Fungal Diversity (2014) 68:159–238
DOI 10.1007/s13225-014-0308-3
Revision of Phaeosphaeriaceae
Rungtiwa Phookamsak & Jian-Kui Liu & Eric H. C. McKenzie &
Dimuthu S. Manamgoda & Hiran Ariyawansa & Kasun M. Thambugala & Dong-Qin Dai &
Erio Camporesi & Ekachai Chukeatirote & Nalin N. Wijayawardene & Ali H. Bahkali &
Peter E. Mortimer & Jian-Chu Xu & Kevin D. Hyde
Received: 19 August 2014 / Accepted: 11 September 2014 / Published online: 7 October 2014
# School of Science 2014
Abstract Phaeosphaeriaceae is a large and important family
in the order Pleosporales which includes economically important plant pathogens. Species may also be endophytes or
saprobes on plant hosts, especially on monocotyledons (e.g.,
Cannaceae, Cyperaceae, Juncaceae, Poaceae); some species
have also been reported on dicotyledons. The family previously accommodated 35 sexual and asexual genera and comprised more than 300 species with a range of morphological
characters. The morphological characters of taxa in this family
are often ambiguous and can be confused with other taxa in
Leptosphaeriaceae and Montagnulaceae. Fourteen specimens
of the type genera of Phaeosphaeriaceae were loaned from
herbaria worldwide and were re-examined and illustrated.
Fresh collections were obtained from Italy and Thailand,
characterized, examined, isolated into pure culture and used
to obtain molecular data. The asexual state was induced where
possible on sterile bamboo pieces placed on water agar.
Multigene phylogenetic analyses of ITS, LSU, SSU, RPB2
and TEF1 sequence datasets were carried out using maximum
likelihood, maximum parsimony and Bayesian analysis.
Molecular analyses shows that 21 genera (Amarenomyces,
Ampelomyces, Chaetosphaeronema, Dematiopleospora,
Entodesmium, Loratospora, Neosetophoma,
Neostagonospora, Nodulosphaeria, Op hiobolus,
Ophiosphaerella, Paraphoma, Parastagonospora,
Phaeosphaeria, Phaeosphaeriopsis, Sclerostagonospora,
Setomelanomma, Setophoma, Vrystaatia, Wojnowicia and
Xenoseptoria) belong in Phaeosphaeriaceae, while seven
Electronic supplementary material The online version of this article
(doi:10.1007/s13225-014-0308-3) contains supplementary material,
which is available to authorized users.
R. Phookamsak : D.<Q. Dai : P. E. Mortimer : J.<C. Xu :
K. D. Hyde (*)
Key Laboratory for Plant Diversity and Biogeography of East Asia,
Kunming Institute of Botany, Chinese Academy of Sciences,
Kunming 650201, Yunnan, People’s Republic of China
e-mail: kdhyde3@gmail.com
R. Phookamsak : D.<Q. Dai : P. E. Mortimer : J.<C. Xu : K. D. Hyde
World Agroforestry Centre, East and Central Asia,
Kunming 650201, Yunnan, People’s Republic of China
R. Phookamsak : J.<K. Liu : D. S. Manamgoda : H. Ariyawansa :
K. M. Thambugala : D.<Q. Dai : E. Chukeatirote :
N. N. Wijayawardene : K. D. Hyde
School of Science, Mae Fah Luang University, Chiang Rai 57100,
Thailand
R. Phookamsak : J.<K. Liu : D. S. Manamgoda : H. Ariyawansa :
K. M. Thambugala : D.<Q. Dai : E. Chukeatirote :
N. N. Wijayawardene : K. D. Hyde
Institute of Excellence in Fungal Research, Mae Fah Luang
University, Chiang Rai 57100, Thailand
A. H. Bahkali : K. D. Hyde
College of Science, Botany and Microbiology Department, King
Saud University, Riyadh 1145, Saudi Arabia
E. Camporesi
A.M.B. Gruppo Micologico Forlivese “Antonio Cicognani”, Via
Roma 18, Forlì, Italy
E. Camporesi
A.M.B. Circolo Micologico “Giovanni Carini”, C.P. 314, Brescia,
Italy
E. Camporesi
Società per gli Studi Naturalistici della Romagna, C.P. 144,
Bagnacavallo, RA, Italy
E. H. C. McKenzie
Manaaki Whenua Landcare Research, Private Bag 92170, Auckland,
New Zealand
160
genera (Amarenographium, Bricookea, Dothideopsella,
Eudarluca, Phaeostagonospora, Scolecosporiella and
Tiarospora) are included based on morphological data.
Amarenomyces is reinstated and Nodulosphaeria is confirmed
in Phaeosphaeriaceae. Eudarluca is distinguished from
Sphaerellopsis based on its morphological characters and is
typical of Phaeosphaeriaceae. ITS gene phylogenetic analysis indicates tha t Sphaere llopsis be longs to
Leptosphaeriaceae. Ophiobolus species form a clade within
Phaeosphaeriaceae while Ophiosphaerella is shown to be
polyphyletic. Phaeosphaeria sensu stricto is redefined. Two
new species of Phaeosphaeria and one of Phaeosphaeriopsis
are introduced while the asexual states of Phaeosphaeria
chiangraina and Phaeosphaeriopsis dracaenicola are reported. Scolicosporium minkeviciusii forms a sister clade with
Neostagonospora and Parastagonospora in
Phaeosphaeriaceae. However, Scolicosporium minkeviciusii
is not the type species. Thus, the placement of Scolicosporium
sensu stricto in Phaeosphaeriaceae is questionable.
Phylogenetic analysis of combined ITS and LSU genes, confirm the placement of Septoriella oudemansii in
Phaeosphaeriaceae. However, it is not represented by the
generic type, thus the placement of Septoriella is questionable.
Setophaeosphaeria is excluded from Phaeosphariaceae as the
type species, Sp. hemerocallidis forms a clade at the base of
Cucurbitariaceae. Wilmia clusters in Didymosphaeriaceae
and is synonymized under Letendraea. Barria, Chaetoplea,
Hadrospora, Lautitia, Metameris, Mixtura and Pleoseptum
are excluded from Phaeosphaeriaceae based on their morphological characters. The asexual genera Mycopappus and
Xenostigmina are excluded from this family based on the
phylogenetic evidence; these genera form a clade close to
Melanommataceae.
Keywords Asexual state . Didymosphaeriaceae .
Montagnulaceae . Phaeosphaeria . Phylogeny .
Pleosporales . Taxonomy
Introduction
Phaeosphaeriaceae is a large and important family in
Pleosporales and was previously reported to include more
than 300 species in 35 genera (18 sexual and 17 asexual
genera; Kirk et al. 2008; Zhang et al. 2009; Hyde et al.
2013; Wijayawardene et al. 2014b). Specie s of
Phaeosphaeriaceae, especially the asexual taxa, are important
plant pathogens, infecting major crops (Shoemaker and
Babcock 1989b; Carson 2005; Stukenbrock et al. 2006;
Zhang et al. 2009; Quaedvlieg et al. 2013; Hyde et al.
2014). For example, Parastagonospora nodorum (Berk.)
Quaedvlieg et al. causes leaf and glume blotch of cereals
crops, especially barley and wheat (Cunfer 2000;
Fungal Diversity (2014) 68:159–238
Stukenbrock et al. 2006; Vergnes et al. 2006; Quaedvlieg
et al. 2013) while Parastagonospora avenae causes leaf
blotch of barley and rye (f.sp. tritici) (Cunfer 2000;
Quaedvlieg et al. 2013). Furthermore, many genera have also
been reported as pathogens causing leaf spots on various
hosts, such as Neosetophoma, Phaeosphaeria,
Phaeosphaeriopsis, Setophoma, Wojnowicia and
Xenoseptoria (Cason 2005; Arzanlou and Crous 2006;
Quaedvlieg et al. 2013; Wijayawardene et al. 2013b; Crous
et al. 2014; Phookamsak et al. 2014). Some species are also
endophytes (Wang et al. 2005; Sánchez Márquez et al. 2007;
Lawrey et al. 2012), Lautitia danica (Berl.) S. Schatz is
obligate parasite on algae (Schatz 1984; Barr 1987b; Zhang
et al. 2012) and many species are saprobic on monocotyledons, especially poaceous hosts, while others may be saprobes
on herbaceous dicotyledonous hosts (Shoemaker 1984;
Shoemaker and Babcock 1989b; Schoch et al. 2006; Zhang
et al. 2009, 2012; De Gruyter et al. 2010; Hyde et al. 2013;
Quaedvlieg et al. 2013).
History of Phaeosphaeriaceae
Introduction to the family
The family Phaeosphaeriaceae was introduced by Barr
(1979) and typified by Phaeosphaeria with Ph. oryzae as
the type species. The important family characters were described by Barr (1979) as “saprobic, pathogenic or hyperparasitic fungi typically on herbaceous stems or monocotyledonous leaves, culms, or flowers, but also on woody substrates.
Ascomata were described as immersed, erumpent or superficial, globose or conical, short papillate, small to medium, asci
as bitunicate, and ascospores as hyaline, yellowish or brown,
narrowly or widely obovoid, aseptate or septate” Subsequent
authors are in agreement with this description (Barr 1987b,
1992a, b; Zhang et al. 2012; Hyde et al. 2013). When Barr
(1979) introduced the family Phaeosphaeriaceae, 15 genera
were included (Table 1); i.e. Comoclathris, Didymella,
Eudarluca, Heptameria, Leptosphaeria, Loculohypoxylon,
Metameris, Microthelia, Nodulosphaeria, Ophiobolus,
Paraphaeosphaeria, Phaeosphaeria, Rhopographus,
Scirrhodothis and Teichospora (Barr 1979; Zhang et al.
2009, 2012).
Arrangement of genera in Phaeosphaeriaceae based
on morphology (1979–1999)
Over the next 20 years the family was revised with additions
and exclusions of genera and this is detailed below (Table 1).
These revisions were based on morphological characters and
were subjective with decisions made based on perceived
importance of characters. During this period it was very
difficult for researchers to develop higher classification
Fungal Diversity (2014) 68:159–238
161
Table 1 Synopsis of Phaeosphaeriaceae from 1979 to 2014
Barr (1979)
Barr (1992a)
Comoclathris
Didymella
Eudarluca
Heptameria
Leptosphaeria
Loculohypoxylon
Metameris
Microthelia
Nodulosphaeria
Ophiobolus
Paraphaeosphaeria
Phaeosphaeria
Rhopographus
Scirrhodothis
Teichospora
Bricookea
Chaetoplea
Didymella
Graphyllium
Hadrospora
Kalmusia
Lautitia
Metameris
Montagnula
Nodulosphaeria
Ophiosphaerella
Paraphaeosphaeria
Phaeosphaeria
Rhopographus
Lumbsch and Huhndorf
(2010)
Barria
Bricookea
Carinispora
Chaetoplea
Entodesmium
Eudarluca
Hadrospora
Isthmosporella
Lautitia
Metameris
Mixtura
Nodulosphaeria
Ocala
Ophiobolus
Ophiosphaerella
Phaeosphaeria
= Amarenomyces
Phaeosphaeriopsis
Pleoseptum
Setomelanomma
Wilmia
Hyde et al. (2011)
(Asexual state reported)
Amarenographium
(Sexual=Amarenomyces)
Ampelomyces
Chaetosphaeronema
Coniothyrium
(Sexual=Ophiobolus)
Hendersonia-like
(Sexual=Austropleospora
and Phaeosphaeria)
Neosetophoma
Parahendersonia
(Sexual=Chaetoplea)
Paraphoma
Phaeoseptoria
(Sexual=Phaeosphaeria)
Phaeostagonospora
(Sexual=Phaeosphaeriopsis)
Phoma
(Sexual=Ophiobolus)
Rhabdospora
(Sexual=Ophiobolus)
Scolecosporiella
(Sexual=Ophiosphaerella
and Phaeosphaeria)
Setophoma
Sphaerellopsis
(Sexual=Eudarluca)
Stagonospora
(Sexual=Phaeosphaeria)
Tiarospora
Eriksson and
Hawksworth
(1993)
Bricookea
Carinispora
Eudarluca
Hadrospora
Lautitia
Metameris
Mixtura
Nodulosphaeria
Ophiosphaerella
Paraphaeosphaeria
Phaeosphaeria
Sulcispora
Teratosphaeria
Zhang et al. (2012)
Barria
Bricookea
Chaetoplea
Eudarluca
Entodesmium
Hadrospora
Lautitia
Loratospora
Metameris
Mixtura
Nodulosphaeria
Ophiobolus
Ophiosphaerella
Phaeosphaeria
Phaeosphaeriopsis
Pleoseptum
Setomelanomma
Wilmia
schemes as it was not possible to confirm the importance of
characters (K.D. Hyde, personal experience). Therefore, the
Kirk et al. (2001)
Lumbsch and
Huhndorf (2007)
Kirk et al. (2008)
Barria
Bricookea
Carinispora
Eudarluca
= Cryptocrea
= Parabotryon
= Xenodimerium
Hadrospora
Isthmosporella
Lautitia
Metameris
= Scirrhodothis
= Scirrhophragma
Mixtura
Nodulosphaeria
= Pocosphaeria
Ophiosphaerella
Paraphaeosphaeria
Phaeodothis
Phaeosphaeria
=Leptosphaerella
=Trematosphaerella
Sulcispora
Hyde et al. (2013)
Barria
Bricookea
Carinispora
Chaetoplea
Eudarluca
Hadrospora
Isthmosporella
Katumotoa
Lautitia
Leptosphaeria
Metameris
Mixtura
Neophaeosphaeria
Nodulosphaeria
Ophiobolus
Ophiosphaerella
Phaeosphaeria
Phaeosphaeriopsis
Pleoseptum
Setomelanomma
Teratosphaeria
Wilmia
Barria
Bricookea
Carinispora
Eudarluca
Hadrospora
Isthmosporella
Katumotoa
Lautitia
Metameris
Mixtura
Nodulosphaeria
Ophiosphaerella
Phaeosphaeria
Phaeosphaeriopsis
Setomelanomma
Sulcospora
Wilmia
Ampelomyces
Barria
Bricookea
Chaetoplea
Chaetosphaeronema
Entodesmium
Eudarluca
Hadrospora
Lautitia
Loratospora
Metameris
Mixtura
Neosetophoma
Nodulosphaeria
Ophiobolus
Ophiosphaerella
Parahendersonia
Paraphoma
Phaeoseptoria
Phaeosphaeria
Phaeosphaeriopsis
Pleoseptum
Setomelanomma
Setophoma
Tiarospora
Wilmia
Wojnowicia
Amarenographium
Amarenomyces
Ampelomyces
Bricookea
Chaetosphaeronema
Dematiopleospora
Dothideopsella
Entodesmium
Eudarluca
Loratospora
Neosetophoma
Neostagonospora
Nodulosphaeria
Ophiobolus
Ophiosphaerella
Paraphoma
Parastagonospora
Phaeosphaeria
= Phaeoseptoria
Phaeosphaeriopsis
Phaeostagonospora
Sclerostagonospora
Scolecosporiella
?? Scolicosporium
??Septoriella
Setomelanomma
Setophoma
Tiarospora
Vrystaatia
Wojnowicia.
Xenoseptoria
Wijayawardene et al. (2014b) and in this
study
researchers did their work to the best of their ability and have
often been proven correct.
162
Barr (1982) included the monotypic genus Bricookea in
Phaeosphaeriaceae, while Schatz (1984) introduced Lautitia,
a parasite on red algae, and accommodated it in the family.
Barr (1987a) transferred Leptosphaeria as the type to establish
the new family Leptosphaeriaceae, because of its large
scleroplectenchymatous, thick-walled peridium cells and host
preference on dicotyledons (Barr 1987a, b; Khashnobish and
Shearer 1996; Câmara et al. 2002). Barr (1987b) also transferred Ophiobolus and Heptameria to Leptosphaeriaceae and
followed by Tanaka and Harada (2005). Eudarluca,
Loculohypoxylon and Teichospora were placed in
Dacampiaceae, while some species of Microthelia were
regarded as synonyms of Kirschsteiniothelia, and subsequently placed in Pleosporaceae (Hawksworth 1985; Barr 1987b).
Montagnula was considered as a part of Pleospora (Barr
1987b), however, the genus was re-established by Crivelli
(1983). Barr (1987b) added Bricookea, Chaetoplea,
Kalmusia, Lautitia and Ophiosphaerella and suggested that
Amarenomyces and Entodesmium could also be accommodated in Phaeosphaeriaceae. Boise (1989) introduced
Hadrospora as a new genus in Phaeosphaeriaceae and additionally, Sulcispora was established in Phaeosphaeriaceae by
Shoemaker and Babcock (1989b). More recently, Mixtura
(Syd.) Eriksson and Yue (1990) was placed, with some uncertainty in Phaeosphaeriaceae.
Eriksson and Hawksworth (1991) included Entodesmium
and Peridiothelia in the family but this was disputed by Barr
(1992a). It was suggested that Entodesmium should be placed
in Lophiostomataceae because of its abrupt, beak-like apex
and the periphysate ostioles which were illustrated by
Shoemaker (1984) and Peridiothelia could be accommodated
in Pleomassariaceae. Thus, Barr (1992a) accepted only 14
genera in Phaeosphaeriaceae: Bricookea, Chaetoplea,
Didymella, Graphyllium, Hadrospora, Kalmusia, Lautitia,
Metameris, Montagnula, Nodulosphaeria, Ophiosphaerella,
Phaeosphaeria, Paraphaeosphaeria and Rhopographus
(Table 1).
Shoemaker and Babcock (1992) revised the taxonomy of
the Pleosporales and transferred Comoclathris to
Diademaceae and Graphyllium was moved to Hysteriaceae
based on its hysterothecia with a slit-like opening (Zhang et al.
2011; Ariyawansa et al. 2014a). The marine fungus,
Carinispora K.D. Hyde (Hyde 1992), a saprobe on the intertidal Nypa palm was placed in Phaeosphaeriaceae, and it was
noted that the genus was closely related to Phaeosphaeria,
although differed in several important aspects. The genus was
tentatively placed in Phaeosphaeriaceae due to lack of molecular data (Hyde 1992, 1994; Jones et al. 2009; Lumbsch
and Huhndorf 2007, 2010).
Eriksson and Hawksworth (1993) listed 13 genera in
Phaeosphaeriaceae: Bricookea, Carinispora, Eudarluca,
H ad ro s p or a , L a u t i t i a, M et am e ri s, M i x t u r a,
Nodulosphaeria, Ophiosphaerella, Paraphaeosphaeria,
Fungal Diversity (2014) 68:159–238
Phaeosphaeria, Sulcispora and Teratosphaeria (Table 1).
Scirrhodothis was synonymised under Metameris, while
Didymella was excluded from the family. Sivanesan
(1984) proposed placing Didymella in Pleosporaceae,
while Reddy et al. (1998) treated it in Venturiaceae
(Dianese et al. 2001; Zhang et al. 2012). Yuan (1994)
established Barria as a monotypic genus from Picea
within Phaeosphaeriaceae. The peridium in this genus is
composed of thin-walled pseudoparenchymatous cells and
it has narrow cellular pseudoparaphyses. Ramaley and
Barr (1995) introduced the monotypic genus Pleoseptum
from Yucca baccata and reported Camarosporium
yuccaesedum Fairm. as the asexual state of the genus.
Pleoseptum shares morphological characters with several
Dothideomycetes genera (Ramaley and Barr 1995).
However there is a lack of molecular phylogenetic evidence to place this genus in Phaeosphaeriaceae (Zhang
et al. 2012; Hyde et al. 2013).
Wilmia, a monotypic genus, was introduced as a pathogen
of Memora pedunculata and formed asexual morphs associated with the sexual morph. The morphology is similar to
several genera such as Barria, Lautitia, and Metameris in the
Phaeosphaeriaceae (Dianese et al. 2001; Zhang et al. 2012;
Ariyawansa et al. 2014b).
Dothideopsella was characterized by broadly pseudoparenchymatous cells, and phragmosporous, brown ascospores.
The genus was introduced by von Höhnel (1915) to accommodate non-congeneric species of Leptosphaeria (Barr and
Rogerson 1999). However, the genus was reinstated under
Leptosphaeria by von Arx and Müller (1975) and this was
followed in Kirk et al. (2001, 2008). Barr and Rogerson
(1999) treated Dothideopsella in Botryosphaeriaceae, while
Lumbsch and Huhndorf (2010) placed the genus in
Dothideomycetes, genera incertae sedis. Recently,
Dothideopsella was reported as a genus in
Leptosphaeriaceae which contained four epithet species.
However, Ariyawansa et al. (2013) observed the type species
and found that the genus was typical in Phaeosphaeriaceae
rather than Leptosphaeriaceae. Thus the genus was transferred to Phaeosphaeriaceae and is followed by
Wijayawardene et al. (2014b).
Various other genera included in Phaeosphaeriaceae by
Barr (1979, 1987a, b, 1990a, 1992a), have been transferred to
other families based on morphology. Comoclathris is currently accommodated in the Diademaceae (Shoemaker and
Babcock 1992; Zhang et al. 2012; Hyde et al. 2013;
Ariyawansa et al. 2014a), Heptameria and Rhopographus
are treated in Dothideomycetes, genera incertae sedis
(Lumbsch and Huhndorf 2007, 2010; Zhang et al. 2012;
Hyde et al. 2013), Loculohypoxylon and Teichospora in the
family Teichosporaceae (Barr 2002; Lumbsch and Huhndorf
2007, 2010; Zhang et al. 2012; Hyde et al. 2013;
Wijayawardene et al. 2014b).
Fungal Diversity (2014) 68:159–238
Initial phylogenetics for resolving Phaeosphaeriaceae
In 1995 the first phylogenetic evidence for placement of
genera in Phaeosphaeriaceae started to emerge. Morales
et al. (1995) attempted to determine the relationships between
Leptosphaeria and Phaeosphaeria species using rRNA gene
sequences. The separation of Leptosphaeria and
Phaeosphaeria was not strongly supported and the asexual
states were phylogenetically uninformative in their analysis.
Phylogenetic analysis indicated that Phaeosphaeria was part
of Leptosphaeriaceae due to the fact that Ph. nodorum and
Ph. microscopica formed a clade close to L. doliolum, the type
species of Leptosphaeria (Morales et al. 1995; Câmara et al.
2002.). Khashnobish and Shearer (1996) found that
Phaeosphaeria formed a distinct group separate from
L e p t o s ph a e r i a b a s e d o n a c l a d i s t i c a n a l y s i s o f
morphological and sequence data. Câmara et al. (2002) concluded that peridial characters, asexual state and host
preferences are taxonomically and phylogenetically
significant at the generic level, with Leptosphaeria sensu
stricto and Phaeosphaeria sharing a more recent common
ancestor in their analysis.
Kruys et al. (2006) investigated the relationships of families in Pleosporales and observed that Phaeosphaeriaceae is
closely related to Leptosphaeriaceae and formed an unresolved monophyletic group. The main features distinguishing
the two families are the ascomata wall characters. In
Leptosphaeriaceae taxa have scleroplectenchymatous
ascomata walls and in Phaeosphaeriaceae taxa have thinwalled, pseudoparenchymatous ascomata walls (Câmara
et al. 2002; Cheng et al. 2004; Schoch et al. 2006). Shiraia,
an uncertain genus grouped with Leptosphaeriaceae and
Phaeosphaeriaceae in the phylogenetic analysis of Kruys
et al. (2006). Cheng et al. (2004) suggested that Shiraia should
be treated as a member of Phaeosphaeriaceae. The genus was
unofficially placed in Shiraiaceae, by Ogawa et al. (2003) (see
GenBank AB105798), but was not validly published (Kruys
et al. 2006; Liu et al. 2013). Liu et al. (2013) illustrated and
epitypified the type species, Shiraia bambusicola from fresh
collection in Zhejiang Province, China. Based on their
phylogenetic investigation, Shiraia formed a distinct clade
separate from Phaeosphaeriaceae. Therefore, Liu et al.
(2013) introduced a new valid family Shiraiaceae to accommodate a monotypic genus Shiraia in Pleosporales and illustrated a coelomycetous asexual state.
Zhang et al. (2009) incorporated multigene phylogenetic
analysis and included 15 families in Pleosporales. They included four families in the suborder Pleosporineae viz.
Didymellaceae, Leptosphaeriaceae, Phaeosphaeriaceae and
Pleosporaceae. In addition, they introduced two new families,
Amniculicolaceae and Lentitheciaceae to accommodate some
freshwater fungi (Zhang et al. 2009, 2012). Zhang et al. (2009)
re-accommodated Ophiobolus in Phaeosphaeriaceae due to
163
its morphological characters and because Ophiobolus is often
associated with the asexual genus Chaetosphaeronema on the
host (Petrak 1944). However, this link has not been confirmed
(Zhang et al. 2009).
Zhang et al. (2012) re-circumscribed the families
Phaeosphaeriaceae in Pleosporales. These authors treated
18 sexual genera base on morphology in Phaeosphaeriaceae
and accepted Entodesmium, Ophiosphaerella, Phaeosphaeria
and Setomelanomma based on phylogenetic analysis
(Table 1). The freshwater genera Isthmosporella Shearer and
Crane (1999) and Ocala Raja et al. (2009) were also accommodated in Phaeosphaeriaceae. Zhang et al. (2012), however,
removed these genera from Phaeosphaeriaceae based on
morphological characters and phylogenetic analysis; Ocala
formed a unique clade basal to Jahnulales (Shearer et al.
2009) and Isthmosporella was treated in Pleosporales, genera
incertae sedis. Hyde et al. (2013) listed 27 sexual and asexual
genera in Phaeosphaeriaceae and later, Wanasinghe et al.
(2014) introduced the monotypic genus, Dematiopleospora
typified by D. mariae in Phaeosphaeriaceae based on molecular data. Furthermore, Crous et al. (2014) included
Setophaeosphaeria Crous & Y. Zhang ter with Sp.
badalingensis Crous & Y. Zhang ter, Sp. hemerocallidis
Crous & Y. Zhang ter and Sp. setosa (Leuchtm.) Crous in
Phaeosphaeriaceae. Setophaeosphaeria is morphologically
and phylogenetically distinct from Phaeosphaeria oryzae,
the type species of Phaeosphaeriaceae, but is similar to Ph.
setosa. Thus the genus was established to accommodate
phaeosphaeria-like species.
Recent molecular studies place Kirschsteiniothelia in a
new family Kirschsteiniotheliaceae based on molecular data
(Boonmee et al. 2012) and Microthelia species are treated in
synonymy of various genera of Dothideomycetes (Hyde et al.
2013). Kalmusia, Montagnula and Paraphaeosphaeria are
accommodated in Montagnulaceae (Boonmee et al. 2012;
Hyde et al. 2013; Lumbsch and Huhndorf 2010; Zhang et al.
2009, 2012; Ariyawansa et al. 2014b). Several genera in
Phaeosphaeriaceae, such as Barria, Bricookea, Chaetoplea,
Eudarluca, Hadrospora, Lautitia, Metameris, Mixtura,
Nodulosphaeria, Ophiobolus, Pleoseptum, and Wilmia lack
molecular data.
History of genera
Amarenomyces Eriksson was introduced as a new genus based
on its multi-layered endotunica and large, thick-walled and
sheathed ascospores (Eriksson 1981). Eriksson (1982) reported Amarenographium to be the asexual state of
Amarenomyces. Amarenomyces was synonymized under
Phaeosphaeria by Zhang et al. (2009) based on phylogenetic
evidence from Amarenomyces ammophilae (Lasch) O.E.
Erikss. which formed a related clade with other
Phaeosphaeria species.
164
Didymella was treated as a member of Phaeosphaeriaceae
by Barr (1979) when she introduced the new family
Phaeosphaeriaceae. However, Silva-Hanlin and Hanlin
(1999) suggested that Didymella belongs in Pleosporaceae
rather than Phaeosphaeriaceae based on phylogenetic relationships, while Lumbsch and Huhndorf (2007) treated
Didymella in Pleosporales, genera incertae sedis. Later, De
Gruyter et al. (2009) introduced a new family Didymellaceae
based on a multigene phylogenetic analysis with Didymella as
the type genus.
Entodesmium was introduced by Reiss (1854) as typified
by E. rude Riess associated with legumes (Zhang et al. 2009).
The genus was previously placed in Lophiostomataceae based
on its periphysate papilla (Eriksson and Hawksworth 1990;
Barr 1992b; Zhang et al. 2009). Liew et al. (2000) sequenced a
strain of E. rude and their phylogenetic analysis indicated that
Entodesmium belongs to Phaeosphariaceae which has been
upheld by subsequent authors (Schoch et al. 2009; Zhang et al.
2009, 2012; Hyde et al. 2013, 2014). However, there is only
one putative strain of Entodesmium rude (CBS 650.86) available in GenBank (Liew et al. 2000), and this is not apparently
linked to any herbarium material.
Eudarluca was introduced by Spegazzini (1908) as a hyperparasite in the uredinia of rust fungi from Canna (Zhang
et al. 2012). Sphaerellopsis was reported to be the asexual
state of this genus (Yuan et al. 1998; Nischwitz et al. 2005;
Zhang et al. 2012). Many strains of Eudarluca caricis (Fr.)
O.E. Erikss. are available in GenBank. Nischwitz et al. (2005)
investigated host specialization and relationships of
Eudarluca caricis with Ampelomyces. Based on the phylogenetic analysis, their results have shown that Eudarluca caricis
formed a clade with other pleosporalean taxa and appeared to
be host-specific (Nischwitz et al. 2005). The phylogenetic
investigation was limited to variation between differentiated
isolates and could not resolve the current placement of
Eudarluca in Phaeosphaeriaceae (Bayon et al. 2006; Zhang
et al. 2012).
Katumotoa was introduced as a monotypic genus in
Phaeosphaeriaceae and was tentatively placed in
Phaeosphaeriaceae (Tanaka and Harada 2005). Later,
Ta n a k a e t a l . ( 2 0 0 9 ) re m o v e d K a t u m o t o a f r o m
Phaeosphaeriaceae and accommodated this genus in the family Lentitheciaceae (Zhang et al. 2009), based on morphological and phylogenetic evidence.
Loratospora was introduced by Kohlmeyer and
Volkmann-Kohlmeyer (1993) as a monotypic genus.
The type species, Loratospora aestuarii Kohlm. &
Volkm.-Kohlm. is an obligate and facultative marine
taxon (Kohlmeyer and Volkmann-Kohlmeyer 1993;
Monkai et al. 2013). Suetrong et al. (2009) transferred
Loratospora to Phaeosphaeriaceae based on phylogenetic
data, whereas based on morphology it had previously been
placed in Planistromellaceae (Barr 1996).
Fungal Diversity (2014) 68:159–238
Ophiosphaerella was introduced by Spegazzini (1909)
with Op. graminicola Speg. as the type species. Barr
(1987b) placed Ophiosphaerella in Phaeosphaeriaceae, due
to its morphological characters (Shoemaker and Babcock
1989b; Dong et al. 1998). The placement in
Phaeosphaeriaceae was confirmed by Zhang et al. (2009,
2012) and Hyde et al. (2013) based on molecular phylogeny.
Phaeosphaeriopsis was introduced to accommodate
Paraphaeosphaeria species that were not congeneric based
on morphological characters and phylogenetic investigation
and that had a Phaeostagonospora asexual state (Câmara et al.
2003; Zhang et al. 2012). The placement of the genus in
Phaeosphaeriaceae was confirmed by multi-gene analysis
(Quaedvlieg et al. 2013; Thambugala et al. 2014).
Setomelanomma was introduced by Morelet (1980) as a
pathogen on blue and white spruce (Morelet 1980; Rossman
et al. 2002). The genus was considered morphologically similar to Phaeosphaeriaceae (Rossman et al. 2002; Zhang et al.
2012). Rossman et al. (2002) confirmed the genus belongs in
Phaeosphaeriaceae based on a phylogenetic analysis and this
was verified with multi-gene analyses (Schoch et al. 2009;
Zhang et al. 2009, 2012; De Gruyter et al. 2012; Hyde et al.
2013; Wijayawardene et al. 2014b).
Placement of asexual genera in Phaeosphaeriaceae
Before the era of molecular phylogeny it was difficult to
establish if asexual genera belonged in Phaeosphaeriaceae
unless single ascospore cultures produced the asexual morph
or where the asexual morph was associated with the sexual
state on the host (Eriksson 1982; Ramaley 1995; Ramaley and
Barr 1995; Yuan et al. 1998; Câmara et al. 2003; Nischwitz
et al. 2005). Previous to the compilation by Hyde et al. (2011)
there were few attempts to incorporate asexual genera in
sexually defined families. Perhaps the first report of an asexual
state of Phaeosphaeriaceae is that of Eriksson (1982) who
reported Amarenographium to be the asexual state of
Amarenomyces. Barr (1987b) listed nine coelomycetous genera, Ascochyta, Chaetodiplodia, Coniothyrium,
Microdiplodia, Microsphaeropsis, Phoma, Scolecosporiella,
Stagonospora and Sphaerellopsis in Phaeosphaeriaceae
based on their holoblastic or enteroblastic conidiogenesis
and aseptate or septate conidia.
Camarosporium yuccaesedum Fairm formed conidiomata
on leaves of Yucca baccata that were associated with
ascomata of Pleoseptum yuccaesedum, the type species of
Pleoseptum, (Ramaley and Barr 1995; Zhang et al. 2012).
Based on its structurally similar and close association,
Ramaley and Barr (1995) linked Camarosporium
yuccaesedum as an asexual state of Pleoseptum.
Camarosporium species had been reported as asexual morphs
in various genera of Botryosphaeriales and Cucurbitariaceae
with doubtful polyphyletic support (Crous et al. 2006; Kirk
Fungal Diversity (2014) 68:159–238
et al. 2008; Liu et al. 2012; Zhang et al. 2012; Doilom et al.
2013). However, Wijayawardene et al. (2014a, c, d) recognized Camarosporium sensu stricto as a distinct phylogenetic
linage in Pleosporineae, Pleosporales hence introduced
Camarosporiaceae, (Wijayawardene et al. 2014a, d)
Hyde et al. (2011) and Wijayawardene et al. (2012) also
listed Hendersonia as an asexual state of Phaeosphaeriaceae.
However, the genus was synonymized under Stagonospora
and is currently placed in Massarinaceae (Swart and Walker
1988; Quaedvlieg et al. 2013).
Parahendersonia Ramaley (1995) was classified by its
ampulliform conidiogenous cells producing thick-walled,
brown, (1–)3-septate conidia. This monotypic genus is represented by P. dasylirionis. The sexual state was reported as
Chaetoplea dasylirionis on Dasylirion (Agavaceae) in
Leptosphaeriaceae (Ramaley 1995; Calatayud and Etayo
2001). However, Barr (1987b) accommodated Chaetoplea
in Phaeosphaeriaceae and reported a microdiplodia-like
asexual state for Chaetoplea (Barr 1990b; Zhang et al.
2012). Recently, Parahendersonia was treated in
Leptosphaeriaceae (Index Fungorum 2014).
Rhabdospora was originally established to accommodate
septoria-like species associated with stems of Nerium
oleander L. (Priest 2006; Quaedvlieg et al. 2013). The
genus was treated in the taxonomic studies of Sutton
(1980) which 11 Rhabdospora species currently classified
under Septoria in Mycosphaerellaceae (Quaedvlieg et al.
2013). Hyde et al. (2011) listed Rhabdospora as the asexual
state of Phaeosphaeriaceae, while Zhang et al. (2012)
treated the genus as an asexual state of Ophiobolus.
