manganese pe oxidase om Phlebia adia a. Appl
En i on Mic obiol 67:4588–4593
Holland RJ, Williams KL, Khan A (1999) In ec ion o Meloidogyne
ja anica by Paecilomyces lilacinus. Nema ology 1:131–139
Hong SB, Kim DH, Samson RA (2015) Aspe gillus associa ed wi h
Meju, a e men ed soybean s a ing ma e ial o adi ional soy
sauce and soybean pas e in Ko ea. Mycobiology 43:218–224
Ho bach R, Quesada ARN, Knogge W, Deising HB (2011) When and
how o kill a plan cell: in ec ion s a egies o plan pa hogenic
ungi. J Plan Physiol 5:722–732
Ho nsey IS (2003) A his o y o bee and b ewing. The Royal Socie y
o Chemis y, Camb idge
Ho nsey IS (2012) Alcohol and i s ole in he e olu ion o human
socie y. Royal Socie y o Chemis y, London
Ho a MAC, Filho JAF, Mu ad NF, de Oli ei a SE e al (2018)
Ne wo k o p o eins, enzymes and genes linked o biomass
deg ada ion sha ed by T ichode ma species. Sci Rep 8:1–11
Hosseini F, Mosaddeghi MR, Dex e AR (2017) E ec o he ungus
Pi i o mospo a indica on physiological cha ac e is ics and oo
mo phology o whea unde combined d ough and mechanical
s esses. Plan Physiol Biochem 118:107–120
Hou XQ, Guo SX (2009) In e ac ion be ween a da k sep a e
endophy ic isola e om Dend obium sp. and oo s o D. nobile
seedlings. J In eg Plan Biol 51:374–381
Hou CW, Jeng KC, Chen YS (2010) Enhancemen o e men a ion
p ocess in Pu-e h ea by ea-lea ex ac . J Food Sci 75:44–48
Howa d GT (2012) Polyu e hane biodeg ada ion. In: Singh SN (ed)
Mic obial deg ada ion o xenobio ics. Sp inge , Be lin, pp 371–
394
Hua MDS, Kuma RS, Shyu LF, Cheng YB e al (2017)
Me abolomic compounds iden i ied in Pi i o mospo a indica-
colonized Chinese cabbage oo s delinea e symbio ic unc ions
o he in e ac ion. Sci Rep 7:1–14
Huang WY, Cai YZ, Su eswa an S, Hyde KD, Co ke H, Sun M
(2009) Molecula phylogene ic iden i ica ion o endophy ic ungi
isola ed om h ee A emisia species. Fungal Di e s 36:69–88
Huang L, Wei PL, Zang R, Xu ZN, Cen PL (2010) High- h oughpu
sc eening o high-yield colonies o Rhizopus o yzae o
enhanced p oduc ion o uma ic acid. Ann Mic obiol 60:287–
292
Huang R, Li GQ, Zhang J, Yang L e al (2011) Con ol o pos ha es
Bo y is ui o o s awbe y by ola ile o ganic compounds o
Candida in e media. Phy opa hology 101:859–869
Huang Y, Kuang Z, Wang W, Cao L (2016) Explo ing po en ial
bac e ial and ungal biocon ol agen s ansmi ed om seeds o
sp ou s o whea . Biol Con ol 98:27–33
Huang MY, Lin KH, Lu CC, Chen LR e al (2017a) The in ensi y o
blue ligh -emi ing diodes in luences he an ioxidan p ope ies
and suga con en o oys e mush ooms (Len inus sajo -caju).
Sci Ho 218:8–13
Huang Z, Nong X, Wang J, Zhang X e al (2017b) An i-HSV-1,
an ioxidan and an i ouling phenolic compounds om he deep-
sea-de i ed ungus Aspe gillus e sicolo SCSIO 41502. Bioo g
Med Chem Le 27:787–789
Huang H, Wang SL, Nguyen V, Kuo YH (2018) Isola ion and
iden i ica ion o po en an idiabe ic compounds om An odia
cinnamomea—an edible Taiwanese mush oom. Molecules 23:1–
12
Hulea A (1939) Con ibu ions a
`la connaissance des champignons
commensaux des U e
´dine
´es. Bulle in de la Sec ion Scien i ique
de l’Acade
´mie de Roumanie 22:1–19
Huseyin CE, O’Toole PW, Co e PD, Scanlan PD (2017) Fo go en
ungi- he gu mycobiome in human heal h and disease. FEMS
Mic obiol Re 41:479–511
Hussain A, Rizwan-ul-Haq M, Al-Ayedh H, Al-Jab M (2014)
Mycoinsec icides: po en ial and u u e pe spec i e. Recen Pa
Food Nu Ag ic 6:45–53
Hu chings ML, Alpha-Cobb CJ, Hille DA, Be o J, S obel SA
(2017) Myco umiga ion h ough p oduc ion o he ola ile DNA
me hyla ing agen N-me hyl-N-ni osoisobu y amide by ungi in
he genus Muscodo . J Biol Chem 292:7358–7371
Hyde KD, Soy ong K (2008) The ungal endophy e dilemma. Fungal
Di e s 33:163–173
Fungal Di e si y (2019) 97:1–136 113
123
Hyde KD, Bahkali AH, Moslem MA (2010) Fungi—an unusual
sou ce o cosme ics. Fungal Di e s 43:1–9
Hyde KD, Nilsson RH, Alias SA, A iyawansa HA e al (2014) One
s op shop: backbones ees o impo an py opa hogenic gene a:
I. Fungal Di e s 67:21–125
Hyde KD, Hongsanan S, Jeewon R, Bha DJ e al (2016) Fungal
