StudieS in Mycology 75: 307–390.
Sizing up Septoria
W. Quaedvlieg1,2, G.J.M. Verkley1, H.-D. Shin3, R.W. Barreto4, A.C. Alfenas4, W.J. Swart5, J.Z. Groenewald1, and P.W. Crous1,2,6*
1
CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; 2Wageningen University and Research Centre (WUR), Laboratory of Phytopathology,
Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands; 3Utrecht University, Department of Biology, Microbiology, Padualaan 8, 3584 CH Utrecht, The Netherlands;
2
Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands; 3Division of Environmental Science and Ecological Engineering,
Korea University, Seoul 136-701, Korea; 4Departamento de Fitopatologia, Universidade Federal de Viçosa, 36750 Viçosa, Minas Gerais, Brazil; 5Department of Plant
Sciences, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa; 6Wageningen University and Research Centre (WUR), Laboratory of Phytopathology,
Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
*Correspondence: Pedro W. Crous, p.crous@cbs.knaw.nl
Studies in Mycology
Abstract: Septoria represents a genus of plant pathogenic fungi with a wide geographic distribution, commonly associated with leaf spots and stem cankers of a broad range of
plant hosts. A major aim of this study was to resolve the phylogenetic generic limits of Septoria, Stagonospora, and other related genera such as Sphaerulina, Phaeosphaeria and
Phaeoseptoria using sequences of the the partial 28S nuclear ribosomal RNA and RPB2 genes of a large set of isolates. Based on these results Septoria is shown to be a distinct
genus in the Mycosphaerellaceae, which has mycosphaerella-like sexual morphs. Several septoria-like species are now accommodated in Sphaerulina, a genus previously linked to
this complex. Phaeosphaeria (based on P. oryzae) is shown to be congeneric with Phaeoseptoria (based on P. papayae), which is reduced to synonymy under the former. Depazea
nodorum (causal agent of nodorum blotch of cereals) and Septoria avenae (causal agent of avenae blotch of barley and rye) are placed in a new genus, Parastagonospora, which
is shown to be distinct from Stagonospora (based on S. paludosa) and Phaeosphaeria. Partial nucleotide sequence data for ive gene loci, ITS, LSU, EF-1α, RPB2 and Btub were
generated for all of these isolates. A total of 47 clades or genera were resolved, leading to the introduction of 14 new genera, 36 new species, and 19 new combinations.
Key words: Capnodiales, Multi-Locus Sequence Typing (MLST), Mycosphaerella, Mycosphaerellaceae, Phaeoseptoria, Phaeosphaeria, Phaeosphaeriaceae, Pleosporales,
Septoria, Sphaerulina, Stagonospora, systematics.
Taxonomic novelties: New genera – Acicuseptoria Quaedvlieg, Verkley & Crous, Cylindroseptoria Quaedvlieg, Verkley & Crous, Kirstenboschia Quaedvlieg, Verkley & Crous,
Neoseptoria Quaedvlieg, Verkley & Crous, Neostagonospora Quaedvlieg, Verkley & Crous, Parastagonospora Quaedvlieg, Verkley & Crous, Polyphialoseptoria Quaedvlieg, R.W.
Barreto, Verkley & Crous, Ruptoseptoria Quaedvlieg, Verkley & Crous, Septorioides Quaedvlieg, Verkley & Crous, Setoseptoria Quaedvlieg, Verkley & Crous, Stromatoseptoria
Quaedvlieg, Verkley & Crous, Vrystaatia Quaedvlieg, W.J. Swart, Verkley & Crous, Xenobotryosphaeria Quaedvlieg, Verkley & Crous, Xenoseptoria Quaedvlieg, H.D. Shin, Verkley
& Crous. New species – Acicuseptoria rumicis Quaedvlieg, Verkley & Crous, Caryophylloseptoria pseudolychnidis Quaedvlieg, H.D. Shin, Verkley & Crous, Coniothyrium sidae
Quaedvlieg, Verkley, R.W. Barreto & Crous, Corynespora leucadendri Quaedvlieg, Verkley & Crous, Cylindroseptoria ceratoniae Quaedvlieg, Verkley & Crous, Cylindroseptoria
pistaciae Quaedvlieg, Verkley & Crous, Kirstenboschia diospyri Quaedvlieg, Verkley & Crous, Neoseptoria caricis Quaedvlieg, Verkley & Crous, Neostagonospora caricis
Quaedvlieg, Verkley & Crous, Neostagonospora elegiae Quaedvlieg, Verkley & Crous, Paraphoma dioscoreae Quaedvlieg, H.D. Shin, Verkley & Crous, Parastagonospora
caricis Quaedvlieg, Verkley & Crous, Parastagonospora poae Quaedvlieg, Verkley & Crous, Phlyctema vincetoxici Quaedvlieg, Verkley & Crous, Polyphialoseptoria tabebuiaeserratifoliae Quaedvlieg, Alfenas & Crous, Polyphialoseptoria terminaliae Quaedvlieg, R.W. Barreto, Verkley & Crous, Pseudoseptoria collariana Quaedvlieg, Verkley & Crous,