Wijayawardene et al. (2014b) treated the genus in
Dothideomycetes, genera incertae sedis. There are 648
epithets listed in Index Fungorum (2014) for
Rhabdospora and it was accommodated in
Mycosphaerellaceae. However, Rhabdospora is a poorly
understood genus and is in need of modern taxonomic and
molecular treatment (Quaedvlieg et al. 2013).
The type species of Scolecosporiella, Sc. typhae
(Oudemans) Petr. was reported as the asexual state of
Phaeosphaeria typharum (Desm.) L. Holm (Nag Raj
1989). The genus has been re-described taxonomic revision by Sutton (1968, 1980) and Nag Raj (1989). Various
sexual genera, such as Ophiobolus, Ophiosphaerella, and
Phaeosphaeria have been reported as Scolecosporiella
sexual states (Farr et al. 1989; Nag Raj 1989;
Shoemaker and Babcock 1989b; Hyde et al. 2011;
Zhang et al. 2012).
Tiarospora was reported as an asexual member of
Phaeosphaeriaceae by Kirk et al. (2008). However, there
are no molecular data to prove that this genus belongs in
Phaeosphaeriaceae. Tiarospora has four epithets in Index
Fungorum (2014) with T. perforans (Sacc.) Höhn being listed
as a synonym of Montagnula perforans (Aptroot 2006).
165
Molecular data has allowed linkage of asexual genera
in Phaeosphaeriaceae
A s c o c h y t a , C h a e t o d i p l o d i a , M i c ro d i p l o d i a a n d
Microsphaeropsis have been reported as asexual states of
Phaeosphaeriaceae (Barr 1987b); however, using phylogenetic evidence Crous et al. (2006) treated Microdiplodia as the
asexual state of Karstenula in Montagnulaceae (Ariyawansa
et al. 2014b). Liu et al. (2012) and Hyde et al. (2013) reported
Microdiplodia as an asexual state in Botryosphaeriaceae.
Ascochyta and Microsphaeropsis were treated in
Didymellaceae based on phylogenetic evidence with the sexual morph of these genera described as Didymella (De Gruyter
et al. 2009; Aveskamp et al. 2010). Ascochyta was shown to
be polyphyletic in Pleosporales by subsequent researchers
(De Gruyter et al. 2009, 2012; Aveskamp et al. 2010).
Furthermore, allied Ascochyta species were determined to
belong in Pleosporaceae by De Gruyter et al. (2012). A
Chaetodiplodia strain formed a clade within
Leptosphaeriaceae; however, the genus is polyphyletic in
Pleosporaceae (De Gruyter et al. 2009, 2012).
Based on phylogenetic evidence, Câmara et al. (2003)
introduced the new genus Phaeosphaeriopsis in
Phaeosphaeriaceae and transferred Paraphaeosphaeria
n o l i n a e A . W. R a m a l e y t o P h a e o s p h a e r i o p s i s .
Phaeostagonospora was reported as the asexual state based
on its morphology (Ramaley 1997). Sexual and asexual
morph connections were studied by Quaedvlieg et al. (2013)
and Thambugala et al. (2014).
De Gruyter et al. (2009) included Wojnowicia hirta (J.
Schröt.) Sacc., the type species in their phylogenetic analysis
and concluded that Wojnowicia hirta has an asexual state in
Phaeosphaeriaceae and this phylogenetic placement was supported by Wijayawardene et al. (2013b, 2014b).
Zhang et al. (2009) listed Ampelomyces,
Chaetosphaeronema, Coniothyrium, Phoma, Plenodomus,
Stagonospora and Wojnowicia (asexual genera) in
Phaeosphaeriaceae. Based on phylogenetic evidence,
Chaetosphaeronema was placed in Phaeosphaeriaceae and
often formed a sister clade with the sexual genus
Entodesmium (Zhang et al. 2009, 2012; Hyde et al. 2013;
Wijayawardene et al. 2014b). Phoma radicina (McAlpine)
Boerema, the type species of Phoma section Paraphoma
formed a sister clade with the sexual genus Setomelanomma
holmii M. Morelet as basal Phaeosphaeriaceae (Zhang et al.
2009, 2012; Hyde et al. 2013; Wijayawardene et al. 2014b).
De Gruyter et al. (2010) introduced two new genera,
Neosetophoma and Setophoma in Phaeosphaeriaceae and
also re-introduced Paraphoma in Phaeosphaeriaceae based
on phylogenetic evidence. Four Phoma species from
Av e s k a m p e t a l . ( 2 0 1 0 ) w h i c h c l u s t e r e d i n
Phaeosphaeriaceae were accommodated in these genera (De
Gruyter et al. 2010). Hyde et al. (2011) reported 17 asexual
166
g e n e r a i n P h a e o s p h a e r i a c e a e ( Ta b l e 1 ) . L a t e r,
Wijayawardene et al. (2012) updated the checklist of asexual
states of Phaeosphaeriaceae and included the
hyphomyceteous genera Harpophora and Mauginiella. In
their compilation of families in Pleosporales, Zhang et al.
(2012) accepted 17 asexual genera in Phaeosphaeriaceae.
They excluded the hyphomycetous genera, based on a broad
familial concept and phylogenetic support.
Hyde et al. (2013) excluded Amarenographium which
formed a clade outside Phaeosphaeriaceae and this is supported by Hodhod et al. (2012). Wijayawardene et al. (2013a)
accommodated Scolicosporium minkeviciusii Treigienė in
Phaeosphaeriaceae as this species formed a clade with other
well-established asexual genera. Furthermore, Crous et al.
(2013) revealed that Xenostigmina and Mycopappus grouped
in Phaeosphaeriaceae in their phylogenetic analysis.
Quaedvlieg et al. (2013) re-circumscribed the pathogenic
fungi genera Septoria, and Stagonospora and related genera
such as Phaeosphaeria and Phaeoseptoria. Based on their
phylogenetic study, they introduced 14 new genera, 36 new
species, and 19 new combinations. The new genera
Neostagonospora, Parastagonospora, Xenoseptoria and
Vrystaatia were placed in Phaeosphaeriaceae. Furthermore,
they epitypified Phaeosphaeria oryzae I. Miyake and
Phaeoseptoria papayae Speg. and confirmed sexual asexual
connections. Phaeoseptoria was confirmed as the asexual
morph of Phaeosphaeria based on the sequenced strain of
P. papayae which formed a well-supported clade with Ph.
oryzae.
Crous et al. (2014) included Septoriella oudemansii
Oudem. in Phaeosphaeriaceae. Septoriella was compared
with species of Phaeosphaeriaceae and a megablast search
of NCBI showed that Septoriella is similar to Phaeosphaeria
caricis, Ph. ammophilae and Ophiosphaerella herpotricha
with high percentage similarities (Crous et al. 2014).
In a new outline of the Dothideomycetes,
Wijayawardene et al. (2014b) proposed synonymies and
suggested names for 34 genera while incorporating asexual
genera into a natural classification. This publication resulted from the new ruling in article 59.1 of International Code
of Nomenclature for Algae, Fungi, and Plants (ICN;
Melbourne Code) that a species or genus can only have
one name. They listed 29 genera (17 only known as asexual
genera) in Phaeosphaeriaceae.
According to phylogenetic evidence, Ampelomyces species
grouped in Didymellaceae and Phaeosphaeriaceae (De
Gruyter et al. 2009; Aveskamp et al. 2010; Hyde et al. 2013;
Wijayawardene et al. 2013a, 2014b). The type species of
Ampelomyces, A. quisqualis Ces. formed a clade within
Phaeosphaeriaceae (De Gruyter et al. 2009; Aveskamp et al.
2010; Wijayawardene et al. 2013a), while A. quercinus (Syd.)
Rudakov grouped in Didymellaceae (De Gruyter et al. 2009).
Therefore, Aveskamp et al. (2010) transferred all
Fungal Diversity (2014) 68:159–238
Ampelomyces species belonging in Didymellaceae, to
Phoma based on phylogenetic relationships.
Coniothyrium Corda (1840) is characterized by pycnidial
c on i d i o m at a, r ed u ce d c on i d i op h or es , a nn e l l i di c
conidiogenous cells, with brown, aseptate or septate, verrucose conidia (De Gruyter et al. 2012). Based on the phylogenetic analyses, Coniothyrium was revealed as polyphyletic in
Pleosporales (Verkley et al. 2004, 2014). The type species of
Co niothyrium , C. palmarum Corda clustered in
Leptosphaeriaceae (De Gruyter et al. 2009). In De Gruyter
et al. (2012), C. palmarum formed a distinct clade with other
Phoma species in the reinstated Coniothyriaceae based on
phylogenetic analysis. De Gruyter et al. (2012) indicated that
Coniothyrium had convergent evolution with similar characters found in other families in Pleosporales such as
Cucurbitariaceae, Didymellaceae, Phaeosphaeriaceae,
Leptosphaeriaceae, Montagnulaceae and Sporormiaceae.
However, Coniothyrium concentricum (Desm.) Sacc. is
related to Phaeosphaeriaceae. A new genus should be
designated to accommodate this coniothyrium-like species
(Hyde et al. 2013).
Harpophora was introduced by Gams (2000) to accommodate phialophora-like species characterized by fast-growing,
thin colonies and sickle-shaped phialoconidia (Gams 2000;
Saleh and Leslie 2004). The genus contains the asexual state
of Gaeumannomyces and Magnaporthe in Magnaporthaceae
(Gams 2000; Saleh and Leslie 2004; Kirk et al. 2008; Yuan
et al. 2010).
Based on a homologous test using ITS sequence data,
Abdullah et al. (2005) indicated that Mauginiella scaettae
Cavara was closely related to species of Phaeosphaeria which
formed a clade with Phaeosphaeria associated with non-grass
hosts. It was concluded that Mauginiella may represent the
asexual state of Phaeosphaeria following the suggestion of
Câmara et al. (2002). Câmara et al. (2002) mentioned that the
morphological characters, asexual state and host preferences
are important to clarify Phaeosphaeria species. It has been
suggested that a great deal of convergent evolution had occurred in species of Leptosphaeria and Phaeosphaeria
(Câmara et al. 2002; Abdullah et al. 2005).
Phoma species have been described as the asexual state of
various genera of Dothideomycetes i.e. Didymella,
Mycosphaerella, Leptosphaeria and Pleospora (Boerema
1997; De Gruyter et al. 2009). De Gruyter et al. (2009) carried
out a re-classification of the Phoma complex based on molecular phylogeny. Their results showed that Phoma was polyphyletic and was subsequently classified in nine sections:
Phoma, Heterospora, Paraphoma, Peyronellaea,
Phyllostictoides, Sclerophomella, Plenodomus, Macrospora,
and Pilosa (Boerema 1997; Boerema et al. 2004; De Gruyter
et al. 2009). Based on phylogenetic evidence, they concluded
that Phoma section Paraphoma, as typified by Ph. radicina
(McAlpine) Boerema can be assigned in Phaeosphaeriaceae,
Fungal Diversity (2014) 68:159–238
while Ph. heteromorphospora, the type species of Phoma
section Heterospora should be treated in Leptosphaeriaceae.
Additionally, the family Didymellaceae was proposed to accommodate others Phoma sections viz. Macrospora,
Peyronellaea, Phoma, Phyllostictoides and Sclerophomella
(De Gruyter et al. 2009). Aveskamp et al. (2010) indicated
that the current Boeremaean subdivision was incorrect as
Phoma is polyphyletic comprising six distinct clades in
Pleosporales and appeared to be common in different families
(Aveskamp et al. 2010). Therefore, De Gruyter et al. (2012)
concluded that Phoma should be restricted only to
Didymellaceae, while other Phoma sections were transferred
to related families. However, Lawrey et al. (2012) treated
lichenicolous Phoma species in Phaeosphaeriaceae based
on their multigene phylogenetic analysis. Therefore, a new
genus should be introduced to accommodate all lichenicolous
Phoma species in Phaeosphaeriaceae (Hyde et al. 2013).
Plenodomus Preuss is typified by Pl. rabenhorstii Preuss to
accommodate the phoma-like species which Boerema (1982)
synonymized under Phoma section Plenodomus (Boerema
et al. 2004; Torres et al. 2005). Torres et al. (2005) mentioned
that Reddy et al. (1998) treated phoma-like species with the
sexual state known as Leptosphaeria in Plenodomus in
Leptosphaeriaceae and concluded that Phoma should be restricted to the species relating to Didymella in
Phaeosphaeriaceae. Zhang et al. (2009) listed Plenodomus
in Phaeosphaeriaceae; however based on phylogenetic evidence, De Gruyter et al. (2012) reinstated the genus
Plenodomus to accommodate Phoma section Plenodomus
within Leptosphaeriaceae.
Sclerostagonospora was typified by S. heraclei (Sacc.)
Höhn. (1917) and characterized with pycnidial conidiomata
with holoblastic, determinate, discrete, ampulliform to irregular conidiogenous cells, and subcylindrical, 3-septate, pale
brown, verruculose conidia (Sutton 1980; Quaedvlieg et al.
2013). Sclerostagonospora differs from Stagonospora in its
pigmented conidia (Quaedvlieg et al. 2013). Crous and Palm
(1999) reported Sclerostagonospora leucadendri Crous &
M.E. Palm as the asexual state of Leptosphaeria leucadendri
Crous & M.E. Palm which occurs on leaves of Leucadendron.
Based on phylogenetic analysis, Sclerostagonospora opuntiae
(Ellis & Everh.) Huhndorf (CBS 118224) formed a clade with
Phaeosphaeria and Phaeosphaeriopsis (Crous et al. 2008).
Thus, Kirk et al. (2008) treated Sclerostagonospora as an
asexual state in the Pleosporales. In Quaedvlieg et al.
(2013), multigene phylogenetic analysis has shown that
Sclerostagonospora phragmiticola Quaedvlieg et al. (CBS
338.86) is related to Phaeosphaeriaceae.
Stagonospora is characterized by holoblastic or annellidic
conidiogenesis and produces phragmoconidia (Schoch et al.
2006; Quaedvlieg et al. 2013). The genus was reported as an
asexual genus in Phaeosphaeriaceae, which often clusters
with Phaeosphaeria and Phoma in phylogenetic analyses
167
(Cunfer and Ueng 1999; Câmara et al. 2002; Solomon et al.
2006; Zhang et al. 2009, 2012; Hyde et al. 2013).
Stagonospora has often been confused with Septoria; however, the genus was clarified by Cunfer and Ueng (1999) and
Solomon et al. (2006). Based on phylogenetic evidence,
Stagonospora is more closely related to other genera in
Pleosporales, while Septoria clustered in
Mycosphaerellaceae, Capnodiales (Quaedvlieg et al. 2013).
Quaedvlieg et al. (2013) re-collected the type species of
Stagonospora, St. paludosa (Sacc. & Speg.) Sacc. and their
phylogenetic analysis showed that this species formed a separate clade with other Stagonospora species which occurred
on Poaceae (i.e. St. avenae (A.B.. Frank) Bissett and St.
nodorum (Berk.) E. Castell. & Germano). Therefore,
Quaedvlieg et al. (2013) concluded that stagonospora-like
species belonged in different genera and introduced the new
genera, Neostagonospora and Parastagonospora to accommodate the stagonospora-like species in Phaeosphaeriaceae.
The type species of Stagonospora, St. paludosa and other
Stagonospora species grouped in Massarinaceae
(Quaedvlieg et al. 2013).
The aim of this study is to revisit all genera of
Phaeosphaeriaceae and provide revised descriptions of the
sexual and asexual morphs of the genera. Available generic
type specimens were examined, described and illustrated. We
have also collected fresh specimens from Thailand and Italy.
Phylogenetic investigation of available sequence data reveals
the current placement of genera in Phaeosphaeriaceae.
Material and methods
Herbarium examination, fungal isolation, morphology
and asexual state study
Type specimens of each genus in Phaeosphaeriaceae were
obtained from BPI, BR, NY, S, and UB herbaria. Morphology
of generic types were examined and re-described. Generic
descriptions were provided based on the original descriptions
and non type herbarium specimens if generic type specimens
could not be located or loaned. Some types were redrawn from
iconotype. Ascomata on herbarium material were rehydrated
by adding 5 % KOH. Free hand sections and squash mounts
were prepared and morphological characters were observed
under stereo microscope and compound microscope.
Collections of Phaeosphaeriaceae were made from Italy
and Thailand and returned to the laboratory for examination. If
the specimens were dry, they were incubated in a moist
chamber for 2–3 days at 25 °C. Ascomata were sectioned by
hand and examined under an Olympus SZH10 stereomicroscope. Macro-morphological characters were photographed
using a Sony DSC-T110 digital camera. The micro-
168
morphological characters were captured by a Cannon 550D
digital camera, using a Nikon ECLIPSE 80i compound microscope with DIC objectives. Indian ink was added to show
mucilaginous sheaths surrounding ascospores. Cotton blue
and congo red reagents were used as stains for checking
ascospore septation and internal elements of the hamathecium.
Permanent slides were prepared by mounting material on
lactoglycerol and sealing with clear nail polish.
Measurements were obtained using a Tarosoft (R) Image
Frame Work version 0.9.7. Photographic plates were prepared
in Adobe Photoshop version CS3 (Adobe Systems Inc., The
United States).
Pure cultures were obtained from single spores following the methods described in Chomnunti et al. (2014) and
Phookamsak et al. (2013). Ascomata were cut at the apex
and sides walls by a razor blade. The contents inside
ascoma was picked and soaked in sterile water and broken
up further mechanically with the sterile needle until a spore
suspension was obtained. The ascospore suspension was
dropped on water agar (WA; 15.0 g/L sterile distilled water)
and incubated at room temperature overnight. The germinating spores were transferred to malt extract agar (MEA;
33.6 g/L sterile distilled water, Difco malt extract) and
cultivated in corn meal agar (CMA, 17 g/l sterile distilled
water, Difco corn meal agar) and potato dextrose agar
(PDA; 39 g/L distilled water, Difco potato dextrose) for
recording growth rates and culture characters. Sterile bamboo pieces on water agar (WA; 15 g/l sterile distilled water)
were used to encourage production of asexual morphs.
Cultures are deposited in Mae Fah Luang University
Culture Collection (MFLUCC), and duplicated in the
International Collection of Microorganisms from Plants
(ICMP), Landcare Research, New Zealand. Herbarium
specimens were prepared by drying the specimens with
silica gel at room temperature for 7–10 days depending on
the humidity and kept in envelopes or small boxes. The
herbarium specimens are deposited in the herbarium of Mae
Fah Luang University (MFLU), Chiang Rai, Thailand and
duplicates in the New Zealand Fungal Herbarium (PDD),
Landcare Research, New Zealand or Université Catholique
de Louvain, Belgium (MUCL).
Molecular and phylogenetic analysis
Fungal DNA extraction, PCR amplification and sequencing
The fungal colonies were grown on MEA/PDA at 25–
30 °C for 2–4 weeks. After 4 weeks, the fungal mycelium was scraped and transferred to micro centrifuge tube.
The fungal genomic DNA was extracted by Biospin
Fungus Genomic DNA Extraction Kit (BioFlux®,
China) following the manufacturer’s instructions
(Hangzhou, P.R. China).
Fungal Diversity (2014) 68:159–238
DNA amplifications were performed by Polymerase Chain
Reaction (PCR). The internal transcribed spacer (ITS) was
amplified by using primers ITS4 and ITS5 as defined by
White et al. (1990). The partial small subunit nuclear rDNA
(SSU) was amplified by using primers NS1 and NS4 (White
et al. 1990). The partial large subunit nuclear rDNA (LSU)
was amplified by using primers LROR and LR5 (Vilgalys and
Hester 1990). The partial RNA polymerase second largest
subunit (RPB2) was amplified by using primers fRPB2-5F
and fRPB2-7cR (Liu et al. 1999). The translation elongation
factor 1-alpha gene (TEF1) was amplified by using primers
EF1-983F and EF1-2218R (Rehner 2001). The amplification
reaction were carried out following protocol: The final volume
of the PCR reaction was 50μl which contained 2.0μl of DNA
template, 1.5μl of each forward and reverse primers, 25μl of
2× Easy Taq PCR SuperMix (mixture of EasyTaqTM DNA
Polymerase, dNTPs, and optimized buffer, Beijing TransGen
Biotech Co., Ltd., Chaoyang District, Beijing, PR China) and
20μl sterilized water (Phookamsak et al. 2013).
The PCR thermal cycle program of ITS, nuSSU, nuLSU
and TEF1 genes amplification were provided as: initially
94 °C for 3 min, followed by 40 cycles of denaturation at
94 °C for 30 s, annealing at 55 °C for 50 s, elongation at 72 °C
for 1 min, and final extension at 72 °C for 10 min. The PCR
thermal cycle program for the partial RNA polymerase second
largest subunit (RPB2) was obtained by step as initially 95 °C
for 5 min, followed by 40 cycles of denaturation at 95 °C for
1 min, annealing at 52 °C for 2 min, elongation at 72 °C for
90 s, and final extension at 72 °C for 10 min. The quality of
PCR products were checked on 1 % agarose gel electrophoresis strained with ethidium bromide. The PCR products were
send for sequencing at Shanghai Sangon Biological
Engineering Technology & Services Co., Ltd (Shanghai,
P.R. China) (Phookamsak et al. 2013).
Phylogenetic analyses
Combined ITS, LSU, SSU, RPB2 and TEF1 sequence data
were used for phylogenetic analysis in this study. The reference nucleotide sequences of Phaeosphaeriaceae and other
selected families in Dothideomycetes were obtained from the
GenBank database and included in the analysis (see
Supplementary table). The fungal sequence strains were combined and aligned in MEGA6 (Tamura et al. 2013) and improved manually where necessary in BioEdit v. 7.2 (Hall
1999). The combined sequences alignment was analyzed by
Bayesian, maximum likelihood and maximum parsimony
methods.
Bayesian analyses was carried out using MrBayes v. 3.0b4
(Ronquist and Huelsenbeck 2003). The best-fit model of
sequences evolution was estimated by using MrModeltest
2.2 (Nylander 2004). Markov Chain Monte Carlo sampling
(BMCMC) in MrBayes v. 3.0b4 (Huelsenbeck and Ronquist
Fungal Diversity (2014) 68:159–238
2001) were used to determine the Posterior probabilities (PP)
(Rannala and Yang 1996; Zhaxybayeva and Gogarten 2002).
Phylogenetic trees were sampled every 100th generation
(resulting in 10,000 total trees) in 1,000,000 generations from
the running of six simultaneous Markov chains. The first
2,000 trees which contained the burn-in phase of the analyses
were discarded. The remaining 8,000 trees were used to
calculate the posterior probabilities (PP) in the majority rule
consensus tree (Liu et al. 2011).
A maximum likelihood analysis (ML) was performed in
RaxmlGUI v.1.0 (Silvestro and Michalak 2011). Alignments
in PHYLIP format were loaded and automatically checked
their compatibility in raxmlGUI. The available substitution
models consisting of a generalized time reversible (GTR) was
applied with four rate classes and a discrete gamma distribution (Yang 1994) for nucleotides, symmetric, Markovian, and
ordered models for morphological characters (Liu et al. 2011;
Silvestro and Michalak 2011). The best scoring tree from a
separate randomized tree under the same model was selected.
Rapid bootstrap with nonparametric bootstrap iterations
(Stamatakis et al. 2008) was run in 1,000 replicates with the
GTR model and a discrete gamma distribution (Liu et al.
2011).
A maximum parsimony (MP) analysis was conducted by
using PAUP v. 4.0b10 (Swofford 2002). The heuristic search
option with 1,000 random sequences addition and treebisection reconnection (TBR) of branch-swapping algorithm
were performed. Maxtrees were setup at 1,000 and a zero of
maximum branch length was collapsed. Gaps were treated as
missing data and all characters were unordered and of equal
weight. All multiple, equally parsimonious trees were saved.
Descriptive tree statistics for parsimony consistency index
(CI), retention index (RI), rescaled consistency index (RC)
and homoplasy index (HI) was calculated. The robustness of
the best parsimonious tree was estimated by a bootstrap (BT)
value with 1,000 replicates, each with 10 replicates of random
stepwise addition of taxa (Liu et al. 2011; Phookamsak et al.
2013). The best scoring phylogram from Bayesian analysis
was selected for representing phylogenetic relationships and
drawn in Treeview (Page 1996) with bootstrap values above
and below the branches. All the sequences generated in this
study have been deposited in GenBank (Liu et al. 2011;
Phookamsak et al. 2013).
Results and discussion
Three phylogenetic reconstructions were generated to clarify
the phylogenetic relationships of genera and species that have
been accommodated in Phaeosphaeriaceae. Figure 1 deals
with the genus and family level placement within the
Phaeosphaeriaceae and Pleosporales. The dataset includes
169
LSU, SSU, RPB2, and TEF1 sequences and were analyzed
using maximum likelihood (ML), maximum parsimony (MP)
and Bayesian analyses. The dataset comprised 85 taxa, with
Massaria inquinans (M 19) selected as the outgroup taxon.
Twenty-nine Phaeosphaeriaceae taxa formed a wellsupported clade (74 % ML/ 1.00 PP) within the suborder
Pleosporinae, while Mycopappus and Xenostigmina form a
single clade close to Melanommataceae. Therefore, we exclude these later genera from Phaeosphaeriaceae in this study.
Wilmia was synonymized under Letendraea by Ariyawansa
et al. (2014b). Phylogenetic evidence shows Letendraea
cordylinicola is related with Didymosphaeriaceae which form
a strongly-supported clade (75 % ML/ 1.00 PP) with
Paraphaeosphaeria michotii (CBS 652.86), Deniquelata
barringtoniae (MFLUCC 11-0422) and Kalmusia brevispora
(KT 2313) in Didymosphaeriaceae. Thus, Letendraea is excluded from Phaeosphariaceae in this study and transferred to
Didymosphaeriaceae. Phaeosphaeriopsis,
Parastagonospora, Ophiosphaerella, Phaeosphaeria and
Setophoma are well-resolved genera and formed distinct
clades, while the other clades comprised groups of genera
without clear combining features or comprising more than
one genus (Fig. 2).
Figure 2 focuses on the phylogenetic relationships of genera in Phaeosphaeriaceae. The multigene combined dataset
(ITS, LSU, SSU and RPB2) were obtained from maximum
likelihood (ML), maximum parsimony (MP) and Bayesian
analysis. Didymella exigua (CBS 183.55) was selected as
the outgroup taxon. The dataset consists of 58 taxa, with 57
taxa belonging to the Phaeosphaeriaceae. Eleven clades (A–
K) can be recognized in Fig. 2. Clade A comprises the genera
Chaetosphaeronema, Dermatiopleospora, Entodesmium,
Loratospora. Nodulosphaeria and Ophiobolus.
Dermatiopleospora, Entodesmium and Loratospora are represented by their ex-type strains and type species. This clade
needs better populating with many more species from the
respective genera as it is presently not well-resolved.
Ophiobolus cirsii (MFLUCC 13-0218) formed a robust clade
(99 % ML/ 97 % MP/ 1.00 PP) with the asexual genus
Chaetosphaeronema, while O. erythrosporus (MFLU 122225) forms a weakly supported clade with Entodesmium
rude. However, Ophiobolus is not represented by its type
species and the strains used have not been morphologically
clearly defined (see Ariyawansa et al. 2014c). Clade B represents the genus Phaeosphaeriopsis and is well resolved in
Phaeosphaeriaceae (97 % ML/ 93 % MP/ 1.00 PP). It is
represented by the type species Ps. glaucopunctata (ex-type
strain), plus other strains and a new species Ps. dracaenicola
is also introduced here (see details in “Taxonomy” section).
Clade C represents Phaeosphaeria sensu stricto with five
species, including the type species and two new species;
detailed phylogenetic relationships among these species are
shown in Fig. 3. Clade D represents two isolates of the genus
170
Fungal Diversity (2014) 68:159–238
Fig. 1 A Bayesian 50 % majority rule consensus tree based on combined
dataset of LSU, SSU, TEF1 and RPB2 alignment. Bootstrap support
values for maximum likelihood (ML, red) and maximum parsimony
(MP, green) equal or greater than 60 % are given above the nodes.
Bayesian posterior probabilities (BYPP, blue) equal or higher than 0.95
are given below the nodes. Massaria inquinans (M 19). Ex-type and exepitype strains are in bold. Newly generated sequences are in red and the
type species are indicated in blue
Ophiosphaerella, which form a strongly supported clade
(100 % ML/ 100 % MP/ 1.00 PP) separate from
Ophiosphaerella herpotricha. The two strains of
Ophiosphaerella agrostidis are clearly defined based on morphology (see under Ophiosphaerella agrostidis). However,
the genus Ophiosphaerella is not represented by its type
species. Further isolates and type strains from Ophiobolus
and Ophiosphaerella are required to better resolve and naturally place these genera. Clade E comprises the genera
Amarenomyces, Sclerostagonospora, and Wojnowicia plus a
putative strain of Ophiosphaerella herpotricha and four
strains of Phaeosphaeria. Phaeosphaeria ammophilae is not
closely related to Phaeosphaeria sensu stricto, the species is
reinstated as Amarenomyces, while other Phaeosphaeria taxa
in this clade may need removing from Phaeosphaeria.
However, the tree needs to be better populated with strains
that are morphologically well-defined before adjustments can
be made. Clade F comprises two strains, Phaeosphaeria
alpina and Ph. typharum which are also unrelated to
Phaeosphaeria sensu stricto and need further study. Clade G
comprises the type species and ex-type strains of
Ampelomyces and Neosetophoma, these genera also need to
Fungal Diversity (2014) 68:159–238
Fig. 2 A Bayesian 50 % majority rule consensus tree based on combined
dataset of ITS, LSU, SSU and RPB2 alignment. Bootstrap support values
for maximum likelihood (ML, blue) and maximum parsimony (MP,
green) equal to or greater than 60 % are given above the nodes. Bayesian
171
posterior probabilities (BYPP, red) equal or higher than 0.95 are given
below the nodes. The tree is rooted to Didymella exigua. Ex-type and exepitype strains are in bold. Newly generated sequences are in red and the
type species are indicated in blue
172
Fungal Diversity (2014) 68:159–238
Fig. 3 Maximum parsimony tree
based on a combined dataset of
ITS, LSU, RPB2 and TEF1.
Bootstrap support values for
maximum parsimony (MP, green)
(equal to or greater than 50 %)
and the values of the Bayesian
posterior probabilities (BYPP,
blue) from MCMC analyses
provided significant (equal or
higher than 95 %) are given above
the nodes. The tree was rooted to
Phaeosphaeria juncicola. Extype and ex-epitype strains are in
bold. Newly generated sequences
are in blue
be better populated with strains that are morphologically
well-defined. Clade H comprises the ex-types strains and
type species of Parastagonospora and, Neostagonospora,
and ex-type strains Sclerostagonospora cycadis,
Scolicosporium minkeviciusii and Wojnowicia viburni (the
latter three species are not generic types). Three
Phaeosphaeria sensu lato strains also cluster here indicating the polyphyletic nature of the genus. Clade I comprises
Xenoseptoria, Setomelanomma and Paraphoma, with
Xenoseptoria and Paraphoma represented by ex-type
strains of their type species. Setomelanomma is closely
related to Xenoseptoria which formed a robust clade
(97 % ML/ 71 % MP) in our multigene phylogenetic analyses. Clade J represents Vrystaatia with single species,
V. aloeicola. Clade K represents the asexual genus
Setophoma with five strains, including the type species,
S. terrestris. The genus is well-resolved in our phylogenetic
analyses which form a strongly supported clade (100 %
ML/ 64 % MP/ 1.00 PP) at the basal of Phaeosphariaceae.
Figure 3 deals with the species complex of Phaeosphaeria
sensu stricto and Parastagonospora. Phaeosphaeria
juncicola (CBS 110108) was selected as the outgroup taxon.
The newly generated strains which were collected from
Thailand form a robust clade with the ex-type species,
Phaeosphaeria oryzae and with Ph. papayae and Ph. musae
in the Phaeosphaeria sensu stricto clade. Phaeosphaeria
sensu stricto is distinguished from Parastagonospora, the
Fig. 4 ITS pair wise comparison of Phaeosphaeria oryzae (CBS
110110), P. oryzae (RP0086; MFLUCC 11-0170), P. papayae (CBS
135416), P. thysanolaenicola (RP0036; MFLUCC 10-0563),
P. chiangraina (RP0131; MFLUCC 13-0231), P. musae (CBS
120026) and P. musae (RP0049; MFLUCC 11-0133 and RP0067;
MFLUCC 11-0151)
Fungal Diversity (2014) 68:159–238
173
174
species having been accommodated in Phaeosphaeria and
Phaeosphaeria sensu lato (Phaeosphaeria alpina and Ph.
typharum).
Phaeosphaeria sensu stricto taxa (MFLUCC 11-0133;
MFLUCC 11-0151) cluster with Ph. musae (CBS 120026),
a pathogen of banana. An ITS pair wise comparison shows
that these three isolates differ in seven base positions (Fig. 4)
while there are only one to two base differentiated in TEF1
gene comparisons. Isolate MFLUCC 11-0133 is slightly morphologically different from the other two isolates (MFLUCC
11-0151 and CBS 120026) in its ascus and ascospore sizes.
However, these three isolates are generally similar in morphology and phylogeny. Therefore, we treat the isolates causing leaf spot disease on Calathea sp. and Cordyline sp. from
Thailand as conspecific with Phaeosphaeria musae.
Phaeosphaeria thysanolaenicola (MFLUCC 10-0563), a
pathogen on Thysanolaena maxima, forms a clade with. Ph.
chiangraina, which is saprobic on rice. These two species
form strongly-supported clades which are well-resolved from
the ex-type species of Phaeosphaeria oryzae.
Phaeosphaeria avenaria, Ph. eustoma and Ph. nigrans
form a clade with Parastagonospora species.
Phaeosphaeria avenaria was synonymized under
Parastagonospora avenae by Quaedvlieg et al. (2013), and
the other two species may need to be synonymized under
Parastagonospora based on the phylogenetic relationships.
However, it was not possible to observe the types of these
species or confirm if they are correctly identified.
Phaeosphaeria alpina and Ph. typharum form a distinct
clade from the Phaeosphaeria sensu stricto species which is
separate with other Phaeosphaeria sensu lato taxa. The type
species need to re-visited and a new genus may need to be
introduced to accommodate these species.
Taxonomy
Phaeosphaeriaceae M.E. Barr Mycologia 71(5): 948 (1979).
Faces of Fungi number: FoF00232
Endophytic, hyperparasitic, pathogenic, or saprobic on
monocotyledonous and some dicotyledonous hosts. Sexual
state: Ascomata scattered, clustered, solitary or gregarious,
immersed to semi-immersed or erumpent through host tissue,
small to large, uniloculate, globose to subglobose, glabrous or
setose, brown to dark brown or black, ostiolate, with short to
long papilla. Peridium with thin to thick walls, composed of
brown to dark brown or black, pseudoparenchymatous cells,
mostly arranged in a textura angularis to textura prismatica.
Hamathecium composed of sparse to numerous, filamentous,
septate, rarely anastomosing, mostly cellular
pseudoparaphyses, or pseudoparaphyses occasionally lacking. Asci 8-spored, bitunicate, fissitunicate, cylindrical to cylindric-clavate, or clavate, sessile to subsessile, or usually with
Fungal Diversity (2014) 68:159–238
short pedicels, apically rounded with typically well-developed
ocular chamber. Ascospores overlapping muriform,
phragmosporous, or scolecosporous, varying in shape from
ellipsoidal, fusiform to broadly fusiform, clavate, and cylindrical to filiform, mostly brown to dark brown or reddishbrown, sometimes hyaline, 1- to multi-septate, constricted or
not constricted at the septum, walls smooth or rough,
echinulate, punctuate or verrucose, some with appendage or
mucilaginous sheath. Asexual state: Coelomycetous.