di e si y no es 367–490: axonomic and phylogene ic con ibu-
ions o ungal axa. Fungal Di e s 80:1–270
Hyde KD, No phanphoun C, Ab eu VP, Bazzicalupo A e al (2017)
Fungal di e si y no es 603–708: axonomic and phylogene ic
no es on gene a and species. Fungal Di e s 87:1–235
Hyde KD, Al-Ha mi AM, Ande sen B, Boekhou T, Buzina W,
Dawson TL, Eas wood DC, Jones EG, de Hoog S, Kang Y,
Longco e JE (2018a) The wo ld’s en mos ea ed ungi. Fungal
Di e s 93:161–194
Hyde KD, Chaiwan N, No phanphoun C, Boonmee S e al (2018b)
Mycosphe e no es 169-224. Mycosphe e 9:271–430
Hyde KD, No phanphoun C, Chen J, Dissanayake AJ e al (2018c)
Thailand’s amazing di e si y: up o 96% o ungi in no he n
Thailand may be no el. Fungal Di e s 93:215–239
Hynninen PH, Ra
¨isa
¨nen R, Elo aa a P, Nokelainen E (2000)
P epa a i e isola ion o an h aquinones om he ungus De mo-
cybe sanguinea using enzyma ic hyd olysis by he endogenous
ß-glucosidase. Z Na u o sch 55:600–610
Hyodo I, Amano N, Eguchi K, Na abayashi M e al (2005)
Na ionwide su ey on complemen a y and al e na i e medicine
in cance pa ien s in Japan. J Clin Oncol 23:2645–2654
Ib ahim AA (1994) E ec o cadusa os, Paecilomyces lilacinus and
Nemou on ep oduc ion and damage po en ial o Meloidogyne
ja anica. Pak J Nema ol 12:141–147
Igi i BE, Okoduwa SIR, Idoko GO, Akabuogu EP e al (2018)
Toxici y and bio emedia ion o hea y me als con amina ed
ecosys em om Tanne y was ewa e : a e iew. J Toxicol
2018:1–16
Ilmbe ge N, Meske D, Jue gensen J, Schul e M e al (2012)
Me agenomic cellulases highly ole an owa ds he p esence o
ionic liquids-linking he mos abili y and halo ole ance. Appl
Mic obiol Bio echnol 95:135–146
Imho JF, Labes A, Wiese J (2011) Bio-mining he mic obial
easu es o he ocean: new na u al p oduc s. Bio echnol Ad
29:468–482
Ina K, Ka aoka T, Ando T (2013) The use o len inan o ea ing
gas ic cance . An icance Agen s Med Chem 13:681–688
Inglis DG, Enke li J, Goe el M (2012) Labo a o y echniques used
o en omopa hogenic ungi. Hypoc eales. In: Lacey L (ed)
Manual o echniques in in e eb a e pa hology, 2nd edn.
Academic P ess, Bos on, pp 189–253
In e s a e Technology and Regula o y Council (ITRC) (2002) A
sys ema ic app oach o in si u bio emedia ion in g ound wa e
including decisions ees on in si u bio emedia ion o ni a es,
ca bon e achlo ide and pe chlo a e. h ps://clu-in.o g/con /i c/
sysisb/. Accessed 3 Ma 2019
Islam MR, Tud yn G, Bucinell R, Schadle L, Picu C (2018)
Mechanical beha io o mycelium-based pa icula e composi es.
J Ma e Sci 53:16371–16382
Isogai A, Kanaoka M, Ma suda H, Ho i Y, Suzuki A (1978) S uc u e
o a new cyclodepsipep ide, Beau e ilide A om Beau e ia
bassiana. Ag ic Biol Chem 42:1797–1798
I elima JU, Bang WJ, Onyimba IA, Egbe e OJ (2018) A e iew:
bio e ilize - a key playe in enhancing soil e ili y and c op
p oduc i i y. J Mic obiol Bio echnol Rep 2:22–28
Jabe LR, Ownley BH (2018) Can we use en omopa hogenic ungi as
endophy es o dual biological con ol o insec pes s and plan
pa hogens? Biol Con ol 116:36–45
Jackson AJ, Wal e s DR, Ma shall G (1997) An agonis ic in e ac ions
be ween he olia pa hogen Bo y is abae and isola es o
Penicillium b e icompac um and Cladospo ium cladospo ioides
on aba beans. Biol Con ol 8:97–106
Jah omi MF, Liang JB, Ho YW, Mohamad R, Goh YM, Shok yazdan
P (2012) Lo as a in p oduc ion by Aspe gillus e eus using
ag o-biomass as subs a e in solid s a e e men a ion. J Biomed
Bio echnol 2012:1–11
Jai el N, Ma imu hu P (2010) Op imiza ion o lo as a in p oduc ion
in solid s a e e men a ion by Aspe gillus e eus. In J Eng Sci
2:2730–2733
Jalaluddin M (1977) A use ul pa hological condi ion o wood. Econ
Bo 31:222–224
Janisiewicz WJ, Je e s SN (1997) E icacy o comme cial o mula-
ion o wo bio ungicides o con ol o blue mold and g ay mold
o apples in cold s o age. C op P o 16:629–633
Janous
ˇko a
´M, K ak K, Vosa
´ ka M, Pu
¨schel D, S
ˇ o cho a
´H (2017)
Inocula ion e ec s on oo -colonizing a buscula myco hizal
ungal communi ies sp ead beyond di ec ly inocula ed plan s.
