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Phy opa hologia Medi e anea (2013) 52, 2, 245−261
Co esponding au ho : J. A mengol
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REVIEW
Black- oo disease o g ape ine: an upda e on axonomy,
epidemiology and managemen s a egies
Ca los aGUsTÍ-B IsaCH and Josep a MeNGol
Ins i u o Ag o o es al Medi e áneo, Uni e sidad Poli écnica de Valencia, Camino de Ve a s/n, 46022-Valencia, Spain
Summa y. Black- oo is one o he mos des uc i e g ape ine unk diseases in nu se ies and young ineya ds,
causing nec o ic oo lesions, wood nec osis o he oo s ock base, and a g adual decline and dea h o g ape ines.
Causal agen s o he disease a e included in o he gene a Campyloca pon, “Cylind oca pon”, Cylind ocladiella and Ily-
onec ia. Recen axonomical s udies o Neonec ia and ela ed gene a wi h “Cylind oca pon”-like anamo phs based
on mo phological and phylogene ic s udies, di ided Neonec ia in o i e gene a. Thus, he cu en axonomical po-
si ion and classi ica ion o he causal agen s o black- oo disease, mainly “Cylind oca pon”/Ilyonec ia, comp ises
one o he main opics o his e iew. The e iew also p o ides an upda e on geog aphical dis ibu ion, epidemiol-
ogy and managemen s a egies o he disease.
Key wo ds: Campyloca pon, “Cylind oca pon”, Cylind ocladiella, Ilyonec ia, Vi is ini e a.
In oduc ion
Black- oo disease o g ape ines is a se ious dis-
ease in mos wine and g ape-p oducing egions
o he wo ld, pa icula ly in nu se ies and young
ineya ds (Halleen e al., 2006a). The causal agen s
a e included in o he gene a Campyloca pon, “Cylin-
d oca pon”, Cylind ocladiella and Ilyonec ia (C ous
e al., 1993; Halleen e al. 2004; Halleen e al., 2006b;
Sch oe s e al., 2008; Cha e i e al., 2011; Cab al e
al., 2012a, c; Lomba d e al., 2012). This disease was
i s desc ibed in 1961 (G asso and Magnano Di San
Lio, 1975), and o e he las decade, i s incidence has
inc eased signi ican ly in mos g ape ine p oduc-
ion a eas o he wo ld (Halleen e al., 2006a; Alaniz
e al., 2007).
Al hough hese pa hogens usually mani es on
ma u e g ape ines, hey ha e also been equen ly
isola ed om symp oma ic o asymp oma ic oo -
s ock mo he -plan s, oo ed oo s ock cu ings,
bench-g a and young g a ed ines in di e en
g ape ine p oduc ion a eas a ound he wo ld, be-
ing conside ed he mos common pa hogenic ungi
associa ed wi h young nu se y ines (Rumbos and
Rumbou, 2001; Halleen e al., 2003; Fou ie and Hal-
leen, 2004; Oli ei a e al., 2004; A oca e al., 2006;
Dub o sky and Fab i ius, 2007; Halleen e al., 2007).
Mo eo e , i is well known ha hese pa hogens a e
common in he soil causing in ec ion o g a ed ines
a e some mon hs o g ow h in nu se y soils (Hal-
leen e al. 2003, 2007; Cha e i e al., 2011).
Cha ac e is ic symp oms o black- oo disease in-
clude a educ ion in oo biomass and oo hai s wi h
sunken and nec o ic oo lesions (Rego e al., 2000;
Halleen e al., 2006a; Alaniz e al., 2007, 2009; Ab eo e
al., 2010). In some cases he oo s ock diame e o old-
e ines is hinne below he second ie . To compen-
sa e o he loss o unc ional oo s, a second c own
o ho izon ally g owing oo s is some imes o med
close o he soil su ace. Remo al o oo s ock ba k
e eals black discolo a ion and nec osis o wood is-
sue which de elops om he base o he oo s ock
(Figu es 1A, 1B). The pi h is also compac ed and dis-
Phy opa hologia Medi e anea
246
C. Agus í-B isach and J. A mengol
colo ed (Scheck e al., 1998b; La ignon, 1999; Fou ie
and Halleen, 2001; Halleen e al., 2006a).
Ex e nal symp oms show educed igou wi h
small-sized unks, sho ened in e nodes, une en
wood ma u i y, spa se oliage, and small lea es wi h
in e einal chlo osis and nec osis (Figu es 1C, 1D).