Conidiomata pycnidial, scattered, solitary or gregarious,
immersed to superficial, uni- to multi-loculate, globose
to subglobose, glabrous or setose, light brown to dark
brown or black, ostiole central, papillate. Conidiomata
walls thin, composed of pseudoparenchymatous cells, arranged in a textura angularis to textura prismatica.
Conidiophores lining inner cavity of the conidioma, typically reduced to conidiogenous cells, hyaline to brown,
aseptate or septate. Conidiogenous cells enteroblastic or
holoblastic, annellidic or phialidic, discrete, oblong to
ampulliform, hyaline to brown. Conidia varied in shape,
hyaline to brown, aseptate or septate, walls smooth or
rough, echinulate, punctuate or verrucose, some with appendage or mucilaginous sheath.
Notes: Phaeosphaeriaceae is one of the largest families
in Pleosporales, and demonstrates variability in morphological characters. Previously, many genera with brown
spores, associated with monocotyledonous hosts, having a
thin-walled peridium and producing coelomycetous asexual states were accommodated in Phaeosphaeriaceae
(Barr 1979, 1987b, 1990a, 1992a; Crivelli 1983; Schatz
1984; Shoemaker 1984; Shoemaker and Babcock 1989b;
Yuan 1994; Ramaley and Barr 1995; Dianese et al. 2001;
Zhang et al. 2009, 2012). Most of genera in
Phaeosphaeriaceae lack molecular data or only limited
sequence data is available in some genera such as
Entodesmium and Phaeosphaeria. Several genera in
Phaeosphaeriaceae share morphological characters with
genera in other families (e.g. Didymosphaeriaceae,
Leptosphaeriaceae and Pleosporaceae) and thus their
placement is confused. Therefore, re-visiting all type genera of Phaeosphaeriaceae to establish their morphology
and to obtain molecular sequence data from fresh collections are essential to provide modern descriptions and to
determine the placement of genera in this family.
Type: Phaeosphaeria I. Miyake, Bot. Mag., Tokyo 23: 93
(1909).
Notes: The following genera are placed in
Phaeosphaeriaceae. Genera are listed in alphabetical order
and provided with genus description and notes, descriptions of type or authentic species, notes on species, material examined and illustrations. If the genus is monotypic, only a single description which also represents the
genus is provided.
Fungal Diversity (2014) 68:159–238
Key to genera of Phaeosphaeriaceae
1. Sexual state . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1. Asexual state . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
2. Ascospores phragmosporous or scolecosporous . . . . . . 3
2. Ascospores dictyosporous, muriform, on Ononis
spinosa (dicotyledon) . . . . . . . . . . . . . Dematiopleospora
3. Ascospores phragmosporous . . . . . . . . . . . . . . . . . . . . . . . . . 4
3. Ascospores scolecosporous . . . . . . . . . . . . . . . . . . . . . . . . . 12
4. Ascospores 2–3-septate . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4. Ascospores mostly more than 3-septate . . . . . . . . . . . . . 10
5. Ascospores mostly 2-septate, associated with rust
fungi . . . . . . . . . . . . . . . . . . . . . . . . Eudarluca
5. Ascospores 3-septate, saprobic or pathogenic on monocots
or dicots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
6. Ascomata in groups or rows with slit-like ostioles;
ascospores hyaline . . . . . . . . . . . . . . . . . . . . . . . Bricookea
6. Ascomata solitary, scattered, opening ostiolate to papillate; ascospores pale brown, yellowish brown to
brown . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .7
7. Asci ovoid to ampulliform, aparaphysate, on Juncus
roemerianus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Loratospora
7. Asci broadly cylindrical, cellular pseudoparaphyses . . . . . 8
8. Ascomata typically glabrous . . . . . . . . . . . . . . . . . . . . . . . 9
8. Ascomata typically setose . . . . . . . . . . . Setomelanomma
9. Ascomata typically immersed, ostioles with minute papilla,
asexual state: Phaeoseptoria . . . . . . . . . . . . . Phaeosphaeria
9. Ascomata semi-immersed to erumpent, near superficial, ostiole with conical, knob-like, asexual:
unknown . . . . . . . . . . . . . . . . . . . Dothideopsella
10. Ascospores cylindrical, with typically one enlarged
cell . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
10. Ascospores broadly fusiform, widest at the middle cell,
saprobic on Ammophila . . . . . . . . . . . . . Amarenomyces
11. Papilla, with numerous long, large setae in the
ostiole, ascospores with one enlarged cell near
apex . . . . . . . . . . . . . . . . . . . . Nodulosphaeria
11. Papilla absent, opening ostiolate, ascospores typically
enlarged cell near the base . . . . . . . . . . Phaeosphaeriopsis
12. Ascospores with enlarged cells . . . . . . . . . . .Ophiobolus
12. Ascospores lacking enlarged cells . . . . . . . . . . . . . . . . 13
13. Ascospores constricted at the septa, breaking into part
spores, saprobic or parasitic on legumes . . . . Entodesmium
13. Ascospores non-constricted at the septum, not
separating into part spores, saprobic on various
monocots . . . . . . . . . . . . . . . . Ophiosphaerella
14. Conidia amerosporous, didymosporous phragmosporous
or scolecosporous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
14. Conidia dictyosporous (muriform) . . . Amarenographium
15. Conidia aseptate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .16
15. Conidia septate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
16. Saprobic or pathogenic, conidiomata setose . . . . . . . . 17
16. Mycoparasitic on powdery mildew . . . . . Ampelomyces
175
17. Conidiomata dark brown, no sexual state
reported . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Paraphoma
17. Conidiomata pale brown, olivaceous to olivaceous-black,
sexual state: ascospores cylindrical, hyaline, 3-septate,
with enlarged in second cell from apex . . . . . . Setophoma
18. Conidiomata setose or covered by mycelium . . . . . . . 19
18. Conidiomata glabrous . . . . . . . . . . . . . . . . . . . . . . . . . . 21
19. Conidia 1–3-septate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
19. Conidia more than 3-septate . . . . . . . . . . . . . . . Wojnowicia
20. Conidiophores present, hyaline, 1-septate
conidia . . . . . . . . . . . . Chaetosphaeronema
20. Conidiophores absent, yellowish, typically 0–1(−3)septate conidia . . . . . . . . . . . . . . . . . . . . . Neosetophoma
21. Conidia 1-septate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
21. Conidia more than 1-septate . . . . . . . . . . . . . . . . . . . . . . . . 23
22. Conidia with appendage . . . . . . . . . . . . . . . . . Tiarospora
22. Conidia without appendage . . . . . . . . Neostagonospora
23. Conidia hyaline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
23. Conidia pigmented . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
24. One type of conidia, cylindrical to obclavate . . . . . . . 25
24. Two types of conidia (macroconidia subcylindrical to
narrowly obclavate; microconidia aseptate, pearshaped to globose or ellipsoid) . . . . . . . . . . . . Vrystaatia
25. Conidiomata exuding a creamy conidial mass, conidiophores absent; sexual state: phaeosphaerialike . . . . . . . . . . . . . . . . . . . Parastagonospora
25. Conidiomata exuding a pink to orange conidial
mass, conidiophores branched; sexual state: ??
Setomelanomma . . . . . . . . . . . . . . Xenoseptoria
26. Conidia usually 3-septate . . . . . . . . . . . . . . . . . . . . . . . . 27
26. Conidia usually more than 3-septate . . . . . . . . . . . . . . 29
27. Conidia produced one type of conidia . . . . . . . . . . . . . . . . 28
27. Conidia produced two types of conidia (microconidia
globose to ellipsoidal, hyaline) . . . . . Phaeostagonospora
28. Conidia subcylindrical, pale brown, minutely
verruculose . . . . . . . . . . . . . . . . . . . Sclerostagonospora
28. Conidia subcylindrical, wider in the middle, yellowishbrown, smooth-walled . . . . . . . Septoriella oudemansii
29. Conidia fusiform, 5–6-septate, apical cell attenuated into a
short, beak-like, appendage . . . . . . . . . . . . Scolecosporiella
29. Conidia curved to sigmoid, 6–7-septate, with hyaline end
cells . . . . . . . . . . . . . . . . . . . . Scolicosporium minkeviciusii
Amarenographium O.E. Erikss., Mycotaxon 15: 199
(1982), Faces of Fungi number: FoF00237.
Saprobic on marine grasses. Sexual state: see notes.
Asexual state: Conidiomata pycnidial, scattered, solitary,
immersed to erumpent through host tissue by papilla,
uniloculate, ellipsoidal to subglobose, glabrous, brown to dark
brown, ostiole central, with papilla. Conidiomata walls thin,
composed of thick-walled, reddish-brown to dark brown cells,
arranged in textura angularis to textura prismatica.
Conidiophores mostly reduced to conidiogenous cells, hyaline to brown, septate, branched. Conidiogenous cells
176
holoblastic, phialidic, discrete, determinate, ampulliform,
rarely cylindrical, hyaline, smooth-walled, produced macroand microconidia. Macroconidia dictyosporous, blasticphialidic, broadly ellipsoidal to clavate or fusiform, brown to
dark brown, paler at the ends cells, muriform, septate, smoothwalled, with mucoid appendage at apex. Microconidia
amerosporous, blastic-phialidic, hyaline, smooth-walled
(from Eriksson 1982; Nag Raj 1989).
Type species: Amarenographium metableticum
Phylogenetic study: Hodhod et al. (2012)
Notes: Amarenographium metableticum (Trail) O.E.
Erikss. is the type of Amarenographium which was introduced
as the asexual state of Amarenomyces (Eriksson 1982; Nag
Raj 1989; Hodhod et al. 2012). Amarenographium
metableticum had previously been identified as
Camarosporium metableticum which was not congeneric with
C a m a ro s p o r i u m st e p h e n s i i , t he g en er i c ty pe o f
Camarosporium at that time (Sutton 1980; Eriksson 1982).
Therefore, Eriksson (1982) transferred Camarosporium
metableticum to a new genus based on the different morphological characters (Hodhod et al. 2012; Hyde et al. 2013).
Amarenographium differs from Camarosporium by its conidiophores and conidia. In Amarenographium conidiophores are
longer and branched and conidia have gelatinous appendages
(Eriksson 1982; Hodhod et al. 2012). Hodhod et al. (2012)
introduced a new species of Amarenographium, Am. solium
Abdel-Wahab et al. from mangroves and noted that
Amarenographium did not belong in Phaeosphaeriaceae but
clusters with Pleosporales, genera incertae sedis, while
Amarenomyces formed a clade with Phaeosphaeria in
Phaeosphaeriaceae (Zhang et al. 2009, 2012). However,
Hodhod et al. (2012) did not study the type species and the
type species of Amarenographium lacks molecular data to
confirm the relationships between these genera. Thus we
presently maintain the genus in Phaeosphaeriaceae.
Amarenographium metableticum (Trail) O.E. Erikss.,
Mycotaxon 15: 199 (1982), Faces of Fungi number:
FoF00238, Fig. 5.
≡ Camarosporium metableticum Trail, Scott. Natural., N.S.
2 (‘8’): 267 (1886) [1885–1886]
Saprobic on Ammophila. Sexual state: see notes. Asexual
state: Conidiomata 160–215.5μm high, 150–270μm diam.,
pycnidial, scattered, solitary, immersed to erumpent, visible as
black spots on host surface, uniloculate, globose to
subglobose, glabrous, dark brown, ostiole central, with short
to long papilla. Conidiomata walls 13–19μm wide, thinwalled, of equal thickness, composed of 3–5 layers of flattened, brown to dark brown, pseudoparenchymatous cells,
arranged in a textura angularis to textura prismatica.
Conidiophores arising from basal cavity of conidioma, mostly
reduced to conidiogenous cells, hyaline to brown, septate.
Conidiogenous cells (1.5–)3–4(−9) × 1.5–2.5(−5) μm
(x = 3.9×2.3μm, n=10), holoblastic, phialidic, discrete,
Fungal Diversity (2014) 68:159–238
oblong to ampulliform, hyaline to brown, 1-septate at the
base, smooth-walled. Conidia (20–)24–27(−29) × 12–
15(−17) μm (x = 25.4 × 13.4 μm, n = 30), solitary,
dictyosporous, muriform, ellipsoidal, ovoid, or lageniform,
with obtuse ends or sometimes truncate at the basal cell,
initially hyaline, becoming brown to yellowish-brown at maturity, mostly 3–4 transverse septa, 1–4 longitudinal septa,
with several segments, smooth and thick-walled, with indistinct mucoid appendage.
Material examined: SWEDEN, Öland, Böda parish,
Lugnet beach, on Ammophila arenari (L.) Link (Poaceae), 2
June 1963, B. Eriksson & O. Eriksson 2022c (S-F207509).
Amarenomyces O.E. Erikss., Op. bot. 60: 124 (1981),
Faces of Fungi number: FoF00235.
Type species: Amarenomyces ammophilae
Phylogenetic study: Zhang et al. (2009, 2012), Hyde et al.
(2013)
Amarenomyces ammophilae (Lasch) O.E. Erikss., Op.
bot. 60: 124 (1981), Faces of Fungi number: FoF00236,
Fig. 6.
≡ Sphaeria ammophilae Lasch Flora, Jena 33: 282 (1850)
Saprobic on Ammophila. Sexual state: Ascomata 170–
290μm high, 170–285μm diam., scattered, immersed to
erumpent through host tissue, visible as small black spots on
host surface, uniloculate, globose to subglobose, glabrous,
dark brown, ostiole central, with short papilla (50–130μm
long). Peridium 7.5–25μm wide, thin-walled, of equal thickness, composed of 3–5 layers of flattened, dark brown,
pseudoparenchymatous cells, arranged in textura angularis
to textura prismatica. Hamathecium composed of numerous, 1.5–3μm wide, filiform, distinctly septate, frequently
anastomosing, narrow cellular pseudoparaphyses, embedded in mucilaginous matrix. Asci (112–)140–160(−173)×
(28–)30–35(−37) μm (x = 140×32.4μm, n=25), 8-spored,
bitunicate, fissitunicate, broadly cylindrical, subsessile
with minute knob-like pedicel, apically rounded, with a
well-developed ocular chamber. Ascospores 39–47(−50)×
12–14 μm (x = 43.4 × 13.2 μm, n = 30), overlapping
1–3-seriate, phragmosporous, broadly fusiform, rarely
cylindric-clavate, widest at the middle cell, pale yellowish
when immature, becoming yellowish-brown to brown at
maturity, 6-septate, slightly constrict at the septum, smooth
and thick-walled.
Material examined: BELGIUM, West-Vlaanderen,
Blankenbergh, on Ammophila arenaria L. (Poaceae),
Westendorp (S-F77691); ITALY, Sardegna, Cagliari, La
Maddelena, March 1866, Marcucci (S-F77741).
Notes: Amarenomyces was introduced by Eriksson (1981)
to accommodate the single species from a marine grass, which
traditionally has been identified as Sphaeria ammophilae
Lasch. Eriksson (1981) mentioned that the genus should belong in Botryosphaeriaceae rather than Phaeosphaeriaceae as
its morphological characters differed from Phaeosphaeria.
Fungal Diversity (2014) 68:159–238
177
Fig. 5 Amarenographium metableticum (S-F207509). a Specimens
and herbarium label of Amarenographium metableticum b Conidiomata
visible on host surface. c Section through conidiomata. d Section through
conidiomata wall. e–g Conidiogenous cells. h–k Conidia. Scale bars: c=
100μm, d=20μm, e, h, i, j, k=10μm, f, g=5μm
Zhang et al. (2009) listed Amarenomyces as a synonym of
Phaeosphaeria based on phylogenetic evidence. The generic
type of Amarenomyces, A. ammophilae often clusters with
other Phaeosphaeria species (Zhang et al. 2009, 2012;
Hyde et al. 2013). Thus the earlier name as proposed by
Kohlmeyer and Kohlmeyer (1965) and Leuchtmann (1984)
was reinstated as Phaeosphaeria ammophilae (Suetrong
et al. 2009; Zhang et al. 2009).
Several Phaeosphaeria species have previously been transferred to other genera based on the phylogenetic evidence and
due to their asexual state. For example Phaeosphaeria
nodorum which was transferred to Parastagonospora, as Pa.
nodorum. On the other hand, Shoemaker and Babcock
(1989b) divided Phaeosphaeria into six subgenera by combining Phaeosphaeria species with similar morphological
characters, but differing in ascospore characters, host
178
Fig. 6 Amarenomyces ammophilae (S-F77691). a Specimens and herbarium label b Ascomata visible on host surface. c Section through
ascoma. d Section through peridium. e Asci with cellular
Fungal Diversity (2014) 68:159–238
pseudoparaphyses. f–i Asci. j–m Ascospores. n Ascospore stained in
indian ink. Scale bars: c=100μm, c, d=50μm, e, f, g, h, i=20μm, j, k,
l, m, n=10μm
Fungal Diversity (2014) 68:159–238
preference and asexual state (Câmara et al. 2002; Zhang et al.
2012; Quaedvlieg et al. 2013). The asexual state of
Phaeosphaeria has been reported as Phaeoseptoria and this
is supported by phylogenetic data (Quaedvlieg et al. 2013).
Quaedvlieg et al. (2013) transferred Phaeosphaeria species
which did not produce Phaeoseptoria asexual states to other
genera. Therefore, the genus Amarenomyces is reinstated in
this study based on the phylogenetic analysis as
A. ammophilae forms a separate clade to the type species,
Phaeosphaeria oryzae. Although A. ammophilae has often
been reported to be the sexual state of Amarenographium
metableticum (Trail) O.E. Erikss., they are not treated as
congeneric here. The presumed link was established as both
species occur on the same host in close proximity. There is,
however, no sequence data for Amarenographium
metableticum and it might be predicted that if both species
were host-specific then it would not be surprising that they
both occur on the same host. We therefore refrain from combining the taxa until molecular data confirms the link.
Ampelomyces Ces. ex Schlecht., Bot. Zeit. 10: 302 (1852),
Faces of Fungi number: FoF00291.
Hyperparasitic on Erysiphales or saprobic. Sexual state:
unknown. Asexual state: Conidiomata pycnidial, scattered,
solitary, superficial, uniloculate, globose or elongated to pyriform, pale brown, ostiolate, sometimes papillate.
Conidiomata walls thick, composed of pale brown cells,
arranged in textura angularis. Conidiophores mostly reduced
to conidiogenous cells. Conidiogenous cells enteroblastic,
phialidic, determinate, discrete, doliiform to ampulliform, hyaline, smooth-walled, channel and collarette minute, periclinal
wall towards apex thickened, formed directly from the pycnidial wall cells. Conidia amerosporous, cylindrical to fusiform, straight to curved, very pale brown, aseptate, thin and
smooth-walled, with guttules. (Sutton 1980)
Type species: Ampelomyces quisqualis Ces., Bot. Ztg. 10:
301 (1852).
Phylogenetic study: Kiss and Nakasone (1998),
Szentiványi et al. (2005), Liang et al. (2007), De Gruyter
et al. (2009), Aveskamp et al. (2010), Hyde et al. (2013),
Wijayawardene et al.(2013a)
Notes: Ampelomyces species have been reported as
mycoparasites on powdery mildews (Erysiphaceae) and are
worldwide in nature (de Bary 1870; Griffith 1899; Kiss 1998;
Kiss et al. 2004). The genus was introduced by Cesati (1852)
to accommodate taxa that formed pycnidia as intracellular
mycoparasites on powdery mildews (De Bary 1870; Kiss
et al. 2004). Previously, Ampelomyces had varied morphological and cultural characteristic with species differentiated
based on pycnidia, cultures and conidial types in isolates of
pycnidial mycoparasites from powdery mildews (Clare 1964;
Belsare et al. 1980; Kiss et al. 2004). In Kiss et al. (2004),
Ampelomyces species could be distinguished into slow and
fast growing types. Based on the rDNA ITS region
179
phylogenetic analysis, Kiss et al. (2004) concluded that strains
from the two types of differentiated growth rate were not
congeneric. The slow-growing isolates, obtained from intracellular pycnidia in powdery mildew mycelia was
Ampelomyces sensu stricto. While fast growing isolates from
sessile pycnidia on mildew-infected leaves, were closely related to Phoma species. Ampelomyces quercinus (Syd.)
Rudakov, A. humuli (Fautrey) Rudakov and A. heraclei
(Dejeva) Rudakov are example of fast growing species
(Rudakov 1979; Kiss and Nakasone 1998; Sullivan and
White 2000). De Gruyter et al. (2009) included two isolates
of the type species; A. quisqualis in their phylogenetic analysis
and showed that the type species of Ampelomyces can be
accommodated in Phaeosphaeriaceae. Whereas
Ampelomyces quercinus grouped in Didymellaceae; thus,
Aveskamp et al. (2010) introduced A. quercinus as new combination within Phoma in Didymellaceae.
Bricookea M.E. Barr, Mycotaxon 15: 346 (1982), Faces of
Fungi number: FoF00239.
Saprobic on Juncaceae. Sexual state: Ascomata scattered
or clustered, immersed to semi-immersed, becoming
erumpent through host tissue or superficial at maturity, unito multi-loculate, globose to subglobose, glabrous, brown to
dark brown, ostiole central, with slit-like opening. Peridium
thin-walled, composed of brown to dark brown, pseudoparenchymatous cells, arranged in a textura angularis.
Hamathecium composed of numerous, filamentous, distinctly
septate, broad cellular pseudoparaphyses, anastomosing at the
apex. Asci 8-spored, bitunicate, fissitunicate, cylindrical to
cylindric-clavate, narrow towards apex, short pedicellate, apically rounded, with well-developed ocular chamber.
Ascospores overlapping, 1–3-seriate, phragmosporous, ellipsoidal to broadly fusiform, hyaline, septate, slightly curved,
constricted at the median septum, smooth and thick-walled.
Asexual state: Unknown.
Type species: Bricookea sepalorum
Phylogenetic study: None
Notes: Barr (1982) introduced Bricookea to accommodate
B. sepalorum that was previously identified as Leptosphaeria
sepalorum (Vleugel) Lind (Lind 1928). Holm (1957)
observed the collections from Sweden and compared the
morphological characters with specimens from North
America. He mentioned that the ascospores and asci of
Swedish collections were smaller than North American
specimens and regarded the species as synonym of Lizonia
emperigonia (Auersw.) de Not. (Barr 1982; Shoemaker and
Babcock 1989a; Zhang et al. 2012). Barr (1982) did not agree
with Holm (1957) and designated the new genus, Bricookea to
accommodate Leptosphaeria sepalorum. Barr (1982)
suggested placing Bricookea in Phaeosphaeriaceae with its
uniquely opening ostioles and lack of known asexual state.
Barr (1982) mentioned that Sphaerulina inquinans Rehm may
be provided as earlier epithet of Bricookea sepalorum.
180
However, Shoemaker and Babcock (1989a) studied the type
specimens of Bricookea from S herbaria and mentioned that
no material was found under the name Sphaerulina inquinans.
Subsequently, Shoemaker and Babcock (1989a) introduced
the new species, Bricookea barrae from a North American
collection which had been examined by Barr (1982).
Bricookea barrae [as Br. barriae] was synonymized under
the name Lophiostoma barriae in Lophiostomataceae by
Eriksson (2007) leaving the genus monotypic. Zhang et al.
(2012) tentatively place Bricookea in Phaeosphaeriaceae.
C u r r e n t l y, B r i c o o k e a i s g e n e r a l l y t r e a t e d i n
Lophiostomataceae based on its slit-like ostioles, but the type
species, Br. sepalorum has been synonymized under the earlier name in Leptosphaeriaceae as Leptosphaeria sepalorum
(Index Fungorum 2014).
We examined the collection from North America and type
specimen from S herbaria. Both collections have similar morphological characters. However, the specimens from North
America differ in having larger ascoma, asci and ascospores
than the type specimen from Europe. In this study, Bricookea
forms a group in pseudostroma, with slit-like ostioles; characters typical of Lophiostomataceae. However, we tentatively
place Bricookea in Pheaosphaeriaceae as its peridium is thinwalled, composed of pseudoparenchymatous cells, asci are
clavate with a subsessile to short acute pedicel and ascospores
are phragmosporous. Fresh collection, epitypification and
molecular analysis are needed to confirm the natural
placement.
Bricookea sepalorum (Vleugel) M.E. Barr, Mycotaxon 15:
346 (1982), Faces of Fungi number: FoF00240, Fig. 7.
≡ Metasphaeria sepalorum Vleugel, Svensk bot. Tidskr.
2(4): 369 (1908)
Saprobic on Juncus spp. Sexual state: Ascomata 130–
210μm high, 170–250μm diam., scattered to clustered, gregarious, immersed to semi-immersed under epidermis, becoming erumpent through host tissue, to superficial at maturity, visible as black dots in rows or groups on host surface,
uni- to multi-loculate, globose to subglobose, glabrous, dark
brown to black, ostioles central, with slit-like opening.
Peridium 10–20μm wide, thin-walled, of equal thickness,
composed of 2–3 layers of large, brown to dark brown,
pseudoparenchymatous cells, arranged in a textura angularis.
Hamathecium composed of numerous, 1.5–2μm wide, filamentous, distinctly septate, cellular pseudoparaphyses, embedded in mucilaginous matrix, anastomosing at the apex.
Asci (60–)65–75(−80)×12–14(−16) μm (x = 71.5×13.5μm,
n=30), 8-spored, bitunicate, fissitunicate, cylindric-clavate,
narrowing towards the apex, with subsessile to shortly acute
pedicel, apically rounded with well-developed ocular chamber. Ascospores 17.5–19(−21)×6–7.5μm (x = 19×6.4μm,
n=30), overlapping 1–2-seriate, phragmosporous, ellipsoidal
to broadly fusiform, hyaline to subhyaline, initially forming
one median septate, becoming 3-septate at maturity, slightly
Fungal Diversity (2014) 68:159–238
curved, constricted at the median septum, easily breaking into
part spores at the median septum, smooth and thin to thickwalled. Asexual state: Unknown.
Material examined: SWEDEN, Suecia. Holmön,
Västerbotten, on dead sepals of Juncus filiformis Linn.
(Juncaceae), July 1907, J. Vleugel (S-F49661, type); USA,
California, Squaw Valley Creek Meadows, Mt. Shasta,
Siskiyou Co. alt. 8,500 ft., on dead sepals of Juncus parryi
Engelm. (Juncaceae), 10 July 1947, W. B. Cooke & V. G.
Cooke (BPI 737398); Washington, Mt. Baker National Forest,
Whatcom Co. Subalpine Meadows along Washington Route
#1 near Baker Lodge, on dead sepals of Juncus parryi
Engelm. (Juncaceae), 12 July 1948, W. B. Cooke & V. G.
Cooke 24247 (BPI 737397); California, King Creek Trail,
Lassen Volcanic National Park. alt. 8,000 ft., on dead sepals
of Juncus parryi Engelm. (Juncaceae), 1 July 1954 W. B.
Cooke & V. G. Cooke 29530 (BPI 737400); California, King
Creek Trail, Lassen Volcanic National Park. alt. 8,000 ft., on
dead sepals of Juncus parryi Engelm. (Juncaceae), 1 July
1954, W. B. Cooke & V. G. Cooke 29530 (BPI 737399);
California, Panther Creek Meadows, Mt. Shasta, Siskiyou
Co. alt. 7,600 ft., on dead sepals of Juncus parryi Engelm.
(Juncaceae), 4 July 1948, W. B. Cooke 24055 (BPI 737401).
Chaetosphaeronema Moesz, Bot. Közl. 14: 152 (1915),
Faces of Fungi number: FoF00241.
Saprobic or pathogenic on Malus, Euphorbia, Anthyllis
and Dorycnium spp. Asexual state: Unknown Conidiomata
pycnidial, scattered, immersed to semi-immersed, uniloculate,
globose, setose, brown to dark brown, ostiole central, with
setose papilla. Conidiomata walls thin, arranged in a textura
prismatica, pale brown, outer layers comprising dark brown,
thick-walled cells. Conidiophores arising from basal cavity of
conidiomata mostly reduced to conidiogenous cells.
Conidiogenous cells enteroblastic, phialidic, discrete or integrated, cylindrical, hyaline, smooth-walled, with minute channel or collarette, hardly distinguishable from the inner wall
cells. Conidia didymosporous, oblong to cylindrical, with
obtuse ends, straight or slightly curved, hyaline, 1-septate,
thin and smooth-walled, with guttules (from Sutton 1980;
Quaedvlieg et al. 2013)
Type species: Chaetosphaeronema hispidulum (Corda)
Moesz, Bot. Közl. 14: 152 (1915)
= Sphaeronaema hispidulum Corda, Icon. fung. (Prague) 4:
39 (1840)
Phylogenetic study: Schoch et al. (2009), De Gruyter et al.
(2009, 2010), Zhang et al. (2009, 2012), Hyde et al. (2013),
Quaedvlieg et al. (2013).
Notes: Chaetosphaeronema was introduced by Moesz
(1915) as typified by Ch. hispidulum to accommodate species
of Sphaeronaema that were not congeneric. A partial morphological treatment of the genus was provided by Sutton (1980).
Petrak (1944) treated Ch. herbarum (Hollós) Moesz as a
synonym of Ch. hispidulum and accepted three species in
Fungal Diversity (2014) 68:159–238
Fig. 7 Bricookea sepalorum (S-F49661, type). a Herbarium label and
specimens b Ascomata on substrate. c Section through stroma d
Section through peridium. e Asci with cellular pseudoparaphyses strained
181
in cotton blue reagent. f–g Asci. h–i Asci stained in cotton blue reagent. j
Ascospores. k–n Ascospores. Scale bars: b=1000μm, c=100μm, e, f, g,
h, i, j=20μm, d, k, l, m, n=10μm
182
the genus; Ch. collivagum (Petr.) Petr., Ch. galii (Petr.) Petr.
a n d C h . h i s p i d u l u m ( S u t t o n 1 9 8 0 ) . H o w e v e r,
Chaetosphaeronema was subsequently limited to the type
species (De Gruyter et al. 2009, 2010; Zhang et al. 2012;
Hyde et al. 2013; Quaedvlieg et al. 2013). De Gruyter et al.
(2009) showed, using molecular data that
Chaetosphaeronema was related to Phaeosphaeriaceae and
Pleosporaceae. De Gruyter et al. (2010) introduced a new
species, Ch. coonsii (Boerema & Loer.) Gruyter et al., and
treat e d Chaetosphaeronema sensu s tricto i n
Phaeosphaeriaceae. This placement has been widely accepted by subsequent authors based on the phylogenetic evidence,
while no sexual state is presently known (Schoch et al. 2009;
Zhang et al. 2009, 2012; Hyde et al. 2013; Quaedvlieg et al.
2013).
In this study, Chaetosphaeronema clusters with various
sexual genera and is closely related to Ophiobolus cirsii
(MFLUCC13-0218) as propose by Petrak (1944) and Zhang
et al. (2009) who suggested that Chaetosphaeronema may be
asexual state of Ophiobolus. The link between these genera
has not yet equivocally been proven. Epitypification with
molecular data is therefore needed to confirmed the natural
placement of these genera and confirm asexual-sexual
connections.
Dematiopleospora Wanasinghe et al., Cryptog. Mycol. 35
(2): 105-11(2014), Faces of Fungi number: FoF00242.
Saprobic on Ononis spinosa L (Fabaceae). Sexual state:
Ascomata scattered, solitary, superficial, uniloculate, globose
to subglobose, glabrous, dark brown to black, coriaceous,
cupulate when dry, ostiole central, minute papilla, with thick,
brown, periphyses. Peridium thin-walled, composed of pseudoparenchymatous cells, outer layer comprising heavily
pigmented, thick-walled, reddish to dark brown cells, arranged in textura angularis, inner layer comprising 2–3 cell
layers of thin-walled, hyaline cells, arranged in a textura
angularis. Hamathecium composed of numerous, filamentous, distinctly septate, broad cellular pseudoparaphyses.
Asci 8-spored, bitunicate, fissitunicate, cylindrical to cylindric-clavate, short pedicellate, apically rounded with minute
ocular chamber. Ascospores overlapping 1–2-seriate,
dictyosporous, muriform, ellipsoidal to subfusiform, widest
in the upper part, slightly curved, 5–9 transverse septa, with 3–
6 longitudinal septa, constricted at the central septum, initially
hyaline, becoming yellowish-brown at maturity, smoothwalled. Asexual state: Unknown (from Wanasinghe et al.
2014)
Type species: Dematiopleospora mariae Wanasinghe et al.,
Cryptog. Mycol. 35 (2): 105-11(2014)
Phylogenetic study: Wanasinghe et al. (2014).
Notes: Dematiopleospora was introduced by Wanasinghe
et al. (2014) to accommodate D. mariae. The genus is characterized by thick, brown, periphyses in the ostiole, superficial
ascomata and muriform ascospores. Dematiopleospora is
Fungal Diversity (2014) 68:159–238
similar to Nodulosphaeria in its periphysate ostiole, but
they differ in peridium structure and ascospore morphology. Dematiopleospora has muriform ascospores similar
to those characterized in Phaeosphaeria vagans (Niessl)
O.E. Erikss., Ph. phragmiticola Leuchtm., Ph. phragmitis
(Hollós) Leuchtm and Pleoseptum yuccaesedum A.W.
Ramaley & M.E. Barr (Shoemaker and Babcock 1989b;
Z h a n g e t a l . 2 0 1 2 ; Wa n a s i n g h e e t a l . 2 0 1 4 ) .
Dematiopleospora is similar to Pleoseptum, but they
differ in peridium structures and papillate ostioles.
Pleoseptum lacks of molecular data to confirm its natural
placement. Therefore, the genus is tentatively placed in
Pleosporaceae based on its muriform ascospores and
thick-walled peridium that are dominant characters in
Pleosporaceae. Multigene phylogenetic analyses indicated that Dematiopleospora belongs to Phaeosphaeriaceae
which forms a separate clade from those Phaeosphaeria
s p e c i e s a n d g r o u p s w i t h C h a e t o s p h a e ro n e m a ,
Entodesmium, Loratospora and Nodulosphaeria. No
asexual morph is known for Dematiopleospora.
Dothideopsella Höhn., Sber. Akad. Wiss. Wien, Math.naturw. Kl., Abt. 1 124: 70 (1915), Faces of Fungi number:
FoF00295
Saprobic on dead wood and stems in terrestrial habitats.
Sexual state: Ascomata scattered, gregarious, immersed to
semi-immersed, or erumpent, nearly superficial, globose,
uniloculate, subglobose or obypyriform, glabrous, dark brown
to black, ostiole central, broadly or narrowly conical, with a
dark brown to black papilla. Peridium thin to thick, of unequal
thickness, slightly thick at the basal ascoma, composed of dark
brown to black, thin-walled, pseudoparenchymatous cells,
arranged in a textura angularis. Hamathecium composed of
numerous, filamentous, distinctly septate, cellular
pseudoparaphyses, anastomosing without a gelatinous coating. Asci 8-spored, bitunicate, fissitunicate, cylindrical to oblong, with a knob like pedicel, apically rounded with welldeveloped ocular chamber Ascospores phragmosporous, ellipsoidal to fusiform, brown or yellowish brown, septate,
slightly constricted at the septum, smooth-walled. Asexual
state: Unknown (from Ariyawansa et al. 2013).