PLoS ONE 12:e0181525
Jansson HB, Jeyap akash A, Zucke man BM (1985) Con ol o oo -
kno nema odes on oma o by endopa asi ic ungus Me ia
coniospo a. J Nema ol 17:327–329
Jansson HB, Lopez-Llo ca LV (2004) Con ol o nema odes by ungi.
In: A o a DK (ed) Fungal bio echnology in ag icul u al, ood,
and en i onmen al applica ions, mycology se ies, ol 21. CRC
P ess, Boca Ra on, pp 205–215
Ja onski ST, Masca in GM (2017) Mass p oduc ion o ungal
en omopa hogens. In: Lacey LA (ed) Mic obial con ol o
insec s and mi e pes s, ol 9. Academic P ess, Ams e dam,
pp 141–155
Jaspe s NG, Raams A, Kelne MJ, Ng JM e al (2002) An i- umou
compounds illudin S and I o ul en induce DNA lesions igno ed
by global epai and exclusi ely p ocessed by ansc ip ion-and
eplica ion-coupled epai pa hways. DNA Repai 1:1027–1038
Jayawa dena RS, Hyde KD, Damm U, Cai L e al (2016) No es on
cu en ly accep ed species o Colle o ichum. Mycosphe e
7:1192–1260
Jenkins MJ, Ha ison KL (2008) The e ec o c ys alline mo phology
on he deg ada ion o polycap olac one in a solu ion o
phospha e bu e and lipase. Polym Ad Technol 19:1901–1906
Jeon S, Bose S, Hu J, Jun K, Kim YK, Cho KS, Koo BS (2011) A
modi ied o mula ion o Chinese adi ional medicine imp o es
memo y impai men and educes Aβle el in he Tg-APPswe/
PS1dE9 mouse model o Alzheime ’s disease. J E hnopha macol
137:783–789
Jeong SC, Jeong YT, Yang BK, Islam R e al (2010) Whi e bu on
mush oom (Aga icus bispo us) lowe s blood glucose and
choles e ol le els in diabe ic and hype choles e olemic a s.
Nu Res 30:49–56
Jeschke R, Iinuma K, Ha de A, Schindle M, Mu akami T (2005)
In luence o he cyclooc adepsipep ides PF1022A and PF1022E
as na u al p oduc s on he design o semi–syn he ic an helmin ics
such as emodepside. Pa asi ol Res 97(1):S11–S16
Jeznabadi EK, Ja a pou M, Eghbalsaied S (2016) King oys e
mush oom p oduc ion using a ious sou ces o ag icul u al
was es in I an. In J Recycl O g Was e Ag ic 5:17–24
Jha BN, Sha ma GD, Shukla AK (2008) E ec o ec omyco hizal
de elopmen on g ow h in pine seedling. J Plan Sci 3:77–84
Ji KP, Cao Y, Zhang CX, He MX e al (2011) Cul i a ion o
Phlebopus po en osus in sou he n China. Mycol P o 10:293–
300
Jiang YF, Chang TJ, Liu Y, Zhang M e al (2017) O e iew o
Ganode ma sinense polysaccha ide–an adjunc i e d ug used
du ing concu en chemo/ adia ion he apy o cance ea men
in China. Biomed Pha maco he 96:865–870
Jime
´nez DJ, Chaib De Ma es M, Salles JF (2018) Tempo al
exp ession dynamics o plan biomass-deg ading enzymes by a
114 Fungal Di e si y (2019) 97:1–136
123
syn he ic bac e ial conso ium g owing on suga cane bagasse.
F on Mic obiol 9:299
Jin X, Cus is D (2011) Mic oencapsula ing ae ial conidia o
T ichode ma ha zianum h ough sp ay d ying a ele a ed
empe a u es. Biol Con ol 56:202–208
Jin Y, Qin S, Gao H, Zhu G e al (2018) An an i-HBV an h aquinone
om acidu ic ungus Penicillium sp. OUCMDZ-4736 unde low
pH s ess. Ex emophiles 22:39–45
Jogaiah S, Abdel ahman M, T an LSP, I o SI (2018) Di e en
mechanisms o T ichode ma i ens-media ed esis ance in
oma o agains Fusa ium wil in ol e he jasmonic and salicylic
acid pa hways. Mol Plan Pa hol 19:870–882
Jogawa A, Vadasse y J, Ve ma N, Oelmu
¨lle R e al (2016) PiHOG1,
a s ess egula o MAP kinase om he oo endophy e ungus
Pi i o mospo a indica, con e s salini y s ess ole ance in ice
plan s. Sci Rep 6:36765
Johjima T, I oh N, Kabu o M, Tokimu a F e al (1999) Di ec
in e ac ion o lignin and lignin pe oxidase om Phane ochae e
ch ysospo ium. PNAS 96:1989–1994
Jones N (2013) Food uelled wi h ungi. Na u e 504:199
Jones M, Bha T, Wang C, Moinuddin K, John S (2017) The mal
deg ada ion and i e p ope ies o ungal mycelium and
mycelium- biomass composi e ma e ials. Sci Rep 8:1–10
Jones M, Bha T, Huynh T, Kanda e E e al (2018) Was e-de i ed
low-cos mycelium composi e cons uc ion ma e ials wi h
imp o ed i e sa e y. Fi e Ma e 9:71–80
Julien MH, G i i hs MW (1998) Biological con ol o weeds, a wo ld
ca alogue o agen s and hei a ge weeds, 4 h edn. CAB
In e na ional, Walling o d, p p223
Jung JH, Lee HW, Lee YJ, Lee HR, Um TH, Pa k JY, Yi SY (2015)
Fou cases o acqui ed aplas ic anemia a ec ing an en i e amily
a e inges ing Ganode malucidum. Ko ean J Medicine 88:94–
100
Jus o A, Hibbe DS (2011) Phylogene ic classi ica ion o T ame es
(Basidiomyco a, Polypo ales) based on a i e-ma ke da ase .