Field symp oms o black- oo disease a ec ed ines
a e equen ly indis inguishable om hose o caused
by Pe i disease (Scheck e al., 1998b; Rego e al., 2000;
Halleen e al., 2006a; Alaniz e al., 2007, 2009; Ab eo e
al., 2010). When young ines a e in ec ed, dea h oc-
cu s quickly, ne e heless as he ine ages, in ec ion
esul s in a mo e g adual decline and dea h migh
only occu a e a yea (Guble e al., 2004). Disease
symp oms on ma u e ines (5 yea s and olde ) a e
no iced ea ly in he g owing season. A ec ed ines
achie e poo new g ow h, ail o o m shoo s a e
win e do mancy, and die by mid-summe . O en
shoo s also d y and die du ing he summe . Vines
wi h educed ege a i e g ow h also die du ing he
subsequen do man win e pe iod (Halleen e al.,
2006a).
Causal agen s
Taxonomy and dis ibu ion
The common name black- oo disease was p o-
posed by Scheck e al. (1998b), o designa e he dis-
ease caused by “Cylind oca pon” des uc ans (Zinnsm.)
B
C
D
A
Figu e 1. A, black discolo a ion and nec osis o wood issue which de elops om he base o he oo s ock, cha ac e is ic
o black- oo disease; B, longi udinal sec ion o a oo s ock showing da k-b own o black discolo a ion; C, Un-sp ou ed
g ape ine p opaga ion ma e ial in a g ape ine nu se y; D, g ape ine plan s showing s unded g ow h, educed igou and
e a ded sp ou ing in a young plan a ion.
247
Vol. 52, No. 2, Augus , 2013
An upda e o black- oo disease o g ape ine
Schol en and “C.” ob usispo um (Cooke & Ha kn.)
Wollenw., which we e he wo species adi ionally
epo ed as he causal agen s o basal o o oo ne-
c osis on g ape ines. Ne e heless, his disease was
al eady named as “pied noi ” in F ench language
since 1969, because o he p esence o black nec osis
on he base o diseased oo s ocks (Badou , 1969).
The i s epo o “C.” des uc ans on g ape ine
was made in F ance in 1961 (Malu a and La ignon,
1991). Since hen, i has been isola ed om diseased
ines in I aly (G asso, 1984), Po ugal (Rego, 1994),
Cali o nia (Scheck e al., 1998b), A gen ina (Ga ica e
al., 2001), Ge many (Fische and Kassemeye , 2003),
Pennsyl ania (Gugino and T a is, 2003), New Zea-
land and Sou h A ica (Halleen e al., 2004), B azil
(Ga ido e al., 2004) and Canada (Pe i e al., 2011).
“Cylind oca pon” ob usispo um, has also been epo -
ed o p oduce black- oo symp oms on g ape ine in
Sicily (G asso and Magnano di San Lio, 1975) and
Cali o nia (Scheck e al., 1998a).
The gene ic name “Cylind oca pon” was in o-
duced in 1913 by Wollenwebe o anamo phs be-
longing o Nec ia sec ion Willkommio es Wollenw.
This sec ion included species wi hou chlamydo-
spo es. Few yea s la e , in 1917, Wollenwebe ex-
panded he concep o “Cylind oca pon” o include
species o ming mycelial chlamydospo es in cul u e,
being “C.” des uc ans he mos impo an membe
o his g oup (B ay o d, 1993). In 1966, Boo h spli
he genus in o ou g oups based on he p esence
o absence o mic oconidia and chlamydospo es:
(i) “Cylind oca pon” magnusianum (Sacc.) Wollenw.,
which was he anamo ph o he ype species o Neo-
nec ia, (ii) “C.” cylind oides Wollenw., which was he
ype species o he genus “Cylind oca pon”, (iii) “C.”
des uc ans, which was he anamo ph o Neonec ia
adicicola, and (i ) membe s o “Cylind oca pon” spe-
cies p edominan ly connec ed wi h eleomo phs o
he ‘Nec ia’ mammoidea g oup (B ay o d, 1993; Hal-
leen e al., 2006a). “Cylind oca pon” ob usispo um was
o iginally desc ibed om he USA (Cali o nia) as oc-
cu ing on Acacia sp., whe e i was obse ed o o m
mac oconidia and chlamydospo es (Boo h, 1966).
“Cylind oca pon” ob usispo um s ains iden i ied by
Boo h (1966) o igina ed om a b oad ange o hos
plan s in Eu ope, New Zealand, No h Ame ica, and,
a leas pa ly, o med mic oconidia.
T adi ionally, ep esen a i es o all ‘Nec ia’
g oups wi h “Cylind oca pon” anamo phs we e
ans e ed in o Neonec ia (Rossman e al., 1999;
Man i i e al., 2001; B ay o d e al., 2004). Man i i e al.
(2001) and B ay o d e al. (2004) analyzed mi ochon-
d ial small subuni (SSU) ibosomal DNA ( DNA)
sequence da a o some o he species and concluded
ha he Neonec ia/“Cylind oca pon” species g ouped
oge he by his eclassi ica ion we e monophyle ic.