Pseudoseptoria obscura Quaedvlieg, Verkley & Crous, Sclerostagonospora phragmiticola Quaedvlieg, Verkley & Crous, Septoria cretae Quaedvlieg, Verkley & Crous, Septoria
glycinicola Quaedvlieg, H.D. Shin, Verkley & Crous, Septoria oenanthicola Quaedvlieg, H.D. Shin, Verkley & Crous, Septoria pseudonapelli Quaedvlieg, H.D. Shin, Verkley & Crous,
Setophoma chromolaenae Quaedvlieg, Verkley, R.W. Barreto & Crous, Setoseptoria phragmitis Quaedvlieg, Verkley & Crous, Sphaerulina amelanchier Quaedvlieg, Verkley &
Crous, Sphaerulina pseudovirgaureae Quaedvlieg, Verkley & Crous, Sphaerulina viciae Quaedvlieg, H.D. Shin, Verkley & Crous, Stagonospora duoseptata Quaedvlieg, Verkley
& Crous, Stagonospora perfecta Quaedvlieg, Verkley & Crous, Stagonospora pseudocaricis Quaedvlieg, Verkley, Gardiennet & Crous, Stagonospora pseudovitensis Quaedvlieg,
Verkley & Crous, Stagonospora uniseptata Quaedvlieg, Verkley & Crous, Vrystaatia aloeicola Quaedvlieg, Verkley, W.J. Swart & Crous, Xenobotryosphaeria calamagrostidis
Quaedvlieg, Verkley & Crous, Xenoseptoria neosaccardoi Quaedvlieg, H.D. Shin, Verkley & Crous. New combinations – Parastagonospora avenae (A.B. Frank) Quaedvlieg,
Verkley & Crous, Parastagonospora nodorum (Berk.) Quaedvlieg, Verkley & Crous, Phaeosphaeria papayae (Speg.) Quaedvlieg, Verkley & Crous, Pseudocercospora domingensis
(Petr. & Cif.) Quaedvlieg, Verkley & Crous, Ruptoseptoria unedonis (Roberge ex Desm.) Quaedvlieg, Verkley & Crous, Septorioides pini-thunbergii (S. Kaneko) Quaedvlieg, Verkley
& Crous, Sphaerulina abeliceae (Hiray.) Quaedvlieg, Verkley & Crous, Sphaerulina azaleae (Voglino) Quaedvlieg, Verkley & Crous, Sphaerulina berberidis (Niessl) Quaedvlieg,
Verkley & Crous, Sphaerulina betulae (Pass.) Quaedvlieg, Verkley & Crous, Sphaerulina cercidis (Fr.) Quaedvlieg, Verkley & Crous, Sphaerulina menispermi (Thüm.) Quaedvlieg,
Verkley & Crous, Sphaerulina musiva (Peck) Quaedvlieg, Verkley & Crous, Sphaerulina oxyacanthae (Kunze & J.C. Schmidt) Quaedvlieg, Verkley & Crous, Sphaerulina patriniae
(Miura) Quaedvlieg, Verkley & Crous, Sphaerulina populicola (Peck) Quaedvlieg, Verkley & Crous, Sphaerulina quercicola (Desm.) Quaedvlieg, Verkley & Crous, Sphaerulina
rhabdoclinis (Butin) Quaedvlieg, Verkley & Crous, Stromatoseptoria castaneicola (Desm.) Quaedvlieg, Verkley & Crous. Typiications: Epitypiications – Phaeosphaeria oryzae I.
Miyake, Phaeoseptoria papayae Speg.; Neotypiication – Hendersonia paludosa Sacc. & Speg.
doi:10.3114/sim0017. Hard copy: June 2013.
INTroducTIoN
Fungal species belonging to Septoria are among the most common
and widespread leaf-spotting fungi worldwide. Septoria Sacc.
(Mycosphaerella, Capnodiales, Dothideomycetes) is based on
Septoria cytisi, which was irst described by Desmazières (1847)
as a pathogen of Cytisus laburnum (= Laburnum anagyroides).
The genus Septoria is extremely large, and during the past 150
years more than 2000 taxa have been ascribed to this asexual
genus (Verkley & Priest 2000, Verkley et al. 2004). Presently,
Septoria s.lat. represents a polyphyletic assembly of genera that
cluster mostly in the Mycosphaerellaceae (a family incorporating
many plant pathogenic coelomycetes), although fungi with
septoria-like morphology have also evolved outside this family
Copyright CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
You are free to share - to copy, distribute and transmit the work, under the following conditions:
Attribution:
You must attribute the work in the manner speciied by the author or licensor (but not in any way that suggests that they endorse you or your use of the work).
Non-commercial:
You may not use this work for commercial purposes.
No derivative works: You may not alter, transform, or build upon this work.
For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get
permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights.
307
Quaedvlieg et al.
(Crous et al. 2009a, c). Although many species of Septoria have
mycosphaerella-like sexual states, the name Mycosphaerella does
not apply to them, and should not be used in this context.
