OPINION
published: 11 Feb ua y 2019
doi: 10.3389/ pls.2019.00090
F on ie s in Plan Science | www. on ie sin.o g 1Feb ua y 2019 | Volume 10 | A icle 90
Edi ed by:
Di k Albe Balme ,
Syngen a, Swi ze land
Re iewed by:
Emilio Gue ie i,
Is i u o pe la P o ezione Sos enibile
delle Pian e (CNR), I aly
*Co espondence:
Riikka Linnakoski
[email p o ec ed]
†These au ho s ha e con ibu ed
equally o his wo k
Special y sec ion:
This a icle was submi ed o
Plan Mic obe In e ac ions,
a sec ion o he jou nal
F on ie s in Plan Science
Recei ed: 05 Sep embe 2018
Accep ed: 21 Janua y 2019
Published: 11 Feb ua y 2019
Ci a ion:
Linnakoski R and Fo bes KM (2019)
Pa hogens—The Hidden Face o
Fo es In asions by Wood-Bo ing
Insec Pes s. F on . Plan Sci. 10:90.
doi: 10.3389/ pls.2019.00090
Pa hogens—The Hidden Face o
Fo es In asions by Wood-Bo ing
Insec Pes s
Riikka Linnakoski1
*†and K is ian M. Fo bes 2†
1Na u al Resou ces Ins i u e Finland (Luke), Helsinki, Finland, 2Depa men o Vi ology, Uni e si y o Helsinki, Helsinki, Finland
Keywo ds: co-in ec ion, disease, o es heal h, ungi, pa hogen, insec pes , in asi e species
INTRODUCTION
Fo es s a e one o he mos impo an global ege a ion ypes, se ing unc ions om suppo ing
heal hy wa e shed, o wildli e habi a , and economic indus ies h ough hei ha es ing and
ou ism alue. Unde s anding and mi iga ing h ea s o hese esou ces is he e o e o g ea socie al
impo ance. Fo es pes s a e among he mos pe inen and ob ious h ea s o o es heal h, wi h
hei impac s ampli ied by con empo a y issues such as clima e change and global ade (Allen e al.,
2010; Wing ield e al., 2016). In pa icula , ecen inc eases in he equency and se e i y o insec
ou b eaks ha e led o he loss o signi ican o es a eas om ac oss he globe (Roy e al., 2014) and
highligh ed he need o igo ous esea ch o unde s and he unde lying basis o hei impac s.
In oduced wood-bo ing bee les ha e been pa icula ly damaging, which a e o en eleased om
compe i o s and p eda o s in hei new en i onmen s, and a ge heal hy ees wi hou e ol ed
esis ance. In hei na i e ange, hey ypically colonize only dead o dying ees and a e, he e o e,
no ecognized as ha m ul. Recen examples o in asi e pes s include he eme ald ash bo e (Ag ilus
planipennis), which p ima ily a acks ash ees, he edbay amb osia bee le (Xylebo us glab a us)
in es ing membe s o he lau el amily (Lau aceae), and he Asian longho ned bee le (Anoplopho a
glab ipennis) and polyphagous sho hole bo e (PSHB), which a e capable o in es ing a wide ange
o ee species (Ba anchiko e al., 2008; F aed ich e al., 2008; Haack e al., 2010; Eskalen e al., 2013;
Paap e al., 2018). Since hei acciden al in oduc ions om Asia, hese agg essi e pes s ha e been
implica ed in he mo ali y o millions o ees in Eu ope and No h Ame ica, and he po en ial o
he u he sp ead o hese and o he pes species poses a majo h ea o he heal h o global o es s.
While o es insec pes s ha e unde s andably a ac ed s ong esea ch a en ion, especially in
coun ies whe e o es y is a majo economic indus y, a less unde s ood a e he pa hogens hey
ca y and how hese con ibu e o o es damage, especially unde clima e change. Fo ins ance, he
edbay amb osia bee le, PSHB and longho ned bee les desc ibed abo e ha e each been ound o
ca y assemblages o ungi, including pa hogenic species (F aed ich e al., 2008;Linnakoski e al.,
2018; Paap e al., 2018). He e we ocus on ungal pa hogens ec o ed by wood-bo ing insec pes s,
and a gue ha hey can ampli y he nega i e e ec s o hese pes s and cause signi ican o es
damage in hei own igh (F aed ich e al., 2008; Ploe z e al., 2013). The pu pose o his opinion
a icle is o shed ligh on hese implica ions, discuss he mechanisms unde lying hei in e ac ions
wi h hos ees, and highligh he esea ch equi ed o esol e gaps in knowledge and p og ess
unde s anding o his opic.