Howe e , hese au ho s also ound ha his o e all
Neonec ia/“Cylind oca pon” clade included dis inc
subclades co esponding o a leas h ee o he ou
g oups delinea ed by Boo h (1966). Signi ican mo-
lecula a ia ion among axa wi h “Cylind oca pon”-
like anamo phs was ound by Sei e e al. (2003) in
a s udy on ungi causing oo o o ginseng (Panax
quinque olius L.) and o he hos s. The dend og ams
in his s udy, based on pa ial β- ubulin gene (TUB),
and nuclea ibosomal in e nal ansc ibed space
(ITS) egion sequences, sugges ed ha subclades
including (i) Neon. adicicola, which consis ed o
nume ous phylogene ically dis inc uni s, (ii) Neon.
mac oconidialis (Samuels & B ay o d) Sei e , and (iii)
a subclade comp ising wo dis inc isola es, one om
V. ini e a in On a io, Canada and he o he om Pi-
cea sp. in Quebec, Canada, we e monophyle ic. O h-
e “Cylind oca pon” species appea ed o be excluded
om his monophyle ic g oup (Halleen e al., 2006a).
Signi ican a ia ion in cul u al and mo phologi-
cal cha ac e s was obse ed among “Cylind oca pon”
s ain isola es om g ape ines in nu se ies and ine-
ya ds o Sou h A ica, New Zealand, Aus alia and
F ance, which we e mo phologically and phyloge-
ne ically cha ac e ized by Halleen e al., (2004). Thus,
hese au ho s desc ibed a no el species, “C.” mac o-
didymum Sch oe s, Halleen & C ous, also associa ed
wi h black- oo disease o g ape ines. Since hen,
his species has been epo ed in Cali o nia (Pe i
and Guble , 2005), Po ugal (Rego e al., 2005), Chile
(Auge e al., 2007), Spain (Alaniz e al., 2007), U u-
guay (Ab eo e al., 2010), no heas e n Uni ed S a es
and sou heas e n Canada (Pe i e al., 2011) and Tu -
key (Özben e al., 2012).
“Cylind oca pon” ob usispo um and “C.” mac o-
didymum had been conside ed as wo di e en spe-
cies associa ed wi h black- oo disease o g ape ines.
Ne e heless, Halleen e al. (2004) sugges ed he pos-
sibili y ha G asso and Magnano di San Lio (1975)
and Scheck e al. (1998a) misiden i ied “C.” ob usispo-
um and ha i was in ac “C.” mac odidymum. In
his sense, Halleen e al. (2004) indica ed ha mac-
oconidia o “C.” mac odidymum measu e [(26–)34–
36–38(–45)×(4–)5.5–6–6.5(–8) μm], whe eas hose o
Phy opa hologia Medi e anea
248
C. Agus í-B isach and J. A mengol
he ype o “C.” ob usispo um measu e (30–35×4–5
μm) (Cooke, 1884). Howe e , he shape o he mac-
oconidia dis inguishes “C.” mac odidymum om he
ype o “C.” ob usispo um, which Cooke (1884) de-
sc ibed as ha ing conidia wi h ob use ends. Boo h
(1966) desc ibed mac oconidia o simila shape in
“C.” ob usispo um. Acco ding o Boo h, howe e ,
2–3-sep a e mac oconidia o “C.” ob usispo um meas-
u e (34–50×6–7.5 μm). “Cylind oca pon” ob usispo um
isola es ob ained om Cali o nia o med pe i hecia
when c oss-inocula ed wi h “C.” mac odidymum,
gi ing u he e idence o suppo he misiden i i-
ca ion heo y. This was also con i med by sequence
compa isons (Halleen e al., 2006a). In 2005, Pe i and
Guble con i med he p esence o “C.” mac odidymum
in he USA, and concluded ha black- oo disease in
Cali o nia is caused by “C.” mac odidymum and “C.”
des uc ans (Pe i and Guble , 2005).
Mo eo e , Halleen e al., (2004) es ablished
a new genus, Campyloca pon Halleen, Sch oe s
& C ous, which is “Cylind oca pon”-like in mo -
phology, associa ed wi h black- oo disease o
g ape ines. Species o his genus and membe s
o he o me “Nec ia” mammoidea g oup, a e ex-
cluded om Neonec ia/“Cylind oca pon”, because
phylogene ic analyses e ealed ha hese spe-
cies a e phylogene ically no closely ela ed o
Neonec ia/“Cylind oca pon” gene a (Halleen e al.,
2004; Sch oe s e al., 2008). F om his genus, wo spe-
cies we e included as he causal agen s o black- oo
disease: Campyloca pon ascicula e Sch oe s, Halleen
& C ous, which has been epo ed in Sou h A ica
(Halleen e al., 2004), B azil (Co eia e al., 2012), and
Spain (Alaniz e al., 2011b) and Campyl. pseudo ascicu-
la e Halleen, Sch oe s & C ous, which has been e-
po ed in Sou h A ica (Halleen e al., 2004), U uguay
(Ab eo e al., 2010), B azil (Co eia e al., 2012) and
Pe ú (Ál a ez e al., 2012).