Type species: Dothideopsella agminalis (Sacc. &
Morthier) Höhn., Sber. Akad. Wiss. Wien, Math.-naturw.
Kl., Abt. 1 124: 70 (1915)
Phylogenetic study: None
Notes: Dothideopsella was introduced by Höhnel (1915)
and is typified by Dothideopsella agminalis (Sacc. &
Morthier) Höhn. The genus was established to accommodate
Dothideomycetes species characterized by a broad peridium
structure, with conical, papillate ostioles, and
phragmosporous, brown ascospores (Ahn and Shearer 1998;
Ariyawansa et al. 2013). Lumbsch and Huhndorf (2010)
treated Dothideopsella in Dothideomycetes, genera incertae
sedis, while Index Fungorum (2014) lists the genus in
Fungal Diversity (2014) 68:159–238
Leptosphaeriaceae. Ariyawansa et al. (2013) tentatively
placed Dothideopsella in Phaeosphaeriaceae based on its
morphological characters which are typical of Chaetoplea.
Dothideopsella however differs from Chaetoplea in having a
peridium composed of pseudoparenchymatous cells, while the
peridium in Chaetoplea is composed of
scleroplectenchymatous cells. The placement of the genus in
Phaeosphaeriaceae was supported by Wijayawardene et al.
(2014b). Thus we tentatively place Dothideopsella in
Phaeosphaeriaceae until molecular date proves otherwise.
Entodesmium Riess, Hedwigia 1(6): 28 (1854), Faces of
Fungi number: FoF00243.
Saprobic or parasitic? on various dicotyledonous and some
monocotyledonous hosts. Sexual state: Ascomata scattered,
solitary to gregarious, immersed to erumpent through host
tissue with long neck, uniloculate, globose to subglobose,
glabrous, dark brown to black, ostiole central, with long neck.
Neck with thick walls of textura angularis, dark brown to
black, cylindrical to cylindric-clavate, carbonaceous, with
periphyses. Peridium thick-walled, composed of brown to
dark brown, pseudoparenchymatous cells, arranged in a
textura angularis. Hamathecium composed of numerous, filamentous, distinctly septate, broad cellular pseudoparaphyses,
not constricted at the septa and anastomosing at the apex. Asci
8-spored, bitunicate, cylindrical to cylindric-clavate, short
pedicellate, apically rounded, with well-developed ocular
chamber. Ascospores fasciculate, scolecosporous, filiform or
filamentous, initially hyaline to pale brown, becoming brown
or reddish-brown at maturity, multi-septate, constricted at the
septa, separating into numerous part spores, smooth-walled.
Asexual state: Unknown.
Type species: Entodesmium rude
Phylogenetic study: Liew et al. (2000), Schoch et al.
(2009), Zhang et al. (2009, 2012)
Notes: Entodesmium was introduced by Riess (1854) and is
typified by E. rude. The genus was introduced to accommodate a Dothideomycete species with long beaked ascomata
and scolecosporous ascospores, which break into numerous
part-spores and occur on legumes. The placement of
Entodesmium was previously unclear as Von Arx and Müller
(1975) disposed the genus in Pleosporaceae, while Barr
(1987b) suggested that Entodesmium should be placed in
Phaeosphaeriaceae and this was accepted by Eriksson and
Hawksworth (1991). Barr (1992b) assigned Entodesmium to
Lophiostomataceae based on its short, blackish beak and
periphysate ostiole. Barr (1992b) mentioned that these characters are more typical of Lophiostomataceae. Zhang et al.
(2009, 2012) disagreed with Barr (1992b) and mentioned that
the morphological characters of Entodesmium best fit in
Phaeosphaeriaceae.
Entodesmium was thought to be family-specific and associated only with legumes (Barr 1992b; Shoemaker 1984;
Zhang et al. 2009, 2012). Holm (1957) and Shoemaker
183
(1984) re-described Entodesmium and reported six species
associated with legumes from Europe; although, Wehmeyer
(1952) identified some collections from North America (Barr
1992b). Furthermore, there is a report of E. niesslianum from
Dieffenbachia (monocotyledon) in West Indies by Minter
et al. (2001) in Farr and Rossman (2014). Six species are
presently accommodated in Entodesmium; E. eliassonii L.
Holm, E. lapponicum (L. Holm) L. Holm, E. mayorii (E.
Müll.) L. Holm, E. nevadense Petr., E. niesslianum (Rabenh.
ex Niessl) L. Holm and E. rude (Index Fungorum 2014).
Entodesmium multiseptatum (G. Winter) L. Holm was
assigned to Leptosphaeriaceae and Entodesmium
vermisporum (Ellis) M.E. Barr (1992b) was treated in
Lophiostomataceae (Winter 1872; Barr 1992b; Zhang et al.
2009, 2012; Index Fungorum 2014). However, Zhang et al.
(2009, 2012) mentioned that E. multiseptatum and
E. niessleanum are more similar to Phaeosphaeria than
Leptosphaeria or Entodesmium.
Zhang et al. (2009) accepted the scolecosporous genera
Entodesmium and Ophiosphaerella in Phaeosphaeriaceae
based on phylogenetic evidence. Multigene phylogenetic
analysis based on this sequence data has indicated that
Entodesmium belongs to Phaeosphaeriaceae which has been
widely accepted (Schoch et al. 2009; Zhang et al. 2009, 2012;
Hyde et al. 2013).
In this study, the iconotype is re-drawn while the type
specimens could not be located. Based on morphology (thinwalled peridium composed of pseudoparenchymatous cells,
and scolecosporous, brown, multi-septate ascospores breaking
into part-spores) and multigene phylogenetic analysis, we
retain Entodesmium in Phaeosphaeriaceae. Entodesmium
forms a weakly-supported clade with other genera
(Chaetosphaeronema, Dematiopleospora, Loratospora,
Nodulosphaeria modesta, Ophiobolus cirsii and
O. erythrosporus) in Phaeosphaeriaceae. However, the sequence data is from a putative strain of Entodesmium rude
from CBS, thus epitypification and molecular work is needed
to confirm its natural placement.
Entodesmium rude Riess, Hedwigia 1(6): 28 (1854),
Faces of Fungi number: FoF00244, Fig. 8, and 9.
Saprobic on Astragalus, Coronilla and Lathyrus spp.
Sexual state: Ascomata 160–240μm high (excluding neck),
160–255μm diam., scattered, solitary to gregarious, immersed
to erumpent through host tissue with long neck, visible as
black dots, in rows or groups on host surface, uniloculate,
globose to subglobose, glabrous, dark brown to black, ostiole
oblique, with long carbonaceous neck. Neck 175.5–295μm
high, 90–150μm diam., thick-walled, cylindrical to cylindricclavate, arranged in a textura angularis, dark brown to black,
carbonaceous, with periphyses. Peridium 15–30μm wide,
thick-walled, of equal thickness, comprising two layers, outer
layer comprising 3–5 cell layers of brown to dark brown,
thick-walled cells, arranged in textura angularis to textura
184
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Fungal Diversity (2014) 68:159–238
Entodesmium rude (BR 5020100367693). a Herbarium packet
and specimens. b Ascomata on substrate. c Section through ascomata. d
Section through neck. e Section through peridium. f Asci with
pseudoparaphyses. g–i Asci. Scale bars: c=100μm, d=50μm, e, f, g, h,
i=20μm
Fig. 8
globulosa, inner layers comprising 1–2 cell layers of thinwalled, hyaline, flattened cells, arranged in textura
angularis to textura prismatica. Hamathecium composed
of numerous, 2–3 μm wide, filiform, distinctly septate,
broad cellular pseudoparaphyses, embedded in mucilaginous matrix, anastomosing at the apex. Asci (124–)130–
145(−156) × (11–)13–15(−18) μm (x = 137.4 × 14.4 μm,
n=25), 8-spored, bitunicate, broadly cylindrical to cylindric-clavate, short pedicellate, apically rounded with welldeveloped ocular chamber. Ascospores (100–)110–
120(−135)×3–4μm (x= 115.5×3.5μm, n=25), fasciculate,
scolecosporous, filiform, initially hyaline to pale brown,
becoming brown to reddish-brown at maturity, multi-septate, with 18–20 septa, constricted at the septa, easily separating into part spores, smooth-walled.
Fig. 9 Entodesmium rude
(iconotype) redrawn from Riess
(1854). a Ascomata on host
surface. b Section through
ascomata. c Ascus with
pseudoparaphyses. d Ascospores
185
Material examined: GERMANY, on stem of Astragalus
glycyphyllos, December 1853, H. Riess, Hedwigia 1(6): Tab
IV, (Fig 4., iconotype) (1854); CZECHOSLOVAKIA, Usti,
on Astragalus glycyphyllos L. (Fabaceae), 6 May 1922, F.
Petrak (BR 5020100367693); CZECHOSLOVAKIA,
Moravia, Hranice (Maehr.-weisskirchen), on branches of
Astragalus glycyphyllos L. (Fabaceae), July 1924, F. Petrak
(BPI 626664).
Eudarluca Speg., Revta Mus. La Plata 15: 22 (1908),
Faces of Fungi number: FoF00245. Hyperparasitic associated with rust species (but not necessarily parasitic) on various
hosts. Sexual state: Ascomata scattered, solitary to gregarious, immersed to semi-immersed under pseudoclypeus, unito multi-loculate, subglobose to irregular in shape, glabrous,
dark brown to black, ostiole central, with minute papilla.
Peridium thin-walled, composed of brown to dark brown,
flattened, pseudoparenchymatous cells, arranged in a textura
angularis. Hamathecium composed of numerous, filamentous, distinctly septate, frequently anastomosing, broadly cellular pseudoparaphyses. Asci 8-spored, bitunicate,
fissitunicate, cylindrical, short pedicellate, apically rounded,
186
with well-developed ocular chamber. Ascospores
phragmosporous, overlapping 2-seriate, fusiform or oblong
with rounded ends, pale brown, septate, smooth-walled.
Asexual state: see notes.
Type species: Eudarluca australis
Phylogenetic study: None
Notes: Eudarluca was introduced by Spegazzini (1908) and
typified by Eu. australis which is associated with a rust on
leaves of Canna. Eriksson (1966) treated Eu. australis as a
synonym of Eudarluca caricis (Fr.) O.E. Erikss. Eudarluca
caricis has been reported from various hosts, mostly in its
presumed asexual state, Sphaerellopsis (Yuan et al. 1998;
Nischwitz et al. 2005; Zhang et al. 2012). The asexual and
sexual state connection between Eudarluca caricis and
Sphaerellopsis filum was derived from ascospores growing on
Puccinia extensicola-oenotherae (Mont.) Arthur on Carex sp.
in Pennsylvania, USA (Keener 1951) and confirmed by Yuan
et al. (1998). Yuan et al. (1998) grew ascospores of Eudarluca
caricis on PDA and derived Sphaerellopsis conidia and
conidiomata after 12 days. Zhang et al. (2012) compared the
ITS sequence of Eudarluca caricis strain MullMK in GenBank
with Leptosphaeria species and mentioned that Eudarluca
should be treated in Leptosphaeriaceae due to comparable
sequences and also morphological characters. However, both
the generic type of Eudarluca and Sphaerellopsis have never
been linked (Wijayawardene et al. 2014b).
Molecular studies on Eudarluca are limited to species
variation and are based on Sphaerellopsis strains (Nischwitz
et al. 2005; Bayon et al. 2006; Zhang et al. 2012). The ITS
gene phylogenetic analysis showed that Eudarluca ciricis
(strains MosID6 and MullMK) cluster in Leptosphaeriaceae.
However, the generic type of Sphaerellopsis has found on
Quercus, while the type of Eudarluca is from Canna. These
two generic types have not been linked by molecular data. We
suggest that caution should be followed when treating these
taxa, as Eu. australis is immersed in the Canna leaves and
although associated with the rust fungi (Sphaerellopsis) on
Canna, it does not seem to grow on the rust.
In this study, we tentatively place Eudarluca in
Phaeosphaeriaceae based on its morphological characters which
are typical of Phaeosphaeria as the peridium is thin-walled, and
composed of pseudoparenchymatous cells, asci are cylindrical,
subsessile to short pedicellate and ascospores are fusiform and
phragmosporous. Fresh collections of Eu. australis are needed
for epitypification and molecular study. Sphaerellopsis may belong in Leptosphaeriaceae where it is tentatively assigned.
Eudarluca australis Speg., Revta Mus. La Plata 15: 22
(1908), Faces of Fungi number: FoF00246, Fig. 10.
Hyperparasitic associated with rust fungi on leaves of
Canna indica L. (Cannaceae). Sexual state: Ascomata 110–
180μm high, 170–280μm diam., scattered, solitary to gregarious, immersed to semi-immersed, visible as raised, black tiny
spots in black pseudostromata on leaf lesions, uniloculate,
Fungal Diversity (2014) 68:159–238
subglobose to irregular, glabrous, dark brown to black, ostiole
central, with minute papilla. Peridium 5–13μm wide, thinwalled, of unequal thickness, slightly thickened at the apex,
composed of 1–3 layers of brown to dark brown, flattened,
pseudoparenchymatous cells, arranged in textura angularis.
Hamathecium composed of numerous, 1.5–3μm wide, filiform, distinctly septate, frequently anastomosing, broadly cellular pseudoparaphyses, embedded in mucilaginous matrix.
Asci (44–)50–65×8–10μm (x = 57×9μm, n=25), 8-spored,
bitunicate, fissitunicate, cylindrical, short pedicellate or
subsessile, apically rounded, with indistinct ocular chamber.
Ascospores 15–17(−18)×3–4.5μm (x = 16.7×4.1μm, n=30),
phragmosporous, overlapping or 2-seriate, fusiform, or oblong with rounded ends, pale brown, 2-septate, rarely 1-septate, slightly curved, not constricted at the septa, smoothwalled. Asexual state: see notes.
Material examined: BRAZIL, São Paulo, Botanical
Gardens, associated with rust (Pucciniaceae) on leaves of
Canna indica L., 10 August 1905, A. Usteri (S-F11420,
isotype).
Loratospora Kohlm. & Volkm.-Kohlm., Syst. Ascom.
12(1–2): 10 (1993), Faces of Fungi number: FoF00247.
Type species: Loratospora aestuarii
Phylogenetic study: Schoch et al. (2009), Suetrong et al.
(2009), Zhang et al. (2012), Hyde et al. (2013).
Loratospora aestuarii Kohlm. & Volkm.-Kohlm., Syst.
Ascom. 12(1–2): 10 (1993), Faces of Fungi number:
FoF00248, Fig. 11.
Saprobic on Juncus roemerianus Scheele. Sexual state:
Ascomata 130–250μm high, 160–310μm diam., scattered to
clustered, solitary, immersed to erumpent through host surface,
visible as small black spots on host surface, uni to biloculate,
globose to subglobose, glabrous, brown to dark brown, ostiole
central, with minute papilla, with brown periphyses. Peridium
18–42μm wide, thin-walled, of unequal thickness, thickened at
the apex, composed of several layers of brown to dark brown,
pseudoparenchymatous cells, arranged in textura angularis to
textura globulosa. Hamathecium absent, visible as mucilaginous matrix between asci. Asci (60–)70–85(−110)×(23–) 25–
30(−35) μm (x = 80.9×28.2μm, n=20), 8-spored, bitunicate,
fissitunicate, ovoid to ampulliform, thick-walled at the apex,
sessile to subsessile, apically rounded with indistinct ocular
chamber, sparse in mucilaginous matrix. Ascospores 40–
50(−55)×5–7(−8) μm (x = 46.7×6.7μm, n=30), overlapping
or parallel, 4–5-seriate, phragmosporous, cylindrical, or narrowly elongate fusiform with rounded ends, initially hyaline
to subhyaline, pale yellowish at maturity, 3-septate, slightly
curved, not constricted at the septa, rough-walled, surrounded
by a thin, distinct sheath. Asexual state: Unknown.
Material examined: USA, North Carolina, on dead culms
of Juncus roemerianus (Juncaceae), Kohlmeyer_5505
(holotype), 5520, 5523, 5525, 5535 (NY_Slide box: 17,
Tray no. 21); ibid. Broad Creek (Atlantic Ocean) 34° 43′ 00″
Fungal Diversity (2014) 68:159–238
187
Fig. 10 Eudarluca australis (S-F11420, isotype). a Herbarium label and
specimens. b Fruiting bodies on host surface. c Section through ascoma. d
Section through peridium. e Pseudoparaphyses. f Asci with
pseudoparaphyses. g–j Asci. k–o Ascospores. Scale bars: c=100μm, d,
f, g, h, i, j=20μm, e=10μm, k, l, m, n, o, = 5μm
N, 76° 55′ 07″W (34.717, −76.919), standing dead culms of
Juncus roemerianus, J. Kohlmeyer 5520 with B. Kohlmeyer,
13 October 1993 (NY 01276343).
Notes: The monotypic genus Loratospora was established
by Kohlmeyer and Volkmann-Kohlmeyer (1993) to accommodate L. aestuarii. The taxon occurs on dead culms of
188
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Fig. 11 Loratospora aestuarii a Herbarium label and specimens
(Kohlmeyer_5505). b, c Ascomata on host surface (Kohlmeyer_5505,
Kohlmeyer_5520). d Section through ascoma (Kohlmeyer_5505). e
Section through peridium (Kohlmeyer_5505) f–g Asci (Kohlmeyer
_5505). h Asci embedded in a gelatinous matrix (Kohlmeyer_5520). i–j
Asci (Kohlmeyer_5520). k Ascospores (Kohlmeyer_5520) l–n Ascospores (Kohlmeyer_5520). o Ascospore (Kohlmeyer_5505). Scale bars:
d=100 μm, e=50μm, f, g, h, I, j, k=20μm, l, m, n, o=10μm
Juncus roemerianus (Jones et al. 2009; Suetrong et al. 2009;
Monkai et al. 2013). Kohlmeyer and Volkmann-Kohlmeyer
(1993) mentioned that the species often developed on culms
which were not regularly submerged in salt water.
Loratospora is similar to Leptosphaerulina (Didymellaceae),
Monascostroma (Didymellaceae) and Wettsteinina
Fungal Diversity (2014) 68:159–238
(Dothideomycetes genera incertae sedis), but Leptosphaerulina
and Monascostroma have smaller ascomata, lack periphyses,
and have a thin-walled peridium. Ascospores in
Leptosphaerulina are muriform and didymosporous in
Monascostroma (Kohlmeyer and Volkmann-Kohlmeyer 1993;
Jones et al. 2009). Loratospora forms large ascomata with
brown ostiolar periphyses, a thick-walled peridium at the apex
and phragmosporous, cylindrical ascospores (Kohlmeyer and
Volkmann-Kohlmeyer 1993; Jones et al. 2009; Suetrong et al.
2009). Wettsteinina differs from Loratospora in lacking ostiolar
periphyses, in having a thick-walled peridium of equal width
and ellipsoidal to broadly fusiform ascospores (Kohlmeyer and
Volkmann-Kohlmeyer 1993)
Loratospora was re-circumscribed by Jones et al. (2009)
and Monkai et al. (2013). The genus was accommodated in
Planistromellaceae by Barr (1996) due to its periphysate
ostiole (Jones et al. 2009; Suetrong et al. 2009; Monkai et al.
2013). Based on multigene phylogenetic analysis,
Loratospora was placed in Phaeosphaeriaceae (Schoch
et al. 2009; Zhang et al. 2012; Hyde et al. 2013).
In the multigene phylogenetic analyses (Fig. 2),
Loratospora forms a strongly supported clade with
Chaetosphaeronema, Dematiopleospora, Entodesmium,
Nodulosphaeria and Ophiobolus. However, the genus has a
differentiated centrum type as compared with other genera.
Loratospora lacks of pseudoparaphyses but has an internal
mucilaginous hamathecium, while most genera in
Phaeosphaeriaceae have pseudoparaphyses. It seem like the
centrum-type is not significant to distinguish genera at the
family level. There is only one species listed in Loratospora in
Index Fungorum (2014) and no asexual state is known. The
sequences data of Loratospora is limited to only one strain.
Neosetophoma Gruyter et al., in Gruyter et al. Mycologia
102(5): 1075 (2010), Faces of Fungi number: FoF00249.
Pathogenic on the grasses, Phlox paniculata L. and Urtica
dioica L., or associated with soil. Sexual state: Unknown.
Asexual state: Conidiomata pycnidial, scattered, solitary or
gregarious, superficial on agar, uniloculate, globose or irregular, setose, olivaceous to dark olivaceous, ostiole central,
with papilla or long neck. Conidiomata walls composed of
pseudoparenchymatous cell. Conidiophores reduced to
conidiogenous cells. Conidiogenous cells phialidic, discrete,
hyaline. Conidia ellipsoidal to cylindrical, attenuate at one
end, yellowish, aseptate or septate, not constricted at the
septum, smooth-walled, with guttules (from De Gruyter
et al. 2010; Quaedvlieg et al. 2013).
Type species: Neosetophoma samararum (Desm.) Gruyter
et al. [as ‘samarorum’], in De Gruyter et al. Mycologia 102(5):
1075 (2010).
= Phoma samararum Desm., Pl. Crypt. Nord France, Edn
1 7: no. 349 (1828)
Phylogenetic study: De Gruyter et al. (2010, 2012), Zhang
et al. (2012), Hyde et al. (2013), Quaedvlieg et al. (2013).
189
Notes: Neosetophoma was introduced by De Gruyter et al.
(2010) to accommodate N. samararum. Neosetophoma often
forms a single clade in Phaeosphaeriaceae. The genus has
been widely accepted in Phaeosphaeriaceae by various authors (De Gruyter et al. 2010, 2012; Zhang et al. 2012; Hyde
et al. 2013; Quaedvlieg et al. 2013).
Neostagonospora Quaedvlieg et al., Stud. Mycol. 75: 364
(2013), Faces of Fungi number: FoF00250.
Pathogenic on Carex acutiformis Ehrh and Elegia
cuspidate Mast., or soil borne. Sexual state: Unknown.
Asexual state: Conidiomata pycnidial, scattered, semiimmersed to superficial, uniloculate, globose, glabrous,
producing pale luteous to creamy conidial mass on host
surface. Conidiomata walls thin, composed of 2–3 layers
of pale brown cells, arranged in a textura angularis.
C o n i d i o p h o re s r e d u c e d t o c o n i d i o g e n o u s c e l l s .
Conidiogenous cells phialidic, integrated, ampulliform to
doliiform, hyaline, smooth-walled, lining the inner cavity,
with prominent periclinal thickening. Conidia narrow
fusoid-ellipsoidal to subcylindrical, apically subobtuse to
rounded, truncate at the base, hyaline, septate, initially nonconstricted at the septum, becoming constricted at the septa
when mature, smooth-walled, with granules (from
Quaedvlieg et al. 2013).
Type species: Neostagonospora caricis Quaedvlieg et al.,
Stud. Mycol. 75: 364 (2013).
Phylogenetic study: Quaedvlieg et al. (2013).
Notes: The asexual genus Neostagonospora was introduced by Quaedvlieg et al. (2013) to accommodate the
stagonospora-like species in Phaeosphaeriaceae. Two species
were placed in this genus; Neostagonospora caricis and Ne.
elegiae Quaedvlieg et al. with Ne. caricis being the type
species. Neostagonospora is similar to Stagonospora but differs in its conidiogenous cells. Neostagonospora has determinate phialidic conidiogenous cells, with prominent periclinal
thickening while Stagonospora has percurrent proliferation of
conidiogenous cells. Based on phylogenetic analysis,
Neostagonospora is related to Phaeosphaeriaceae, while the
type species of Stagonospora, St. paludosa clusters in
Massarinaceae (Quaedvlieg et al. 2013). In the phylogeny
in Fig. 2, Neostagonospora forms a sister clade with
Parastagonospora for which no sexual state is known.
Phaeosphaeria sensu lato taxa are polyphyletic and therefore,
it is likely that Neostagonospora may be an asexual state of
phaeosphaeria-like species.
Nodulosphaeria Rabenh., Klotzschii Herb. Viv. Mycol.,
Edn 2: no. 725 (in sched.) (1858), Faces of Fungi number:
FoF00251.
Saprobic or hemibiotrophic mostly on herbaceous dicotyledons. Sexual state: Ascomata scattered, solitary to gregarious, immersed to semi-immersed, or erumpent through host
epidermis at maturity, visible as black dots on host surface,
uniloculate, globose to subglobose, setose, covered by
190
hyphae, dark brown to black, ostiole central, papillate, with
broad setae in ostiolar canal, towards the apex. Peridium thinto thick-walled, of equal thickness, composed of two types of
brown to dark brown, pseudoparenchymatous cells, arranged
in a textura angularis to textura globulosa. Hamathecium
composed of numerous, filamentous, anastomosing, broad
cellular pseudoparaphyses, with distinct septa. Asci 8-spored,
bitunicate, fissitunicate, clavate to cylindric-clavate,
subsessile to short pedicellate, apically rounded with indistinct
ocular chamber. Ascospores overlapping 2–4-seriate,
phragmosporous, cylindrical or elongated fusiform, brown to
yellowish-brown, septate, with an enlarged cell near apex,
smooth-walled. Asexual state: Unknown.
Type species: Nodulosphaeria hirta
Phylogenetic study: this study.
Notes: Nodulosphaeria was introduced by Rabenhorst
(1858) to accommodate Dothideomycete species forming
phragmosporous, brown, septate ascospores with an enlarged
cell, and setose ascomata with broad setae in the papilla apex,
mostly found on herbaceous dicotyledonous especially
Asteraceae (Shoemaker 1984; Zhang et al. 2012).
Nodulosphaeria has been reported from various hosts and
may be host-specific with more than 60 species named, however it is lacking in molecular data (Shoemaker 1984). The
genus was previously treated as a synonym of Leptosphaeria,
but later reinstated by Holm (1957) as typified by N. hirta
(Clements and Shear 1931; Zhang et al. 2012).
Nodulosphaeria was treated in Phaeosphaeriaceae by Barr
(1979) based on its morphological characters which are similar to Ophiobolus as the ascospores form an enlarged cell(s).
The genera have often been confused and the identification of
species can be subjective (Zhang et al. 2012). Shoemaker
(1976) re-circumscribed the genus Nodulosphaeria and transferred various species to Ophiobolus. Later many species were
added to Nodulosphaeria based on morphology by various
authors, but no asexual morph is known (Shoemaker 1984;
Shoemaker and Babcock 1987; Zhang et al. 2012). There are
64 epithets listed under Nodulosphaeria and unfortunately no
sequences available for this genus in GenBank.
Multigene phylogenetic analyses (Figs. 1 and 2) indicate
that Nodulosphaeria belongs in Phaeosphaeriaceae. The genus clusters with Chaetosphaeronema, Dematiopleospora,
Entodesmium, Loratospora and Ophiobolus.
Nodulosphaeria hirta Rabenh., Klotzschii Herb. Viv.
Mycol., Edn 2: no. 725 (in sched.) (1858), Faces of Fungi
number: FoF00252, Fig. 12.
Saprobic on herbaceous dicotyledons. Sexual state:
Ascomata 230–380μm high (including papilla), 225–395μm
diam., scattered, solitary to gregarious, semi-immersed, or
erumpent through host epidermis at maturity, visible as black
dots on host surface, uniloculate, globose to subglobose,
setose, covered by hyphae, dark brown to black, ostiole central, papillate, with broad setae in ostiolar canal, towards the
Fungal Diversity (2014) 68:159–238
Fig. 12 Nodulosphaeria hirta (S-F70410, type). a Herbarium label and
specimen of Nodulosphaeria hirta. b Ascostromata on host surface. c
Section through ascostroma. d Section through peridium. e Asci with
cellular pseudoparaphyses. f–i Asci. j–n Ascospores. Scale bars: c=
100μm, d, e, f, g, h, i=20μm, j, k, l, m, n=10μm
apex. Peridium 21–44μm wide, thin, of equal thickness, composed of several layers of brown to dark brown, pseudoparenchymatous cells, outer layer comprising 1–2 layers of
brown to dark brown, thickened cells, arranged in textura
angularis to textura globulosa, inner layers comprised 2–3
layers of brown to dark brown, flattened cells, arranged in
textura angularis. Hamathecium composed of numerous, 3–
5μm wide, filamentous, broad cellular pseudoparaphyses,
with distinct septa, embedded in mucilaginous matrix, anastomosing at the apex. Asci (83–)90–110(−115)×(13.5–)15–
20 μm (x = 100 × 16.8 μm, n = 25), 8-spored, bitunicate,
fissitunicate, clavate to cylindric-clavate, subsessile or short
pedicellate, apically rounded with well-developed ocular
chamber. Ascospores 48–55 × 5–7(−7.5) μm (x = 51.2 ×
6.5μm, n=30), overlapping 3–4-seriate, phragmosporous, cylindrical or elongated fusiform, with narrow ends, brown to
yellowish-brown, 8-septate, slightly curved, smooth-walled,
enlarged at the forth cell from the apex. Asexual state:
Unknown.
Material examined: GERMANY, Sachsen, Dresdae, on
dead stems, May 1858, G.L. Rabenhorst (S-F70410, type).
Nodulosphaeria modesta (Desm.) Munk ex L. Holm, in
Holm, Symb. bot. upsal. 14(no. 3): 80 (1957), Faces of Fungi
number: FoF00253, Fig. 13.
≡ Sphaeria modesta Desm., Ann. Mag. nat. Hist., Ser. 1:
1786 (1840)
Saprobic on dead stems. Sexual state: Ascomata 130–
200μm high, 150–250μm diam., scattered, solitary to gregarious, immersed, erumpent to superficial, base not easy to
remove from the substrate, visible as small, black dots on
the host surface, uniloculate, coriaceous, globose to
subglobose, setose, covered by hyphae, dark brown to black,
ostiole central, with blunt brown hairs around the ostiole,
papillate. Peridium 7–10μm wide, thin-walled, of equal thickness, composed of two layers of pseudoparenchymatous cells,
outer layer comprising 2–3 cell layers of dark brown to black,
thickened cells, arranged in a textura angularis, inner layer
comprising 3–5 cell layers of thin-walled cells, hyaline, flattened cells, arranged in textura angularis to textura
prismatica. Hamathecium composed of numerous, 2–3μm
wide, filamentous, broad cellular pseudoparaphyses, with distinct septa, embedded in a mucilaginous matrix, anastomosing
at the apex. Asci 60–70×13–17μm (x= 67×15μm, n=20), 8spored, bitunicate, fissitunicate, cylindrical to cylindric-clavate, subsessile to short pedicellate, apically rounded, with
well-developed ocular chamber. Ascospores 29–40×5–6μm
(x = 35×6μm, n=40), partially overlapping 1–2 seriate,
Fungal Diversity (2014) 68:159–238
191
192
Fungal Diversity (2014) 68:159–238
Fungal Diversity (2014) 68:159–238
Nodulosphaeria modesta (MFLU 12-2214). a Ascomata on
host substrate. b Close up of ascoma. c−d Section of ascoma. e Close
up of the peridium. f Hamathecium of dense long cellular
pseudoparaphyses. g−j Asci with short, broad pedicel bearing 8 spores.
k−n Mature and immature ascospores. Scale bars: c=100μm, e=20μm,
d, f, g, h, i, j, k, l, m, n, o=10μm
Fig. 13
phragmosporous, cylindrical with slightly narrow ends, initially hyaline to subhyaline with small guttules, becoming
yellowish-brown to brown at maturity, 4-septate, slightly
curved, constricted at the septa, smooth-walled, with small,
globose appendages, without a refractive sphere near the
apices, enlarged at the second cell below the apex. Asexual
state: Unknown.
Material examined: ITALY, Forlì-Cesena, Montevescovo,
on dead stem, 8 February 2012, E. Camporesi (MFLU 140304), living culture=MFLUCC 11-0461=MUCL.
Notes: Based on the morphological comparison, our isolate
is similar to Nodulosphaeria modesta due to its small
ascomata covered by hairs and short, broad setae at the papilla
apex, the asci are bitunicate and clavate and the ascospores
are cylindrical, brown, 4-septate with narrow apices,
and an enlarged cell at the second cell below the apex.
The multigene phylogenetic analysis indicates that
Nodulosphaeria belongs to Phaeosphaeriaceae (Figs. 1
and 2).
Ophiobolus Riess, Hedwigia 1(6): 27 (1854), Faces of
Fungi number: FoF00254.
Saprobic or hemibiotrophic on various hosts. Ascomata
solitary to gregarious, scattered, semi-immersed to erumpent
though host tissue with short to long beak, uniloculate,
subglobose or ovoid or ampulliform, glabrous or covered by
hyphae, dark brown to black, ostiolate, papillate. Peridium
thick-walled, composed of dark brown to black,
scleroplectenchymatous cells, arrange in textura angularis to
textura globulosa. Hamathecium composed of numerous, filiform, cellular pseudoparaphyses, with distinct septa, anastomosing at the apex. Asci 8-spored, bitunicate, cylindrical to
cylindric-clavate, short pedicellate, apically rounded with indistinct ocular chamber. Ascospores fasciculate, 3–4-seriate,
scolecosporous, filiform or filamentous, with enlarged central
cells, yellowish-brown to brown, multi-septate, nonconstricted at the septa, separating into two part spores,
smooth-walled, with or without appendages.
Type species: Ophiobolus disseminans
Phylogenetic study: Dong et al. 1998; Ariyawansa et al.
(2014c)
Notes: Ophiobolus was introduced by Riess (1854) and
typified by O. disseminans. Ascomata were described as
discrete with distinct ostioles and ascospores as filiform and
multi-septate (Zhang et al. 2012). Ophiobolus has been found
on a wide range of hosts, mostly reported from Europe and
North America (Farr and Rossman 2014). Holm (1948) and
Müller (1952) used a broad concept of the genus Ophiobolus;
193
however, Holm (1957) treated Ophiobolus in a much
narrower sense, based on European collections (Shoemaker
1976). Three species were accepted by Holm (1957) and most
Ophiobolus species were transferred to Nodulosphaeria and
Leptospora (Holm 1957; Shoemaker 1976; Zhang et al.
2012). Shoemaker (1976) re-circumscribed species of
Ophiobolus from Canada and some North American
collections and accepted 31 species with two new species
and five new combinations. Walker (1980) provided various
illustrations of scolecosporous taxa from type material which
had previously been accommodated in Ophiobolus (Saccardo
1883; Zhang et al. 2012). Ophiobolus species were also transferred to Acanthophiobolus, Entodesmium,
Gaeumannomyces, Leptosphaeria and Leptospora
(Shoemaker 1976; Walker 1980; Zhang et al. 2012). Barr
(1979) initially accommodated Ophiobolus in
Phaeosphaeriaceae and later transferred it to
Leptosphaeriaceae (Barr 1987b). However, Zhang et al.
(2012) reinstated the genus in Phaeosphaeriaceae based on
morphological characters which are similar to
Nodulosphaeria and Ophiosphaerella. There are 357 epithets
listed in Ophiobolus in Index Fungorum (2014).
There is very little sequence data for Ophiobolus available
in GenBank with two sequences of O. fulgidus. Zhang et al.
(2012) mentioned that the genus should be placed in
Phaeosphaeriaceae based on morphology and the phylogenetic investigation of Dong et al. (1998). However, Dong et al.
(1998) could not resolve the placement of Ophiobolus as too
few strains were used in their molecular analysis. Thus the
genus needs to re-circumscribed using fresh collections
(Zhang et al. 2012).