WOOD-BORING INSECTS AS FUNGAL VECTORS
In e ac ions be ween ungi and wood-bo ing ba k and amb osia bee les (Figu e 1) a e he mos
in ensi ely s udied pa hogen-insec ela ionships in o es ecosys ems. The na u es o hese
in e ac ions a e di e se, anging om inciden al associa ions in sha ed habi a s o co-e ol ed
obliga e nu i ional mu ualisms (Fa ell e al., 2001; Roe e al., 2011; Hulc and S elinski, 2017).
Linnakoski and Fo bes Fo es Pa hogens
Fungal pa ne s bene i om hese associa ions h ough
enhanced ansmission, ia anspo o new ees and habi a s.
An inc ease in he global ade o wood p oduc s has enhanced
he isk o exo ic insec and ungi in oduc ions (Sikes e al.,
2018), which may be p esen in poo ly ea ed imbe and wood
packaging ma e ials. Scoly ine bee les a e he mos common
g oup o in asi e insec s de ec ed a bo de inspec ions (Lee
e al., 2007; Lawson e al., 2018). Thei niches o e lap wi h na i e
o es insec s in many egions, and as a esul , no el insec - ungal
in e ac ions a e likely o a ise. Unde his scena io, in oduced
in asi e pa hogens may be passed o na i e insec species o
ec o , and in asi e insec pes s may become ec o s o na i e o
al eady es ablished in asi e pa hogens (Haack, 2006; Wing ield
e al., 2016). In bo h cases, no el ungi-hos ee in e ac ions
a e likely o a ise, wi h unp edic able implica ions, and indeed,
such ela ionships a e inc easingly ecognized as a conce n o
o es ecosys ems (Lu e al., 2011; Ploe z e al., 2013; Wing ield
e al., 2016). Less well acknowledged is he possibili y ha he
same ype o no el in e ac ions could esul om dis ibu ional
changes o endemic insec and ee species unde condi ions o
clima e change.
No el bee le- ungus in e ac ions include some o he mos
impo an in asi e species a ec ing o es ecosys ems, such as
he Du ch elm disease and beech ba k disease (Ploe z e al.,
2013; San ini and Faccoli, 2013; Cale e al., 2017). Howe e ,
an unde s anding o he associa ed ungal assemblages such
as hese is a e. Indeed, no el and unexpec ed ec o s and
hos ees ha e e en ecen ly been de ec ed o he ex ensi ely
s udied Du ch elm disease (Jankowiak e al., in p ess). Mos
insec and ungal species a e no ecognized as ha m ul in
hei na i e anges and ha e he e o e ecei ed li le esea ch
a en ion. Such undamen al esea ch is u he complica ed
by he need o accu a e iden i ica ion o insec s and ungi—
hese a e wo o he mos species ich g oups o o ganisms,
he majo i y o which a e undesc ibed (S o k e al., 2015;
Hawkswo h and Lücking, 2017)—bu aided by he con inual
e icacy and a o dabili y o geno yping me hods. Es ablishing
baseline in o ma ion on insec - ungal associa ions is impo an
o unde s anding pa hogenic po en ial when bee les expand in o
new a eas, and a lack o such in o ma ion could hinde he
imeliness o isk assessmen s and mi iga ion s a egies ollowing
insec pes ange expansions.
TREE DAMAGE
T ee damage by ungi is inhe en ly linked o he bee le
li ecycle (Ra a e al., 2015; Hulc and S elinski, 2017). Bee les
play impo an oles in na u al (undis u bed by human
ac i i y) o es ecosys ems, whe e hey ypically in es dead o
weakened ees and hus pa icipa e in o es succession/ enewal
h ough he b eakdown o bioma e (Ra a e al., 2015).