As highligh ed be o e, “C.” des uc ans was o igi-
nally iden i ied as he causal agen o black- oo dis-
ease (Malu a and La ignon, 1991), bu he s a us o
“C.” des uc ans as he causal agen o he disease
was since hen ques ioned. In ac , Halleen e al.
(2006b), compa ed “C.” des uc ans s ains isola ed
om diseased g ape ines in F ance, New Zealand,
Po ugal and Sou h A ica wi h “C.” des uc ans-like
anamo phs ob ained om a ious he baceous o
woody hos s. DNA analyses o hei ITS and TUB
showed ha hese isola es we e gene ically iden i-
cal wi h “C.” li iodend i J.D. MacDon. & E.E. Bu le ,
which was i s associa ed wi h oo o o ulip pop-
la (Li iodend on ulipi e a L.) in Cali o nia by Mac-
Donald and Bu le (1981). Thus, because hese spe-
cies had iden ical sequences, “C.” des uc ans isola es
collec ed om asymp oma ic o diseased g ape ines
a ec ed by black- oo disease we e enamed as “C.”
li iodend i, associa ing “C.” des uc ans only wi h
oo o on o he he baceous o woody hos s (Hal-
leen e al., 2006b). In addi ion, in o de o cla i y he
axonomy o “C.” des uc ans causing black- oo in
Cali o nia, Pe i and Guble (2007) also compa ed
“C.” des uc ans isola es ob ained om g ape ines in
Cali o nia wi h “C.” li iodend i isola es om Sou h
A ica. All o hem we e iden ical, and consequen ly
“C.” des uc ans isola es we e also enamed as “C.”
li iodend i. This species has been la e epo ed as
a black- oo pa hogen o g ape ine in Aus alia
(Whi elaw-Wecke e al., 2007), Spain (Alaniz e al.,
2007), B azil (Russi e al., 2010), I an (Mohammadi e
al., 2009), Swi ze land (Casie i e al., 2009), U uguay
(Ab eo e al., 2010) and no heas e n Uni ed S a es
and sou heas e n Canada (Pe i e al., 2011). The ele-
omo phs o “C.” li iodend i and “C.” mac odidymum
we e desc ibed as Neonec ia li iodend i Halleen,
Rego & C ous and N. mac odidyma Halleen, Sch oe s
& C ous (Halleen e al., 2004, 2006b).
In 2008, a new species associa ed wi h black- oo
disease o g ape ines, “C.” paucisep a um Sch oe s &
C ous, was desc ibed in New Zealand and Slo enia
(Sch oe s e al., 2008). To da e, his species has been
isola ed om a ec ed g ape ines in U uguay (Ab eo
e al., 2010), Canada (O’Go man and Haag, 2011),
Spain (Ma in e al., 2011) and Po ugal (Cab al e al.,
2012a). Phylogene ic s udies ca ied ou in New Zea-
land and Slo enia by Sch oe s e al. (2008), indica ed
ha “C.” paucisep a um is he closes phylogene ic
sis e - axon o “C.” mac odidymum and bo h species
a e closely ela ed o he “C.” des uc ans-complex,
which also includes “C.” li iodend i.
Thus, a his momen , “C.” des uc ans, “C.” li i-
odend i, “C.” mac odidymum, “C.” ob usispo um, “C.”
paucisep a um, Campyl. ascicula e and Campyl. pseu-
do ascicula e we e conside ed as he main species
associa ed wi h young ines showing symp oms o
black- oo disease in mos o g ape ine p oducing
a eas wo ldwide. In addi ion, o he “Cylind oca pon”
species ha e been associa ed occasionally wi h black-
oo disease o g ape ine: “Cylind oca pon” didymum
(Ha ing) Wollenw. in Canada (Pe i e al., 2011), “C.”
olidum (Wollenw.) Wollenw. in Spain (De F ancisco
249
Vol. 52, No. 2, Augus , 2013
An upda e o black- oo disease o g ape ine
e al., 2009) and “C.” olidum a . c assum Ge lach in
U uguay (Ab eo e al., 2010).