The asexual state of Ophiobolus has been reported in
several genera such as coniothyrium-like, Rhabdospora,
phoma-like and Scolecosporiella (Shoemaker 1976;
Sivanesan 1984; Hyde et al. 2011; Wijayawardene et al.
2012; Zhang et al. 2012). However, these need confirmation
as Ophiobolus is probably polyphyletic.
In this study, two species of Ophiobolus are included in the
phylogenetic analysis. The detailed descriptions are provided
in Ariyawansa et al. (2014c) and a description of the generic
type is provided below. Based on multigene phylogenetic
analysis (Figs. 1 and 2), Ophiobolus clusters in
Phaeosphaeriaceae. However, there are limited sequences in
GenBank and the type species lacks molecular data to confirm
its natural placement. Thus Ophiobolus is tentatively placed in
Phaeosphariaceae until the generic type strain is sequenced to
confirm the natural placement (Table 2).
Ophiobolus disseminans Riess, Hedwigia 1(6): 27 (1854),
Faces of Fungi number: FoF00255, Figs. 14, and 15.
Saprobic on Cirsium (Asteraceae). Sexual state:
Ascomata 140–390μm high (excluding papilla), 160–340μm
diam., scattered or sometimes clustered, solitary to gregarious,
semi-immersed, or erumpent through host tissue, visible as
Not observed Not observed Dead wood
Brown
15
350–420
170–210×4–10
O. cirsii
142–170×4–5
Ascomata
(diam.)
Asci
Ascospores
Up to 15 septa Brown
Not observed 2
16–20
Hyaline to pale yellowish Absent
No
Hosts
Enlarge cells
Appendage
Ascospore color
Septation
Size (μm)
Species
Table 2 Synopsis of Ophiobolus species discussed in this study
O. disseminans (isotype) 150–160×2–3
170–190×10–12 160–340
O. erythrosporus
100–125×3–3.5 100–150×8–10 230–400
Source references
Ariyawansa et al. (2014c)
Fungal Diversity (2014) 68:159–238
Cirsium arvense
This study
Urtica brandnetel Ariyawansa et al. (2014c)
194
Fig. 14 Ophiobolus disseminans (BPI 629021, isotype). a Herbarium
label and specimen. b Ascomata on substrate. c Section through ascoma.
d Section through peridium. e Papilla. f Asci with cellular
pseudoparaphyses. g–i Ascus. j Ascospores in ascus. Note the swollen
part of the ascospores (arrowed). Scale bars: c=100μm, d, e, f, g, h, i, j=
20μm
slightly raised, small, black dots on the host surface,
uniloculate, subglobose to ovoid or ampulliform, glabrous,
dark brown to black, ostiole central, with periphyses, short
papillate. Necks 60–150μm high, 85–140μm diam, with
thick-walled cells, arranged in a textura angularis, subglobose
to oblong, dark brown to black, apically rounded or obtuse,
coriaceous. Peridium 30–50μm wide, thick-walled, of unequal thickness, slightly thick at the base, composed of several
layers of broadly scleroplectenchymatous cells, outer layers
consisting of several layers of brown to dark brown, thickened
cells, arranged in a textura angularis, inner layers comprising
several layers of hyaline, flattened cells, arranged in a textura
epidermoidea to textura porrecta. Hamathecium composed of
numerous, 2–3 μm wide, filamentous, broad cellular
pseudoparaphyses, with distinct septa, embedded in mucilaginous matrix, anastomosing at the apex. Asci (156–)170–
190(−203)×10–12(−13) μm (x = 178.9×11.4μm, n=20), 8spored, bitunicate, cylindrical to cylindric-clavate, short pedicellate, apically rounded with indistinct ocular chamber.
Ascospores (125–)150–160(−163) × 2–3 μm (x = 152.8 ×
2.9 μm, n = 15), fasciculate, in parallel or spiral,
scolecosporous, filiform or filamentous, with two enlarged
cells near the centre, but with 3–4 narrow cells in between
the enlarged cells, brown, multi-septate, with up to 15 septa,
not constricted at the septa, smooth-walled, separating into
two part spores in the centre of the spores between the enlarged cells. Asexual state: Unknown.
Material examined: ITALY, Cassellas Vicinity, on dead
stem of Cirsium arvense, 1853, Riess 1823 (BPI 629021,
isotype); ibid on dead stem of Cirsium arvense, 1853, H.
Riess, Hedwigia 1(6): Tab IV, (Fig. 8, iconotype) (1854).
Ophiosphaerella Speg., Anal. Mus. nac. B. Aires, Ser. 3
12: 401 (1909), Faces of Fungi number: FoF00256.
Pathogenic or saprobic mostly on various monocotyledons
and some flowering shrubs or dicotyledons especially
Poaceae, Asteraceae and Fagaceae (Farr and Rossman
2014). Sexual state: Ascomata scattered, solitary, semi-immersed, or erumpent through host tissue with papilla visible as
raised, small, black dots on host surface, uniloculate, globose
to subglobose, glabrous, dark brown to black, ostiole central,
with periphyses, papillate. Peridium thick-walled, composed
of hyaline to brown or dark brown, pseudoparenchymatous
cells, arranged in a textura angularis. Hamathecium composed of numerous, filamentous, broad cellular
pseudoparaphyses, with distinct septa, embedded in mucilaginous matrix, anastomosing at the apex. Asci 8-spored,
bitunicate, cylindrical to cylindric-clavate, short pedicellate,
Fungal Diversity (2014) 68:159–238
195
196
Fungal Diversity (2014) 68:159–238
Fig. 15 Ophiobolus
disseminans (iconotype) redrawn
from Riess (1854). a
Section through ascoma. b Ascus
and pseudoparaphyses. c
Ascospores
apically rounded with indistinct ocular chamber. Ascospores
fasciculate, lying parallel or spiral, scolecosporous, filiform or
filamentous, pale brown to brown, multi-septate, not constricted at the septum, smooth-walled. Asexual state: see under
Scolecosporiella.
Type species: Ophiosphaerella graminicola
Phylogenetic study: Wetzel et al. (1999), Câmara et al.
(2000), Hsiang et al. (2003), Schoch et al. (2006, 2009),
Zhang et al. (2009, 2012), Hyde et al. (2013).
Notes: Ophiosphaerella was introduced by Spegazzini
(1909) as typified by Op. graminicola. Most species of
Ophiosphaerella are often found as pathogens or saprobes
worldwide on Poaceae and Cyperaceae (Câmara et al.
2000). Spegazzini (1909) did not introduce the genus separately but described and illustrated a new species, and later the
genus was validly published by Stafleu et al. (1972) (Walker
1980; Zhang et al. 2012). However, Petrak and Sydow (1936)
treated Ophiosphaerella graminicola as a synonym of
Ophiobolus graminicolus (Speg.) after observing the type
specimens which was accepted by Ainsworth et al. (1971)
and von Arx and Müller (1975) (Walker 1980; Zhang et al.
2012). Walker (1980) examined the type specimens of
Ophiosphaerella and confirmed that the genus belongs to
Pleosporales, but differs from Ophiobolus. Ophiosphaerella
is most similar to Ophiobolus and subsequently often confused in morphological characters. However Ophiosphaerella
differs from Ophiobolus by the lack of central swollen ascospore cells which do not separate into part spores (Zhang et al.
2012).
The phylogenetic relationships of Ophiosphaerella were
first investigated by Wetzel et al. (1999) who treated
Ophiosphaerella as monophyletic genus distinguished from
Fungal Diversity (2014) 68:159–238
Phaeosphaeria and other pleosporaceous genera. Various
authors subsequently accepted the genus in
Phaeosphaeriaceae based on the multigene phylogenetic investigation with Ophiosphaerella forming a monophyletic
clade as a sister group of Phaeosphaeria (Schoch et al.
2006, 2009; Zhang et al. 2009, 2012; Hyde et al. 2013).
However, the phylogenetic analysis was limited to one strain
(Ophiosphaerella herpotricha CBS 620.86).
In the present multigene phylogenetic analyses, two strains
of Ophiosphaerella agrostidis (MFLUCC 11-0152 and
MFLUCC 12-0007) and Op. herpotricha (CBS 620.86) are
included. The phylogenetic relationships show that Op.
agrostidis (MFLUCC 11-0152 and MFLUCC 12-0007) forms
a distinct clade separated from Op. herpotricha (CBS 620.86)
in Phaeosphaeriaceae. Thus Ophiosphaerella seem to be
polyphyletic genus. However, there are few sequences available in GenBank, thus fresh collections and molecular data are
needed to for more natural understanding.
Ophiosphaerella graminicola Speg., Anal. Mus. nac. B.
Aires, Ser. 3 12: 401 (1909), Faces of Fungi number:
FoF00257, Fig. 16, and 17.
Pathogenic or saprobic on monocotyledons. Sexual state:
Ascomata 230–300μm high, 170–230μm diam., scattered,
solitary, immersed to semi immersed or erumpent through
host tissue with minute papilla, visible as raised, small black
dots on host surface, uniloculate, globose to subglobose,
glabrous, dark brown to black, ostiole central, with
periphyses, with minute papilla. Peridium 20–40μm wide,
thick-walled, of unequal thickness, broad at the apex towards
sides of ascoma, composed of several layers of pseudoparenchymatous cells, outer layers comprising several layers of
brown to dark brown thickened cells at sides and apex, arranged in a textura angularis, hyaline at the base of ascoma,
inner layers comprising several layers of thin-walled, flattened, hyaline cells of textura prismatica. Hamathecium composed of numerous, 2–3μm wide, filamentous, broadly cellular pseudoparaphyses, with distinct septa, embedded in a
mucilaginous matrix, anastomosing at the apex. Asci
(128–)133–150(−160) × 9–12(−12.5) μm (x = 148.7 ×
11.2μm, n=20), 8-spored, bitunicate, cylindrical to cylindric-clavate, short pedicellate, apically rounded with indistinct
ocular chamber. Ascospores (118–)130–150(−160)×3–3.5μm
(x= 142.4×3.2μm, n=30), fasciculate, lying parallel or spiral
in the centre, scolecosporous, filiform or filamentous,
narrowing towards the ends, pale brown to brown, 15–18septate, not constricted at the septa, smooth-walled. Asexual
state: Unknown.
Material examined: ARGENTINA, in garden near
Tucumán, on leaf sheath of Leptochloa virgata (L.) P.
Beauv. (Poaceae), April 1906, C. Spegazzini (iconotype);
VENEZUELA, Edo, Aragua, Parque Nacional Henri Pittier,
on the Maracay-Ocumare Rd., ca. 15 km north of Maracay,
4.5 km south of Rancho Grande Biological Station where
197
creek crosses road, alt. 950 m. ca. 10°21′N 67°41″W, on grass
culm, 5 December 1990, G.J. Samuels, B. Hein, S.M.
Huhndorf (BPI 748267).
Ophiosphaerella agrostidis Dern. et al. [as ‘agrostis’], in
Câmara et al., Mycologia 92(2): 320 (2000), Faces of Fungi
number: FoF00258, Fig. 18.
Pathogenic or saprobic on monocotyledonous hosts.
Sexual state: Ascomata 275–355μm high (including papilla),
175–310μm diam., scattered, solitary, semi immersed or
erumpent through host tissue with papilla, visible as raised,
small black dots on host surface, uniloculate, globose to
subglobose, glabrous, dark brown to black, ostiole central,
oblique, papilla, carbonaceous. Peridium 15–25μm wide,
thin-walled, of equal thickness, composed of several layers
of brown to dark brown, pseudoparenchymatous cells, arranged in a textura angularis to textura globulosa.
Hamathecium composed of numerous, 1.5–2.5μm wide, filamentous, broad cellular pseudoparaphyses, with distinct septa,
embedded in mucilaginous matrix, anastomosing at the apex.
Asci (97–)100–135×7–9(−11) μm (x= 111.5×8.5μm, n=25),
8-spored, bitunicate, fissitunicate, cylindrical to cylindric-clavate, short pedicellate, apically rounded, with a welldeveloped ocular chamber. Ascospores (90–)98–120(−130)×
2–2.5μm (x = 110.3× 2.3μm, n=30), fasciculate, parallel or
spiral, scolecosporous, filiform, narrowing towards ends, pale
brown to brown, 15-septate, not constricted at the septa,
smooth-walled. Asexual state: Unknown.
Material examined: THAILAND, Phrae, Rongkwang
District, Maejo University Phrae Campus, on dead culms of
grass, 20 August 2010, R. Phookamsak (MFLU 11-0188),
living culture = MFLUCC 11-0152; Chiang Rai, Muang
District, Ta Sai, on dead culm of grass, 30 June 2011, R.
Phookamsak (MFLU 11-0246), living culture=MFLUCC
12-0007.
Notes: The scolecosporous specimens were collected from
dead culms of grass in Thailand. These collections are morphologically similar to Ophiosphaerella agrostidis, Op.
graminicola, and Op. herpotricha with these species sharing
similar ascomata, asci and ascospores, including septation of
ascospores. The Thailand collections are most similar to Op.
agrostidis according to the size of the ascomata, asci and
ascospores, and also the septation of ascospores. However,
Op. agrostidis has been reported as a pathogen on grass while
the collections in the present study were saprobes. Therefore
these collections are named as Op. agrostidis based on the
morphological characters and these can be treated as authentic
specimens until epitypification. The phylogenetic tree (Figs. 1
and 2) shows that two isolates of Op. agrostidis form a single
clade in Phaeosphaeriaceae (Table 3).
Paraphoma Morgan-Jones & J.F. White, Mycotaxon
18(1): 58 (1983), Faces of Fungi number: FoF00259.
Saprobic on various hosts, or soil borne. Mycelium abundance branched, septate, subhyaline to pale brown, smooth-
198
walled. Sexual state: Unknown. Asexual state: Conidiomata
pycnidial, scattered, solitary to gregarious, in agar semi-
Fungal Diversity (2014) 68:159–238
immersed to superficial, uniloculate, globose to subglobose,
setose, brown to dark brown, ostiole central, circular.
Fungal Diversity (2014) 68:159–238
Ophiosphaerella graminicola (BPI 748267). a Herbarium label
and specimens of Ophiosphaerella graminicola. b Ascomata on host
surface. c Section through ascoma d Section through peridium. e
Papilla with periphyses. f Pseudoparaphyses stained in Meltzer’s
reagent. g Ascus. h–j Asci stained in Meltzer’s reagent. k–l
Ascospores. m–o Ascospores stained in Meltzer’s reagent. Scale bars:
c=100μm, e=50μm, d, f, g, h, i, j, k, l, m, n, o=20μm
Fig. 16
Conidiomata walls thick, outer layers comprising 2 layers of
scleroplectenchymatous cells, dark brown, inner layers comprising 4–5 layers of pseudoparenchymatous cells, arranged in
a textura angularis, subhyaline to pale brown. Setae numerous,
thick-walled, straight to slightly curved, acuminate, septate,
smooth to verruculose. Conidiophores reduced to
conidiogenous cells. Conidiogenous cells monophialidic, discrete, determined, lageniform, hyaline to subhyaline, lining the
inner cavity. Conidia enteroblastic, amerosporous, ellipsoidal,
hyaline, aseptate, smooth-walled, with guttules (from Sutton
1980; De Gruyter et al. 2009, 2010; Quaedvlieg et al. 2013).
Fig. 17 Ophiosphaerella
graminicola (iconotype) redrawn
from Spegazzini (1909). a
Ascoma. b Ascomata immersed
on host tissue. c Asci. d
Ascospore
199
Type species: Paraphoma radicina (McAlpine) MorganJones & J.F. White, Mycotaxon 18(1): 60 (1983)
≡ Pyrenochaeta radicina McAlpine, Fungus Diseases of
stone-fruit trees in Australia: 127 (1902)
Phylogenetic study: De Gruyter et al. (2009, 2010, 2012),
Aveskamp et al. (2010), Zhang et al. (2012), Hyde et al.
(2013), Quaedvlieg et al. (2013).
Notes: Paraphoma as typified by P. radicina was previously treated in Pyrenochaeta by McAlpine (1902) and later,
Boerema and Dorenbosch (1979) transferred the species to
Phoma. Morgan-Jones and White (1983) introduced a new
genus, Paraphoma to accommodate the species that produced
heavily setose pycnidia and transferred P. radicina to this
genus. However, the genus was treated as a section of
Phoma (Boerema 1997) until De Gruyter et al. (2010) reinstated the genus and placed it in Phaeosphaeriaceae based on
phylogenetic evidence. Recently, four species are accommodated in this genus for which no sexual state is known.
200
Fungal Diversity (2014) 68:159–238
Fig. 18 Ophiosphaerella agrostidis (MFLU 11-0188). a Ascomata on host surface. b Section through ascoma c Section through peridium. d Cellular
pseudoparaphyses stained in congo red. e–i Asci. j–n Ascospores. Scale bars: b=100μm, c–n=20μm
Fungal Diversity (2014) 68:159–238
201
Table 3 Synopsis of Ophiosphaerella species discussed in this study
Species
Size (μm)
Septation
Hosts
Source references
Câmara et al. (2000),
Farr and Rossman
(2014)
This study
Ascospores
Asci
Ascomata
(diam.)
Op. agrostidis
75–150×2–2.5
100–230×10–15
130–350
6–15
Agrostis and
Cynodon×dactylon
Op. agrostidis
(MFLUCC11-0152)
Op. graminicola
(holotype)
Op. graminicola
(BPI748267)
Op. herpotricha
98–130×2–2.5
98–130×7–9(−11)
175–310
15
Grass culm
140×3
150×10
180–200
12–20
Leptochloa virgata
142.4×3.2
148.7×11.2
170–230
15–18
grass culm
140–180×2–2.5(−3)
150–190×7–9
300–400
12–16
Op. korrae
120–180×4–5(−5.5)
145–200×10–13(−15)
300–500
(3–6)7(−15)
Arrhenatherum, Bromus,
Buchloe, Cynodon,
Dactylis, Puccinellia,
Secale, Triticum,
Vetiveria, Zoysia
Axonopus, Cynodon,
Poa, Zoysia
Parastagonospora Stud. Mycol. 75: 362 (2013), Faces of
Fungi number: FoF00260.
Pathogenic on various cereal crops (Poaceae). Sexual
state: Ascomata scattered, solitary to gregarious, immersed,
uniloculate, globose, glabrous, brown to black, ostiole central,
with papilla. Peridium thick-walled, composed of 3–6 layers
of brown pseudoparenchymatous cells, arranged in a textura
angularis. Hamathecium composed of numerous, filiform,
cellular pseudoparaphyses, with distinct septa. Asci 8-spored,
bitunicate, cylindrical to clavate, short pedicellate. Ascospores
phragmosporous, fusiform, subhyaline to pale brown, septate
(−3 septa), constricted at the septa, swollen at penultimate cell.
Asexual state: Conidiomata pycnidial, scattered, immersed to
semi-immersed, uniloculate, subglobose, glabrous, black, exuding creamy conidial mass, ostiole central. Conidiomata
walls thin, composed of 2–3 layers of brown cells, arranged
in textura angularis. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells phialidic, integrate, ampulliform to
subcylindrical, hyaline, smooth-walled, lining the inner cavity, with percurrent proliferation near apex. Conidia
phragmosporous, cylindrical, apically obtuse with truncate
base, hyaline, septate, thin and smooth-walled, with granules
or multiguttules (from Quaedvlieg et al. 2013).
Type species: Parastagonospora nodorum (Berk.)
Quaedvlieg et al. Stud. Mycol. 75: 363 (2013)
≡ Depazea nodorum Berk., Gard. Chron., London: 601
(1845)
Phylogenetic study: Quaedvlieg et al. (2013)
Notes: Parastagonospora was introduced by Quaedvlieg
et al. (2013) to accommodate stagonospora-like species which
have been reported as asexual state of phaeosphaeria-like taxa.
The genus accommodated five species; Pa. avenae (A.B..
Spegazzini (1909),
Walker (1980)
Farr and Rossman
(2014)
Farr and Rossman
(2014)
Walker (1980)
Farr and Rossman
(2014)
Frank) Quaedvlieg et al., Pa. caricis Quaedvlieg et al., Pa.
nodorum (Berk.) Quaedvlieg et al., Pa. poae Quaedvlieg et al.
and Pa. poagena Crous & Quaedvlieg with Pa. nodorum as
the type (Index Fungorum, 2014). Parastagonospora is similar to Stagonospora; however, they differ in the morphology
of the conidiogenous cells (Quaedvlieg et al. 2013). Based on
multigene phylogenetic analysis, Parastagonospora clusters
in Phaeosphaeriaceae which forms a clade with
Phaeosphaeria avenaria (synonymized under
Parastagonospora avenae), Ph. eustoma and Ph. nigrans.
These Phaeosphaeria species may be the sexual states of
Parastagonospora.
Phaeosphaeria I. Miyake, Bot. Mag., Tokyo 23: 93
(1909), Faces of Fungi number: FoF00233.
= Phaeoseptoria Speg., Revta Mus. La Plata 15: 39. 1908.
Saprobic or pathogenic mostly on monocotyledons.
Sexual state: Ascomata solitary to gregarious, immersed,
visible as slightly raised, small, black dots on the host surface,
uniloculate, globose to subglobose, glabrous, brown, ostiole
central, with minute papilla. Peridium thin-walled, of equal
thickness, composed of flattened, brown, pseudoparenchymatous cells, arranged in textura angularis. Hamathecium composed of sparse, filiform, broad cellular pseudoparaphyses,
with distinct septa, slightly constricted at the septa, rarely
anastomosing at the apex. Asci 8-spored, bitunicate,
fissitunicate, broadly cylindrical, short pedicellate or
subsessile, apically rounded, with an indistinct ocular chamber. Ascospores overlapping 2–3-seriate, phragmosporous,
narrowly fusiform, pale brown to brown or yellowish-brown,
septate, straight or slightly curved, constricted or not constricted at the septa, walls smooth or rough, echinulate or
verruculose, with or without mucilaginous sheaths. Asexual
202
state: Conidiomata stromatic, pycnidial, scattered to gregarious, immersed, uni- to multi-loculate, globose to subglobose,
brown. Conidiomata walls thin, composed of thin-walled, of
brown pseudoparenchymatous cells, arranged in textura
angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells holoblastic, phialidic, flattened
ampulliform to doliiform, hyaline to pale brown, hardly distinguishable from inner cells walls of conidioma. Conidia
phragmosporous, oblong to cylindrical, pale brown to brown,
septate, straight or slightly curved with obtuse at the base,
smooth-walled with guttules.
Type species: Phaeosphaeria oryzae
Phylogenetic study: Câmara et al. (2002); Schoch et al.
(2006, 2009); Zhang et al. (2009, 2012); De Gruyter et al.
(2010, 2012); Quaedvlieg et al. (2013); Hyde et al. (2013,
2014); Wijayawardene et al. (2014b)
Notes: Phaeosphaeria was established by Miyake (1909).
Miyake (1910) accommodated Phaeosphaeria in
Mycosphaerellaceae and mentioned that the genus differs from
Sphaerulina and Leptosphaeria in ascospore colour and lack
of pseudoparaphyses (Eriksson 1967). Phaeosphaeria was
considered as a synonym of Leptosphaeria for a long time
(Müller 1950; Munk 1957; Zhang et al. 2009, 2012). The
genus was however, reinstated by Holm (1957) who found
pseudoparaphyses in Phaeosphaeria oryzae and 17 mostly
graminicolous species were transferred to Phaeosphaeria
(Eriksson 1967; Zhang et al. 2009). Barr (1979) established
the new family Phaeosphaeriaceae and designated
Phaeosphaeria as the generic type and later, Eriksson (1981)
introduced a broad generic concept for Phaeosphaeria which
included relatively small ascomata, dictyospores, as well as
ascospores with several wall layers, and an occurrence on
monocotyledons (Câmara et al. 2002; Zhang et al. 2012).
Subsequent authors also included Phaeosphaeria species from
dicotyledonous hosts (Dennis 1978; Sivanesan 1984; von Arx
and Müller 1975; Eriksson 1967; Hedjaroude 1969;
Shoemaker and Babcock 1989b; Zhang et al. 2012).
Shoemaker and Babcock (1989b) re-circumscribed
Phaeosphaeria and divided the genus into six subgenera based
on the differences in ascospore shape and septation viz.
Fusispora, Ovispora, Phaeosphaeria, Sicispora, Spathispora
and Vagispora. Various authors subsequently indicated that
Phaeosphaeria was heterogeneous and shared several characters with Leptosphaeria. Phaeosphaeria however, differs from
Leptosphaeria in morphology and these genera have been
distinguished in different families by phylogenetic analysis
(Câmara et al. 2002; Schoch et al. 2009; Zhang et al. 2009,
2012; Hyde et al. 2013). Presently, there are 200 epithets for
Phaeosphaeria in Index Fungorum (2014) with 18,983 nucleotide sequences available in GenBank. However, several species of Leptosphaeria sensu stricto and Phaeosphaeria are
confused in having similar morphology and lack phylogenetic
investigation.
Fungal Diversity (2014) 68:159–238
The asexual states of Phaeosphaeria have been reported as
coelomycetes and some as hyphomycetes namely
hendersonia-like, Mauginiella, Microsphaeropsis,
Neostagonospora, Parastagonospora, Phaeoseptoria,
Scolecosporiella and stagonospora-like (Leuchtmann 1984;
Shoemaker and Babcock 1989b; Câmara et al. 2002;
Abdullah et al. 2005; Kirk et al. 2008; Hyde et al. 2011,
2013; Wijayawardene et al. 2012; Zhang et al. 2012;
Quaedvlieg et al. 2013). However, Leuchtmann (1984) treated
the asexual state of Phaeosphaeria as species of
Stagonospora and mentioned that the asexual state of
Phaeosphaeria often formed pycnidial conidiomata, possessed holoblastic conidiogenous cells and had elongated to
filiform, hyaline to pale brown, multiseptate conidia, which
was also mentioned by Câmara et al. (2002). Câmara et al.
(2002) suggested that Phaeosphaeria shares common ancestors with Leptosphaeria and that multigene phylogenetic analysis was necessary to understand the boundaries of taxa. The
peridium type, asexual state and host preferences can distinguish fungal taxa in these two genera (Câmara et al. 2002)
Quaedvlieg et al. (2013) studied Septoria, Stagonospora
and related genera such as Phaeosphaeria and Phaeoseptoria
using molecular analysis and concluded that Stagonospora
(based on the type species, S. paludosa) belongs to
Massarinaceae. They introduced two new genera
(Neostagonospora and Parastagonospora) to accommodate
stagonospora-like genera in Phaeosphaeriaceae (Quaedvlieg
et al. 2013). Additionally, Phaeosphaeria was linked to the
asexual state Phaeoseptoria based on the phylogenetic analysis with the type species of Phaeosphaeria, Ph. oryzae
forming a well-supported clade with Phaeoseptoria papayae,
the type species of Phaeoseptoria (Quaedvlieg et al. 2013).
Thus Quaedvlieg et al. (2013) synonymized the earlier name
Phaeoseptoria under Phaeosphaeria as the latter was wellstudied and taxonomy less confused than Phaeoseptoria
which have been confused with several septoria-like in
pigmented conidia (Walker et al. 1992). Hendersonia, which
was treated as a synonym of Stagonospora, and
Microsphaeropsis were placed in Didymellaceae (Sutton
1977; Swart and Walker 1988; Kirk et al. 2008; De Gruyter
et al. 2009; Aveskamp et al. 2010). Mauginiella was treated as
an asexual state of Phaeosphaeria by Abdullah et al. (2005);
however, this has not been confirmed by phylogenetic investigation. In this study Mauginiella could not be resolved in
Phaeosphaeriaceae. The genus is currently placed in asexual
Pezizomycotina (Kirk et al. 2008). Therefore we exclude
Mauginiella from Phaeosphaeriaceae. Other asexual genera
of Phaeosphaeria still lack phylogenetic investigation.
Therefore we accept three asexual genera (Neostagonospora
Quaedvlieg et al., Parastagonospora Quaedvlieg et al., and
Phaeoseptoria Speg.) for Phaeosphaeria sensu lato.
Phaeosphaeria oryzae was designated as typified of
Phaeosphaeria by Miyake (1909). However, Miyake (1909)
Fungal Diversity (2014) 68:159–238
did not mention the detail of the type specimen in his
publication and this type has not been found in any
herbarium in Japan. Eriksson (1967) translated the protologue
and found Miyake’s specimen in Sydow’s herbarium as labeled “Leptosphaeria oryzae Hori=Phaeosphaeria oryzae
Miy. — on Oryza sativa L. — Prov. Susuya Shizuoka —
1907.09”. He found that most characters of this specimen
match with the diagnosis except the presence of
pseudoparaphyses. Thus Eriksson (1967) designated
Sydow’s specimen as a lectotype of Phaeosphaeria oryzae.
However, the mucilaginous sheath or appendages were not
seen in Eriksson’s (1967) observation (Shoemaker and
Babcock 1989b). Shoemaker and Babcock (1989b) carried
out a monograph of Phaeosphaeria with Phaeosphaeria
oryzae treated in subgenus Phaeosphaeria. The species description included echinulate ascospores; however Miyake
(1909, 1910) and Eriksson (1967) did not mention this character. Quaedvlieg et al. (2013) epitypified Phaeosphaeria
oryzae and Phaeoseptoria papayae, the type species of
Phaeosphaeria and Phaeoseptoria and indicated that
Phaeoseptoria is the asexual state of Phaeosphaeria based
on phylogenies.
In the present study the lectotype of Phaeosphaeria oryzae
was examined and the morphological characters compared
with the diagnosis of Miyake (1910). On examination it
appears that Phaeosphaeria oryzae lectotype has smoothwalled ascospores, but this was not mentioned by Miyake
(1910) either. In addition, the asci and ascospores size in the
lectotype are larger than Miyake’s diagnosis (1910) (see
Table 4). Quaedvlieg et al. (2013) epitypified Phaeosphaeria
oryzae and described the ascospores as echinulate following
the description of Shoemaker and Babcock (1989b). Further
specimens that have been determined to be Phaeosphaeria
oryzae from BPI have been examined in the present study and
some specimens have echinulate ascospores, while others do
not. It appears that Phaeosphaeria oryzae may be a species
complex which has been epitypified by a specimen that is
probably a different species to the lectotype.
Based on our multigene phylogenetic analysis,
Phaeosphaeria species separated in several subclades in
Phaeosphaeriaceae. Several Phaeosphaeria sensu stricto
specimens collected from various hosts in Thailand formed a
strongly supported clade with the type species, Phaeosphaeria
oryzae and also Ph. papayae and Ph. musae. These
Phaeosphaeria (sensu stricto) species differ morphologically
(see Table 4), but the phylogenies indicate that they are closely
related species. We therefore analyzed the phylogenetic relationships among species, with Phaeosphaeria sensu stricto
strains forming a distinct clade with high bootstrap support. A
pair wise comparison of ITS and TEF1 helped to significantly
differentiate the cryptic species (ITS pair wise comparison see
Fig. 4). Currently, many plant pathogens causing serious
disease of economic crops are reported as the species
203
complexes (Wikee et al. 2011; Cannon et al. 2012;
Manamgoda et al. 2012; Udayanga et al. 2012; Weir et al.
2012) which seem to be the case in Phaeosphaeria.
Phaeosphaeria sensu stricto species are morphologically similar, but differ in the size of ascomata, asci, and ascospores,
habitat and host occurrence. The combined gene phylogenetic
analysis can distinguish taxa of Phaeosphaeria sensu stricto at
the species level.
The Phaeosphaeria sensu stricto taxa collected from various monocotyledons in Thailand are introduced as two novel
species and Phaeosphaeria musae is reported on other hosts
from Thailand with descriptions and illustrations below.
Phaeosphaeria oryzae I. Miyake, Bot. Mag., Tokyo 23: 93
(1909), Faces of Fungi number: FoF00234, Fig. 19.
= Phaeoseptoria oryzae I. Miyake (1910).
Saprobic on leaves of Oryza sativa. Ascomata 70–130μm
high, 90–150μm diam., solitary, sometimes clustered, immersed, visible as slightly raised, small, black dots on the host
surface, uniloculate, globose to subglobose, glabrous, brown
to dark brown, ostiole central, with minute papilla. Peridium
5–10μm wide, of equal thickness, composed of 2–3 layers of
thin-walled, brown to dark brown, flattened pseudoparenchymatous cells, arranged in textura angularis. Hamathecium
composed of sparse, 2.5–4μm wide, filiform, broad cellular
pseudoparaphyses, distinctly constricted at the septa, rarely
anastomosing at the apex. Asci (50–)55–70(−80) × 10–
13.5(−15) μm (x= 65.4×11.9μm, n=25), 8-spored, bitunicate,
fissitunicate, broadly cylindrical, short pedicellate or
subsessile, apically rounded with indistinct ocular chamber.
Ascospores (22–)25–27(−29)×5–6μm (x = 26×5.2μm, n=
30), overlapping 2-seriate, phragmosporous, narrowly fusiform, brown, mostly 3-septate, rarely 1–2 septa, indistinctly
constricted at the septa, slightly curved, smooth-walled.
Asexual state: Phaeoseptoria.
Material examined: JAPAN, Shizuoka, Suruya, on Oryza
sativa L. (Poaceae), September 1907 (S-F9572, lectotype); EL
SALVADOR, intercepted Washington Dc #26812, on Oryza
sativa, 10 March 1952, F.P. Hubert (BPI 622541); JAPAN,
intercepted San Diego California #4872, on Oryza sativa L.,
27 December 1957, E.B. Francis (BPI 622542); JAPAN,
intercepted San Francisco California #17349, 17352, 17367,
on Oryza sativa, 13 December 1940, F.J. Phelan (BPI 622544);
NICARAGUA, Monagua, on living leaves of Oryza sativa, 4
November 1954, C. Pineda 37, (BPI 622545); THAILAND,
Chiang Mai Province, Mae Wang District, Mae Sapok Royal
Project, on dead branches of Etlingera sp. (Zingiberaceae), 5
October 2010, R. Phookamsak RP0086 (MFLU 11-0206),
living culture=MFLUCC 11-0170.
Phaeosphaeria chiangraina Phookamsak & K.D. Hyde,
sp. nov., Index Fungorum number: IF550736; Faces of Fungi
number: FoF00261, Fig. 20.
Etymology: Referring to Province in Thailand, in which
the fungus was found.
Thysanolaena maxima
Not constricted
Present
Echinulate
(41.5–)43–50(−57)×7–9μm
70–100×100–130μm
(15–)17–19(−20)×3–4μm
Etlingera sp.
Not constricted
Slightly constrict Oryza sativa
Undetected
Present
Echinulate
Smooth
(22–)25–27(−29)×5–6μm
(50–)55–70(−80)×10–13.5(−15) μm
(36–)43–57(−62)×(7–)8–10(−11) μm 13–15(−17)×3–4μm
90–140×130–200μm
70–130×90–150μm
P. oryzae (collection in
Thailand)
Ph. thysanolaenicola
Oryza sativa
Slightly curved
Present
Verruculose
30–55×7–9μm
Up to 150μm diam.
Ph. oryzae (epitype;
Quaedvlieg et al. 2013)
P. oryzae (lectotype)
(15–)17–20(−23)×4–5μm
Cordyline sp.
Not constricted
Present
Musa sp.