Following a proposal accepted by the International Code of
Nomenclature for algae, fungi and plants (ICN), the generic name
Septoria Sacc. was conserved over the older synonym Septaria
Fr. (original spelling). The arguments preceding the typiication
of Septoria and subsequent proposals for name conservation
by Wakeield (1940), Rogers (1949) and Donk (1964) between
Septoria sensu Saccardo or Septaria Fries were various. In the
end the committee for fungi appointed by the ICN followed the
recommendation of Donk (1964), and decided on Septoria Sacc.
over Septaria Fr., arguing that Septoria Sacc. had already been in
prevalent use for many years, and should therefore be accepted as
the correct name.
After examining several herbarium specimens of S. cytisi, Sutton
(1980) circumscribed Septoria as follows: Mycelium immersed,
branched, septate, pale brown. Conidiomata pycnidial, immersed,
separate or aggregated (but not conluent), globose, papillate (or
not), brown, thin-walled of pale brown textura angularis, often with
a smaller-celled inner layer, somewhat darker and more thickwalled around the ostiole. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells holoblastic, either determinate or
indeterminate, with a limited number of sympodial proliferations.
Each locus has a broad, lat, unthickened scar, discrete, hyaline,
smooth, ampulliform, doliiform or lageniform to short cylindrical.
Conidia hyaline, multiseptate, iliform, smooth and either continuous
or constricted at septa. Later work by Constantinescu (1984),
Sutton & Pascoe (1987, 1989) and Farr (1991, 1992) augmented
Sutton’s previous generic circumscription by also including species
with sympodial, enteroblastic and percurrent conidial proliferation.
Furthermore, based on similarities in conidiomatal development,
von Arx (1983) and Braun (1995) adopted an even wider concept of
Septoria that included the acervular forms normally accommodated
in Phloeospora.
Morphological traits in Septoria are generally conserved,
and speciic morphological characters by which to describe and
identify Septoria and septoria-like species are limited. This lack
of speciic morphological characters caused Septoria taxonomy
to be largely dependent on associated host data, leading to many
of the described species only being identiiable by host plant, and
by variation in informative supplementary characters like conidial
length, width and septation (Jørstad 1965, 1967, Sutton 1980). Of
these supplementary characters, conidial width appears to be the
most stable (i.e. it shows the least amount of intraspeciic variation)
and in most Septoria species, intraspeciic conidial width rarely
varies more than 1 μm (Priest 2006).
This reliance on host data in Septoria taxonomy is far from
perfect, and should be avoided for identiication purposes (see
Verkley et al. 2013, this volume). Extensive host inoculation
experiments by Beach (1919) and Teterevnikova-Babayan (1987)
have shown that identiication of Septoria spp. by host speciicity
alone is error prone because many Septoria species are not
restricted to a single speciic host (i.e. several taxa have broader
host ranges). Septoria species like S. lactucicola and S. lycopersici
can not only infect multiple plant species within the same genus,
but can also infect plants belonging to closely allied families and
genera. In contrast to this, morphologically well distinguishable
Septoria species can also parasitise the same hosts (e.g. multiple
distinct Septoria species can be found on both Chrysanthemum
and Rubus hosts) (Demaree & Wilcox 1943, Punithalingam
1976, Shin & Sameva 2004). Because host speciicity has been
308
one of the main criteria used for describing new, morphologically
indistinguishable Septoria species over the past 150 years, one
can expect that a certain number of described taxa are in fact
synonyms of species from related hosts.
Septoria and septoria-like genera in the molecular
era
Although it had previously been speculated by Sutton (1980) that
Septoria was in fact polyphyletic, deinitive proof of this hypothesis
awaited the introduction of molecular techniques. Cunfer & Ueng
(1999) were the irst to use rDNA sequence data of the internal
transcribed spacer region (ITS) to postulate that Zymoseptoria tritici
(then known as Septoria tritici) and several Stagonospora spp. (a
morphologically similar genus, previously linked to Septoria) actually
belonged to two distinct genera. Verkley et al. (2004) extended this
study by employing a combination of 28S nrDNA (LSU) and ITS
data to prove that Septoria was in fact both poly- and paraphyletic.
Their work showed that septoria-like species such as Z. tritici and
Z. passerinii were more closely related to Ramularia than to the
majority of the other Septoria species used in their datasets.
Feau et al. (2006) were the irst to use a multi-locus polyphasic
sequencing approach to reliably identify Septoria spp. Besides ITS
and LSU sequence data, they also used β-tubulin (Btub) sequence
data to separate closely related species into distinct monophyletic
groups that frequently correlated with their respective host
families. These results supported the approach of using multi-gene
sequence data for studying a large collection of Septoria strains at
species level.
Septoria s. str. was inally demarcated when Quaedvlieg et
al. (2011) managed to obtain both ITS and LSU sequence data
from S. cytisi herbarium specimens. Phylogenetic analysis of the
obtained S. cytisi LSU sequence data clearly proved that Z. tritici
and Z. passerinii [as previously indicated by Cunfer & Ueng (1999)
and Verkley et al. (2004)] did not belong to Septoria s. str., but in
fact belonged to a separate genus, closely related to Ramularia.
These two species were subsequently split off from Septoria and
placed in a new genus, Zymoseptoria (named for the yeast-like
state produced in culture). Since the initial Zymoseptoria paper, ive
additional species from members of Poaceae have been described
in this genus (Crous et al. 2012a, Stukenbrock et al. 2012).