Howe e , occasionally bee les agg ega e, especially a e na u al
dis u bance e en s, and mass a ack heal hy ees in densi ies
su icien o cause signi ican damage (Ra a e al., 2015). As pa
o his p ocess, ungal spo es ca ied on he bee le exoskele on,
in specialized s uc u es called mycangia o ia o he associa ed
o ganisms (such as pho e ic mi es), a e inocula ed in o he ee
sapwood (Linnakoski e al., 2016; Hulc and S elinski, 2017).
I is no well-known why some bee les ha usually colonize
dead o s essed hos s in hei na i e ange a ack heal hy ees
when a i ing in a new a ea (Hulc and Dunn, 2011). Recen
examples o his p ocess include bo h insec s capable a acking
a wide ange o hos ees (A. glab ipennis and PSHB), and hose
in es ing a na ow ange o hos s (such as A. planipennis and X.
glab a us) (Ba anchiko e al., 2008; F aed ich e al., 2008; Haack
e al., 2010; Eskalen e al., 2013; Paap e al., 2018).
Al hough connec ions be ween insec damage and ungal
ac i i y in wood we e ecognized as ea ly as he 19 h cen u y
(Ha ig, 1878), i has been di icul o elucida e he ela i e oles
o each in ee damage as hey ypically occu in mul ipa i e
associa ions in “noisy” na u al sys ems. Howe e , ecen s udies
ha e shed ligh on he po en ial o pa hogens o ampli y
insec damage (and ice e sa), indica ing ha a leas some
ungal associa es ha e he abili y o ca abolize coni e de ense
compounds and imp o e bee le unneling beha io (Wadke e al.,
2016; Zhao e al., 2018). Indeed, Zhao e al. (2018) ound
ha ba k bee les p e e ed subs a e colonized by ungi and
a oided phenolics (plan de ense compounds). Al hough ee
damage is o en a ibu ed o insec s, he ole o ungal pa hogens
in lowe ing hos de enses is likely o be impo an in many
cases: pa i ioning damage caused by ungi and bee les may be
impo an o a ge ing mi iga ing s a egies and should be a
p io i y o u u e esea ch.
Clea ly ee esis ance is a c i ical pa ame e when
conside ing he nega i e impac s o insec pes s and pa hogens.
En i onmen al pe u ba ions, especially hose associa ed wi h
clima e change, such as d ough s, loods, s o ms, and ele a ed
empe a u es, a e pa icula ly conce ning. These e en s can
cause physical damage o ees (Allen e al., 2010), enhancing he
ease o coloniza ion by insec s and hei accompanying ungal
pa hogens, while p olonged s ess may also impai he abili y
o ees o di ec esou ces owa d de ense and epai (Bol on,
2009). Fo example, inocula ion expe imen s wi h No way
sp uce seedlings ha e demons a ed ha empe a u e and CO2
le el inc eases based on u u e clima e p edic ions, as well as
educed wa e a ailabili y, can ampli y he damage caused by
ce ain ungal species (Linnakoski e al., 2017a,b); al hough
he ex en o which hese indings a e caused by changes in
ungal i ulence as opposed o hos esis ance, emains o
be de e mined.
CONCURRENT INFECTIONS
As pa o hei li ecycle, bee les can acqui e and deposi mul iple
ungi (bo h co-e ol ed symbio ic and oppo unis ic species) a
he same ime. Fo example, o 298 sp uce ba k bee les sampled
du ing an ou b eak in Finland, mo e han wo ungal species we e
concu en ly ound on o e 40% o indi iduals (Linnakoski e al.,
2016). Indeed, i is e y likely ha mos ees a e simul aneously
in ec ed by mul iple pa hogens (co-in ec ions). Howe e , up un il
ecen ly he p e ailing pa adigm o in ec ion biology was based
on a single pa hogen causing a single disease (shown using Koch’s
F on ie s in Plan Science | www. on ie sin.o g 2Feb ua y 2019 | Volume 10 | A icle 90
Linnakoski and Fo bes Fo es Pa hogens
FIGURE 1 | The bee le li ecycle and ole in ungi ansmission. T ee damage caused by ungi associa ed wi h wood-bo ing insec s is inhe en ly linked o he bee le
li ecycle. The bee le li e cycle begins ollowing ha ching om an egg in a ma e nal galle y ( unnel) unde he ee ba k. The la ae emains in he unnels, eeds on he
phloem and gnaws unnels. Du ing his s age, ungi g ow and spo ula e and can se e as a sou ce o nu i ion o bee le la ae. La ae pupa e and de elop in o adul s
unde he ba k, be o e lying in sea ch o new hos ees and anspo ing ungi wi h hem. Fungal spo es ca ied on hei exoskele on, in specialized s uc u es called
mycangia o ia o he associa ed o ganisms, a e hen inocula ed in o a new hos ee.
pos ula es), and his ou -da ed model emains dominan in o es
pa hology (Tollenae e e al., 2016).