Not mentioned Not mentioned Slightly constrict Oryza sativa
Verruculose
90–125×70–125μm
P. oryzae (Miyake 1910)
16–18×3–4μm
40–50 (−53)×9–10(−13) μm
35–55×7–9μm
P. musae (MFLUCC 11-0151) 70–105×85–130μm
16–23×4–5μm
Present
Verruculose
25–30(−33.5)×5–7.5μm
P. musae (MFLUCC 11-0133) 110–140.5×120–160μm (58.5–)65–70(−76)×13–15(−17) μm
Present
Not mentioned Not constricted
Verruculose
(13.5–)15–17(−18)×3.5–4.5μm Smooth
(44–)47–60(−65)×8–9(−10) μm
38–60×7–8μm
120–180×130–180μm
Up to 130μm diam.
P. chiangraina
P. musae (CBS 120026; type)
Ascospore (l/w)
Asci (l/w)
Ascomata
(high×diam.)
15–)17–19(−21)×(3.5–)4μm
Host
Constricted
at the septum
Ascospore
sheath
Ascospore
walls
Size
Species name
Table 4 Synopsis of Phaeosphaeria discussed in this study
Slightly constrict Calathea sp.
Fungal Diversity (2014) 68:159–238
Slightly constrict Oryza sativa
204
Holotypus: MFLU 12-2472
Saprobic on leaves of Oryza sativa. Sexual state:
Ascomata 120–180μm high, 130–180 μm diam., scattered,
immersed, visible as slightly raised, small, black dots on the
host surface, uniloculate, globose to subglobose or irregular in
shape, glabrous, brown to dark brown, ostiole central with
minute papilla. Peridium 7–16μm wide, thin-walled, of equal
thickness, composed of 1–3 layers of flattened, brown to dark
brown, elongated, pseudoparenchymatous cells, arranged in
textura angularis. Hamathecium composed of numerous, 1.5–
3μm wide, filiform, broad cellular pseudoparaphyses, with
small guttules, indistinctly constricted at the septa, embedded
in mucilaginous matrix, rarely anastomosing at the apex. Asci
(44–)47–60(−65)×8–9(−10) μm (x= 52.6×8.9μm, n=25), 8spored, bitunicate, fissitunicate, broadly cylindrical, short pedicellate or subsessile, apically rounded with ocular chamber.
Ascospores (13.5–)15–17(−18) × 3.5–4.5 μm (x = 16.4 ×
4.1μm, n=30), overlapping 2-seriate, phragmosporous, fusiform with obtuse ends, pale brown when young, becoming
yellowish-brown to brown at maturity, dark brown when
stained in 5 % of KOH, 3-septate, not constricted at the septa,
slightly curved, smooth-walled with small to large guttules in
each cell, surrounded by a distinct mucilaginous sheath.
Asexual state: produced on media agar after 8 weeks.
Conidiomata 100–305μm high, 120–290μm diam., pycnidial, scattered to clustered, immersed, with dark brown to black
stromatic tissues embedded in the media agar, uni- to multiloculate, globose to irregular, ostioles not observed, brown to
dark brown. Conidiomata walls 13–35μm wide, composed of
several layers of brown, pseudoparenchymatous cells, arranged in a textura angularis, covered by vegetative hyphae.
C o n i d i o p h o re s r e d u c e d t o c o n i d i o g e n o u s c e l l s .
Conidiogenous cells (2–)3–6×(2–)4–7μm (x = 4.4×4.3μm,
n=20), holoblastic, phialidic, ampulliform or flattened, hyaline to pale brown, difficult to distinguish from the pycnidial
wall. Conidia (15–)17–21.5(−26)×2–3μm (x = 19.4×2.5μm,
n=30), solitary, cylindrical, pale brown to brown, 1–3-septate,
slightly curved, obtuse at the apex, truncate at the base, not
constricted at the septa, smooth-walled with guttules.
Culture characters: Colonies on PDA 77–80 mm diam.
after 4 weeks at 25–30 °C, white to pale yellowish at the edge,
pale yellowish to grey in the centre, forming different colour
sectors of grey to dark grey; reverse pale yellowish at the
edges, becoming yellowish-brown to brown at the centre,
slightly radiating outwardly, forming dark sectors; medium
dense, forming black stromatic tissues immersed in media
after 8 weeks, circular to irregular, flattened to slightly raised,
dull with entire edge, floccose to fairly fluffy, slightly radiating at the lower part, not pigmented.
Material examined: THAILAND, Chiang Rai Province,
Muang District, Nanglae Village, on dead leaves of Oryza sativa,
20 January 2013, R. Phookamsak RP0131 (MFLU 12-2472,
holotype), ex-type living culture=MFLUCC 13-0231=MUCL.
Fungal Diversity (2014) 68:159–238
Fig. 19 Phaeosphaeria oryzae (S-F9572, lectotype) a Herbarium label
and specimens. b Ascomata on host surface. c Section through ascoma.
d Section through peridium. e Asci with sparse pseudoparaphyses. f–i
205
Asci. j–o Ascospores. Scale bars: c=50μm, e, f, g, h, i, j=20μm, d, k,
l, m, n, o=10μm
206
Fungal Diversity (2014) 68:159–238
Fig. 20 Phaeosphaeria chiangraina (MFLU 12-2472, holotype). a
Ascomata of Phaeosphaeria oryzae on host surface. b Ascomata visualized under compound microscope. c Section through ascoma. d
Section through peridium. e Asci with rare pseudoparaphyses. f, i Asci.
g, h Asci stained in 5 % KOH. j- o Ascospores stained in 5 % of KOH. m,
n Ascospores. p Ascospore germination on WA. q Section through
conidioma. r Section through conidioma wall. s–u Conidiogenous cells.
v–z Conidia. Scale bars: q=100μm, b, c=50μm, d, r=20μm, e, f, g, h, i,
p=10μm, j, k, l, m, n, o, s, t, u, v, w, x, y, z=5μm
Notes: Phaeosphaeria chiangraina was collected on Oryza
in Thailand. This is the same host of the generic type of
Phaeosphaeria, P. oryzae. A morphological comparison
based on species described in Shoemaker and Babcock
Fungal Diversity (2014) 68:159–238
(1989b) shows that Ph. chiangraina is similar to
Phaeosphaeria avenaria, Ph. eustoma, Ph. oryzae and Ph.
tritici. Phaeosphaeria chiangraina differs from Ph. oryzae in
the size of ascomata, asci and ascospores. Phaeosphaeria
chiangraina has smaller ascospores (13.5–18×3.5–4.5μm)
than Ph. oryzae (15–23×4–5μm). Phaeosphaeria tritici has
similar sized ascospores to Ph. chiangraina; however, Ph.
tritici has a larger asci and smaller ascomata. Additionally,
Phaeosphaeria tritici ascospores are enlarged at the second
cell and slightly constricted at the first septa and produce a
phoma-like asexual state, as while Ph. chiangraina lacks an
enlarged cell, is not constricted at the septa and forms a
septoria-like asexual state.
Multigene phylogenetic analysis using MP shows that
Phaeosphaeria chiangraina can be distinguished from
Phaeosphaeria avenaria and Ph. eustoma, and forms a
strongly supported clade with Ph. thysanolaenicola and Ph.
oryzae (CBS 110110) (Fig. 3). However, Ph. chiangraina
morphologically differs from Ph. thysanolaenicola and can
be separated from the epitype of Ph. oryzae due to its smoothwalled ascospores with a distinct sheath and based on phylogenetic evidence (Fig 3).
Phaeosphaeria musae Sawada, Special Publication
College of Agriculture, National Taiwan University 8: 66
(1959) Faces of Fungi number: FoF00262, Fig. 21.
Pathogen on Asparagaceae and Marantaceae. Sexual
state: Ascomata 110–140.5μm high, 120–160μm diam., solitary, scattered, immersed, visible as slightly raised, small
black dots on host surface, uniloculate, brown to dark brown,
globose to subglobose, central ostiole with minute papilla.
Peridium 7–24μm wide, thin-walled, of unequal thickness,
slightly thick at the apex, composed of 1–3 layers of brown to
dark brown, pseudoparenchymatous cells multi-layered and
elongated, at the apex, arranged in textura angularis.
Hamathecium composed of numerous, 1.5–3μm wide, filiform, broad cellular pseudoparaphyses, with distinct septa,
slightly constricted at the basal septa, embedded in gelatinous
matrix, rarely anastomosing at the apex. Asci (40–)65–
70(−76)×(9–)13–15(−17) μm (x = 69×14.2μm, n=25), 8spored, bitunicate, fissitunicate, broadly cylindric-clavate to
clavate, subsessile, with acute ends, apically rounded with
indistinct ocular chamber. Ascospores (16–)25–30(−33.5)×
5–7.5μm (x = 27.6×5.8μm, n=30), overlapping 2–3-seriate,
phragmosporous, fusiform, yellowish-brown to brown, becoming dark brown when stained in 5 % KOH, 3-septate,
slightly constricted at the central septa, enlarged at the second
cell, slightly curved, rarely straight, rough-walled, echinulate,
surrounded by narrow mucilaginous sheath. Asexual state:
Unknown.
Culture characters: Colonies on MEA 25–27 mm diam.
after 4 weeks at 25–30 °C, white yellowish or grey in the
centre and edges; reverse yellowish-brown to greyish-yellow
or olive brown, with rare tufting, radiating with dark brown
207
colouration separating the margin from the centre; medium
dense, irregular, flattened to slightly raised, dull with undulate
edge, floccose or velvety, forming black stromatic tissues,
embedded in agar after 8 weeks, agar tinted with yellowishbrown pigmentation.
Material examined: THAILAND, Pha Yao Province,
Mae Jai District, Sri Don Kaew Village, on living leaves
of Calathea sp. (Marantaceae), 19 August 2010, R.
Phookamsak RP0049 (MFLU 11-0169), living culture=
MFLUCC 11-0133; THAILAND, Chiang Rai Province,
Muang District, Pakha village, on living leaves of
Cordyline sp. (Asparagaceae), 15August 2010, S. Wikee
(RP0067), MFLU11-0187, living culture = MFLUCC
11-0151.
Notes: Phaeosphaeria species (MFLUCC 11-0133 and
MFLUCC 11-0151) were isolated from necrotic leaf spots
symptoms on Calathea sp. and Cordyline sp. from Thailand.
These two collections have similar morphological characters
with Phaeosphaeria musae and Ph. panici (P. Syd.)
Shoemaker & C.E. Babc. However they differ from
Phaeosphaeria panici in having larger ascomata and asci
and being associated with a different host. Phaeosphaeria
panici lacks molecular data to confirm a natural placement,
while these isolates form a strongly-supported clade (70 %
MP) with Ph. musae in the Phaeosphaeria sensu stricto clade.
Based on the ITS and TEF1 pair wise comparisons and
multigene phylogenetic evidence, it appears that these isolates
are conspecific with Phaeosphaeria musae. Thus, they are
identified as Phaeosphaeria musae, and the species is reported
associated with leaf spot disease on Calathea sp. and
Cordyline sp. from Thailand. Pathogenicity was not
confirmed.
Phaeosphaeria thysanolaenicola Phookamsak & K.D.
Hyde, sp. nov., Index Fungorum number: IF550735; Faces
of Fungi number: FoF00263, Fig. 22.
Etymology: Referring to the host on which the fungus was
found.
Holotypus: MFLU 11-0157
Pathogen associated with Paraphaeosphaeria on leaves of
Thysanolaena maxima. Sexual state: Ascomata 70–100μm
high, 100–130μm diam., scattered or sometimes clustered,
immersed, visible as raised, black dots on the host surface,
uni- to bi-loculate, subglobose, brown to dark brown, ostiole
central, with minute papilla. Peridium 5–10μm wide, thinwalled, of equal thickness, composed of 1–3 layers of brown
to dark brown, pseudoparenchymatous cells, arranged in
textura angularis. Hamathecium composed of numerous, 2–
5μm wide, filiform, broad cellular pseudoparaphyses, with
distinct septa, slightly constricted at the septa, embedded in
a gelatinous matrix, rarely anastomosing at the apex. Asci
(41.5–)43–50(−57)×7–9μm (x = 49.3×8.4μm, n=25), 8spored, bitunicate, fissitunicate, broadly cylindrical or cylindric-clavate, sessile to subsessile, apically rounded with ocular
208
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Fig. 21 Phaeosphaeria musae. (MFLU 11-0169). a Ascomata on host surface. b Section through ascoma. c Section through peridium. d
Pseudoparaphyses. e–h Asci. i–m Ascospores. Note sheath in m. Scale bars: b=50μm, c, d, e, f, g, h, = 20μm, i, j, k, l, m=10μm
chamber. Ascospores (15–)17–19(−20)×3–4μm (x = 17.8×
3.8μm, n=30), overlapping 1–3-seriate, phragmosporous,
narrowly fusiform, with obtuse ends, yellowish-brown to
brown, 3-septate, rarely 1–2-septate, slightly constrict at the
central septum, straight to curved, rough-walled, echinulate,
surrounded by mucilaginous sheath. Asexual state:
Unknown.
Culture characters: Colonies on PDA 33–35 mm diam.
after 4 weeks at 25–30 °C, white to pale yellowish-brown at
the edge, white with grey sectors in the centre; reverse white to
yellowish at the edges, becoming orange brown to grey at the
centre with orange radiations separating the edges from the
centre; medium dense, circular to irregular, flattened to raised,
or umbonate, rough with entire to slightly undulate edge,
floccose to velvety or cottony, radiating in the lower part,
not producing pigments.
Material examined: THAILAND, Chiang Rai Province,
Phan District, Pukang Waterfall, on living leaves of
Thysanolaena maxima Kuntze (Poaceae), 22 May 2010, R.
Phookamsak (RP0036) (MFLU 11-0157, holotype), ex-type
living culture=MFLUCC 10-0563=MUCL.
Notes: Phaeosphaeria thysanolaenicola is most similar to
Ph. oryzae as they share a similar ascoma, asci and ascospore
size range. However, they differ in habitat and host preferences, as Ph. thysanolaenicola is associated with other fungi
on leaf spots of Thysanolaena maxima. Whereas Ph. oryzae
was found as a saprobe on Oryzae sativa. The ITS pair wise
comparison shows that they differ in eight base positions.
Phylogenetic analysis performed with a combination of ITS,
LSU, RPB2 and TEF1 genes shows that Ph. thysanolaenicola
forms a clade with Ph. chiangraina. Phaeosphaeria
thysanolaenicola differs from Ph. chiangraina in its smaller
asci and ascospores, habitat, host occurrence and ascospore
ornamentation. Phaeosphaeria thysanolaenicola has
echinulate ascospores while Ph. chiangraina has smoothwalled ascospores.
Fungal Diversity (2014) 68:159–238
209
Fig. 22 Phaeosphaeria thysanolaenicola (MFLU 11-0157, holotype). a Ascomata on host surface. b Section through ascoma. c Section through
peridium. d Cellular pseudoparaphyses. e–h Asci. i–l Ascospores. Scale bars: b=20μm, c, e, f, g, h, = 10μm, d, i, j, k, l=5μm
Phaeosphaeriopsis M.P.S. Câmara et al., in Câmara et al.,
Mycol. Res. 107(5): 519 (2003), Faces of Fungi number:
FoF00264.
Saprobic or pathogenic on various monocotyledons.
Sexual state: Ascomata scattered to clustered, immersed,
visible as small, black spots on host surface, uni- to biloculate, globose to subglobose, glabrous, brown, ostiole central, penetrating through host surface. Peridium thin-walled,
of equal thickness, composed of brown to dark brown, pseudoparenchymatous cells of textura angularis. Hamathecium
composed of numerous, filiform, frequently anastomosing,
broad cellular pseudoparaphyses, with distinct septa and constricted at the septa. Asci 8-spored, bitunicate, fissitunicate,
broadly cylindrical to cylindric-clavate, subsessile to short
pedicellate, apically rounded, with indistinct ocular chamber.
Ascospores overlapping 1–3-seriate, phragmosporous, oblong
to cylindrical, often with one enlarged cell, yellowish-brown
to brown or reddish-brown, 3–5-transeptate, slightly curved,
not constricted at the septa, walls smooth or rough, echinulate
or verruculose, surrounded by mucilaginous sheath. Asexual
state: see under Phaeostagonospora.
Type species: Phaeosphaeriopsis glaucopunctata
Phylogenetic study: Câmara et al. (2003); Schoch et al.
(2009); Zhang et al. (2012); Quaedvlieg et al. (2013); Hyde
et al. (2013), Thambugala et al. (2014).
Notes: Phaeosphaeriopsis was introduced by Câmara et al.
(2003) and typified by Ps. glaucopunctata to accommodate non
congeneric species of Paraphaeosphaeria. Phaeosphaeriopsis
210
agavensis (A.W. Ramaley et al.) Câmara et al., Ps. amblyspora
A.W. Ramaley, Ps. glaucopunctata (Grev.) Câmara et al., Ps.
nolinae (A.W. Ramaley) Câmara et al., and Ps. obtusispora
(Speg.) Câmara et al. were introduced in the genus based
on morphological characters and phylogenetic analyses of
Phaeosphaeriopsis glaucopunctata (CBS 653.86) (Câmara
et al. 2003; Zhang et al. 2012; Thambugala et al. 2014).
Farr et al. (2006) transferred Sphaeria phacidiomorpha to
Phaeosphaeriopsis phacidiomorpha based on the type morphological characters and microsphaeropsis-like asexual state
which was most similar to Phaeosphaeriopsis. However,
Sphaeria phacidiomorpha differs from other
Phaeosphaeriopsis species by its hyaline ascospores (Farr
et al. 2006; Thambugala et al. 2014). Phaeosphaeriopsis
phacidiomorpha is currently synonymized under the name
Glomerella phacidiomorpha (Ces.) Petr. (Index Fungorum
2014; Thambugala et al. 2014).
Phaeosphaeriopsis musae was introduced and
accommodated in Phaeosphaeriaceae by Arzanlou and
Crous (2006) and is a pathogen causing leaf spots on banana.
Subsequent phylogenetic analysis indicated that Ps. musae
clusters with Phaeosphaeria oryzae and separate to
Phaeosphaeriopsis glaucopunctata (Zhang et al. 2012; Hyde
et al. 2013; Phookamsak et al. 2013, 2014). Thus,
Thambugala et al. (2014) synonymized Phaeosphaeriopsis
musae under the older name Phaeosphaeria musae Sawada
(1959) based on morphological characters and phylogenetic
evidence. Additionally, Thambugala et al. (2014) epitypified
Phaeosphaeriopsis glaucopunctata and described the new
species Phaeosphaeriopsis triseptata K.M. Thambugala &
K.D. Hyde with sexual and asexual morphs. Six species are
listed in Index Fungorum (2014) and 59 sequences are available in GenBank. Molecular analysis confirms the placement
of Phaeosphaeriopsis in Phaeosphaeriaceae (Zhang et al.
2012; Hyde et al. 2013; Quaedvlieg et al. 2013; Thambugala
et al. 2014; Wijayawardene et al. 2014b).
A collection of Phaeosphaeriopsis was made which causes
leaf spots on leaves of Dracaena lourieri Gagnep in Thailand.
Based on morphological characters and multigene phylogenetic analysis, a new species, Phaeosphaeriopsis
dracaenicola, is introduced to accommodate this taxon in
the present paper.
Phaeosphaeriopsis glaucopunctata (Grev.) M.P.S.
Câmara et al. [as ‘glauco-punctata’], in Câmara et al.,
Mycol. Res. 107(5): 519 (2003), Faces of Fungi number:
FoF00265, Fig. 23.
≡ Cryptosphaeria glaucopunctata Grev., Fl. Edin.: 1-478
(1824)
Saprobic on Ruscus aculeatus (Asparagaceae). Sexual
state: Ascomata 110–145 μm high, 130–220 μm diam,
scattered, solitary, immersed, visible as small, brown spots
surrounded by pale yellowish region, uniloculate, subglobose,
glabrous, with central black ostiole penetrating through host
Fungal Diversity (2014) 68:159–238
surface. Peridium 7–18μm wide, thin-walled, of unequal
thickness, composed of 3–4 layers of thickened, brown, pseudoparenchymatous cells, arranged in a textura angularis.
Hamathecium composed of sparse, 1–3μm wide, filiform,
frequently anastomosing, broad cellular pseudoparaphyses,
with distinct septa, constricted at the septa. Asci (55–)60–
75(−76)×(11–)12–14(−15) μm (x = 68.2×13.4μm, n=20),
bitunicate, 8-spored, broadly cylindrical to cylindric-clavate,
subsessile to short pedicellate, apically rounded with indistinct
ocular chamber. Ascospores 18–20(−22) × (3–)4–5.5 μm
(x = 20 × 4.8 μm, n = 20), overlapping 1–3-seriate,
phragmosporous, cylindrical, narrower and longer at the lower
cell, brown to dark brown, 4-septate, often enlarged at the
forth cell, rough-walled, echinulate, surrounded by mucilaginous sheath. Asexual state: Conidiomata pycnidial, scattered,
solitary, immersed to superficial (in agar), uniloculate, globose, glabrous, brown to black, ostiolate, with black droplets.
Conidiomata walls thin, comprising 2–3 layers of yellowishbrown to brown, pseudoparenchymatous cells, arranged in
textura angularis. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells holoblastic, phialidic, annellidic,
with a short collarette, ampulliform to subcylindrical, hyaline,
lining the inner cavity of conidioma. Conidia amerosporous,
cylindrical to oblong, with rounded ends, hyaline to yellow,
becoming yellowish-brown at maturity, aseptate, smooth to
finely verruculose, accumulating in a huge bluish-black slimy
mass at the tip of ostiole (from Thambugala et al. 2014).
Material examined: UK, near Edinburgh, Slateford, on
dead leaves of Ruscus aculeatus L. (Asparagaceae), 15
August 1824, R.K. Greville (E 00074283, syntype).
Phaeosphaeriopsis dracaenicola Phookamsak & K.D.
Hyde, sp. nov., Index Fungorum number: IF550737; Faces
of Fungi number: FoF00266, Fig. 24.
Etymology: referring to the host, of which the fungus was
found.
Holotypus: MFLU 11-0193
Pathogenic causing necrotic leaf spot on Dracaena
lourieri; lesions 3–6 cm, infecting mostly on leaf margin,
oval-shaped, pale brown to yellowish-brown, separated from
healthy tissue by a reddish-brown to orange-brown margin.
Sexual state: Ascomata 88.5–170μm high, 140–200μm
diam., solitary to gregarious, immersed, visible as slightly
raised, small black spots on host surface, subglobose, brown
to dark brown, ostiole central. Peridium 5–17.5μm wide, thinwalled, of equal thickness, composed of 3–4 layers of dark
brown, pseudoparenchymatous cells, arranged in textura
angularis, outer layer comprising 2–3 layers of thick-walled
cells, inner layers comprising 1–2 layers of thin-walled hyaline cells. Hamathecium composed of numerous, 1.5–4μm
wide, frequently septate, frequently anastomosing, branching,
broad cellular pseudoparaphyses, embedded in mucilaginous
matrix. Asci 62–78×9–12μm (x = 71.5×10.8μm, n=25), 8spored, bitunicate, fissitunicate, cylindrical to cylindric-
Fungal Diversity (2014) 68:159–238
211
Fig. 23 Phaeosphaeriopsis glaucopunctata (E00074283, syntype). a
Herbarium label and specimens of Phaeosphaeriopsis glaucopunctata. b
Ascomata on host surface. c Section through ascomata d Section through
peridium. e Asci with pseudoparaphyses. f Cellular pseudoparaphyses. g
Ascus. h–i Asci stained by KOH reagent. j–o Ascospores. Scale bars: c=
100μm, d–i=20μm, j–o=5μm
clavate, short pedicelate, apically rounded, with welldeveloped ocular chamber. Ascospores 16–19×(3.5–)4–5μm
(x = 17.4 × 4.5 μm, n = 30), overlapping 2–3-seriate,
phragmosporous, oblong to cylindrical, initially yellowish
becoming brown to reddish-brown, 4–5 septate, usually widest in the third cell, narrower at the lowest cell, smooth-walled,
guttulate, surrounded by thick mucilaginous sheath. Asexual
state: forming on bamboo pieces on water agar (WA) after
8 weeks. Conidiomata 42–135.5μm high, 50–140μm diam.,
pycnidial, solitary, superficial on bamboo pieces, or semiimmersed on agar, visible as black slimy or shiny spots on
surface, globose to subglobose or cup-shaped when sectioned
through conidiomata, centrally ostiolate. Conidiomata walls
5–12μm wide, composed of 3–4 layers of dark brown cells,
arranged in textura angularis, outer layers comprising 2–3
layers of thick-walled cells, brown to dark brown, paler at the
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Fungal Diversity (2014) 68:159–238
Phaeosphaeriopsis dracaenicola (MFLU11-0193, holotype).
on living leaves of Dracaena lourieri. a Leaf lesion on host. b Ascomata
visible on host surface. c Section through ascoma. d Section through
peridium. e Asci with pseudoparaphyses. f–i Asci. j Ascospores stained in
Indian ink. k–n Ascospores. o Conidiomata forming on bamboo pieces
on water agar. p Pycnidia. q Section through pycnidium. r
Section through pycnidial wall. s–u Conidiogenous cells. v Conidia. w–
ab Conidia. Scale bars: c=100μm, p, q=50μm, d, e, f, g, h, i=20μm, j, k,
l, m, n, r, s, v=10μm, t, u, w, x, y, z, aa, ab=2μm
Fig. 24
base, inner layer comprising 2–3 layers of thin-walled cells,
hyaline. Conidiophores simple, rarely branched, doliiform to
cylindrical or ampulliform, septate, hyaline, mostly reduced to
conidiogenous cells. Conidiogenous cells 4–12×3–4μm, holoblastic, phialidic, single, discrete, sometimes integrated,
ampulliform or cylindric-clavate, hyaline, arising from basal
stratum. Conidia 3–4.5×3–4.5μm (x = 3.9×3.6μm, n=30),
amerosporous, globose to subglobose, initially hyaline, becoming brown to dark brown, aseptate, smooth-walled.
Culture characters: Colonies on malt extract agar (MEA)
34–34.5 mm diam. after 20 days at 25–30 °C, white to cream
at the margins, pale yellowish to yellowish-brown in the
middle and pale brown to brown or orange-brown at the
centre, with small white to grey droplets; reverse white to
cream at the margins, brown to orange-brown in the middle
and pale yellowish to yellowish at the centre; medium dense,
irregular, flattened to slightly raised, with rough surface, undulate edge with entire to slightly radiating margins, floccose
to fairly fluffy, no pigment produced in agar.
Material examined: THAILAND, Chiang Rai Province,
Muang District, Nang Lae Village, on living leaves of
Dracaena lourieri Gagnep (Asparagaceae), 21 September
2010, S. Wikee, RP0073 (MFLU11-0193, holotype), extype living culture = MFLUCC 11-0157 = MUCL; ibid.
Chiang Mai Province, Mae Wang District, Doi Inthanon,
Royal Project, on living Dracaena loureiri, 16 November
2010, R. Phookamsak, RP0109 (MFLU 11-0229, paratype),
ex-paratype living culture=MFLUCC 11-0193=MUCL.
Notes: Phaeosphaeriopsis dracaenicola is typical of
Phaeosphaeriopsis, due to the asexual state, habitat and host
preferences and it shares similar morphological characters to
Ps. agavensis, Ps. nolinae, and Ps. obtusispora in its brown,
5-septate ascospores. However, these can be differentiated by
size of ascomata, asci and ascospores. Phaeosphaeriopsis
dracaenicola has smaller ascospores, asci and ascomata than
the other species in the genus, and ascospores are smoothwalled, while the other species have rough-walled, echinulate
or punctuate ascospore ornamentation. In addition,
Phaeosphaeriopsis dracaenicola was found associated with
lesions on leaves of Dracaena, while the other species are
saprobic on Agave and Nolina (Ramaley 1997; Câmara et al.
2001, 2003; Thambugala et al. 2014). Pathogenicity was not
confirmed. Phaeosphaeriopsis dracaenicola formed an
213
asexual state similar to Ps. agavensis and Ps. obtusispora,
but differed from Ps. nolinae as conidia are globose.
Multigene phylogenetic analysis shows that Ps. dracaenicola
formed a robust clade (100 % ML/ 100 % MP/ 1.00 PP) at the
basal of Phaeosphaeriopsis species in Phaeosphaeriaceae.
Phaeostagonospora A.W. Ramaley, Mycotaxon 61: 351
(1997), Faces of Fungi number: FoF00267.
Saprobic on Nolina erumpens (Torr.) S. Wats. Sexual
state: reported as Phaeosphaeriopsis. Asexual state:
Conidiomata pycnidial, scattered, solitary, immersed or subepidermal, uniloculate, elongated to globose, flattened at the
apex against the host epidermis, with small papilla penetrating
the host epidermis. Conidiomata walls thick, composed of 3–
6 layers of brown-walled cells, with 1–2 hyaline interior
layers, abundant light brown hyphae from walls associated
with host substrate. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells holoblastic, discrete, doliiform,
ampulliform or irregular in shape, hyaline, smooth-walled,
lining inner cavity of conidiomata. Macroconidia
phragmosporous, ellipsoidal to cylindrical, with rounded
ends, brown, 1–3-septate, rough-walled, foveolate.
Microconidia globose or ellipsoidal, hyaline, smooth-walled,
forming on the conidiomatal wall near the ostiole (from
Ramaley 1997).
Type species: Phaeostagonospora nolinae A.W. Ramaley,
Mycotaxon 61: 351 (1997).
Phylogenetic study: None
Notes: When Câmara et al. (2003) introduced the genus
Phaeosphaeriopsis; they also mentioned the asexual state of
this genus as Phaeostagonospora. This was based on cooccurrence on the host (Ramaley 1997; Câmara et al. 2001).
The sexual and asexual connection was, however, not
equivocally confirmed. Thambugala et al. (2014) epitypified
Phaeosphaeriopsis glaucopunctata and described the asexual
state from cultures. The asexual state of P. glaucopunctata
differs from Phaeostagonospora nolinae as conidia are
aseptate, smaller, and verruculose, while Phaeostagonospora
nolinae has septate conidia and it produces larger
microconidia (Ramaley 1997; Thambugala et al. 2014).
Therefore the link between Phaeostagonospora and
Phaeosphaeriopsis requires confirmation.
Sclerostagonospora Höhn., Hedwigia 59: 252 (1917),
Faces of Fungi number: FoF00268.
Pathogenic or saprobic on various monocotyledons and
dicotyledons. Sexual state: phaeosphaeria-like. Asexual
state: Conidiomata pycnidial, scattered, solitary, immersed,
uniloculate, globose, glabrous, dark brown to black, ostiole
central, with papilla. Conidiomata walls thin, composed of
thick-walled cells, arranged in textura angularis, dark brown,
inner layers lined with a hyaline cells bearing conidiogenous
cells. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells holoblastic, discrete, determinate,
ampulliform to irregular, hyaline, smooth-walled, lining inner
214
cavity of conidiomata. Conidia phragmosporous, cylindrical
to tapered slightly to the base, obtuse at the apex, with truncate
base, pale brown, septate, slightly constricted at the septa, thin
and rough-walled, verruculose (from Quaedvlieg et al. 2013).
Type species: Sclerostagonospora heraclei (Sacc.) Höhn.,
Hedwigia 59: 252. 1917.
Phylogenetic study: Crous et al. (2008), Quaedvlieg et al.
(2013).
Notes: Sclerostagonospora was introduced by Höhnel
(1917) and typified by S. heraclei (Sacc.) Höhn. The genus
is similar to Stagonospora but differs in having pigmented
conidia (Sutton 1980; Quaedvlieg et al. 2013). Crous et al.
(2008) included Sclerostagonospora species in their phylogenetic analysis and Sclerostagonospora form a clade with other
Phaeosphaeria species. Quaedvlieg et al. (2013) introduced a
new species, S. phragmiticola from Phragmites australis
(Poaceae) and confirmed that Sclerostagonospora is asexual
genus belongs to Phaeosphaeriaceae based on their phylogenetic investigation. Quaedvlieg et al. (2013) mentioned that
the sexual state of this genus is phaeosphaeria-like.
In this study, two species of Sclerostagonospora form a
distinct clade in our multigene phylogenetic analyses (Fig. 2).
Sclerostagonospora phragmiticola (CBS 338.86) groups with
Phaeosphaeria phragmiticola (CBS 459.84) in clade E and
other genera in Phaeosphaeriaceae with weak bootstrap support. Whereas Sclerostagonospora cycadis (CBS 123538)
clusters with Parastagonospora in clade H (Fig. 2).
However, Sclerostagonospora is not represented by their type
species. This genus needs better populating as it is presently
not well-resolved.
Scolecosporiella Petr., Annls mycol. 19(1/2): 30 (1921),
Faces of Fungi number: FoF00269.
Saprobic or pathogenic on various host plants. Sexual
state: reported as Ophiosphaerella and Phaeosphaeria.
Asexual state: Conidiomata stromatic, pycnidial,
amphigenous, scattered to gregarious, immersed to subepidermal, uniloculate, glabrous, depressed-globose to globose or
ovoid, pale brown to brown, ostiole central, circular, nonpapillate, with dark tendrils of conidia extruding through
ostiole. Conidiomata walls thin, composed of thin-walled,
subhyaline to pale brown cells, arranged in textura angularis.
Conidiophores reduced to conidiogenous cells. Conidiogenous
cells holoblastic, annellidic, discrete, ampulliform, globose or
irregular, hyaline, smooth-walled. Conidia phragmosporous,
fusiform, with acute apex and a truncate base, subhyaline to
pale brown, multi-septate, constricted at the septa, thick and
smooth-walled, apical cell attenuated into a short, beak-like,
appendage (from Nag Raj 1989).
Type species: Scolecosporiella typhae (Oudem.) Petr.,
Annls mycol. 19(1/2): 31 (1921).
≡ Hendersonia typhae Oudem., Ned. kruidk. Archf, 2 sér.
1: 255 (1873)
Phylogenetic study: None
Fungal Diversity (2014) 68:159–238
Notes: Scolecosporiella was introduced by Petrak (1921)
with S. typhae (Oudemans) Petr. as the type species. The
genus was treated by Sutton (1968, 1980) and Sutton and
Alcorn (1974) with five species being accommodated. Nag
Raj (1989) re-examined the type species of Scolecosporiella,
S. typhae and described the morphological characters in detail.
Nag Raj (1989) distinguished Urohendersoniella
mastigospora Petr. from Scolecosporiella typhae and reinstated the genus Urohendersoniella as this monospecific genus
had been synonymized as Scolecosporiella mastigospora
(Petr.) B. Sutton in Sutton (1980). Additionally, a new genus
Orphanocoela was established to accommodate noncongeneric species of Scolecosporiella (Nag Raj 1989). Six
species are listed in Index Fungorum (2014).
Scolecosporiella has been reported as the asexual state of
Ophiosphaerella herpotricha (Farr et al. 1989; Câmara et al.
2000; Zhang et al. 2012). However, there are no phylogenic
evidence to confirm the connection between the sexual and
asexual state, thus the generic connection is still questionable.
Scolicosporium Lib. ex Roum., Fungi Selecti Galliaei
Exs.: no. 676 (1880)
Type species: Scolicosporium fagi Lib. ex Roum., in
Roumeguère, Revue mycol., Toulouse 2: 22, 676 (1880)
Phylogenetic study: Wijayawardene et al. (2013a)
Notes: Scolicosporium Lib. ex Roum. was introduced by
Roumeguère (1880) and typified by S. fagi Lib. ex Roum.