Taxon 60:1567–1583
Kabaluk JT, S i ce AM, Goe el MS, Woo SG (eds) (2010) The use
and egula ion o mic obial pes icides in ep esen a i e ju isdic-
ions wo ldwide. IOBC Global, S . Paul
Kabi Y, Kimu a S (1989) Die a y mush ooms educe blood p eassu e
in spon aneously hype ensi e a s (SHR). J Nu Sci Vi aminol
35:91–94
Kabi Y, Kimu a S, Tamu a T (1988) Die a y e ec o Ganode ma
lucidum mush oom on blood p essu e and lipid le els in
spon aneously hype ensi e a s (SHR). J Nu Sci Vi aminol
34:433–438
Kaewchai S, Soy ong K, Hyde KD (2009) Myco ungicides and ungal
bio e ilize s. Fungal Di e s 38:25–50
Kaewg ajang T, Sangwani U, Kodama M, Yamo a M (2013)
Ec omyco hizal ungal communi ies o Dip e oca pus ala us
seedlings in oduced by soil inocula om a na u al o es and a
plan a ion. J Fo Res 9:260–267
Kalac
ˇP (2013) A e iew o chemical composi ion and nu i ional
alue o wild-g owing and cul i a ed mush ooms. J Sci Food
Ag ic 93:209–218
Kal a EK (2003) Nu aceu ical-de ini ion and in oduc ion. AAPS
Pha m Sci 5:27–28
Kamei I, Takagi K, Kondo R (2011) Deg ada ion o endosul an and
endosul an sul a e by whi e- o ungus T ame es hi su a. J Wood
Sci 57:317–322
Kam han R, Tiwa i I (2017) Ag icul u al was es – Po en ial subs a es
o mush oom cul i a ion. Eu Exp Biol 7:31
Kaneko M, Wa ashi K, Kamisuki S, Ma sunaga H e al (2015) A
no el icyclic polyke ide, ani a acin A, speci ically inhibi s he
en y o hepa i is B and D i uses by a ge ing sodium
au ochola e co- anspo ing polypep ide. J Vi ol 89:11945–
11953
Kaplan GG (2015) The global bu den o IBD: om 2015 o 2025. Na
Re Gas oen e ol Hepa ol 12:720–727
Kapple A, Wues ne ML, Ruecke A, Ha e J e al (2014) Biocha as
an elec on shu le be ween bac e ia and Fe(III) mine als.
En i on Sci Technol Le 1:339–344
Ka wehl S, S adle M (2017) Exploi a ion o ungal biodi e si y o
disco e y o no el an ibio ics he an ibio ic c isis— ac s,
challenges, echnologies & u u e pe spec i e. Cu Top Mic o-
biol Immunol 398:303–338
Ka hi esan K, Mani annan S (2006) α-Amylase p oduc ion by
Penicillium ellu anum isola ed om mang o e hizosphe e soil.
A J Bio echnol 5:829–832
Kau G, Kalia A, Sodhi HS (2018) Selenium bio o i ica ion o
Pleu o us species and i s e ec on yield, phy ochemical p o iles,
and p o ein chemis y o ui ing bodies. J Food Biochem
42:12467
Kayama M, Yamanaka T (2016) G ow h cha ac e is ics o ec omy-
co hizal seedlings o Que cus glauca, Que cus salicina, Que -
cus my sinae olia, and Cas anopsis cuspida e plan ed in
calca eous soil. Fo es s 7:266
Kazan K, Lyons R (2014) In e en ion o phy oho mone pa hways by
pa hogen e ec o s. Plan Cell 26:2285–2309
Keene PD (1954) Cladospo ium aecidiicola Thuem. and Tube colina
pe sicina (Di m). Sacc. associa ed wi h Puccinia conspicua
(A h.) Mains on Helenium hoopesii A. G ay in A izona. Plan
Dis Rep 38:691–694
Ke ialew Y, Ayalew A (2008) Pos ha es biological con ol o
an h acnose (Colle o ichum gloeospo ioides) on mango (Man-
gi e a indica). Pos ha es Biol Technol 50:8–11
Kend ick B (1992) The i h kingdom. Hacke Publishing,
Indianapolis
Ken JM (1994) Plan p o ec ion B—no es and eadings: weeds.