Cha e i e al. (2011) pe o med a phylogene ic
s udy o Neonec ia, “Cylind oca pon” and ela ed
gene a wi h “Cylind oca pon”-like anamo phs. Mo -
phological and molecula phylogene ic analyses
da a accumula ed o e se e al yea s ha e indica ed
ha Neonec ia sensu s ic o and “Cylind oca pon”
sensu s ic o a e phylogene ically congene ic, while
Neonec ia sensu la o and “Cylind oca pon” sensu la o
do no o m a monophyle ic g oup, sugges ing ha
Neonec ia/“Cylind oca pon” ep esen s mo e han
one genus. Thus, based on esul s o he phylogene -
ic s udy, hese au ho s di ided Neonec ia in o i e
gene a based on a combina ion o cha ac e s linked
o pe i hecial ana omy and conidial sep a ion:
Neonec ia/“Cylind oca pon” sensu s ic o (Boo h’s
g oups 1 and 4), Rugonec ia, Thelonec ia (g oup 2),
Ilyonec ia (g oup 3) and anamo ph genus Campy-
loca pon. Acco ding o his, only Neonec ia has
“Cylind oca pon” anamo phs, while he emaining
gene a ha e “Cylind oca pon”-like anamo phs, and
since hen a e e e ed o as “Cylind oca pon”. Con-
sequen ly, “C.” li iodend i and “C.” mac odidymum
we e included in o Ilyonec ia genus, wi h I. adici-
cola as he ype species, and e-iden i ied as Ilyonec-
ia li iodend i (Halleen, Rego & C ous) Cha e i &
Salgado and I. mac odidyma (Halleen, Sch oe s &
C ous) P. Cha e i & Salgado, espec i ely (Cha e -
i e al., 2011).
Mo eo e , Cab al e al. (2012a) we e able o deline-
a e 12 new axa in he I. adicicola-complex, p e ious-
ly known as he “C.” des uc ans-complex, by using
a mul i-gene DNA analysis suppo ed by mo pho-
logical cha ac e s. O he Ilyonec ia species wi hin I.
adicicola-complex ha e been also ound associa ed
wi h black- oo disease o g ape ine: Ilyonec ia eu o-
paea A. Cab al, Rego & C ous, I. lusi anica A. Cab al,
Rego & C ous, I. pseudodes uc ans A. Cab al, Rego &
C ous and I. obus a (A.A. Hildeb .) A. Cab al, Rego
& C ous, epo ed in Po ugal (Cab al e al., 2012a,
2012c). Ano he Ilyonec ia spp., I. i is has also been
desc ibed in Po ugal (Cab al e al., 2012a), and iso-
la es belonging o Neonec ia mammoidea g oup ha e
also been associa ed wi h he disease in Canada (Pe -
i e al., 2011). Soon he ea e , ollowing his s udy,
Cab al e al. (2012c), demons a ed he exis ence o
polymo phism in o I. mac odidyma-complex. This
hypo hesis was in ag eemen wi h he esul s ob-
ained by Alaniz e al. (2009), who al eady de ec ed
ele an gene ic di e si y in “C.” mac odidymum by
using in e -simple sequence epea (ISSR) echnique.
Howe e , p e ious phylogene ic analysis showed
low a ia ion in he la ge subuni (LSU) ibosomal
DNA ( DNA), TUB and ITS sequences o “C.” mac o-
didymum isola es ob ained om g ape ine in di e -
en coun ies (Halleen e al, 2004; Pe i and Guble ,
2005; Alaniz e al., 2007). Thus, in o de o cla i y
his hypo hesis, Cab al e al. (2012c) pe o med a
phylogene ic s udy o I. mac odidyma-complex by
using ITS, TUB, his one H3 gene (HIS) and ansla-
ion elonga ion ac o 1-α (TEF) sequence analysis.
Consequen ly, six new species o Ilyonec ia (I. al-
cace ensis A. Cab al, Oli ei a & C ous, I. es emocen-
sis A. Cab al, Nascimen o & C ous, I. no ozelandica
A. Cab al & C ous, I. o esensis A. Cab al, Rego &
C ous, and Ilyonec ia sp. 1, I. sp. 2,) and I. mac o-
didyma, which a e mo phologically a he simila ,
we e ecognised in o he I. mac odidyma-complex. All
hese species ha e been epo ed in Po ugal, wi h
he excep ion o I. no ozelandica which has been e-
po ed in Sou h A ica, USA, New Zealand (Cab al
e al., 2012a, 2012c). Recen ly, I. alcace ensis, I. mac o-
didyma, I. no ozelandica, and I. o esensis ha e also
been ound on g ape ines in Spain (Agus í-B isach
e al., 2013a, 2013b).
Rega ding, “C.” paucisep a um, i is no clea in
which gene a i has o be included, al hough i is e y
simila in mo phology o I. an hu iicola A. Cab al &
C ous (Cab al e al., 2012a).