Sutton (1980) treated Scolicosporium fagi, the type species of
Scolicosporium as a synonym of S. macrosporium (Berk.) B.
Sutton and designated S. macrosporium as the type species of
Scolicosporium. However, Scolicosporium fagi is currently
reported as the type species in Index Fungorum (2014).
Scolicosporium was treated as a hyphomycete by Spooner
and Kirk (1982) and Seifert et al. (2011). However,
Treigiene and Mel’nik (2002) introduced S. minkeviciusii
Treigiene as coelomycete, while Wijayawardene et al.
(2013a) confirmed the species as a coelomycete.
Furthermore, Wijayawardene et al. (2013a) showed that
S. minkeviciusii belongs to Phaeosphaeriaceae,
Pleosporales, in their molecular analyses. However, the genus
was not represented by the type species, hence further collections of the type species of Scolicosporium, S. fagi are essential to confirm the familial placement of Scolicosporium sensu
stricto. Below we only discuss S. minkeviciusii.
Scolicosporium minkeviciusii Treigiene., in Treigiene.&
Mel’nik, Mikol. Fitopatol. 36(6): 45 (2002), Faces of Fungi
number: FoF00270.
Saprobic on bark of Quercus pubescens Willd. and
Q. robur L. Sexual state: Unknown. Asexual state:
Conidiomata 100–120μm high, 120–180μm diam., pycnidial, solitary to gregarious, uniloculate, elongate-globose, dark
brown. Ostiole central, sometimes towards one side, papillate
when young, opening longitudinally at maturity. Conidiomata
walls comprising 3–4 layers, outer layers 8–10μm wide, dark
Fungal Diversity (2014) 68:159–238
brown, cells of textura angularis, inner layers hyaline, 5–
40μm wide. Conidiophores 13–30×2–3μm, 1–2-septate,
branched at the base, hyaline, cylindrical. Conidiogenous
cells annellidic, hyaline, cylindrical. Conidia 60–65×7–9μm
(x = 62.2×7.7μm, n=20), phragmosporous, curved to sigmoid, pale to moderately dark brown, with hyaline end cells,
6–7-transverse eusepta, smooth-walled, tapered to the obtuse
apex, base truncate (Wijayawardene et al. 2013a).
Septoriella Oudem., Ned. kruidk. Archf, 2 sér. 5: 52 (1889)
Type species: Septoriella phragmitis Oudem. [as
‘phragmitidis’], Ned. kruidk. Archf, 2 sér. 5: 54 (1889)
Phylogenetic study: Crous et al. (2014)
Notes: Septoriella was introduced by Oudemans (1889)
with the generic type Septoriella phragmitis. Crous et al.
(2014) introduced a new species Septoriella oudemansii based
on a megablast nucleotide search in GenBank. The species
was similar to Phaeosphaeria caricis, Ph. ammophilae and
Ophiosphaerella herpotricha (Crous et al. 2014). The taxon
clusters with the asexual species, Wojnowicia hirta and
Amarenomyces ammophilae in Phaeosphaeriaceae in LSU
gene phylogenetic analysis (data is not shown). However,
the type species of Septoriella is not represented in
GenBank. Thus, we tentatively include Septoriella in
Phaeosphaeriaceae. Below we only discuss S. oudemansii.
Septoriella oudemansii Crous & Quaedvl., Persoonia,
Mol. Phyl. Evol. Fungi 32: 281 (2014), Faces of Fungi
number: FoF000304.
Saprobic on Phragmites australis (Cav.) Trin. ex Steud
(Poaceae). Sexual state: Unknown. Asexual state:
Conidiomata up to 250μm diam., pycnidial, solitary, immersed, uniloculate, globose, glabrous, brown, ostiole central,
with a brown, oozing, conidial cirrhus. Conidiomata walls
composed of 3–4 layers, brown, arranged in textura angularis.
C o n i d i o p h o re s r e d u c e d t o c o n i d i o g e n o u s c e l l s .
Conidiogenous cells 5–11×4–5μm, ampulliform, hyaline,
smooth-walled, apex with minute periclinal thickening or
percurrent proliferation, lining the inner cavity. Conidia
(17–)23–32(−35)×(3.5–)4(−6), solitary, subcylindrical, with
obtuse ends, slightly wider in the middle, yellowish-brown,
3(−5)-septate, becoming slightly constricted at the septa with
age, smooth-walled, with guttules and flared mucoid appendages at the ends (from Crous et al. 2014).
Setomelanomma M. Morelet, Bull. Soc. Sci. nat. Arch.
Toulon et du Var 227: 15 (1980), Faces of Fungi number:
FoF00271.
Type species: Setomelanomma holmii.
Phylogenetic study: Rossman et al. (2002), Schoch et al.
(2009), Zhang et al. (2009, 2012), Hyde et al. (2013),
Wijayawardene et al. (2014b).
Notes: Setomelanomma was introduced by Morelet (1980)
as typified by S. holmii to accommodate the monotypic genus
from France associated with branches of Picea. Morelet
(1980) however, did not illustrate the fungus and did not
215
provide a detailed description (Rossman et al. 2002; Zhang
et al. 2012). Rossman et al. (2002) re-circumscribed the type
species and compared the morphological characters with
North American collections. Detailed descriptions using morphology and molecular phylogeny were given by Zhang et al.
(2012). Rossman et al. (2002) placed the genus in
Phaeosphaeriaceae due to the morphology and phylogenetic
data and this was later accepted by various authors (Kodsueb
et al. 2006, 2007; Schoch et al. 2009; Zhang et al. 2009, 2012;
Hyde et al. 2013). The genus is morphologically typical of
Phaeosphaeriaceae as the ascomata are relatively small, the
peridium is thin-walled comprising pseudoparenchymatous
cells, pseudoparaphyses are cellular; and brown to yellowish-brown, and ascospores are phragmosporous (Rossman
et al. 2002; Zhang et al. 2012). Setomelanomma however,
differs from other genera in Phaeosphaeriaceae by its setose
ascomata. No asexual state is known for the genus. There are
two species, S. holmii and S. prolata K.J. Leonard & Suggs
listed in Index Fungorum (2014)
Based on the multigene phylogenetic analyses
(Figs. 1 and 2), Setomelanomma forms a strongly supported clade with the asexual species, Xenoseptoria
neosaccardoi and Paraphoma radicina (CBS 111.79)
in Phaeosphaeriaceae and these genera may be the
asexual morphs of Setomelanomma.
Setomelanomma holmii M. Morelet, Bull. Soc. Sci. nat.
Arch. Toulon et du Var 36(no. 227): 15 (1980), Faces of Fungi
number: FoF00272, Fig. 25.
Pathogenic on branches of Picea. Sexual state: Ascomata
100–150μm high, 140–175μm diam., scattered, gregarious
semi-immersed to erumpent through host tissue, becoming
superficial, visible as abundant, small black dots on the host
surface, uniloculate, globose to subglobose, covered by setae,
dark brown to black, with central ostiole. Peridium 12.5–
26μm wide, thin-walled, of equal thickness, composed of 5–
7 layers of black, broadly pseudoparenchymatous cells, arranged in a textura angularis to textura globulosa.
Hamathecium composed of numerous, 1.5–3μm wide, filamentous, frequently anastomosing, broad cellular
pseudoparaphyses, with distinct septa, embedded in mucilaginous matrix. Asci (67–)68–77(−85)×(13–)15–17(−20) μm
(x = 75.2×15.2μm, n=20), 8-spored, bitunicate, fissitunicate,
broadly cylindrical to cylindric-clavate, subsessile to short
pedicellate, apically rounded with well-developed ocular
chamber. Ascospores (18–)21–23(−24)×(6–)7–9(−11) μm
(x = 21.3 × 8.2 μm, n = 20), overlapping 1–2-seriate,
phragmosporous, ellipsoidal to broadly fusiform, initially hyaline to pale yellowish, becoming light brown to
brown or yellowish-brown at maturity, initially forming
one median septum, becoming 3-septate at maturity,
slightly curved, often constricted at the median septum,
smooth and thick-walled. Asexual state: see under
Xenoseptoria neosaccardoi Quaedvlieg et al. (2013)
216
Fungal Diversity (2014) 68:159–238
Fig. 25 Setomelanomma holmii (BPI 620251) a Herbarium label and specimens. b Ascomata on substrate. c Section through ascoma. d
Section through peridium. e Cellular pseudoparaphyses. f–i Asci. j–n Ascospores. Scale bars: c=50μm, d, e, f, g, h, i=20μm, j, k, l, m, n=10μm
Fungal Diversity (2014) 68:159–238
Material examined: USA, Kansas, Shawnee Coounty, on
branches of Picea pungens Engelm (Pinaceae), 5 May 1959,
B. Herbert (BPI 620251).
Setophoma Gruyter et al., in De Gruyter et al. Mycologia
102(5): 1077 (2010), Faces of Fungi number: FoF00273,
Fig. 26.
Pathogenic or saprobic on various hosts (Alliaceae,
Asteraceae and Poaceae). Sexual state: Ascomata, scattered,
gregarious, immersed, visible as raised, minute black dots on
host surface, uniloculate, globose to subglobose, glabrous,
brown to dark brown, ostiole central, with minute papilla.
Peridium thin-walled, of equal thickness, composed of pseudoparenchymatous cells, arranged in flattened textura
angularis to textura prismatica. Hamathecium composed of
numerous, filiform, broad cellular, pseudoparaphyses, with
distinct septa, anastomosing at the apex. Asci 8-spored,
bitunicate, fissitunicate, cylindrical to cylindric-clavate,
short pedicellate, apically rounded, with well-developed
narrowly ocular chamber. Ascospores overlapping 2-seriate,
phragmosporous, cylindrical to cylindric-clavate, hyaline,
3-septate, usually enlarge at the second cell from apex,
smooth-walled with large guttules. Asexual state: produced on rice straw and bamboo pieces on water agar
after four weeks. Conidiomata scattered to clustered, gregarious, superficial, globose to subglobose, setose, and
sometimes glabrous when mature, initially light brown,
becoming brown to dark brown. Conidiomata walls thin,
composed of light brown to brown pseudoparenchymatous
cells, arranged in a textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells
enteroblastic, phialidic, determinate, discrete, unbranched,
oblong to cylindrical, or ampulliform, hyaline, slightly
curved, aseptate, lining the inner cavity of conidioma.
Conidia amerosporous, oblong to ellipsoidal, rarely irregular, with rounded or obtuse ends, hyaline, aseptate,
smooth-walled (from De Gruyter et al. 2010;
Phookamsak et al. 2014).
Type species: Setophoma terrestris (H.N. Hansen) Gruyter
et al., in De Gruyter et al. Mycologia 102(5): 1077 (2010).
≡ Phoma terrestris H.N. Hansen, Phytopathology 19(8):
699 (1929)
Phylogenetic study: De Gruyter et al. (2010), Quaedvlieg
et al. (2013), Phookamsak et al. (2014)
Notes: Setophoma was introduced by De Gruyter et al.
(2010) to accommodate phoma-like species and is typified
by S. terrestris. Two species, S. sacchari (Bitanc.) Gruyter
et al. and S. terrestris (H.N. Hansen) Gruyter were accommodated in this genus. Quaedvlieg et al. (2013) introduced a new
species Setophoma chromolaenae Quaedvlieg et al. on leaves
of Chromolaena odorata from Brazil. No sexual state was
reported. Phookamsak et al. (2014) reported the sexual state of
Setophoma based on asexual-sexual connection of S. sacchari
and phylogenetic data. The sexual state of Setophoma is
217
similar to Phaeosphaeria species, but differs in ascospore
colour and asexual state (Phookamsak et al. 2014).
Setophoma chromolaenae, S. sacchari, S. terrestris and
S. vernoniae Crous & Alfenas are presently accommodated
in the genus (Index Fungorum 2014; Crous et al. 2014;
Phookamsak et al. 2014). Based on multigene phylogenetic
analysis, we accept Setophoma in Phaeosphaeriaceae which
forms a single clade at basal of the family (Fig. 2).
Tiarospora Sacc. & Marchal, Revue mycol., Toulouse
7(no. 26): 148 (1885), Faces of Fungi number: FoF00274.
Saprobic or pathogenic on Ammophila Host, Deschampsia
P. Beauv., Elymus L. (Poaceae) and Dryas grandis Jurtzev
(Rosaceae). Sexual state: Unknown. Asexual state:
Conidiomata scattered, gregarious, immersed to semi-immersed, uniloculate, globose, glabrous, brown, ostiole central,
with short papilla. Conidiomata walls thick, composed on
several layers, outer layers comprising thick-walled dark
brown, flattened cells of textura angularis, inner layers comprising thin-walled paler cells. Conidiophores reduced to
conidiogenous cells. Conidiogenous cells holoblastic, sympodial, discrete, doliiform, cylindrical or lageniform, hyaline,
smooth-walled. Conidia didymosporous, broadly ellipsoid,
with obtuse to flattened ends, hyaline to pale brown, 1-septate,
continuous, thick and smooth-walled, with guttules or irregular or cap-like gelatinous appendage (from Sutton 1980).
Type species: Tiarospora westendorpii Sacc. & Marchal,
Revue mycol., Toulouse 7(no. 26): 148 (1885).
Phylogenetic study: None
Notes: Tiarospora was introduced by Saccardo and
Marchal (1885) and is typified by T. westendorpii Sacc. &
Marchal. Four species were accommodated under Tiarospora;
T. deschampsiae Krusch., T. perforans (Sacc.) Höhn.,
T. pirozynskii Chleb. and T. westendorpii Sacc. & Marchal.
However, Tiarospora perforans was transferred to
Montagnulaceae by Aptroot (2006). Tiarospora is similar to
Tiarosporella Höhn.; however, they differ in the morphology
of their conidia. Tiarospora has 1-septate conidia, while
Tiarosporella has aseptate conidia (Abbas et al. 2012).
Tiarospora was described in Sutton (1980); however, no
family placement was given for the genus. Kirk et al. (2001,
2008) treated the genus under Phaeosphaeriaceae but did not
mention any literature to confirm this and this was accepted by
Wijayawardene et al. (2012). Oertel (2011) however, mentioned that the type species of Tiarospora, T. westendorpii
is a synanamoph of Amarenographium metableticum,
which is the asexual state of Amarenomyces, also in
Phaeosphaeriaceae. Therefore the current placement of
this genus is somewhat unclear. The genus is relatively
poorly known, lacks molecular data and no sexual state is
known. We tentatively place Tiarospora in Phaeosphaeriaceae
until molecular data resolves this issue.
Vrystaatia Quaedvlieg et al. Stud. Mycol. 75: 372 (2013),
Faces of Fungi number: FoF00275, Fig. 27.
218
Saprobic on Aloe maculata (Aloaceae). Sexual state:
Unknown. Asexual state: Conidiomata pycnidial, clustered,
gregarious, erumpent on culture, with substromata on host,
Fungal Diversity (2014) 68:159–238
globose, glabrous, black, ostiole central, surrounded by dark
brown area exuding cirrhus of orange conidia. Conidiomata
walls thin, composed of 6–8 layers, arranged in textura
Fungal Diversity (2014) 68:159–238
Setophoma sacchari (MFLU 11-0190 and MFLU 12-2470) on
living leaves of Saccharum officinarum. a Symptoms on host (MFLU 110190). b Ascomata immersed in host tissue (MFLU 11-0190). c
Section through ascoma (MFLU 11-0190). d Section through peridium
(MFLU 11-0190). e Cellular pseudoparaphyses (MFLU 11-0190). f–h
Asci (MFLU 11-0190). i–k Ascospores (MFLU 11-0190). l Spore
germination (MFLU 11-0190). m Immature conidiomata on living
culture (MFLU 11-0190) n Conidiomata on WA (MFLU 12-2470). o
Section through conidiomata (MFLU 12-2470). p Section through
conidiomata walls (MFLU 12-2470). q–r Conidiogenous cells (MFLU
12-2470). s, t Conidia (MFLU 11-0190). u, v Conidia (MFLU 12-2470)
Scale bars: n, o=100μm, c=50μm, d, e, f, g, h, l, p=20μm, q=10μm, i, j,
k, r, s, t, u, v=5μm
Fig. 26
angularis, pale brown. Conidiophores reduced to
conidiogenous cells. Conidiogenous cells enteroblastic,
annellidic, discrete, globose to ampulliform, hyaline,
smooth-walled, with prominent periclinal thickening, or proliferating several times percurrently near apex, producing
macro- and microconidia. Macroconidia scolecosporous,
subcylindrical to narrowly obclavate, apex obtuse to
subobtuse, with truncate base, hyaline, (1–)3-septate,
smooth-walled, with guttules, widest at the basal septum.
Microconidia pear-shaped to globose or ellipsoidal, apex obtuse, with truncate base, hyaline, aseptate, smooth-walled
(from Quaedvlieg et al. 2013).
Type species: Vrystaatia aloeicola Quaedvlieg et al. Stud.
Mycol. 75: 372 (2013)
Phylogenetic study: Quaedvlieg et al. (2013).
Notes: Vrystaatia was introduced by Quaedvlieg et al.
(2013) to accommodate a non-congeneric species of
Septoria sensu stricto and typified by V. aloeicola.
Vrystaatia is similar to Septoria sensu stricto, but differs in
Fig. 27 Vrystaatia aloeicola,
redrawn from Quaedvlieg et al.
(2013). Scale bars=10μm
219
conidiogenous cells morphology and forms macro- and
microconidia in culture, which was not typical of Septoria
(Quaedvlieg et al. 2013). Based on multigene phylogenetic
analysis (Fig. 2), Vrystaatia forms a single clade at the basal of
Paraphoma, Setomelanomma and Xenoseptoria clade. Thus
we accept Vrystaatia for which no sexual state is known in
Phaeosphaeriaceae.
Wojnowicia Sacc., Syll. fung. (Abellini) 10: 328 (1892),
Faces of Fungi number: FoF00276.
Pathogenic on monocotyledonous or dicotyledonous
hosts. Sexual state: Unknown. Asexual state: Conidiomata
pycnidial, scattered, solitary, immersed to superficial on host
tissue, globose, glabrous or setose, dark brown, ostiole central,
with minute papillate or pore-like opening. Conidiomata walls
thick, composed of pseudoparenchymatous cells, outer layers
thick-walled, arranged in textura angularis, dark brown, inner
layers thin-walled, hyaline, thinner towards inner
conidiogenous cells. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells enteroblastic, phialidic, discrete,
determine, doliiform to ampulliform, hyaline, smooth-walled,
with minute collarette and channel, lining inner cavity of
conidiomata. Conidia phragmosporous, fusiform to cylindrical,
with obtuse ends, pale brown to brown, continuous, septate,
straight to curved, thin and smooth-walled, guttulate.
Type species: Wojnowicia hirta (J. Schröt.) Sacc., in
Saccardo & Sydow, Syll. fung. (Abellini) 14(2): 960 (1899).
Phylogenetic study: De Gruyter et al. (2009),
Wijayawardene et al. (2013b).
Notes: Wojnowicia was introduced by Saccardo (1892) and
is typified by W. hirta. The genus was discussed by Sutton
(1975, 1980) who accepted two species, W. hirta and
220
W. ephedrae Hollós. Sutton (1980) treated W. tenella Pat. and
W. graminis (McAlpine) Sacc. & D. Sacc as synonyms of
W. hirta. Farr and Bills (1995) named a collection from
Juniperus deppeana Steud. and Pinus edulis Engelm. As
W. colluvium D.F. Farr & Bills. Eleven species are listed in
Index Fungorum (2014). Molecular data is only available for
two species in GenBank. De Gruter et al. (2009) included two
strains of Wojnowicia hirta in their analysis and showed that
W. hirta belongs to Phaeosphaeriaceae. Wijayawardene et al.
(2013b) introduced a new species, W. viburni Wijayaw. et al.
on leaves of Viburnum utile Hemsl. ex Forb. & Hemsl.
from China and confirmed that Wojnowicia belongs in
Phaeosphaeriaceae. They also suggested that Wojnowicia
should be the asexual state of Ophiosphaerella based on
phylogenetic evidence (Wijayawardene et al. 2013b).
However, Wijayawardene et al. (2013b) and De Gruyter
et al. (2009) did not include many isolates of
Phaeosphaeriaceae in their analysis. In this study with
several sexual and asexual genera, the multigene phylogenetic analysis (Fig. 2) indicates that Wojnowicia hirta
(CBS 160.73, CBS 295.69) clusters with Amarenomyces,
Ophiosphaerella herpotricha (CBS 620.86) and other
Phaeosphaeria sensu lato species while W. viburni forms
a single clade at the base of Neostagonospora. Therefore the
findings of Wijayawardene et al. (2013b) and De Gruyter et al.
(2009) that Wojnowicia may be an asexual state of
Ophiosphaerella is questionable, while Ophiosphaerella is
obviously polyphyletic and requires further work.
Xenoseptoria Quaedvlieg et al. Stud. Mycol. 75: 371
(2013), Faces of Fungi number: FoF00277.
Pathogenic on Lysimachia vulgaris var. davurica (Ledeb.)
R. Knuth (Primulaceae). Sexual state: unknown but possibly
Setomelanomma. Asexual state: Conidiomata pycnidial,
scattered, solitary, immersed to erumpent, uniloculate, globose, glabrous, brown, ostiole developing 1–3 papilla or
necks, exuding a pink to orange conidial mass.
Conidiomata walls thin, composed of 4–8 layers of brown
cells, arranged in textura angularis. Conidiophores reduced
to conidiogenous cells, hyaline, septate, branched, smoothwalled. Conidiogenous cells enteroblastic, mono- to
polyphialidic, with prominent periclinal thickening, or
percurrent proliferation, discrete or integrated, ampulliform
to doliiform or subcylindrical, hyaline, smooth-walled.
Conidia scolecosporous, cylindrical to obclavate, tapering
to subobtuse apex, with obtuse base, straight to irregular
curved, hyaline, septate, smooth-walled, with guttules (from
Quaedvlieg et al. 2013)
Type species: Xenoseptoria neosaccardoi Quaedvlieg
et al., Stud. Mycol. 75: 371 (2013).
Phylogenetic study: Quaedvlieg et al. (2013)
Notes: Xenoseptoria was introduced by Quaedvlieg et al.
(2013) and was typified by X. neosaccardoi. The genus was
introduced to accommodate a single species associated with
Fungal Diversity (2014) 68:159–238
leaf spot disease of Lysimachia vulgaris var. davurica
(Primulaceae). The genus can be distinguished from
Septoria sensu stricto as Xenoseptoria has multi-papillate
conidiomata and mono- to polyphialidic conidiogenous cells
(Quaedvlieg et al. 2013). In multigene phylogenetic analysis,
Xenoseptoria clusters with the sexual genus Setomelanomma
and the asexual genus Paraphoma with strong support
(91 % ML, 1.00 PP). The genus is closely related to
Setomelanomma. These genera may need placing in synonymy with Setomelanomma, but it would be unwise to do so
until the tree becomes better populated.
Genera transferred to other families
Botryosphaeriaceae
Recent accounts of Botryosphaeriaceae include those of Liu
et al. (2012) and Hyde et al. (2013, 2014)
Metameris Theiss. & Syd., Annls mycol. 13(3/4): 342
(1915), Faces of Fungi number: FoF00289.
Saprobic or parasitic on ferns and Bougainvillea. Sexual
state: Ascostromata scattered, solitary to gregarious,
erumpent through host epidermis, visible as slightly raised,
black lines or black spots on the host surface. Locules
clustered in pseudostroma, uni to bi-loculate, globose to
subglobose, glabrous, black, ostiole in centre of each locule, with minute papilla. Peridium thick-walled, composed
of thickened, black, scleroplectenchymatous cells, arranged
in a textura angularis. Hamathecium composed of numerous, filamentous, broad cellular pseudoparaphyses, anastomosing at the apex. Asci 8-spored, bitunicate, cylindrical to
cylindric-clavate, subsessile to short pedicellate, apically
rounded, with well-developed ocular chamber. Ascospores
overlapping 1–2-seriate, 2-celled, oblong to cylindrical, narrow towards lower end cell, hyaline, septate, smoothwalled, cytoplasm stains blue in cotton blue reagent, the
large guttules in the upper part of the upper cell not
staining. Asexual state: Unknown.
Type species: Metameris japonica
Phylogenetic study: None.
Notes: Metameris was established to accommodate
Monographus japonicus Syd. by Theissen and Sydow
(1915). Metameris forms linear pseudostromata, and has hyaline, 1-septate ascospores and Clements and Shear (1931)
treated the genus under Dothideaceae (Zhang et al. 2012).
Müller and von Arx (1962) treated Metameris as a synonym
of Scirrhia and placed the genus in Mycosphaerellaceae
(Crous et al. 2011). Later, von Arx and Müller (1975) assigned
the genus to Pleosporaceae and did not accept that
Metameris was synonymous with Scirrhia (Crous et al.
2011; Zhang et al. 2012). Recently, Metameris was accommodated in Phaeosphaeriaceae due to its small ascomata,
Fungal Diversity (2014) 68:159–238
broad cylindrical to obclavate asci with a knob-like pedicel
and monocotyledons host preferences (Eriksson 2006;
Lumbsch and Huhndorf 2007, 2010; Crous et al. 2011;
Zhang et al. 2012; Hyde et al. 2013). However, the genus
lacks molecular data to confirm its familial placement
(Crous et al. 2011; Zhang et al. 2012).
There are five epithets listed for Metameris in Index
Fungorum (2014); however, three species are synonymized
under Scirrhia. In this study, we exclude Metameris from
Phaeosphaeriaceae. The large, elongated pseudostromata,
with a peridium of thickened scleroplectenchymatous cells,
broad, or irregularly cellular pseudoparaphyses, ascus morphology and didymosporous ascospores are characters typical of genera in Botryosphaeriaceae where it is tentatively
referred. Leptoguignardia is probably most similar (Liu
et al. 2012) and should be compared in future studies of
fresh collections.
Metameris japonica (Syd.& P. Syd.) Syd., in Theissen &
Sydow, Annls mycol. 13(3/4): 342 (1915), Faces of Fungi
number: FoF00290, Fig. 28.
≡ Monographus japonicus Syd. & P. Syd., Annls mycol.
10(4): 408 (1912)
Saprobic on Osmunda regalis var. japonica L. Sexual
state: Ascostromata 170–240μm high, 370–640μm diam.,
clustered, solitary to gregarious, erumpent through host
epidermis, visible as slightly raised, black, elongate
lining on host surface. Locules 160–240μm high, 200–
250μm diam, clustered, immersed in pseudostroma, uni
to bi-loculate, globose to subglobose, glabrous, black,
ostiole in centre of each locule, with minute papilla.
Peridium 23–67 μm wide, thick-walled, of unequal
thickness, slightly thick at the base towards sides of
pseudostroma, composed of several layers of thickened,
dark brown to black, scleroplectenchymatous cells, arranged in textura angularis. Hamathecium composed of
numerous, 3–7μm wide, filamentous, broad, irregular
cellular pseudoparaphyses, with distinct septa which
are constricted at the septum, embedded in mucilaginous
matrix, anastomosing at the apex. Asci 80–110(−118)×
(12.5–)13–18μm (x = 99.2×14.9μm, n=25), 8-spored,
bitunicate, cylindrical to cylindric-clavate, narrow towards the apex, subsessile to short pedicellate, apically
rounded with well-developed ocular chamber, arising
from the basal ascoma. Ascospores (22–)24–28×6–8μm
(x = 26.7×6.8μm, n=30), overlapping 1–2 seriate, 2-celled,
oblong to cylindrical, narrow towards lower end cell, hyaline,
1-septate, constricted at the septum, smooth-walled, mostly
upper cell larger than lower cell, cytoplasm stains blue in
cotton blue reagent, the large guttules in the upper part of
the upper cell not staining. Asexual state: Unknown.
Material examined: Japan, Mino, Kawauye-mura, on
Osmunda regalis L. var. japonica (Osmundaceae), 10 May
1912, K. Hara (S-F7166, holotype).
221
Didymellaceae
For a discussion of Didymellaceae see Hyde et al. (2013).
Zhang et al. (2012) questioned whether the placement Mixtura
in Phaeosphaeriaceae was natural. The genus is considered to
belong in Didymellaceae and is transferred herein.
Mixtura O.E. Erikss. & J.Z. Yue, Mycotaxon 38: 203
(1990), Faces of Fungi number: FoF00278.
Type species: Mixtura saginata
Phylogenetic study: None.
Mixtura saginata (Syd.) O.E. Erikss. & J.Z. Yue,
Mycotaxon 38: 203 (1990), Faces of Fungi number:
FoF00279, Fig. 29.
≡ Leptosphaeria saginata Syd., Annls mycol. 37(4/5): 377
(1939).
Pathogen causing necrotic leaf spots on Chusquea
serrulata Pilger. Lesions up to 2–5 cm long, infecting mostly
the leaf margin, elongate cylindrical, pale brown to yellowishbrown, dry, separated from healthy tissue by a reddish-brown
to purple-brown or black margin. Sexual state: Ascomata
120–260μm high, 180–335μm diam., scattered, sometimes
clustered, solitary, immersed, visible as raised, small black
dots on leaf lesions, uniloculate, globose to subglobose, glabrous, dark brown to black, ostiole central with minute papilla.
Peridium 12–40μm wide, thin-walled, of unequal thickness,
thickened at apex at sides, composed of 3 or more layers of
brown to dark brown, pseudoparenchymatous cells, arranged
in a textura angularis, outer layers comprising 2–5 layers of
thickened cells, brown to dark brown, inner layers comprising
several layers of flattened cells, hyaline to pale brown.
Hamathecium composed of numerous, 3–8μm wide, filamentous, frequently anastomosing, broad cellular
pseudoparaphyses, with distinct septa which are constricted
at the septa, embedded in mucilaginous matrix. Asci
(105–)112–135(−142)×(57–)60–100(−127) μm (x = 121.3×
80.3μm, n=20), 8-spored, bitunicate, fissitunicate, globose to
subglobose, or ovoid, sessile to subsessile, apically rounded
with well-developed ocular chamber, producing a few asci,
arising from the basal ascoma. Ascospores 60–
90(−95)×(19–)22–25(−27) μm (x = 81.2×23μm, n=30), irregular overlapping 4-seriate, phragmosporous, broadly fusiform with rounded, germ pore at the ends, initially hyaline to
pale brown, becoming yellowish-brown or brown at maturity,
paler at the end cells, distoseptate with 7-septa, slightly
curved, rough, thick-walled, surrounded by thin, distinct
sheath. Asexual state: Unknown.
Material examined: ECUADOR, Tungurahua, Hacienda
San Antonio pr. Baños, on leaves of Chusquea serrulata
Pilger (Poaceae), 9 January 1938, H. Sydow (S-F8935,
lectotype).
Notes: The monotypic genus Mixtura was introduced by
Eriksson and Yue (1990) to accommodate Mi. saginata which
causes leaf spots on Chusquea serrulata. Mixtura is an
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Fungal Diversity (2014) 68:159–238
Fig. 28 Metameris japonica (holotype). a Herbarium label and specimens.
b Ascostromata on host surface. c Section through ascostroma. d
Section through peridium. e Pseudoparaphyses. f Asci and pseudoparaphyses
strained in cotton blue reagent. g Ascus stained in cotton blue reagent. h–j
Asci. k–m Ascospores. n–o Ascospores stained in cotton blue reagent. Scale
bars: c=100μm, d, e, f, g, h, i, j=20μm, k, l, m, n, o=10μm
uncertain genus with morphological characters and habitat
agreeing with several genera such as Mycosphaerella,
Phaeosphaeria, Teratosphaeria, Trematosphaeria and
Wettsteinina (Eriksson and Yue 1990; Zhang et al. 2012).
Mixtura is similar to Mycosphaerella and Phaeosphaeria
species in causing a leaf spot disease on monocotyledons,
Fungal Diversity (2014) 68:159–238
223
Fig. 29 Mixtura saginata (S-F8935, lectotype). a Herbarium label and
specimens. b Ascomata on leaf lesion. c Section through ascoma d
Section through peridium. e Pseudoparaphyses stained in cotton blue
reagent. f Immature ascus. g–i Asci. j Ocular chamber of asci stained in
cotton blue reagent. k Immature ascospore stained in cotton blue reagent.
l–m Mature ascospores. Scale bars: c=100μm, d–m=20μm
but differs from Mycosphaerella species in its centrum type
(Eriksson and Yue 1990). Mixtura differs from
Trematosphaeria due to its fusiform, olive brown ascospores
and the genus differs from Wettsteinina as its rather thick-walled
peridium and ellipsoidal asci (Eriksson and Yue 1990). Eriksson
and Yue (1990) treated the genus in Phaeosphaeriaceae based
on the peridium structure. However, Zhang et al. (2012)
disagreed with Eriksson and Yue (1990) and placed the genus
in Teratosphaeriaceae with Mixtura having relatively similar
morphology to the type species of Teratosphaeria.
224
Mixtura is similar to other genera in Phaeosphaeriaceae
such as Hadrospora and Loratospora in its saccate asci and
large ascospores in Hadrospora. However, these genera differ
in their centrum type. Mixtura forms dense, thick, cellular
pseudoparaphyses, while Hadrospora forms trabeculate
pseudoparaphyses, and pseudoparaphyses are lacking in
Loratospora. Hadrospora is excluded as a member of
Phaeosphaeriaceae in this study, but Loratospora is
confirmed based on phylogenetic evidence. Mixtura is
similar to Leptosphaerulina in habitat on host and asci.
However, they differ in the ascospores and centrum type as
Leptosphaerulina lacks pseudoparaphyses and has muriform
ascospores. Mixtura has dense pseudoparaphyses and
phragmosporous ascospores with distosepta. Therefore, we
agree with Zhang et al. (2012) and exclude Mixtura from
Phaeosphaeriaceae. The genus is tentatively placed in
Didymellaceae.
Didymosphaeriaceae
For an account of this family see Ariyawansa et al. (2014b).
Barria and Wilmia were transferred from Phaeosphaeriaceae
to Didymosphaeriaceae in Ariyawansa et al. (2014b and are
only briefly discussed here.
Barria Z.Q. Yuan, Mycotaxon 51: 313 (1994), Faces of
fungi number: FoF00031.
Type species: Barria piceae Z.Q. Yuan, Mycotaxon 51:
314 (1994).
Phylogenetic study: None.
Notes: Barria is a monotypic genus introduced by Yuan
(1994) based on Barria piceae. The genus was reported as
pathogenic on needles of Picea schrenkiana Fisch. & C.A.
Mey. Barria is excluded from Phaeosphaeriaceae in this
study based on its morphology. Barria is associated with
gymnosperms, asci are clavate and short pedicellate, and
ascospores are didymosporous with thick walls. Whereas the
generic type, Phaeosphaeria is associated mostly with angiosperms, asci are often broad cylindrical to cylindric-clavate
and subsessile and ascospores are phragmosporous (Yuan
1994; Zhang et al. 2012; Hyde et al. 2013; Quaedvlieg et al.