Cha les S u Uni e si y, Sydney Olympic Pa k
Keppanan R, Si ape umal S, Ramos Aguila LC, Hussain M e al
(2018) Isola ion and cha ac e iza ion o Me a hizium anisopliae
TK29 and i s mycoinsec icide e ec s agains sub e anean
e mi e Cop o e mes o mosanus. Mic ob Pa hog 123:52–59
Ke igan RW (2005) Aga icus sub u escens, a cul i a ed edible and
medicinal mush oom, and i s synonyms. Mycologia 97:12–24
Ke sey PJ, Lawson D, Bi ney E, De wen PS e al (2010) Ensembl
genomes: ex ending Ensembl ac oss he axonomic space.
Nucleic Acids Res 38:D563–D569
Ke shaw MJ, Moo house ER, Ba eman R, Reynolds SE, Cha nley AK
(1999) The ole o des uxins in he pa hogenici y o Me a hiz-
ium anisopliae o h ee species o insec . J In e Pa hol
74:213–223
Kesha a z B, Khalesi M (2016) T ichode ma eesei, a supe io
cellulase sou ce o indus ial applica ions. Bio uels 7:713–721
Khan AL, Hamayun M, Kang SM, Kim YH e al (2012) Endophy ic
ungal associa ion ia gibbe ellins and indole ace ic acid can
imp o e plan g ow h unde abio ic s ess: an example o
Paecilomyces o mosus LHL10. BMC Mic obiol 12:1–14
Khan AL, Hussain J, Al-Ha asi A, Al-Rawahi A, Lee IJ (2015a)
Endophy ic ungi: esou ce o gibbe ellins and c op abio ic
s ess esis ance. C i Re Bio echnol 35:62–74
Khan AR, Ullah I, Waqas M, Shahzad R e al (2015b) Plan g ow h-
p omo ing po en ial o endophy ic ungi isola ed om Solanum
nig um lea es. Wo ld J Mic obiol Bio echnol 31:1461–1466
Khan S, Nadi S, Shah ZU, Shah AA e al (2017) Biodeg ada ion o
polyes e polyu e hane by Aspe gillus ubingensis. En i on
Pollu 225:469–480
Kiho T, Yamane A, Hui J, Usui S, Ukai S (1996) Polysaccha ides in
ungi. XXXVI Hypoglycemic ac i i y o a polysaccha ide (CS-
F30) om he cul u al mycelium o Co dyceps sinensis and i s
Fungal Di e si y (2019) 97:1–136 115
123
e ec on glucoseme abolism in mouse li e . Biol Pha m Bull
19:294–296
Kildgaa d S, Mansson M, Dosen I, Kli gaa d A e al (2014) Accu a e
de eplica ion o bioac i e seconda y me aboli es om ma ine-
de i ed ungi by UHPLC-DAD-QTOFMS and a MS/HRMS
lib a y. Ma D ugs 12:3681–3705
Kim AY (2005) Applica ion o bio echnology o he p oduc ion o
na u al la o and ag ance chemicals. In: ACS symposium
se ies. Ox o d Uni e si y P ess, pp 60–75
Kim JD (2007) Pu i ica ion and cha ac e iza ion o a ke a inase om
a ea he -deg ading ungus, Aspe gillus la us S ain K-03.
Mycobiology 35:219–225
Kim DY, Rhee YH (2003) Biodeg ada ion o mic obial and syn he ic
polyes e s by ungi. Appl Mic obiol Bio echnol 61:300–308
Kim S, Dale BE (2004) Global po en ial bioe hanol p oduc ion om
was ed c ops and c op esidues. Biomass Bioene g 26:361–375
Kim KH, Kim JY, Cho TS, Choi JW (2012) In luence o py olysis
empe a u e on physicochemical p ope ies o biocha ob ained
om he as py olysis o pi ch pine (Pinus igida). Bio esou
Technol 118:158–162
Kim YW, Kim KH, Choi HJ, Lee DS (2005) An i-diabe ic ac i i y o
β-glucans and hei enzyma ically hyd olyzed oligosaccha ides
om Aga icus blazei. Bio echnol Le 27:483–487
Kinsella JE, Hwang DH, Dwi edi B (1976) Enzymes o Penicillium
oque o i in ol ed in he biosyn hesis o cheese la o . C i Re
Food Sci Nu 8:191–228
Kip e T, Wohlgemu h T, an de Heiden MGA, Ghazoul J, Egli S
(2012) G ow h esponse o d ough -s essed Pinus syl es is
seedlings o single- and mul i-species inocula ion wi h ec omy-
co hizal ungi. PLoS ONE 7:e35275
Ki k O, Bo che TV, Fuglsang CC (2002) Indus ial enzyme
applica ions. Cu Opin Bio echnol 13:345–351
Ki k MD, Pi es SM, Black RE, Caipo M (2015) Wo ld Heal h
O ganiza ion es ima es o he global and egional disease bu den
o 22 oodbo ne bac e ial, p o ozoal, and i al diseases, 2010: a
da a syn hesis. PLoS Med 12(12):e1001921
Klinsupa W, Phansi i S, Thongp adis P, Yongsmi h B, Po hi a ana C
(2016) Enhancemen o yellow pigmen p oduc ion by
in aspeci ic p o oplas usion o Monascus spp. yellow mu an
(ade-) and whi e mu an (p o o oph). J Bio echnol 217:62–71
Kloa eg B, Qua ano RS (1988) S uc u e o he cell walls o ma ine
algae and ecophysiological unc ions o he ma ix polysaccha-
ides. Oceanog Ma Biol Annu Re 26:259–315
Klomklung N, Ka una a hna SC, Chukea i o e E, Hyde KD (2012)
Domes ica ion o wild s ain o Pleu o us gigan eus. Sydowia
60:39–53
Klu
¨p el L, Keiluwei M, Klebe M, Sande M (2014) Redox
p ope ies o plan biomass-de i ed black ca bon (Biocha ).