Finally, ano he genus, Cylind ocladiella Boesew.,
which is also Cylind oca pon-like in mo phology, has
ecen ly been associa ed wi h black- oo disease o
g ape ines (Van Colle e al., 2005; Agus í-B isach
e al., 2012; Jones e al., 2012). This genus was es ab-
lished by Boesewinkel (1982) o accommoda e i e
Cylind ocladium-like species p oducing small and cy-
lind ical conidia. This decision was based on he ac
ha species o Cylind ocladiella had di e en conidi-
opho es b anching pa e ns, conidial shapes, dimen-
sions, cul u al cha ac e is ics and eleomo phs om
hose o Cylind ocladium (Van Colle e al., 2005; Lom-
ba d e al. 2012). Since hen, se e al axonomic s ud-
ies o hese ungi ha e elied on mo phologically and
o lesse ex en on DNA sequence compa isons o he
ITS and TUB gene egions, ecognizing nine species
o Cylind ocladiella (C ous and Wing ield, 1993; Vic-
o e al., 1998; Van Colle e al., 2005). Lomba d e
al. (2012), ha e jus desc ibed 18 new Cylind ocladiella
species based on mo phological and phylogene ic
Phy opa hologia Medi e anea
250
C. Agus í-B isach and J. A mengol
s udies employing ITS, TUB, HIS and TEF gene e-
gions. Ne e heless, only wo species in o his genus
ha e been ound associa ed wi h black- oo disease
on g ape ines: Cylind ocladiella pa a (P.J. Ande son)
Boesew., which has been epo ed in Sou h A ica
(Van Colle e al., 2005), New Zealand (Jones e al.,
2012) and Spain (Agus í-B isach e al., 2012) and Cyl.
pe u iana (Ba ., J.L. Beze a & M.P. He e a) Boesew.,
which has been epo ed in Sou h A ica (Van Colle
e al., 2005), Pe ú (Ál a ez e al., 2012) and Spain
(Agus í-B isach e al., 2012).
A lis o all “Cylind oca pon”/Ilyonec ia, Campylo-
ca pon and Cylind ocladiella species, which ha e been
epo ed associa ed wi h black- oo disease o g ape-
ine and hei geog aphical dis ibu ion, is p esen -
ed in Table 1.
Mo phological and cul u al cha ac e iza ion
“Cylind oca pon”/Ilyonec ia, Campyloca pon and
Cylind ocladiella species ha e cha ac e is ic dis inc-
i e mo phological and cul u al pa e ns (Figu es 2
and 3; Table 2). The anamo phs o “Cylind oca pon”/
Ilyonec ia p oduce abundan mic oconidia and chla-
mydospo es. Mac o- and mic oconidia appa en ly
a e p oduced om he same conidiopho es which
a e 40–160 μm long, gene ally simple, unb anched
o spa sely b anched, i egula ly o e icilla ely
b anched, a ely densely b anched, and wi h cy-
lind ical phialides. Mac oconidia a e s aigh o
cu ed, hyaline, 1–3-sep a e, a ely > 3-sep a e [25–
50(–55)×5–7.5 μm], gene ally wi h a p ominen ba-
sal o la e al abscission sca o hilum. Mic oconidia
a e ellipsoidal o o oid, hyaline, 0–1-sep a e, wi h a
la e al o basal hilum [3–15×2.5–5(–6) μm] (Figu es
2A, 2B). Chlamydospo es a e abundan , gene ally
in e cala y, globose, single o in chains, becoming
b ownish. In addi ion, colony mo phology on PDA
is e y he e ogeneous (Figu e 2C). Ae ial mycelium
is loccose o el ed, and he colou a ies om whi e
o yellow o ligh o da k b own. The ma gin o he
colony can be en i e, sligh ly lobula ed, o lobula ed
(Figu es 3A–3H) (Boo h, 1966; Samuels and B ay-
o d, 1990; Cha e i e al., 2011).
Table 1. Fungal species which ha e been epo ed associa ed wi h black- oo disease o g ape ines and hei geog aphical
dis ibu ion.
Species Dis ibu ion
Campyloca pon ascicula e Sch oe s, Halleen & C ous Sou h A ica (Halleen e al., 2004), Spain (Alaniz e al., 2011b) and
B azil (Co eia e al., 2012).
Campyloca pon pseudo ascicula e Halleen, Sch oe s &
C ous
Sou h A ica (Halleen e al., 2004), U uguay (Ab eo e al., 2010),
B azil (Co eia e al., 2012) and Pe ú (Ál a ez e al., 2012)
“Cylind oca pon” des uc ans (Zinssm.) Schol en F ance (Malu a and La ignon, 1991), I aly (G asso, 1984),
A gen ina (Ga ica e al., 2001), Ge many (Fische and Kassemeye ,
2003), Pennsyl ania (Gugino and T a is, 2003), B azil (Ga ido e
al., 2004) and Canada (Pe i e al., 2011)
“Cylind oca pon” didymum (Ha ing) Wollenw. Canada (Pe i e al., 2011)
“Cylind oca pon” ob usispo um (Cooke & Ha kn.)