Septoria-like asexual genera
Since the description of Septoria by Desmazières (1847), several
additional septoria-like genera (pycnidial/acervular/stromatic
conidioma with iliform conidia) have been described which could
be mistaken for Septoria s. str.
The two economically most important septoria-like genera are
probably Zymoseptoria (sexual morph mycosphaerella-like) and
Parastagonospora (sexual morph phaeosphaeria-like; see below).
Both of these genera are pathogenic on Poaceae (grasses) and are
directly or indirectly responsible for signiicant annual crop losses
worldwide on cereals such as barley and wheat (Eyal et al. 1987).
Quaedvlieg et al. (2011) determined that Zymoseptoria formed a
distinct clade in the Mycosphaerellaceae, while Stagonospora was
found to cluster in the Phaeosphaeriaceae within the Pleosporales,
near other genera like Phoma and Phaeosphaeria (Cunfer &
Ueng 1999, Solomon et al. 2006) which contain important plant
pathogens. However, besides Zymoseptoria and Parastagonospora
there are many other, lesser-known septoria-like genera awaiting
Sizing up Septoria
elucidation. The goal of the present study is therefore to conduct an
in-depth morphological and molecular analysis of these septorialike genera, and resolve the afinities of Stagonospora and its
purported sexual morph, Phaeosphaeria. To this end a collection of
370 Septoria and septoria-like isolates (Table 1) were subjected to
morphological examination and multi-gene DNA analyses.
MaTErials aNd METhods
Isolates
Symptomatic leaves were incubated in moist chambers for up
to 1 wk to enhance sporulation before single conidial colonies
were established on 2 % malt extract agar (MEA) (Crous et al.
2009d). Leaf spots bearing ascomata were soaked in water for
approximately 2 h, after which they were attached to the inner
surface of Petri dish lids over plates containing MEA. Ascospore
germination patterns were examined after 24 h, and single
ascospore cultures established as described previously (Crous et
al. 1991, Crous 1998). Colonies were sub-cultured onto synthetic
nutrient-poor agar (SNA) containing sterile Hordeum vulgare
(barley) and Urtica dioica (stinging nettle) stems, potato-dextrose
agar (PDA), oatmeal agar (OA), and MEA (Crous et al. 2009d),
and incubated at 25 °C under continuous near-ultraviolet light to
promote sporulation. Isolates were also obtained from the culture
collections of the CBS-KNAW Fungal Biodiversity Centre (CBS)
in Utrecht, and the working collection of Pedro Crous (CPC).
Reference strains were deposited CBS (Table 1).
dNa extraction, ampliication and sequencing
Genomic DNA was extracted from fungal mycelium growing on
MEA, using the UltraClean® Microbial DNA Isolation Kit (Mo Bio
Laboratories, Inc., Solana Beach, CA, USA). Strains (Table 1) were
screened for ive loci (β-tubulin (Btub), internal transcribed spacer
(ITS), Translation elongation factor 1-alpha (EF-1α) 28S nrDNA
(LSU) and RNA polymerase II second largest subunit (RPB2) using
the primer sets listed in Table 2. The PCR ampliications were
performed in a total volume of 12.5 µL solution containing 10–20
ng of template DNA, 1 × PCR buffer, 0.7 µL DMSO (99.9 %), 2 mM
MgCl2, 0.4 µM of each primer, 25 µM of each dNTP and 1.0 U Taq
DNA polymerase (GoTaq, Promega). PCR ampliication conditions
were set as follows: an initial denaturation temperature of 96 °C
for 2 min, followed by 40 cycles of denaturation temperature of 96
°C for 45 s, primer annealing at the temperature stipulated in Table
2, primer extension at 72 °C for 90 s and a inal extension step at
72 °C for 2 min. The resulting fragments were sequenced using the
PCR primers together with a BigDye Terminator Cycle Sequencing
Kit v. 3.1 (Applied Biosystems, Foster City, CA). Sequencing
reactions were performed as described by Cheewangkoon et al.
(2008). All novel sequences were deposited in NCBI’s GenBank
database and alignments and phylogenetic trees in TreeBASE.
Phylogenetic analyses
A basic alignment of the obtained sequence data was irst done
using MAFFT v. 7 [(http://mafft.cbrc.jp/alignment /server/index. html)
(Katoh et al. 2002)] and if necessary, manually improved in BioEdit
v. 7.0.5.2 (Hall 1999). To check the congruency of the RPB2 and
LSU dataset, a 70 % neighbour-joining (NJ) reciprocal bootstrap
www.studiesinmycology.org
method with maximum likelihood distance was performed (MasonGamer & Kellogg 1996, Lombard et al. 2010). Bayesian analyses
(critical value for the topological convergence diagnostic set to
0.01) were performed on the concatenated loci using MrBayes
v. 3.2.1 (Huelsenbeck & Ronquist 2001) as described by Crous
et al. (2006) using nucleotide substitution models that were
selected using MrModeltest v.2.3 (Table 3) (Nylander 2004). In
order to keep the trees manageable for publication, two separate
Bayesian trees were run. The irst tree was run with all the Septoria
and septoria-like isolates that either belonged to, or where more
closely related to the Mycosphaerellaceae (Fig. 1) while the second
tree contained all the septoria-like isolates either belonging to, or
being more closely related to the Phaeosphaeriaceae (Fig. 2).