En i on Sci Technol 48:5601–5611
Knigh DW, Pa enden G (1976) Syn hesis o he pul inic acid
pigmen s o lichen and ungi. J Chem Soc Chem Com 639:660–
661
Ko HG, Pa k SH, Kim SH, Pa k HG, Pa k WM (2005) De ec ion and
eco e y o hyd oly ic enzymes om spen compos o ou
mush oom species. Folia Mic obiol 50:103–106
Konno S, Alexande B, Zade J, Choudhu y M (2013) Possible
hypoglycemic ac ion o SX- ac ion a ge ing insulin signal
ansduc ion pa hway. In J Gen Med 6:181
Koza ski M, Klaus A, Niksic M, Jako lje ic D e al (2011)
An ioxida i e and immunomodula ing ac i i ies o polysaccha-
ide ex ac s o he medicinal mush ooms Aga icus bispo us,
Aga icus b asiliensis, Ganode ma lucidum, and Phellinus
lin eus. Food Chem 129:1667–1675
Kozubal MA, Macu RE, A niel YC, Sus ainable Biop oduc s, Inc.
(2019) Filamen ous ungal bioma s, me hods o hei p oduc ion
and me hods o hei use. US pa en applica ion 16/118:370
K anz J (1981) Hype pa asi ism o bio ophic ungi. In: Blakeman JP
(ed) Mic obial ecology o he phylloplane. Academic P ess,
London, pp 327–352
K asowska K, Janik H, G adys A, Ru kowska M (2012) Deg ada ion
o polyu e hanes in compos unde na u al condi ions. J Appl
Polym Sci 125:4252–4260
K ings U, Be ge RG (1998) Bio echnological p oduc ion o la o s
and ag ances. Appl Mic obiol Bio echnol 49:1–8
K is iansen KA, Taylo DL, Kjolle R, Rasmussen HN, Rosendahl S
(2001) Iden i ica ion o myco hizal ungi om single pelo ons
o Dac ylo hiza majalis (O chidaceae) using single-s and con-
o ma ion polymo phism and mi ochond ial ibosomal la ge
subuni DNA sequences. Mol Ecol 10(8):2089–2093
K is iansen KA, F eudens ein JV, Rasmussen FN, Rasmussen HN
(2004) Molecula iden i ica ion o myco hizal ungi in Neuwie-
dia e a i olia (O chidaceae). Mol Phylogene E ol 33:251–258
K is
ˇ o ı
´ko a
´L, Rosenbe g M, Vlno a A, S
ˇajbido J, C
ˇe ı
´k M (1991)
Selec ion o Rhizopus s ains o l (?)-lac ic acid andγ-linolenic
acid p oduc ion. Folia Mic obiol 36:451–455
K oge us K, Magalha
˜es F, Vidg en V, Gibson B (2017) No el
b ewing yeas hyb ids: c ea ion and applica ion. Appl Mic obiol
Bio echnol 101:65–78
K u
¨gene S, K ings U, Zo n H, Be ge RG (2010) A dioxygenase o
Pleu o us sapidus ans o ms (?)- alencene egio-speci ically o
(?)-noo ka one ia a s e eo-speci ic allylic hyd ope oxida ion.
Bio esou Technol 101:457–462
K u
¨ge D, K eisel H (2003) P oposing Mo ganella subgen. Apiop-
e don subgen. no . o he pu ball Lycope don py i o me.