Wollenw.
Sicily (G asso and Magnano di San Lio, 1975) and Cali o nia
(Scheck e al., 1998a)
“Cylind oca pon” olidum (Wollenw.) Wollenw. Spain (De F ancisco e al., 2009)
“Cylind oca pon” olidum a . c assum Ge lach U uguay (Ab eo e al., 2010)
“Cylind oca pon” paucisep a um Sch oe s & C ous New Zealand and Slo enia (Sch oe s e al., 2008), U uguay (Ab eo
e al., 2010) Canada (O’Go man and Haag, 2011), Spain (Ma in e
al., 2011) and Po ugal (Cab al e al., 2012a)
Cylind ocladiella pa a (P.J. Ande son) Boesew. Sou h A ica (Van Colle e al., 2005), New Zealand (Jones e al.,
2012) and Spain (Agus í-B isach e al., 2012)
(Con inued)
251
Vol. 52, No. 2, Augus , 2013
An upda e o black- oo disease o g ape ine
Campyloca pon is simila o “Cylind oca pon”/Ily-
onec ia, al hough Campyloca pon spp. p oduce mac-
oconidia mos ly cu ed, while mic oconidia a e
absen and chlamydospo es a e a e o also absen .
Conidiopho es appea a ising la e ally om single
o ascicula e ae ial hyphae o om c eeping sub-
s a e hyphae, singly o in loose o dense agg ega es
(Figu e 2D). Conidial heads o m pionno es-like ag-
g ega es. Conidiopho e show a s ipe base o 16 μm
wide, which bea se e al phialides o a penicillus o
i egula b anches wi h e minal b anches bea ing 1
o se e al phialides. Mac oconidia a e as in Ilyonec-
ia, bu ypically cu ed, and wi h up o 6 sep a,
[(24–)35–60(–62)×6.5–9 μm], apical cell ob use, basal
cell ob use o wi h inconspicuous hilum (Figu e 2E).
Rega ding colony mo phology on PDA, ae ial myce-
lium is abundan , co e ing he whole o sec o s o he
colony, whi e o o -whi e o sligh ly b ownish, hick-
ly co ony o el y, in e mingled wi h o gi ing ise
o e ec whi e o b own hyphal s ands. This s ands
some imes a e pa ly co e ed by o -whi e slime (Fig-
u es 3I, 3J) (Halleen e al., 2004; Cha e i e al., 2011).
Cylind ocladiella species p oduce hyaline, single,
sub e icilla e, as well as penicillia e conidiopho es,
Species Dis ibu ion
Cylind ocladiella pe u iana (Ba ., J.L. Beze a & M.P.
He e a) Boesew.
Sou h A ica (Van Colle e al., 2005), Spain (Agus í-B isach e al.,
2012) and Pe ú (Ál a ez e al., 2012)
Ilyonec ia alcace ensis A. Cab al, Oli ei a & C ous Po ugal (Cab al e al., 2012c) and Spain (Agus í-B isach e al.,
2013b)
Ilyonec ia es emocensis A. Cab al & C ous Po ugal (Cab al e al., 2012c)
Ilyonec ia eu opaea A. Cab al, Rego & C ous Po ugal (Cab al e al., 2012a)
Ilyonec ia li iodend i (Halleen, Rego & C ous)
Cha e i & Salgado F ance, New Zealand, Po ugal and Sou h A ica (Halleen e al.,
2006b), Aus alia (Whi elaw-Wecke e al., 2007), Cali o nia (Pe i
and Guble , 2007), Spain (Alaniz e al., 2007), I an (Mohammadi
e al., 2009), Swi ze land (Casie i e al., 2009), B azil (Russi e al.,
2010), U uguay (Ab eo e al., 2010), no heas e n Uni ed S a es
and sou heas e n Canada (Pe i e al., 2011),
Ilyonec ia lusi anica A. Cab al, Rego & C ous Po ugal (Cab al e al., 2012a)
Ilyonec ia mac odidyma (Halleen, Sch oe s & C ous)
P. Cha e i & C. Salgado Aus alia, F ance, New Zealand and Sou h A ica (Halleen e
al., 2004), Cali o nia (Pe i and Guble , 2005), Chile (Auge e al.,
2007), U uguay (Ab eo e al., 2010), no heas e n Uni ed S a es
and sou heas e n Canada (Pe i e al., 2011), Po ugal (Cab al e al.,
2012c), Tu key (Özben e al., 2012) and Spain (Agus í-B isach e al.,
2013b).