Mos esea ch ocused on he po en ial ole o co-in ec ions
in plan diseases comes om ag icul u al sys ems (Lamichhane
and Ven u i, 2015; Tollenae e e al., 2016). He e s udies ha e
demons a ed cases in which se e e plan disease can esul
om co-in ec ions bu no om single in ec ions (Rochow
and Ross, 1955)—bu also ha co-in ec ions can educe he
nega i e impac s o a se e e pa hogen (Round and Wheele ,
1978). In o es y, a ecen s udy demons a ed he ole o co-
in ec ions as a cause o Acu e Oak Decline (Denman e al.,
2018). Fungal i uses (myco i uses) may also cause changes
in ungus agg essi eness (Pea son e al., 2009; Vainio e al.,
2018) and he e o e al e ee disease ou comes. I is es ablished
om o es pa hosys ems ha ungal species and s ains in e ac
wi h each o he and di e in hei pa hogenic po en ial
(K okene and Solheim, 1998; Repe e al., 2015; Linnakoski
e al., 2017a,b). As a esul , seconda y in ec ions wi h less
i ulen species o s ains may p o ide mi iga ion ools agains
disease ou b eaks.
CONTROL OF FUNGAL FOREST
INFECTIONS
The mos e icien s a egy o p o ec ees is o p e en he
in oduc ion o wood-bo ing insec s and hei associa ed
pa hogens. Un o una ely, cu en egula o y e o s a e
inadequa e o de ec unknown species (Roy e al., 2014), and
in se e al cases, damaging in asi e o es pes s and pa hogens
F on ie s in Plan Science | www. on ie sin.o g 3Feb ua y 2019 | Volume 10 | A icle 90
Linnakoski and Fo bes Fo es Pa hogens
ha e been no el o science, o poo ly unde s ood in hei
na i e en i onmen .
Wha hen can be done? As he ans e o ungal pa hogens
is in ima ely connec ed o wood-bo ing insec s, con ol e o s
a ge ed a insec ec o s a e likely o be mos e ec i e.
Inno a i e biocon ol ools, such as ola ile compounds (VOCs),
can o m pa o an in eg a ed s a egy. These egula e insec
communica ion and can be u ilized as po en ial epellen s agains
bee les a ou bound anspo poin s o inc ease he e icacy
o lu ing aps (Kandasamy e al., 2016; Hughes e al., 2017).
Following p e en ion, ea ly de ec ion and ange minimiza ion
a e impo an , and should occu in u ban a eas ha se e
as en y poin s o in asions (Colunga-Ga cia e al., 2010;
Paap e al., 2017), and by o es moni o ing and emo al o
in es ed ees by sani a ion cu ings. Mo e widesp ead s a egies
include he use o o he pa hogens as biocon ol agen s o
enhance he na u al de ense mechanism o ees and in e e e
wi h in ec ions (Pos ma and Goossen- an de Geijn, 2016). Fo
example, en omopa hogens can be used as biocon ol agen s
agains wood-bo ing bee les (Hajek and an F ankenhuyzen,
2017), and myco i uses can be u ilized in he con ol o ungal
o es pa hogens (Pea son e al., 2009; Vainio e al., 2018).
Howe e , he de elopmen o any biological con ol ool is a
long p ocess, which i s equi es sound knowledge o each
o ganism in ol ed.
CONCLUSIONS
Managing inc easingly dis u bed o es s will be an impo an
global challenge mo ing o wa d. While signi ican esea ch
e o has been de o ed o unde s anding and mi iga ing he
e ec s o insec pes s on o es heal h (Vega and Ho s e e , 2015),
in his a icle we highligh he compa a i ely neglec ed ole o he
ungal pa hogens hey ca y. These a e able o in lic signi ican
o es damage (Wing ield e al., 2016), and i is likely ha hei
nega i e impac s will be ampli ied o e u u e decades due o
en i onmen al pe u ba ions associa ed wi h clima e change.