Parastagonospora nodorum (CBS 259.49) was used as outgroup
for the Mycosphaerellaceae dataset, while Dothistroma pini (CBS
121005) was used as outgroup for the Phaeosphaeriaceae dataset.
As the novel genera and species described in this study were
already clearly distinquishable in the LSU/RPB2 trees, the ITS,
EF-1α and Btub sequence data of these isolates were deposited
in GenBank without their subsequent trees being published in this
paper.
Taxonomy
Taxonomic descriptions were based on isolates sporulating in
culture. Diseased leaf tissue was viewed under a Zeiss V20
Discovery stereo-microscope, while a Zeiss Axio Imager 2 light
microscope with differential interference contrast (DIC) illumination
and an AxioCam MRc5 camera with Zen software was used to
capture morphological structures. Adobe Photoshop CS3 was
used for the inal editing of acquired images and photographic
preparations. For measurements, 30–50 replicates of all relevant
morphological features were made at ×1000 magniication. Colony
characters and pigment production were noted after 2–4 wk of
growth on MEA, PDA and OA (Crous et al. 2009d) incubated at
25 ºC in the dark. Colony colours (surface and reverse) were rated
according to the colour charts of Rayner (1970).
rEsulTs
dNa sequencing and phylogenetic analysis
The RPB2 and LSU sequence datasets did not show any conicts
in both the Mycosphaerellaceae and Phaeosphaeriaceae tree
topologies for the 70 % reciprocal bootstrap trees, allowing us to
combine them in the multigene analyses. For the Mycosphaerellaceae
tree, the gene boundaries were: 1–327 bp for RPB2 and 332–1120
bp for LSU. For the Phaeosphaeriaceae tree (Fig. 2), the gene
boundaries were 1–777 bp for LSU and 782–1108 bp for RPB2.
During the generation of the Mycosphaerellaceae tree (Fig. 1), a total
of 57 048 trees were sampled out of the generated 76 062 trees (75
%). During the generation of the Phaeosphaeriaceae tree (Fig. 2),
a total of 2844 trees were sampled out of the generated 3792 trees
(75 %).
Taxonomy
A total of 347 isolates representing 170 species were subjected to
DNA analysis and morphological comparison. Phylogenetic analyses
based on the LSU and RPB2 genes resolved a total of 47 clades of
309
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Acicuseptoria rumicis
CBS 522.78
Rumex alpinus
France
H.A. van der Aa
KF253105
KF252643
KF252153
KF251648
KF251144
Boeremia telephii
CBS 135415; S670
Lavatera thuringiaca
Germany
U. Damm
–
KF252644
KF252154
KF251649
KF251145
Caryophylloseptoria lychnidis
CBS 109098
Silene pratensis
Austria
G.J.M. Verkley
KF253234
KF252768
KF252292
KF251790
KF251286
CBS 109099
Silene pratensis
Austria
G.J.M. Verkley
KF253235
KF252769
KF252293
KF251791
KF251287
CBS 109101
Silene pratensis
Austria
G.J.M. Verkley
KF253236
KF252770
KF252294
KF251792
KF251288
CBS 109102
Silene pratensis
Austria
G.J.M. Verkley
KF253237
KF252771
KF252295
KF251793
KF251289
CBS 128614
Lychnis cognata
South Korea
H.D. Shin
KF253238
KF252772
KF252296
KF251794
KF251290
CBS 128630
Lychnis cognata
South Korea
H.D. Shin
KF253239
KF252773
KF252297
KF251795
KF251291
CBS 109100
Silene nutans
Austria
G.J.M. Verkley
KF253240
KF252774
KF252298
KF251796
KF251292
CBS 109103
Silene pratensis
Austria
G.J.M. Verkley
KF253241
KF252775
KF252299
KF251797
KF251293
CBS 397.52
Dianthus caryophyllus
Netherlands
Schouten
KF253243
KF252777
KF252301
KF251799
KF251295
CBS 109010
Spergula morisonii
Netherlands
A. Aptroot
KF253242
KF252776
KF252300
KF251798
KF251294
Cercospora beticola
CBS 124.31; CPC 5070
Beta vulgaris
Romania
–
KF253106
KF252645
KF252155
KF251650
KF251146
Cer. capsici
CBS 118712
–
Fiji
P. Tyler
KF253244
KF252778
KF252302
KF251800
KF251296
Cer. zebrina
CBS 137.56
Hedysarum coronarium
Italy
M. Ribaldi
KF253245
KF252779
KF252303
KF251801
KF251297
CBS 118790; IMI 262766
Trifolium subterraneum
Australia
M.J. Barbetti
KF253107
KF252646
KF252156
KF251651
KF251147
Chaetosphaeronema hispidulum
CBS 216.75
Anthyllis vulneraria
Germany
R. Schneider
KF253108
KF252647
KF252157
KF251652
KF251148
Coniothyrium carteri
CBS 105.91
Quercus robur
Germany
H. Schill
KF253165
KF252700
KF252214
KF251712
KF251209
Car. pseudolychnidis
Car. silenes
Car. spergulae
GenBank accession no.2
CBS 101633
Quercus sp.