2013). Additionally, most genera with confirmed phylogenetic placement in Phaeosphaeriaceae have phragmospores,
scolecospores, or muriform ascospores, but there are no
didymosporous taxa (Zhang et al. 2012; Hyde et al. 2013;
Quaedvlieg et al. 2013). Barria is associated in the same host
family as Setomelanomma which was confirmed as
phaeosphaeriacous based on phylogenetic evidence. Barria
has didymosporous ascospores, while Setomelanomma has
phragmosporous ascospores. Most didymosporous genera in
Phaeosphaeriaceae lack molecular phylogenetic data to confirm their current placements. Furthermore, Barria is more
similar to genera in Didymosphaeriaceae rather than
Phaeosphaeriaceae (Ariyawansa et al. 2014b), where is it
Fungal Diversity (2014) 68:159–238
tentatively accommodated. Zhang et al. (2012) accepted
Lautitia in Phaeosphaeriaceae; in contrast, all genera of marine and freshwater fungi (Carinispora, Isthmosporella and
Ocala) were excluded from Phaeosphaeriaceae in Zhang
et al. (2012). However, Lautitia differs from other genera in
Phaeosphaeriaceae in having clavate asci with long pedicels
and forming a pseudostromata with the peridium arranged in a
textura porrecta. Other genera in Phaeosphaeriaceae mostly
have cylindrical asci with subsessile to short pedicels and
uniloculate ascomata with the peridium arranged in a textura
angularis. Metameris forms large, elongated pseudostromata,
with a thick-walled peridium of scleroplectenchymatous cells
which is rarely found in other genera of Phaeosphaeriaceae.
A new species of Letendraea (=Wilmia) was introduced based
on phylogenetic evidence and belongs in Didymosphaeriaceae
(see Ariyawansa et al. 2014b).
Wilmia Dianese et al., Mycologia 93(5): 1014 (2001),
Faces of fungi number: FoF00046.
Type species: Wilmia brasiliensis Dianese et al.,
Mycologia 93(5): 1014 (2001).
Phylogenetic study: Ariyawansa et al. (2014a).
Notes: Wilmia was introduced by Dianese et al. (2001) to
accommodate a monotypic genus, Wilmia brasiliensis that
caused a leaf spot disease of Memora pedunculata (Vell.)
Miers. in Brazil. Dianese et al. (2001) treated Wilmia in
Phaeosphaeriaceae based on the morphological characters
which fitted Barr’s concept (Barr 1987b, 1992a). Wilmia is
similar to other genera in Phaeosphaeriaceae viz. Barria,
Lautitia and Metameris in having didymosporous ascospores
and a coelomycetous asexual morph (Dianese et al. 2001;
Zhang et al. 2012). Zhang et al. (2012) tentatively placed
Wilmia in Phaeosphaeriaceae as the genus is poorly known
and lacks molecular data, although Zhang et al. (2012) mentioned that the genus should be accommodated in
Leptosphaeriaceae based on its dicotyledonous host habit.
A Dothideomycete species was collected from living and
dead leaves of Cordyline sp. in Thailand. The species also
caused leaf spot disease and had similar morphological characters to Wilmia brasiliensis. Ariyawansa et al. (2014b synonymized Wilmia under Letendraea based on morphology
and phylogeny. Thus, the new species collected from
Cordyline sp. was accommodated in Didymosphaeriaceae
and named Letendraea cordylinicola Phookamsak et al.
(Ariyawansa et al. 2014b).
Leptosphaeriaceae
For a discussion on Leptosphaeriaceae see Hyde et al. (2013);
Chaetoplea is considered to belong in this family and is
transferred herein.
Chaetoplea (Sacc.) Clem., in Clements & Shear, Gen.
fung., Edn 2 (Minneapolis): 275 (1931), Faces of Fungi
number: FoF00280.
Fungal Diversity (2014) 68:159–238
≡ Pyrenophora subgen. Chaetoplea Sacc., Syll. fung.
(Abellini) 2: 279 (1883)
Saprobic on woody stems or herbaceous dicotyledonous.
Sexual state: Ascomata solitary, gregarious, semi-immersed
to superficial, or erumpent through host tissue, uniloculate,
subglobose, glabrous, brown to dark brown, ostioles central,
with short papilla. Peridium thick-walled, of equal thickness,
composed of dark brown to black, scleroplectenchymatous
cells of textura angularis or textura globulosa. Hamathecium
composed of numerous, filamentous, distinctly septate, broad
cellular pseudoparaphyses, anastomosing at the apex. Asci 8spored, bitunicate, clavate to cylindric-clavate, short pedicellate, apically rounded, with an ocular chamber. Ascospores
overlapping 1–2-seriate, phragmosporous, fusiform or broadly fusiform to ellipsoidal, brown to yellowish-brown, septate,
slightly constricted at the septa, smooth-walled. Asexual
state: Conidiomata pycnidial, scattered, solitary to gregarious, semi-immersed to erumpent, uniloculate, ellipsoidal to
broadly fusiform with rounded apex, glabrous, dark brown
to black, ostioles central, with pore-like opening.
Conidiomata walls thin-walled, composed of flattened,
scleroplectenchymatous cells, arranged in textura angularis
to textura prismatica, brown to dark brown. Conidiophores
reduced to conidiogenous cells. Conidiogenous cells holoblastic, phialidic, discrete, ampulliform, hyaline, smoothwalled, hard to distinguish from the inner wall cells.
Conidia oblong to ellipsoidal, with obtuse ends, brown,
1-septate, smooth-walled.
Type species: Chaetoplea calvescens
Phylogenetic study: None
Notes: Chaetoplea was introduced by Clements and Shear
(1931) to accommodate Dothideomycete species from woody
substrates which included species transferred from
Cucurbitaria, Leptosphaeria, Pleospora, Pyrenophora,
Sphaeria and Teichospora (Shoemaker 1961; Wehmeyer
1961; von Arx and Müller 1975; Barr 1990b; Yuan and Barr
1994; Zhang et al. 2012). Barr (1987b, 1990a, b) treated
Chaetoplea sensu lato in Phaeosphaeriaceae. The type specimen has not been recovered from any herbaria worldwide.
Zhang et al. (2012) however observed the isotype which is a
slide from the Farlow Herbarium (FH) and has only asci and
ascospores. Zhang et al. (2012) mentioned that Chaetoplea
may be heterogeneous in nature and occurs in a wide range of
substrates such as herbaceous stalks, decorticated wood and
periderm tissues.
The asexual state of Chaetoplea (for Pyrenophora
calvescens (Fr.) Sacc.) was first reported as Dendryphium
comosum Walk. (Saccardo 1883). Later Webster and Lucas
(1959) treated Microdiplodia henningsii Staritz. as the asexual
state of Chaetoplea and this was accepted by Barr (1987b).
However, Crous et al. (2006) treated Microdiplodia as an asexual state of Karstenula placed in the family Montagnulaceae.
Ramaley (1995) reported Parahendersonia as the asexual state
225
of Chaetoplea dasylirionis being saprobic on Dasylirion
(Agavaceae) and placed it in Leptosphaeriaceae. In this study,
the asexual state of Chaetoplea was observed occurring on the
same host as the lectotype. The asexual state of Chaetoplea
forms oblong to ellipsoidal, brown, 1-septate, smooth-walled
conidia which are microdiplodia-like.
After examining Fries exsiccatus (Scler. Suecicae
exsiccatus no. 401) in the US National Fungus Collections
(BPI) it was determined that this should be designated as a
lectotype in this study. Based on morphology, Chaetoplea is
more similar to Leptosphaeriaceae than Phaeosphaeriaceae
and this supports the current placement of Chaetoplea as listed
in Index Fungorum (2014). Therefore Chaetoplea should
currently be placed in Leptosphaeriaceae. Recollection,
epitypification, and molecular data are needed to confirm the
natural placement of Chaetoplea.
Chaetoplea calvescens (Fr.) Clem., in Clements & Shear,
Gen. fung., Edn 2 (Minneapolis): 275 (1931), Faces of Fungi
number: FoF00281, Fig. 30.
≡ Sphaeria calvescens Fr., Sclerom. Suec.: no. 401 (1822)
Saprobic on herbaceous dicotyledonous hosts. Sexual
state: Ascomata 140–220 μm high, 280–350 μm diam.,
scattered, solitary to gregarious, semi-immersed to superficial,
visible as small black dots on the host surface, uniloculate,
subglobose, glabrous, dark brown to black, ostiole central,
with short papilla. Peridium 15–40μm wide, thick-walled, of
equa l thickness, compose d o f seve ral layers of
scleroplectenchymatous cells, outer layers comprising 2–3
cell layers of thick-walled, black, textura angularis to textura
globulosa, inner layers comprising 4–5 cell layers of thinwalled, hyaline to pale brown, flattened cells of textura
angularis to textura prismatica. Hamathecium composed of
numerous, 2–3 μm wide, filamentous, broad cellular
pseudoparaphyses, with distinct septa, not constricted at the
septa, anastomosing at the apex. Asci (80–)90–115(−120)×
11–13(−15) μm (x = 100 × 12.1 μm, n = 20), 8-spored,
bitunicate, fissitunicate, clavate, short pedicellate, apically
rounded, with indistinct ocular chamber. Ascospores (14–)
15–17(−119)×6–8.5μm (x = 16.7×7.4μm, n=30), overlapping 1–2-seriate, phragmosporous, broadly fusiform to ellipsoidal, enlarged at the second cell, brown to yellowish-brown,
3-septate, rarely 2-septate, straight or curved, constricted at the
septa, smooth-walled. Asexual state: Conidiomata growing
with sexual state, 170–190μm high, 150–190μm diam., pycnidial, solitary to gregarious, semi-immersed to erumpent,
visible as black dots on the host surface, uniloculate, ellipsoidal to broadly fusiform, with rounded apex, glabrous, dark
brown to black, ostiole central, with minute papilla.
Conidiomata walls 13.5–25μm wide, thick-walled, of equal
thickness, composed of several layers of flattened,
scleroplectenchymatous cells, outer layers comprising 2–3
cell layers of thick-walled, dark brown to black cells, arranged
in a textura angularis, inner layers comprising 3–5 layers of
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Fungal Diversity (2014) 68:159–238
Chaetoplea calvescens (lectotype of Sphaeria calvescens). a
Label and specimen of Chaetoplea calvescens. b Ascomata on host
surface. c Section through ascoma. d Section through peridium. e
Immature asci with pseudoparaphyses. f–i Asci. j–n Ascospores. o
Section through conidioma. p Section through conidioma wall. q, s
Conidiogenous cells stained in cotton blue reagent. r Conidiogenous
cell. t Conidia stained in cotton blue reagent. u–x Conidia. Scale bars:
c, o=100μm, e=50μm, d, f, g, h, i, p, t=20μm, j, k, l, m, n=10μm, q, r, s,
u, v, w, x=5μm
Fig. 30
thin-walled, hyaline to pale brown cells, arranged in textura
angularis to textura prismatica. Conidiophores arising from
basal cavity of conidioma, mostly reduced to conidiogenous
cells, hyaline, aseptate. Conidiogenous cells (3–)5–7(−11)×
(3–)4–6(−7) μm (x = 6.2 × 4.6 μm, n = 25) holoblastic,
phialidic, discrete, ampulliform or lageniform, hyaline,
aseptate, smooth-walled, hardly distinguished from inner
wall cells. Conidia (11–)12–14(−15)×4–6(−7) μm (x= 13×
5.2μm, n=30), solitary, didymosporous, oblong to ellipsoidal,
with rounded or obtuse ends, brown, 1-septate, smooth-walled.
Material examined: SWEDEN, on dead wood, 1822, E.M.
Fries, no. 401 (Fries SBARBARO COLLECTION), BPI
(lectotype of Sphaeria calvescens designated here).
Sphaerellopsis Cooke, Grevillea 12(no. 61): 23 (1883),
Faces of Fungi number: FoF00292.
Type species: Sphaerellopsis quercuum Cooke, Grevillea
12(no. 61): 23 (1883).
Phylogenetic study: Nischwitz et al. (2005), Bayon et al.
(2006).
Notes: Based on ITS gene phylogenetic analysis (data not
s h o w n ) , S p h a e re l l o p s i s f o r m s a b a s a l c l a d e i n
Leptosphaeriaceae. For details see under Eudarluca.
Pleosporaceae
Pleoseptum is considered to belong in this family and is
transferred herein. For an account of the family see Hyde
et al. (2013).
Pleoseptum A.W. Ramaley & M.E. Barr, Mycotaxon 54:
76 (1995), Faces of Fungi number: FoF00282.
Type species: Pleoseptum yuccaesedum.
Phylogenetic study: None.
Pleoseptum yuccaesedum A.W. Ramaley & M.E. Barr,
Mycotaxon 54: 76 (1995), Faces of Fungi number:
FoF00283, Fig. 31.
= Camarosporium yuccaesedum Fairm., Mycologia 10(5):
261 (1918)
Saprobic on leaves of Yucca baccata Torr. Sexual state:
Ascomata 250–360μm high, 230–470μm diam., scattered,
solitary, immersed, visible as numerous black spots on host
surface, uniloculate, globose to ovoid or conoid, dark brown
to black, glabrous, with centrally opening ostiole penetrating
the host epidermis. Peridium 70–90μm wide, thick-walled, of
unequal thickness, broad at the apex, composed of two layers
227
of thickened pseudoparenchymatous cells, outer layer comprising several layers of thick-walled cells, arranged in a
textura angularis, brown to dark brown, inner layers comprising several layers of thin-walled cells, hyaline, arranged in
textura angularis. Hamathecium composed of numerous, 2–
3μm wide, filiform, distinctly septate, frequently anastomosing, narrow cellular pseudoparaphyses, embedded in mucilaginous matrix. Asci (125–)130–170(−185)×18–22(−24) μm
(x= 153.7×20.9μm, n=25), 8-spored, bitunicate, fissitunicate,
cylindrical to cylindric-clavate, short pedicellate, apically
rounded, with well-developed ocular chamber. Ascospores
(23–)25–28(−29)×10–12(−13.5) μm (x = 25.9×11.7μm, n=
30), overlapping 1-seriate, dictyosporous, muriform, ellipsoidal to fusiform or obovoid, brown to dark brown, with 3–5
transverse septa, and 0–2 longitudinal septa, constricted at the
central septum, smooth-walled, with distinct mucilaginous
sheath. Asexual state: Conidiomata growing with the sexual
state, 270–355μm high, 265–390.5μm diam., pycnidial,
scattered, solitary to gregarious, immersed, visible as black
spots on host surface, uniloculate, globose to ovoid or conoid,
brown to dark brown, glabrous, with ostiolar opening penetrating the host epidermis. Conidiomata walls 30–65μm wide,
thick-walled, of unequal thickness, broad at the apex, composed of several layers of thickened pseudoparenchymatous
cells, arranged in textura angularis, brown to dark brown.
Conidiophores (10–)15–30(−45)×5–7(−8.5) μm (x = 23.8×
6.4μm, n=20), discrete, oblong to cylindrical, usually unbranched, hyaline to brown, septate, arising from basal cavity
of conidiomata. Conidiogenous cells enteroblastic, annellidic
or sympodial. Conidia (22–)24–27(−28)×10–12(−14) μm (x=
25.9×11.7μm, n=30), muriform, oblong to obovoid or ellipsoidal with rounded or obtuse ends, with truncate base, initially hyaline, becoming brown to reddish-brown or dark
brown at maturity, mostly with 3–5 transverse septa and 1–3
longitudinal septa, with several segments, smooth-walled.
Material examined: USA, Colorado. Montezuma County,
hillside near entrance to Mesa Verde National Park, on leaves
of Yucca baccata Torr. (Asparagaceae), 11 October 1992, A.
Ramaley 9237 (BPI 802381, holotype).
Notes: The monotypic genus Pleoseptum was established
by Ramaley and Barr (1995) to accommodate P. yuccaesedum.
The genus was tentatively treated in Phaeosphaeriaceae
based on its morphological characters and asexual morph
(Lumbsch and Huhndorf 2010; Zhang et al. 2012; Hyde
et al. 2013). Pleoseptum was compared with many genera
such as Chaetoplea, Curreya, Heptameria and was considered most similar to Leptosphaeria based on its peridium structure (Ramaley and Barr 1995; Zhang et al.
2012). However, these genera differ in asexual states as
in Pleoseptum conidia are dictyosporous, whereas in
Leptosphaeria, they are stated to be amerosporous (De
Gruyter et al. 2012; Hyde et al. 2013; Wijayawardene
et al. 2014b).
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Fungal Diversity (2014) 68:159–238
31 Pleoseptum yuccaesedum (BPI 802381, holotype). a
Herbarium label and specimens of Pleoseptum yuccaesedum. b
Ascomata on host surface. c Section through ascoma. d Section through
peridium. e Pseudoparaphyses. f–h Ascospores. i Ascospore stained in
Indian ink. j–l Asci. m Section through conidiomata. n Pycnidial wall. o
Conidiogenous cells. p–q Conidiogenous cells stained in congo red
reagent (p= annellidic, q= sympodial proliferation). r–u Conidia.
Scale bars: c, m=100μm, e, j, k, l=50μm, d, n, o, r, = 20μm, f, g,
h, i, p, q, s, t, u=10μm
Fig.
229
reported macroconidia from Camarosporium psoraleae
Crous & M.J. Wingf. (current name Paracamarosporium
psoraleae (Crous & M.J. Wingf.) Wijayaw. & K.D.
Hyde fide Wijayawardene et al. 2014c), hence the status
o f C a m a ro s p o r i u m y u c c a e s e d u m i s u n c e r t a i n .
Camarosporium yuccaesedum is synonymized under
Pleoseptum yuccaesedum herein.
Trematosphaeriaceae
Pleoseptum is a poorly known genus represented by only
one species in Index Fungorum (2014) that lacks molecular
sequence data in GenBank. The species has muriform spores
which are similar to Dematiopleospora (Wanasinghe et al.
2014). Pleoseptum differs from Dematiopleospora by its peridium structure which is very thick, composed of heavily
pigmented, thick-walled cells with ostiole and typical of
Pleosporaceae in the former. Whereas the peridium is thinner,
composed of lighter pigmented, thin-walled cells, with thick
periphyses in the ostioles and typical of Phaeosphaeriaceae in
Dematiopleospora. In Pleoseptum pseudoparaphyses are narrow, and additionally Pleoseptum forms a camarosporiumlike asexual state. Pleoseptum is therefore excluded for
Phaeosphaeriaceae whose genera typically have a thinwalled peridium and broad cellular pseudoparaphyses and
tentatively placed in Pleosporaceae. However, Pleoseptum
yuccaesedum needs recollecting and subjected to molecular
study to confirm this placement is correct.
Camarosporium yuccaesedum was introduced as the asexual state of Pleoseptum yuccaesedum by Ramaley and Barr
(1995) as both states co-inhabited the same host. Sexualasexual links were connected by culture comparisons with conidia produced in culture from a sexual state (Ramaley and Barr
(1995). Camarosporium however, has also been reported as the
asexual state in various genera in Botryosphaeriales and
Cucurbitariaceae (Kirk et al. 2008; Zhang et al. 2012; Hyde
et al. 2013). Recent molecular based research on
Camarosporium by Crous et al. (2014) and Wijayawardene
et al. (2014a, c, d) showed that Camarosporium sensu lato is
highly polyphyletic in Pleosporales, while Camarosporium
sensu stricto is well-established genus in Pleosporineae,
Pleosporales (Wijayawardene et al. 2014a). Thus,
Neocamarosporium Crous & M.J. Wingf. (Pleosporales
incertae sedis fide Crous et al. 2014), Paracamarosporium
Wijayaw. & K.D. Hyde (Montagnulaceae fide Wijayawardene
et al. 2014a), Pseudocamarosporium Wijayaw. & K.D. Hyde
(Montagnulaceae fide Wijayawardene et al. 2014c) and
Eucamarosporium Wijayaw. & K.D. Hyde (Didymellaceae
fide Wijayawardene et al. 2014d) have been introduced to accommodate several camarosporium-like taxa in Pleosporales.
Significantly, Ramaley and Barr (1995) reported microconidia
from Camarosporium yuccaesedum which have not been reported from Camarosporium sensu stricto (Crous et al. 2013;
Wijayawardene et al. 2014a). However, Crous et al. (2013)
For accounts of this family see Suetrong et al. (2011) and
Hyde et al. (2013).
Hadrospora Boise, Mem. N. Y. bot. Gdn 49: 310 (1989),
Faces of Fungi number: FoF00285.
Saprobic on woody or monocotyledonous hosts. Sexual
state: Ascomata scattered, solitary, immersed to semi-immersed, or erumpent through host tissue, visible as tiny, small,
black dots on the host surface, uniloculate, globose to
subglobose, glabrous, dark brown to black, ostiole central
with a minute papilla. Peridium thin-walled, composed of
black, broad pseudoparenchymatous cells, arranged in a
textura angularis. Hamathecium composed of numerous, filamentous, distinctly septate, frequently anastomosing, narrow
cellular pseudoparaphyses. Asci 8-spored, bitunicate,
fissitunicate, ovoid to ampulliform, sessile to minutely pedicellate, apically rounded, with indistinct ocular chamber.
Ascospores overlapping 1–3-seriate, phragmosporous, broadly fusiform, vermiform, brown to reddish-brown, paler at the
end cells, septate, smooth-walled. Asexual state: Unknown.
Type species: Hadrospora fallax
Phylogenetic study: None
Notes: Hadrospora was introduced to accommodate two
species, originally placed in Trematosphaeria by Boise
(1989), and was typified by Hadrospora fallax. Hadrospora
has been reported from various hosts and habitats, both terrestrial and freshwater, from Belgium, China, Italy, Japan,
Switzerland, and the United States (Boise 1989; Shearer and
Crane 1971; Fisher and Webster 1992; Webster 1993; Tanaka
and Harada 2003; Zhang et al. 2012). The genus was tentatively placed in Phaeosphaeriaceae due to its small ascomata,
thin-walled peridium and narrow pseudoparaphyses (Boise
1989; Zhang et al. 2012). However, Hadrospora differs from
other genera in Phaeosphaeriaceae by its large vermiform
ascospores, ampulliform to saccate asci, trabeculate
pseudoparaphyses and the hyphomycetous asexual morph
with the type species which was treated as an amphibious
species (Shearer 1993; Boise 1989; Tanaka and Harada 2003;
Zhang et al. 2012). Other genera of Phaeosphaeriaceae are
mostly terrestial and have cylindrical to cylindri-clavate asci
with broad cellular pseudoparaphyses and produce
coelomycetous asexual morphs. Hadrospora is similar to
Mixtura in its large ascospores, and saccate asci; although
Hardrospora has been reported as saprobic on various hosts,
230
while Mixtura was found as plant pathogen of bamboo. The
second species, Hadrospora clarkii (Sivan.) Boise is listed as
Trematosphaeria clarkii Sivan. in Index fungorum (2014).
A zalerion-like asexual morph was reported for
Hadrospora with conidia being produced on PDA after
4 months (Tanaka and Harada 2003). The genus is characterized by holoblastic, helicoid, multiseptate, brown to dark
brown, smooth-walled conidia which are constricted at the
septum (Tanaka and Harada 2003). Jones et al. (2009), however, treated Zalerion maritima as asexual morph of Lulwoana
(Lulworthiales) and introduced a new genus, Halenospora to
accommodate a non-congeneric species of Zalerion maritima.
Hardrospora is a poorly known genus which lacks sequences in GenBank. In this study, the proposal of Zhang
et al. (2012) is followed excluding the genus from
Phaeosphaeriaceae, based on its morphological characters,
and it is tentatively placed in Trematosphaeriaceae.
Hadrospora fallax (Mouton) Boise, Mem. N. Y. bot. Gdn
49: 310 (1989), Faces of Fungi number: FoF00286, Fig. 32.
≡ Trematosphaeria fallax Mouton, Bull. Soc. R. Bot. Belg.
25: 155 (1886)
Saprobic on woody hosts. Ascomata 200–350μm high,
180–400μm diam., scattered, sometimes clustered, solitary,
immersed to semi-immersed, becoming erumpent through
host tissue, visible as tiny, black dots on the host surface,
uniloculate, globose to subglobose, glabrous, dark brown to
black, ostiole central, with minute papilla, truncate at the apex.
Peridium 20–50μm wide, thick-walled, of equal thickness,
composed of several layers of black, broad pseudoparenchymatous cells, arranged in a textura angularis. Hamathecium
composed of numerous, 1–1.7μm wide, filamentous, distinctly septate, anastomosing, narrow cellular pseudoparaphyses,
embedded in mucilaginous matrix, with few asci. Asci 140–
160(−186)×(54–)60–67μm (x = 157.3×61.8μm, n=10), 8spored, bitunicate, fissitunicate, ovoid to ampulliform, sessile
to minutely pedicellate, apically rounded with indistinct ocular chamber, broad at the apex. Ascospores (50–)65–75(−80)×
(18–)21–23(−28) μm (x = 72×21.3μm, n=25), irregularly
overlapping 1–3-seriate, phragmosporous, broad fusiform,
vermiform, widest at the median cells, reddish-brown to dark
brown, with lighter end cells, 8-septate, slightly constricted at
the median septum, smooth and thick-walled.
Material examined: BELGIUM, Beaufays, on recently cut
wood, V. Mouton 245, (BR5 020009617141, holotype,
microslide); SLOVAKIA, Kal’niste (East Slovakia), on stems
of over wintered Triticum aestivum L. (Poaceae), 20 February
2009, M. Pastircak (BPI 878936).
Pleosporales, genera incertae sedis
For notes on Pleosporales, genera incertae sedis see
Hyde et al. (2013)
Fungal Diversity (2014) 68:159–238
Setophaeosphaeria Crous & Y. Zhang ter, Persoonia, Mol.
Phyl. Evol. Fungi 32: 271 (2014), Faces of Fungi number:
FOF000305.
Pathogenic on Hemerocallis fulva L. (Hemerocallidaceae).
Sexual state: Ascomata scattered, immersed to subepidermal,
uniloculate, globose, glabrous, ostiole central, somewhat
papillate. Peridium composed of 2–3 layers of brown cells
arranged in textura angularis. Hamathecium composed of
hyaline, hyphal pseudoparaphyses. Asci 8-spored, bitunicate,
narrowly ellipsoid, rostrate, short pedicellate, apically
rounded with inconspicuous ocular chamber. Ascospores
2–3-seriate, fusoid to ellipsoidal, pale brown, 5-septate,
enlarged at the second cell from apex, smooth-walled, with
guttules and mucoid caps at each end. Asexual state:
forming in culture. Conidiomata pycnidial, scattered,
erumpent with papilla, uniloculate, globose, setose, brown,
ostiole central, with round to ellipsoid papilla. Conidiomata
walls thin, composed of 2–3 layers, of pale brown cells,
arranged in textura angularis. Conidiophores reduced to
conidiogenous cells. Conidiogenous cells ampulliform, hyaline, smooth, percurrently proliferating at the apex. Conidia
subcylindrical, rounded or obtuse at the apex, base truncate,
with marginal frill, hyaline, aseptate, smooth-walled, with
guttules (from Crous et al. 2014).
Type species: Setophaeosphaeria hemerocallidis Crous &
Y. Zhang ter, Persoonia, Mol. Phyl. Evol. Fungi 32: 271
(2014).
Phylogenetic study: Crous et al. (2014).
Notes: Setophaeosphaeria was introduced by Crous et al.
(2014). The genus was established to accommodate noncongeneric species of Phaeosphaeria. Crous et al. (2014) introduced two new species, Setophaeosphaeria badalingensis
and Sp. hemerocallidis and synonymized Phaeosphaeria
setosa under the genus. Crous et al. (2014) mentioned that
Setophaeosphaeria differs from the type species of
Phaeosphaeria, Ph. oryzae, based on its asexual state.
Phaeosphaeria oryzae forms a septoria-like asexual state,
while Setophaeosphaeria species form phoma-like asexual
states (Quaedvlieg et al. 2013; Crous et al. 2014). Based on
phylogenetic analysis, the type species, Setophaeosphaeria
hemerocallidis is closely related to Phaeosphaeria setosa,
but can be distinguished by dimensions of their spores
(Crous et al. 2014). Thus, Crous et al. (2014) introduced
a new genus to accommodate these three species in
Phaeosphaeriaceae. Phylogenetic analysis of ITS and
LSU combined genes (data is not shown) indicates that
the type species, Setophaeosphaeria hemerocallidis forms a
clade outside Phaeosphaeriaceae, close to Cucurbitariaceae,
while Sp. badalingensis clusters with Phaeosphaeria sensu
stricto in Phaeosphaeriaceae. Thus, Setophaeosphaeria is
polyphyletic and excluded from Phaeosphaeriaceae and tentatively placed in Pleosporales, genera incertae sedis. The
second species, Setophaeosphaeria badalingensis may
Fungal Diversity (2014) 68:159–238
231
Fig. 32 Hadrospora fallax (BR 5020009617141, holotype). a Fruiting
bodies on host surface (BPI 878936). b Section through ascoma (BPI
878936). c Section through peridium (BPI 878936). d Pseudoparaphyses
(BPI 878936). e–g Asci (BPI 878936). h–i Ascospores (BPI 878936). j–l
Ascospores (BR5020009617141). Scale bars: B=100μm, d, e, f, g=50μm,
c, h, i, j, k, l=20μm
need to be synonymized under Phaeosphaeria based on its
phylogenetic relationships.
Lautitia danica (Berl.) S. Schatz, Can. J. Bot. 62(1): 31
(1984), Faces of Fungi number: FoF00288, Fig. 33.
≡ Leptosphaeria danica Berl., Icon. fung. (Abellini) 1(2):
87 (1892)
Biotrophic in red algae (Chondrus crispus Stackh.).
Ascostromata 600–1000μm diam., scattered, immersed to
semi-immersed, visible as raised, black circular or irregular
regions on the host surface. Locules 180–240μm high, 170–
270μm diam., uni to multi-loculate under pseudoclypeus,
globose to subglobose, glabrous, pale brown, ostiole central,
with pore-like opening. Peridium 10–22 μm wide, thinwalled, of unequal thickness, slightly thickened at the base,
composed of several layers of prosenchymatous cells, arranged in textura epidermoidea at the apex and sides, with
subhyaline to pale brown cells of textura porrecta at the base.
Dothideomycetes, genera incertae sedis
One-hundred and sixteen genera are listed as genera incertae
sedis in the class Dothideomycetes in Lumbsch and Huhndorf
(2010) and updated to 322 genera in Wijayawardene et al.
(2014b), as this included asexual genera. Lautitia previously
placed in Phaeosphaeriaceae were also added here.
Lautitia S. Schatz, Can. J. Bot. 62(1): 31 (1984), Faces of
Fungi number: FoF00287. Type species: Lautitia danica.
Phylogenetic study: None.
232
Fig. 33 Lautitia danica (NY 01390859). a Herbarium label and specimens of Lautitia danica. b Ascostromata on host tissue. c Section through
ascostroma. d Section through peridium stained in congo red. e Asci with
Fungal Diversity (2014) 68:159–238
pseudoparaphyses strained in congo red. f–h Asci. i–j Asci stained in
congo red. k–n Ascospores. o Ascospore stained in Indian ink. Scale bars:
c=100μm, d, e=20μm, f–j=10μm, = 20μm
Fungal Diversity (2014) 68:159–238
Hamathecium composed of numerous, 1–1.5μm wide, filamentous, anastomosing, rough-walled, narrow cellular
pseudoparaphyses, with distinct septa, embedded in a mucilaginous matrix. Asci (57–)70–90(−104)×(12–)15–18(−20)
μm (x = 78.8×15.9μm, n=25), 8-spored, bitunicate, clavate,
long pedicellate, apically rounded to truncate, with an indistinct ocular chamber. Ascospores (31–)35–40(−42)×5–7μm
(x = 35.9×5.8μm, n=30), overlapping 1–3-seriate, 2-celled,
obclavate with narrow upper cell, mostly the upper cell longer
than the lower cell, hyaline, 1-septate, slightly constricted at
the septum, rough-walled with appendage on upper cell.
Material examined: FRANCE, Belclem near Roscoff,
Finistère (Atlantic Ocean), on Chondrus crispus
(Gigartinaceae), 5 October 1971 J. Kohlmeyer no. 2920
(NY 01390859); USA, Massachusetts, Gloucester, Halibus
Point, 2 m deep, on Chondrus crispus, 28 September
1980, Kate van den Bosch; ibid. Rhode Island, Watch
Hill Lighthouse (Atlantic Ocean), on Laminaria, 20
August 1966, J. Kohlmeyer_no. 1988 (NY 01390747);
no. 1988a, (NY 01389139); Slide Box 15, Tray 20, S.
Schatz (NY 01319510–NY 01319526).
Notes: The monotypic genus Lautitia was introduced by
Schatz (1984) as typified by L. danica and placed in
Dothideomycetes (Schatz 1984). A detailed description and
taxonomic history were given by Wilson and Knoyle (1961)
who treated the species then named Didymosphaeria danica
(Schatz 1984). Berlese (1892) considered the species as a
Leptosphaeria based on its hyaline, 1-septate, immature ascospores. Lind (1913) transferred the species to Didymosphaeria
as D. marina (Rostrup) Lind, due to the ascospores turning
brown and being 1-septate at maturity.Wilson and Knoyle
(1961) could not find brown ascospores, but retained the
species in Didymosphaeria. Schatz (1984) disagreed with
Wilson and Knoyle (1961) as the species has cellular
pseudoparaphyses, while genera in Didymosphaeria have trabeculate pseudoparaphyses. Thus Schatz (1984) designated a
new genus, Lautitia, to accommodate the taxon. Schatz (1984)
treated Lautitia as a member Phaeosphaeriaceae due to its
pseudoparenchymatous to prosenchymatous peridium, and
elongate, hyaline asymmetric ascospores. The genus was
accepted in Phaeosphaeriaceae by Zhang et al. (2012) and
Hyde et al. (2013).
In this study, we exclude Lautitia from Phaeaosphaeriaceae
based on its morphology. Lautitia can be distingiushed
from other genera in Phaeosphaeriaceae which differ in
peridium structure, asci and ascospores. Lautitia has
prosenchymatous perdial cells, clavate asci with long pedicels, and asymmetric didymosporous ascospores, while
other genera in Phaeoaperiaceae have pseudoparenchymatous peridial cells, cylindrical to cylindric-clavate asci which
are subsessile to short pedicellate, and phragmosporous,
scolecosporous or muriform ascospores (Zhang et al.
2009, 2012; Hyde et al. 2013). It is difficult to place this
233
species in any family or order any thus we refer it to
Dothideomycetes, genera incertae sedis.
Acknowledgments The Royal Golden Jubilee Ph. D. Program (PHD/
0090/2551) under Thailand Research Fund, Humidtropics, a CGIAR
Research Program that aims to develop new opportunities for improved
livelihoods in a sustainable environment and Mae Fah Luang University
(grant for study Dothideomycetes No. 56101020032) are gratefully
thanked for partially funding this work. KD Hyde acknowledges The
Chinese Academy of Sciences, project number 2013T2S0030, for the
award of Visiting Professorship for Senior International Scientists at
Kunming Institute of Botany. Wen Jing Li and International Fungal
Research & Development Centre, Research Institute of Resource Insects,
Chinese Academy of Forestry; Ruvishika S. Jayawardena and Institute of
Plant and Environment Protection, Beijing Academy of Agriculture and
Forestry Sciences; Jun-Bo Yang and Plant Germplasm and Genomics
Center in Germplasm Bank of Wild Species, Kunming Institute of Botany
are gratefully thanked for the molecular laboratory support. The curators
from BPI, BR, NY, S, and UB herbaria are gratefully thanked for loaning
specimens and type information. Amy Y. Rossman, Chatsachee
Chatpapamon, Dhanushka N. Wanasinghe, Dhanushka Udayanga, E. B.
Gareth Jones, Joanne E. Taylor, Saowanee Wikee, Saranyaphat Boonme
and Supalak Yacharoen are gratefully thanked for taxonomic literature
information, cultures preparation and general assistance.
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