Myco axon 86:169–177
Kuanyshe N, Adamo GM, Po o D, B andua di P (2017) The
spoilage yeas Zygosaccha omyces bailii: Foe o iend? Yeas
34:359–370
Kubo K, Namba H (1997) An i-hype liposis e ec o Mai ake ui
body (G i ola ondosa). Biol Pha m Bull 20:781–785
Kubo T, Te abayashi S, Takeda S, Sasaki H e al (2006) Indoo
cul i a ion and cul u al cha ac e is ics o Wol ipo ia cocos
scle o ia using mush oom cul u e bo les. Biol Pha m Bull
29:1191–1196
Kudalka P, S obel G, Hassan S, Gea y B, Sea s J (2012) Muscodo
su u a, a no el endophy ic ungus wi h ola ile an ibio ic
ac i i ies. Mycoscience 53:319–325
Kuhne E, Li Y, Lan N, Yue Q e al (2018) En uma ungin syn hase
ep esen s a no el lineage o ungal i e pene cyclases. En i-
onm Mic obiol 1:12. h ps://doi.o g/10.1111/1462-2920.14333
Kulsh esh ha S, Ma hu N, Bha naga P (2014) Mush oom as a
p oduc and hei ole in myco emedia ion. AMB Exp ess 4:29
Kuma R, Kaushik P (2004) Isola ion o a cellulose p oducing
myco hizal ungus Rhizoc onia solani om Zeuxine s a eu-
ma ica (Linn.) Schl . J O chid Soc India 18:11108
Kuma U, Be line J, Adak T, Ra h PC e al (2017) Non- a ge e ec
o con inuous applica ion o chlo py i os on soil mic obes,
nema odes and i s pe sis ence unde sub-humid opical ice- ice
c opping sys em. Eco oxicol En i on Sa 135:225–235
Kumla J, Danell E, Bussaban B, Lumyong S (2011) Sui able g ow h
condi ions and nu i ion ac o s on in i o cul u e o Phlebopus
po en osus (Bole ales). Chiang Mai J Sci 38:156–159
Kumla J, Danell E, Lumyong S (2015) Imp o emen o yield o a
opical black bole e, Phlebopus po en osus, cul i a ion in
no he n Thailand. Mycoscience 56:114–117
Kumla J, Suwanna ach N, Lumyong S (2016) Cha ac e iza ion o
Pisoli hus o ien alis in cul u e and in i o myco hiza ion wi h
Eucalyp us camaldulensis and Pinus kesiya. Mycosphe e
7:1415–1424
Kumu a H, Tanoue Y, Tsukaha a M, Tanaka T e al (2004) Sc eening
o dai y yeas s ains o p obio ic applica ions. J Dai y Sci
87:4050–4056
116 Fungal Di e si y (2019) 97:1–136
123
Kupco a
´K, S e ano a I, Pla co a Z, Hosek J e al (2018)
An imic obial, cy o oxic, an i-In lamma o y, and an ioxidan
ac i i y o culina y p ocessed shii ake medicinal mush oom
(Len inus edodes, Aga icomyce es) and i s majo sul u senso y-
ac i e compound-Len hionine. In J Med Mush ooms 20:165–
175
Ku zman CP, Fell JW, Boekhou T (2011) The yeas s, a axonomic
s udy, 5 h edn. Else ie , Bu ling on
Kwon H, Tha i ha goon S (2004) Mush oom g owing o a li ing
wo ldwide: mush oom g owing in No he n Thailand. In: Gush
R (ed) Mush oom g owe s’ handbook 1: oys e mush oom
cul i a ion. Mush Wo ld-Heinea Inc, Seoul
Ku
¨es U (2015) Fungal enzymes o en i onmen al managemen . Cu
Opin Bio echnol 33:268–278
Lacey LA, Kaya HK (2007) Field manual o echniques in
in e eb a e pa hology. Applica ion and e alua ion o pa hogens
o con ol o insec s and o he in e eb a e pes s, 2nd edn.
Sp inge , Do d ech , p 484
Lacey LA, Ne en LG (2006) The po en ial o he ungus, Muscodo
albus, as a mic obial con ol agen o po a o ube mo h
(Lepidop e a: Gelechiidae) in s o ed po a oes. J In e eb Pa hol
91:195–198
Lacey LA, G zywacz D, Shapi o-Ilan DI, F u os R, B ownb idge M,
Goe el MS (2015) Insec pa hogens as biological con ol agen s:
back o he u u e. J In e Pa hol 132:1–41
Lai LST, Pan CC, Tzeng BK (2003) The in luence o medium design
on lo as a in p oduc ion and pelle o ma ion wi h a high-
p oducing mu an o Aspe gillus e eus in subme ged cul u es.
P ocess Biochem 38:1317–1326
Lal RJ, Sinha OK, Bha naga S, Lal S, Awas hi SK (2009) Biological
con ol o suga cane smu (Spo iso ium sci amineum) h ough
bo anicals and T ichode ma i ide. Suga Tech 11:381–386
Lale G, Jogdand VV, Gad e RV (2006) Mo phological mu an s o
Gibbe ella ujiku oi o enhanced p oduc ion o gibbe ellic acid.
J Appl Mic obiol 100:65–72
Lama RT, Whi e RB (2001) Myco emedia ion: comme cial s a us
and ecen de elopmen s. In: Maga VS e al (eds) P oceedings
o he six h in e na ional symposium on in si u and on-si e
bio emedia ion, San Diego, CA, ol 6, pp 263–278
Lambe C, Wend L, Hladki AI, S adle M, Si EB (2019)
Hypomon agnella (Hypoxylaceae): a new genus seg ega ed om
Hypoxylon by a polyphasic axonomic app oach. Mycol P og
18:187–201
Lang E, E’Ue G, Kleebe g I, Ma ens R, Zad azil F (1995)
In e ac ion o whi e o ungi and soil mic oo ganisms leading
o biodeg ada ion o soil pollu an s. In: Van Den B ink WJ,
Bosman R, A end F (eds) Con amina ed soil ’95. Soil &
en i onmen , ol 5. Sp inge , Do d ech
Lange L, Pilgaa d B, He bes F-A, Busk PK, Gleason F, Pede sen AG
(2018) O igin o ungal biomass deg ading enzymes: e olu ion,
di e si y and unc ion o enzymes o ea ly lineage ungi. Fungal
Biol Re 33:82–97
La gen DL, B adshaw DE, Wood WF (1990) The candy-like odo o
Nolanea uc u ag ans. Mycologia 82:786–787
La sson E, Jeppson M (2008) Phylogene ic ela ionships among
species and gene a o Lycope daceae based on ITS and LSU
sequence da a om No h Eu opean axa. Mycol Res 112:4–22
Lassois L, de Bellai e LDL, Jijakli MH (2008) Biological con ol o
c own o o bananas wi h Pichia anomala s ain K and Candida
oleophila s ain O. Biol Con ol 45:410–418
Lau ie JD, Ali S, Linning R, Mannhaup G e al (2012) Genome
compa ison o ba ley and maize smu ungi e eals a ge ed loss
o RNA silencing componen s and species-speci ic p esence o
ansposable elemen s. Plan Cell 24:1733–1745
Le Bloc’h J, Pauquai T, Bou ges C (2015) Au ho ised EU heal h
claim o ed yeas ice. In: Sadle M (ed) Foods, nu ien s and
ood ing edien s wi h au ho ised EU heal h claims, ol 2.