Netherlands
–
KF253166
KF252701
KF252215
KF251713
KF251210
Con. glycinicola
CBS 124141
Glycine max
Zimbabwe
C. Lavy
KF253167
KF252702
KF252216
KF251714
KF251211
Con. sidae
CBS 135108; CPC 19602
Sida sp.
Brazil
R.W. Barreto
KF253109
KF252648
KF252158
KF251653
KF251149
Corynespora leucadendri
CBS 135133; CPC 19345
Leucadendron sp.
South Africa
S. Lee
KF253110
KF252639
KF252159
KF251654
KF251150
Cylindroseptoria ceratoniae
CBS 477.69
Ceratonia siliqua
Spain
H.A. van der Aa
KF253111
KF252649
KF252160
KF251655
KF251151
Cyl. pistaciae
CBS 471.69
Pistacia lentiscus
Spain
H.A. van der Aa
KF253112
KF252650
KF252161
KF251656
KF251152
Cytostagonospora martiniana
CBS 135102; CPC 17727
Acacia pycnantha
Australia
P.W. Crous
KF253113
KF252651
KF252162
KF251657
KF251153
Dissoconium commune
CPC 12397
Eucalyptus globulus
Australia
I. Smith
KF253190
KF252724
KF252242
KF251740
KF251237
Dothistroma pini
CBS 116484
Pinus nigra
USA
G. Adams
JX901622
JX902193
JX901948
JX901824
JX901736
CBS 116485
Pinus nigra
USA
G. Adams
JX901625
JX902196
JX901951
JX901827
JX901739
CBS 116487
Pinus nigra
USA
G. Adams
JX901620
JX902191
JX901946
JX901822
GU214532
CBS 121005
Pinus pallasiana
Russia
T. S. Bulgakov
KF253115
KF252653
–
KF251659
KF251155
CBS 121011
Pinus pallasiana
Russia
A.C. Usichenko
KF253250
–
KF252307
KF251806
KF251302
CBS 383.74
Pinus coulteri
France
M. Morelet
KF253251
–
KF252308
KF251807
KF251303
Dot. septosporum
Quaedvlieg et al.
310
Table 1. Collection details and GenBank accession numbers of isolates included in this study.
Table 1. (Continued).
www.studiesinmycology.org
Species
Isolate no.1
host
location
GenBank accession no.2
collector
EF-1α
Btub
rPB2
lsu
ITS
CPC 16798
Pinus mugo ‘Rostrata’
Netherlands
W. Quaedvlieg
JX901627
JX902198
JX901953
JX901829
JX901741
CPC 16799
Pinus mugo
Netherlands
W. Quaedvlieg
JX901628
JX902199
JX901954
JX901830
JX901742
CBS 134911; CPC 19869
Diospyros whyteana
South Africa
P.W. Crous
KF253116
KF252640
KF252164
KF251660
KF251156
CPC 19870
Diospyros whyteana
South Africa
P.W. Crous
KF253117
KF252641
KF252165
KF251661
KF251157
CBS 322.33
–
–
P.V. Siggers
JX901639
JX902213
JX901968
JX901844
JX901755
CBS 133791
Pinus strobus
USA
B. Ostrofsky
KC013002
KC013008
KC013014
KC013017
KC012999
Lec. brevispora
CBS 133601
Pinus sp.
Mexico
J.Y. Morales
JX901649
JX902224
JX901979
JX901855
JX901763
Lec. guatamalensis
IMI 281598
Pinus oocarpa
Guatemala
H.C. Evans
JX901650
JX902225
JX901980
JX901856
JX901764
Lec. longispora
CBS 133602
Pinus sp.
Mexico
J.Y. Morales
JX901651
JX902227
JX901982
JX901858
JX901766
Leptosphaeria albopunctata
CBS 254.64
Spartina alternilora
USA
J. Kohlmeyer
KF253118
KF252654
KF252166
KF251662
KF251158
Mycosphaerella brassicicola
CBS 228.32
Brassica oleracea
Denmark
C.A. Jörgensen
KF253252
KF252783
KF252309
KF251808
KF251304
CBS 267.53
Brassica oleracea
Netherlands
F. Quak
KF253253
KF252784
KF252310
KF251809
KF251305
Mycosphaerella sp.
CBS 135464; CPC 11677
Draba nemorosa var.
hebecarpa
South Korea
H.D. Shin
–
KF252786
KF252312
KF251811
KF251307
Neoseptoria caricis
CBS 135097; S653
Carex acutiformis
Netherlands
W. Quaedvlieg
–
–
KF252167
KF251663
KF251159
Neosetophoma samarorum
CBS 138.96
Phlox paniculata
Netherlands
–
KF253119
KF252655
KF252168
KF251664
KF251160
CBS 139.96
Poa sp.