Fundamen al baseline in o ma ion on he di e si y and
equency o mos insec - ungal associa ions is cu en ly
lacking. Such in o ma ion is impo an o ecognizing
no el ec o - ungi associa ions, which ha e he po en ial
o cause se ious o es damage (Ploe z e al., 2013;
Wing ield e al., 2016), and may aid in he imeliness
o isk assessmen s and mi iga ion s a egies ollowing
dis ibu ional changes o insec pes s. The equency and
ex en o which ungal associa es acili a e and ampli y
insec damage is an in iguing line o enqui y and ano he
a ea in need o esea ch a en ion. Al hough e idence is
cu en ly limi ed o a small numbe o s udies and sys ems,
such as Du ch elm disease (Ploe z e al., 2013; San ini and
Faccoli, 2013), i may be a common phenomenon associa ed
wi h insec damage and p o ide a po en ial means o limi
hei impac .
While impo an ad ances ha e been made in unde s anding
he impac s o ungal pa hogens associa ed wi h o es insec
pes s, many pe inen ques ions emain and we hope his a icle
will help s imula e esea ch o in es iga e hem.
AUTHOR CONTRIBUTIONS
All au ho s lis ed ha e made a subs an ial, di ec and
in ellec ual con ibu ion o he wo k, and app o ed i
o publica ion.
ACKNOWLEDGMENTS
We hank D . Ris o Kasanen o commen ing on an ea lie
e sion o he manusc ip .
REFERENCES
Allen, C. D., Macalady, A. K., Chenchouni, H., Baachele , D., McDowell, N.,
Venne ie , M., e al. (2010). A global o e iew o d ough and hea induced ee
mo ali y e eals eme ging clima e change isks o o es s. Fo es Ecol. Manag.
259, 660–684. doi: 10.1016/j. o eco.2009.09.001
Ba anchiko , Y., Mozole skaya, E., Yu chenko, G., and Kenis, M. (2008).
Occu ence o he eme ald ash bo e , Ag ilus planipennis in Russia and
i s po en ial impac on Eu opean o es y. EPPO Bull. 38, 233–238.
doi: 10.1111/j.1365-2338.2008.01210.x
Bol on, M. D. (2009). P ima y me abolism and plan de ense- uel o he i e. Mol.
Plan Mic obe In e ac . 22, 487–497. doi: 10.1094/MPMI-22-5-0487
Cale, J. A., Ga ison-Johns on, M. T., Teale, S. A., and Cas ello, J. D. (2017). Beech
ba k disease in No h Ame ica: o e a cen u y o esea ch e isi ed. Fo es Ecol.
Manag. 394, 86–103. doi: 10.1016/j. o eco.2017.03.031
Colunga-Ga cia, M., Maga ey, R. A., Haack, R. A., Gage, S. H., and Qi, J.
(2010). Enhancing ea ly de ec ion o exo ic pes s in ag icul u al and o es
ecosys ems using an u ban-g adien amewo k. Ecol. Appl. 20, 303–310.
doi: 10.1890/09-0193.1
Denman, S., Doonan, J., Ransom-Jones, E., B obe g, M., Plumme , S., Ki k, S.,
e al. (2018). Mic obiome and in ec i i y s udies e eal complex polyspecies
ee disease in acu e oak decline. ISME J. 12, 386–399. doi: 10.1038/ismej.
2017.170
Eskalen, A., S ou hame , R., Lynch, S. C., and Twizeyimana, M. (2013). Hos ange
o Fusa ium dieback and i s amb osia bee le (Coleop e a: Scoly inae) ec o in
sou he n Cali o nia. Plan . Dis. 97, 938–951. doi: 10.1094/PDIS-11-12-1026-RE
Fa ell, B. D., Sequei a, A. S., O’Mea a, B. C., No ma k, B. B., Chung,
J. H., and Jo dal, B. H. (2001). The e olu ion o ag icul u e in bee les
(Cu lulionidae:Scoly inae and Pla ypodinae). E olu ion 55, 2011–2027.
doi: 10.1111/j.0014-3820.2001. b01318.x
F aed ich, S. W., Ha ing on, T. C., Rabaglia, R. J., Ulyshen, M. D., May ield, A.