Ilyonec ia no ozelandica A. Cab al, Nascimen o &
C ous
Sou h A ica, USA and New Zealand (Cab al e al., 2012c) and
Spain (Agus í-B isach e al., 2013a, b)
Ilyonec ia pseudodes uc ans A. Cab al, Rego &
C ous
Po ugal (Cab al e al., 2012a)
Ilyonec ia obus a (A.A. Hildeb .) A. Cab al, Rego &
C ous
Po ugal (Cab al e al., 2012a)
Ilyonec ia o esensis A. Cab al, Rego & C ous Aus alia, Canada, New Zealand, Po ugal, Sou h A ica, Spain
and USA (Cab al e al., 2012c; Agus í-B isach e al., 2013a, b)
Ilyonec ia i is A. Cab al, Rego & C ous Po ugal (Cab al e al., 2012a)
Ilyonec ia sp. 2 (Cab al e al., 2012c) Po ugal (Cab al e al., 2012c)
Isola es belonging o Neonec ia mammoidea g oup Canada (Pe i e al., 2011)
Table 1. Con inues.
Phy opa hologia Medi e anea
252
C. Agus í-B isach and J. A mengol
wi h p ima y and seconda y b anches. The phial-
ides a e e minal, hyaline, in who ls o 2–4, wi h o
wi hou ob ious colla e s. In gene al, s ipe is cen-
ally a anged on conidiopho es, wi h a single basal
sep um, e mina ing in a hin-walled, hyaline esicle
o cha ac e is ic shape (Figu es 2F, 2G). Conidia a e
cylind ical, ounded a bo h ends, s aigh , hyaline,
(0)–1-sep a e, [(9–)11–13(–15)×2–4 μm], some imes
H
I
F
G
A
B
C
E
D
Figu e 2. A, Conidiopho es o I. li iodend i; B, Mac o- and mic oconidia o Ilyonec ia li iodend i; C, Chlamydospo es in
chains o “Cylind oca pon” paucisep a um; D, Conidiopho es o Campyl. ascicula e; E, Mac oconidia o Campyloca pon as-
cicula e; F, Penicilla e conidiopho es o Cylind ocladiella pa a; G, Te minal esicles o Cyl. pa a; H, Conidia o Cyl. pa a; H,
Chlamydospo es in chains o Cyl. pa a. Scale ba s: a‒c, ‒i = 10 μm; d‒e = 25 μm.
253
Vol. 52, No. 2, Augus , 2013
An upda e o black- oo disease o g ape ine
becoming swollen a one end wi h age (Figu e 2H).
Chlamydospo es a e abundan o mode a e, mo e
equen ly a anged in chains han clus e s (Fig-
u e 2I). Ae ial mycelium anges om da k o ligh
b own (Figu es 3K, 3L) (C ous and Wing ield, 1993;
Lomba d e al., 2012).
Epidemiology
Campyloca pon, “Cylind oca pon”, Cylind oclad-
iella and Ilyonec ia species a e gene ally ega ded as
pa hogens and/o sap obes o a wide ange o angio-
spe m and gymnospe m hos s and subs a es in em-
pe a e, sub- opical and opical egions wo ldwide
(Vic o e al., 1998; Cha e i e al., 2011; Lomba d e al.,
2012). In addi ion o g ape ine, hey ha e also been
associa ed wi h oo o diseases o o he economi-
cally impo an hos s (Cha e i e al., 2011; Lomba d
e al., 2012), such as: Ac inidia chinensis Planch. (E -
pe e al., 2011), Li iodend on ulipi e a L. (MacDonald
and Bu le , 1981), Olea eu opaea L. (Ú bez-To es e
al., 2012), Panax quinque olius L. (Rahman and Punja,
2005), Pe sea ame icana Mill. (Vi ale e al., 2012), Pinus
adia a D. Don (Agus í-B isach e al., 2011b) o Pinus
syl es is L. (Menkis and Bu okiene, 2012). Lomba d
e al. (2013) ha e jus epo ed black oo o disease
associa ed wi h he cul i a ion o P o eaceae cu low-
e s in Sou h A ica, and desc ibed ou new Ilyonec-
A
D
C
I
E
F
G
H
L
K
J
B
Figu e 3. Colonies o black- oo pa hogens g own on PDA. A, “Cylind oca pon” des uc ans (CBS 301.93); B, “C.” paucisep-
a um; C, “C.” ob usispo um; D, Ilyonec ia alcace ensis; E, I. li iodend i; F, I. no ozelandica; G, I. mac odidyma; H, I. o esensis; I,
Campyloca pon ascicula e; J, Campyl. pseudo ascicula e; K, Cylind ocladiella pa a; L, Cyl. pe u iana.
Phy opa hologia Medi e anea
260
C. Agus í-B isach and J. A mengol
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Accep ed o publica ion: June 17, 2013