Netherlands
–
KF253120
KF252656
KF252169
KF251665
KF251161
CBS 568.94
Urtica dioica
Netherlands
G.J.M. Verkley
KF253121
KF252657
KF252170
KF251666
KF251162
Neostagonospora caricis
CBS 135092; S616
Carex acutiformis
Netherlands
W. Quaedvlieg
–
KF252658
KF252171
KF251667
KF251163
Neost. elegiae
CBS 135101; CPC 16977
Elegia cuspidata
South Africa
S. Lee
KF253122
KF252659
KF252172
KF251668
KF251164
Paraphoma chrysanthemicola
CBS 172.70
Chrysanthemum morifolium
Netherlands
R. Schneider
KF253123
KF252660
KF252173
KF251669
KF251165
CBS 522.66
Chrysanthemum morifolium
UK
–
KF253124
KF252661
KF252174
KF251670
KF251166
CBS 135100; CPC 11357
Dioscorea tokoro
South Korea
H.D. Shin
KF253125
KF252662
KF252175
KF251671
KF251167
KF251168
Kirstenboschia diospyri
Lecanosticta acicola
Parap. dioscoreae
Parap. imeti
Parap. radicina
Paras. caricis
311
Dioscorea tokoro
South Korea
H.D. Shin
KF253126
KF252663
KF252176
CPC 11361
Dioscorea tokoro
South Korea
H.D. Shin
KF253127
KF252664
KF252177
KF251673
KF251169
CBS 170.70
Apium graveolens
Netherlands
M.A. de Waard
KF253128
KF252665
KF252178
KF251674
KF251170
CBS 368.91
Juniperus communis
Switzerland
–
KF253129
KF252666
KF252179
KF251675
KF251171
CBS 111.79
Malus sylvestris
Netherlands
G.H. Boerema
KF253130
KF252667
KF252180
KF251676
KF251172
CBS 102875
Lycopersicon esculentum
Germany
–
KF253131
KF252668
KF252181
KF251677
KF251173
CBS 289.69
Lolium perenne
Germany
U.G. Schlösser
KF253132
KF252669
KF252182
KF251678
KF251174
CBS 290.69
Lolium perenne
Germany
U.G. Schlösser
KF253133
KF252670
KF252183
KF251679
KF251175
CBS 135671; S615
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253134
KF252671
KF252184
KF251680
KF251176
Sizing up Septoria
Parastagonospora avenae
CPC 11355
KF251672
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Paras. nodorum
CBS 110109
Lolium perenne
Denmark
M.P.S. Câmara
KF253135
KF252672
KF252185
KF251681
KF251177
Paras. “nodorum”
CBS 259.49
Triticum sp.
Canada
–
KF253143
KF252679
KF252192
KF251688
KF251185
Paras. poae
CBS 135089; S606
Poa sp.
Netherlands
S.I.R. Videira
KF253136
KF252673
KF252186
KF251682
KF251178
GenBank accession no.2
CBS 135091; S613
Poa sp.
Netherlands
S.I.R. Videira
KF253137
KF252674
KF252187
KF251683
KF251179
Passalora depressa
CPC 14915
Angelica gigas
South Korea
H.D. Shin
KF253256
KF252788
KF252314
KF251813
KF251309
Pas. dioscoreae
CBS 135460; CPC 10855
Dioscorea tokoro
South Korea
H.D. Shin
KF253257
KF252789
KF252315
KF251814
KF251310
CBS 135463; CPC 11513
Dioscorea tenuipes
South Korea
H.D. Shin
KF253258
KF252790
KF252316
KF251815
KF251311
CPC 15143
Eugenia unilora
Brazil
A.C. Alfenas
KF253138
KF252642
–
JX901875
KF251180
CPC 15159
Eugenia unilora
Brazil
A.C. Alfenas
JX901667
JX902245
JX901999
JX901876
FJ493189
“Phaeosphaeria” alpina
CBS 456.84
Phleum alpinum
Switzerland
A. Leuchtmann
KF253139
KF252675
KF252188
KF251684
KF251181
Phaeos. caricicola
CBS 603.86
Carex pendula
Switzerland
A. Leuchtmann
KF253140
KF252676
KF252189
KF251685
KF251182
Phaeos. juncicola
CBS 110108
Phlox sp.
Netherlands
M.P.S. Câmara
KF253141
KF252677
KF252190
KF251686
KF251183
Phaeos. nigrans
CBS 307.79
Zea mays
Switzerland
–
KF253142
KF252678
KF252191
KF251687
KF251184
Phaeos. oryzae
CBS 110110
Oryza sativa
South Korea
L. Hausch
–
KF252680
KF252193
KF251689
KF251186
Phaeos. papayae
CBS 135416
Carica papaya
Brazil
A.C. Alfenas
–
KF252681
KF252194
KF251690
KF251187
“Phaeos.” phragmiticola
CBS 459.84
Phragmites australis
Switzerland
A. Leuchtmann
KF253144
KF252682
KF252195
KF251691
KF251188
“Phaeos.” pontiformis
CBS 117487
–
Netherlands
J. Harrak
KF253145
KF252683
KF252196
KF251692
KF251189
Phaeosphaeria sp.