E. III, Hanula, J. L., e al. (2008). A ungal symbion o he edbay amb osia
bee le causes a le hal wil in edbay and o he Lau aceae in he sou heas e n
Uni ed S a es. Plan Dis. 92, 215–224 doi: 10.1094/PDIS-92-2-0215
Haack, R. A. (2006). Exo ic ba k- and wood-bo ing Coleop e a in he Uni ed S a es:
ecen es ablishmen s and in e cep ions. Can. J. Fo es Res. 36, 269–288.
doi: 10.1139/x05-249
Haack, R. A., Hé a d, F., Sun, J., and Tu geon, J. J. (2010). Managing
in asi e popula ions o Asian longho ned bee le and ci us longho ned
bee le: a wo ldwide pe spec i e. Annu. Re . En omol. 55, 521–546.
doi: 10.1146/annu e -en o-112408-085427
Hajek, A. E., and an F ankenhuyzen, K. (2017). “Use o en omopa hogens agains
o es pes s,” in Mic obial Con ol o Insec and Mi e Pes s, ed L. A. Lacey (San
Diego, CA: Academic P ess), 313–330.
Ha ig, R. (1878). Die Ze se zungse scheinungen des Holsez de Nadelbäume und
de Eiche in Fo s liche , Bo anische und Chemische Rich ung. Be lin: Sp inge
F on ie s in Plan Science | www. on ie sin.o g 4Feb ua y 2019 | Volume 10 | A icle 90
Linnakoski and Fo bes Fo es Pa hogens
Hawkswo h, D., and Lücking, R. (2017). Fungal di e si y e isi ed:
2.2 o 3.8 million species. Mic obiol. Spec um 5:FUNK-0052-2016.
doi: 10.1128/mic obiolspec.FUNK-0052-2016
Hughes, M. A., Ma ini, X., Kuhns, E., Colee, J., Ma a-Ne o, A., S elinski, L. L.,
e al. (2017). E alua ion o epellen s o he edbay amb osia bee le, Xylebo us
glab a us, ec o o he lau el wil pa hogen. J. Appl. En omol. 141, 653–664.
doi: 10.1111/jen.12387
Hulc , J., and Dunn, R. R. (2011). The sudden eme gence o pa hogenici y in
insec - ungus symbioses h ea ens naï e o es ecosys ems. P oc. Biol. Sci. 1720,
2866–2873. doi: 10.1098/ spb.2011.1130
Hulc , J., and S elinski, L. (2017). The amb osia symbiosis: om e olu iona y
ecology o p ac ical managemen . Annu. Re . En omol. 62, 285–303.
doi: 10.1146/annu e -en o-031616-035105
Jankowiak, R., S załka, B., Bila´
nski, P., Kacp zyk, M., Wieczo ek, P., and
Linnakoski, R. (in p ess). Ophios oma oid ungi associa ed wi h ha dwood-
in es ing ba k and amb osia bee les in Poland: axonomic di e si y and ec o
speci ici y. Fungal Ecol.
Kandasamy, D., Ge shenzon, J., and Hamme bache , A. (2016). Vola ile
o ganic compounds emi ed by ungal associa es o coni e ba k bee les
and hei po en ial in ba k bee le con ol. J. Chem. Ecol. 42, 952–969.
doi: 10.1007/s10886-016-0768-x
K okene, P., and Solheim, H. (1998). Assessing he i ulence o ou ba k bee le-
associa ed blues ain ungi using No way sp uce seedlings. Plan Pa hol. 47,
537–540. doi: 10.1046/j.1365-3059.1998.00268.x
Lamichhane, J. R., and Ven u i, V. (2015). Syne gism be ween mic obial
pa hogens in plan disease complexes: a g owing end. F on . Plan Sci. 6:385.
doi: 10.3389/ pls.2015.00385
Lawson, S. A., Ca negie, A. J., Came on, N., Wa dlaw, T., and Venn, T. J. (2018).