Else ie , Ams e dam, pp 139–142
Le Jeune C, Lollie M, Demuy e C, E ny C e al (2007)
Cha ac e iza ion o na u al hyb ids o Saccha omyces ce e isiae
and Saccha omyces bayanus a . u a um. FEMS Yeas Res
7:540–549
Leake JR (2004) Myco-he e o oph/epipa asi ic plan in e ac ions
wi h ec omyco hizal and a buscula myco hizal ungi. Cu
Opin Plan Biol 7:422–428
Lecom e C, Alabou e e C, Edel-He mann V, Robe F, S einbe g C
(2016) Biological con ol o o namen al plan diseases caused by
Fusa ium oxyspo um: a e iew. Biol Con ol 101:17–30
Lee G, A epally GM (2012) An icoagula ion echniques in aphe esis:
om hepa in o ci a e and beyond. J Clin Aphe esis 27:117–125
Lee SY, Mohamed R (2016) The o igin and domes ica ion o
Aquila ia, an impo an aga wood-p oducing genus. In:
Mohamed R (ed) Aga wood. Sp inge , Singapo e, pp 1–20
Lee IK, Yun BS (2006) Hispidin analogs om he mush oom
Inono us xe an icus and hei ee adical sca enging ac i i y.
Bioo g Med Chem Le 16:2376–2379
Lee KH, Wi SG, Singh AP, Kim YS (2004) Mic omo phological
cha ac e is ics o decayed wood and laccase p oduced by he
b own- o ungus Coniopho a pu eana. J Wood Sci 50:281–284
Lee JS, Baik HS, Pa k SS (2006) Pu i ica ion and cha ac e iza ion o
wo no el ib inoly ic p o eases om mush oom Fomi ella
axinea. J Mic obiol Bio echnol 16:264–271
Lee SS, Pa ahayah M, Chong WS, Lapey ie F (2008a) Success ul
ec omyco hizal inocula ion o wo dip e oca p species wi h a
locally isola ed ungus in Peninsula Malaysia. J T op Fo Sci
20:237–247
Lee SW, Lee EH, Eom AH (2008b) E ec s o o ganic a ming on
communi ies o a buscula myco hizal ungi. Mycobiology
36:19–23
Lee SO, Kim HY, Choi GJ, Lee HB e al (2009a) Myco umiga ion
wi h Oxypo us la ema gina us EF069 o con ol o pos ha es
apple decay and Rhizoc onia oo o on mo h o chid. J Appl
Mic obiol 106:1213–1219
Lee SS, Chang YS, No aswa i MNR (2009b) U iliza ion o mac o-
ungi by some indigenous communi ies o ood and medicine in
Peninsula Malaysia. Fo Ecol Manag 257:2062–2065
Lee KH, Mo is-Na schke SL, Yang X, Huang R e al (2012) Recen
p og ess o esea ch on medicinal mush ooms, oods, and o he
he bal p oduc s used in adi ional Chinese medicine. J T ad
Complemen Med 2:1–12
Lehmann J, Joseph S (2009) Biocha o en i onmen al managemen :
an in oduc ion. In: Lehmann J, Joseph S (eds) Biocha o
en i onmen al managemen : science and echnology. Ea hscan,
London, pp 1–12
Leland JE, Mullins DE, Vaughan LJ, Wa en HL (2005) E ec s o
media composi ion on subme ged cul u e spo es o he en o-
mopa hogenic ungus, Me a hizium anisopliae a . ac idum Pa
2: E ec s o media osmolali y on cell wall cha ac e is ics,
ca bohyd a e concen a ions, d ying s abili y, and pa hogenici y.
Biocon ol Sci Technol 15:379–392
Lembeck H (1983) G ossman’s guide o wines, bee s, & spi i s, 7 h
edn. Cha les Sc ibne ’s Sons, New Yo k
Leong HY, Show PL, Lim MH, Ooi CW, Ling TC (2018) Na u al ed
pigmen s om plan s and hei heal h bene i s: a e iew. Food
Re In 34:463–482
Lesage-Meessen L, Dela e M, Haon M, Thibaul JF e al (1996) A
wo-s ep biocon e sion p ocess o anillin p oduc ion om
e ulic acid combining Aspe gillus nige and Pycnopo us
cinnaba inus. J Bio echnol 50:107–113
Lesage-Meessen L, Bou M, Ginies C, Che e D, Na a o D e al
(2018) La ende - and la andin-dis illed s aws: an un apped
eeds ock wi h g ea po en ial o he p oduc ion o high-added
Fungal Di e si y (2019) 97:1–136 117
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