Risk o exo ic pes s o he Aus alian o es indus y. Aus . Fo es y 81, 3–13.
doi: 10.1080/00049158.2018.1433119
Lee, J. C., Haack, R. A., Neg ón, J. F., Wi cosky, J. J., and Seybold, S. J. (2007).
In asi e Ba k bee les. US Depa men o Ag icul u e, US Fo es Se ice, Fo es
Insec and Disease Lea le 176. A ailable online a : h p://pu l.access.gpo.go /
GPO/LPS90197 (Accessed July 8, 2018).
Linnakoski, R., Fo bes, K. M., Wing ield, M. J., Pulkkinen, P., and Asiegbu, F. O.
(2017a). Tes ing p ojec ed clima e change condi ions on he Endoconidiopho a
polonica / No way sp uce pa hosys em shows ungal s ain speci ic e ec s.
F on . Plan Sci. 8:883. doi: 10.3389/ pls.2017.00883
Linnakoski, R., Kasanen, R., Lasa o , I., Ma inen, T., Ogheneka o, A. O.,
Asiegbu, F. O., e al. (2018). Cadopho a ma ga i a a sp. no . and o he
ungi associa ed wi h he longho n bee les Anoplopho a glab ipennis
and Sape da ca cha ias in Finland. An onie Leeuwenhoek 111, 2195–2211.
doi: 10.1007/s10482-018-1112-y
Linnakoski, R., Mahilainen, S., Ha ing on, A., Vanhanen, H., E iksson,
M., Meh ä alo, L., e al. (2016). Seasonal succession o ungi associa ed
wi h Ips ypog aphus bee les and hei pho e ic mi es in an ou b eak
egion o Finland. PLoS ONE 11:e0155622. doi: 10.1371/jou nal.pone.01
55622
Linnakoski, R., Sugano, J., Jun ila, S., Pulkkinen, P., Asiegbu, F. O., and
Fo bes, K. M. (2017b). E ec s o wa e a ailabili y on a o es y pa hosys em:
ungal s ain-speci ic a ia ion in disease se e i y. Sci. Rep. 7:13501.
doi: 10.1038/s41598-017-13512-y
Lu, M., Wing ield, M. J., Gille e, N. E., and Sun, J.-H. (2011). Do no el geno ypes
d i e he success o an in asi e ba k bee le- ungus complex? Implica ions o
po en ial ein asion. Ecology 92, 2013–2019. doi: 10.1890/11-0687.1
Paap, T., Bu gess, T. I., and Wing ield, M. J. (2017). U ban ees: b idge o o es
pes in asions and sen inels o ea ly de ec ion. Biol. In asions 19, 3515–3526.
doi: 10.1007/s10530-017-1595-x
Paap, T., de Bee , Z. W., Miglio ini, D., Nel, W., and Wing ield, M. J. (2018).
The polyphagous sho hole bo e (PSHB) and i s ungal symbion Fusa ium
euwallaceae: a new in asion in Sou h A ica. Aus alas. Plan Pa hol. 47,
231–237. doi: 10.1007/s13313-018-0545-0
Pea son, M. N., Bee e , R. E., Boine, B., and A hu , K. (2009). Myco i uses o
ilamen ous ungi and hei ele ance o plan pa hology. Mol. Plan . Pa hol.
10, 115–128. doi: 10.1111/j.1364-3703.2008.00503.x
Ploe z, R. C., Hulc , J., Wing ield, M. J., and de Bee , Z. W. (2013). Des uc i e ee
diseases associa ed wi h amb osia and ba k bee les: black swan e en s in ee
pa hology? Plan Dis. 97, 856–872. doi: 10.1094/PDIS-01-13-0056-FE
Pos ma, J., and Goossen- an de Geijn, H. (2016). Twen y- ou yea s o du ch
ig applica ion o con ol du ch elm disease. Biocon ol 61, 305–312.
doi: 10.1007/s10526-016-9731-6
Ra a, K. F., G égoi e, J.-L., and Lindg en, B. S. (2015). “Na u al his o y and ecology
o ba k bee les,” in Ba k bee les: Biology and Ecology o Na i e and In asi e
Species, eds F. Vega and R. Ho s e e (London: Academic P ess), 1–40.
Repe, A., Bojo i´
c, S., and Ju c, M. (2015). Pa hogenici y o ophios oma oid ungi
on Picea abies in Slo enia. Fo . Pa hol. 45, 290–297. doi: 10.1111/e p.12170
Rochow, W. F., and Ross, A. F. (1955). Vi us mul iplica ion in plan s
double in ec ed by po a o i uses X and Y. Vi ology 1, 10–27.
doi: 10.1016/0042-6822(55)90003-9
Roe, A. D., James, P. A. M., Rice, A. V., Cooke, J. E. K., and Spe ling, F. A. H. (2011).
Spa ial communi y s uc u e o moun ain pine bee le ungal symbion s ac oss a
la i udinal g adien . Mic ob. Ecol. 62, 347–360. doi: 10.1007/s00248-011-9841-8
Round, P. A., and Wheele , B. E. J. (1978). In e ac ions o Puccinia ho dei
and E ysiphe g aminis on seedling ba ley. Ann. Appl. Biol. 89, 21–35.
doi: 10.1111/j.1744-7348.1978. b02563.x
Roy, B. A., Alexande , H. M., Da idson, J., Campbell, F. T., Bu don, J. J., Sniezko,
R., e al. (2014). Inc easing o es loss wo ldwide om in asi e pes s equi es
new ade egula ions. F on . Ecol. En i on. 12, 457–465. doi: 10.1890/130240
San ini, A., and Faccoli, M. (2013). Du ch elm disease and elm ba k
bee les: a cen u y o associa ion. iFo es Biogeosci. Fo es . 8, 126–134.
doi: 10.3832/i o 1231-008
Sikes, B. A., Bu o d, J. L., Hulme, P. E., Coope , J. A., Johns on, P. R., and Duncan,
R. P. (2018). Impo olumes and biosecu i y in e en ions shape he a i al
a e o ungal pa hogens. PLoS Biol. 16:e2006025.
S o k, N. E., McB oom, J., Gely, C., and Hamil on, A. J. (2015). New app oaches
na ow global species es ima es o bee les, insec s, and e es ial a h opods.
P oc. Na l. Acad. Sci. U.S.A. 116, 7519–7523. doi: 10.1073/pnas.1502408112
Tollenae e, C., Susi, H., and Laine, A.-L. (2016). E olu iona y and epidemiological
implica ions o mul iple in ec ion in plan s. T ends Plan Sci. 21, 80–90.
doi: 10.1016/j. plan s.2015.10.014
Vainio, E. J., Ju ansuu, J., Hyde , R., Kashi , M., Pi i, T., Tuomi i a, T., e al.
(2018). He e obasidion pa i i i us 13 media es se e e g ow h debili a ion and
majo al e na ions in he gene exp essiono a ungal o es pa hogen. J. Vi ol.
92:e01744–e01717. doi: 10.1128/JVI.01744-17
Vega, F., and Ho s e e , R. (eds.). (2015). Ba k Bee les: Biology and Ecology o
Na i e and In asi e Species. London: Academic P ess.
Wadke, N., Kandasamy, D., Vogel, H., Lah, L., Wing ield, B. D., Pae z, C., e al.
(2016). The ba k bee le-associa ed ungus, Endoconidiopho a polonica, u ilizes
he phenolic de ense compounds o i s hos as a ca bon sou ce. Plan Physiol.
171, 914–931. doi: 10.1104/pp.15.01916
Wing ield, M. J., Ga nas, J. R., Hajek, A., Hu ley, B. P., de Bee , Z. W., and
Tae um, S. J. (2016). No el and co-e ol ed associa ions be ween insec s and
mic oo ganisms as d i e s o o es pes ilence. Biol. In asions 18, 1045–1056.
doi: 10.1007/s10530-016-1084-7
Zhao, T., Kandasamy, D., K okene, P., Chen, J., Ge shenzon, J., and
Hamme bache , A. (2018). Fungal associa ed o he ee-killing ba k
bee le, Ips ypog aphus, a y in i ulence, abili y o deg ade coni e
phenolics and in luence ba k bee le unnelling beha iou . Fungal Ecol.
doi: 10.1016/j. uneco.2018.06.003. [Epub ahead o p in ].
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F on ie s in Plan Science | www. on ie sin.o g 5Feb ua y 2019 | Volume 10 | A icle 90