CBS 206.87
Zea mays
Gabon
J.L. Notteghem
KF253146
KF252684
KF252197
KF251693
KF251190
Phaeophleospora eugeniae
CBS 135465; CPC 11894
Zea mays
South Africa
P.W. Crous
KF253147
KF252685
KF252198
KF251694
KF251191
“Phaeos.” typharum
CBS 296.54
Nardus stricta
Switzerland
L.E. Wehmeyer
KF253148
KF252686
KF252199
KF251695
KF251192
“Phaeos.” vagans
CBS 604.86
Calamagrostis arundinacea
Sweden
A. Leuchtmann
KF253149
KF252687
KF252200
KF251696
KF251193
phaeosphaeria-like sp.
CBS 123.76
Prunus domestica
Serbia
M. Arseijevic
KF253150
KF252688
KF252201
KF251697
KF251194
CBS 135461; CPC 11231
Musa sp.
Mauritius
Y. Jaufeerally-Fakim
KF253151
KF252689
KF252202
KF251698
KF251195
CBS 135466; CPC 12131
Acacia crassicarpa
Thailand
W. Himaman
KF253153
KF252691
KF252204
KF251700
KF251197
CBS 135469; CPC 12881
Pinus monticola
USA
G. Newcombe & R.G.
Ganley
KF253154
KF252692
KF252205
KF251701
KF251198
CPC 12130
Acacia crassicarpa
Thailand
W. Himaman
KF253152
KF252690
KF252203
KF251699
KF251196
Phaeosphaeriopsis glaucopunctata
CBS 653.86
Ruscus aculeatus
Switzerland
A. Leuchtmann
KF253155
KF252693
KF252206
KF251702
KF251199
Phloeospora ulmi
CBS 344.97
Ulmus glabra
Austria
W. Gams
KF253158
KF252696
–
KF251705
KF251202
CBS 613.81
Ulmus sp.
Austria
H.A. van der Aa
KF253159
KF252697
KF252208
KF251706
KF251203
CBS 101564
Ulmus sp.
Netherlands
H.A. van der Aa
KF253156
KF252694
KF252207
KF251703
KF251200
CBS 109835
Ulmus sp.
Netherlands
G.J.M. Verkley
KF253157
KF252695
–
KF251704
KF251201
CBS 111680
Eucalyptus nitens
Australia
P.W. Crous
KF253160
KF252698
KF252209
KF251707
KF251204
Phlogicylindrium eucalyptorum
Quaedvlieg et al.
312
Table 1. (Continued).
Table 1. (Continued).
www.studiesinmycology.org
Species
Isolate no.1
host
location
GenBank accession no.2
collector
EF-1α
Btub
rPB2
lsu
ITS
CBS 111689
Eucalyptus nitens
Australia
KF253161
–
KF252210
KF251708
KF251205
CBS 123726
Vincetoxicum oficinale
Czech Republic G.J.M. Verkley
KF253162
KF252699
KF252211
KF251709
KF251206
CBS 123727
Vincetoxicum oficinale
Czech Republic G.J.M. Verkley
KF253163
–
KF252212
KF251710
KF251207
CBS 123743
Vincetoxicum oficinale
Czech Republic G.J.M. Verkley
KF253164
–
KF252213
KF251711
KF251208
Phoma herbarum
CBS 615.75
Rosa multilora
Netherlands
G.H. Boerema
KF253168
KF252703
KF252217
KF251715
KF251212
Polyphialoseptoria tabebuiaeserratifoliae
CBS 112650
Tabebuia serratifolia
Brazil
A.C. Alfenas
KF253169
KF252704
KF252218
KF251716
KF251213
Pol. terminaliae
CBS 135106; CPC 19611
Terminalia catappa
Brazil
R.W. Barreto
KF253170
KF252705
KF252219
KF251717
KF251214
Phlyctema vincetoxici
P.W. Crous
Terminalia catappa
Brazil
R.W. Barreto
KF253171
–
KF252220
KF251718
KF251215
CBS 123244
Eucalyptus camaldurensis
Thailand
R. Cheewangkoon
JX901676
JX902254
JX902008
JX901885
JX901781
Pse. eucalyptorum
CBS 116303
Eucalyptus nitens
South Africa
P.W. Crous
KF253172
KF252706
KF252221
KF251719
KF251216
CPC 13816
Eucalyptus glaucescens
UK
S. Denman
KF253230
KF252764
KF252288
KF251786
KF251282
Pse. madagascariensis
CBS 124155
Eucalyptus camaldulensis
Madagascar
M.J. Wingield
KF253265
–
KF252322
KF251822
KF251318
Pse. natalensis
CBS 111069
Eucalyptus nitens
South Africa
T. Coutinho
KF302389
KF302384
KF302393
KF302405
KF302399
Pse. norchiensis
CBS 120738
Eucalyptus sp.
Italy
W. Gams
JX901684
JX902263
JX902017
JX901894
JX901785
Pse. robusta
CBS 111175
Eucalyptus robur
Malaysia
M.J. Wingield
JX901694
JX902273
JX902027
JX901904
DQ303081
Pse. schizolobii
CBS 120029
Schizolobium parahybum
Ecuador
M.J. Wingield
KF253269
KF252798
KF252326
KF251826
KF251322
Pse. tereticornis
CPC 13299
Eucalyptus tereticornis
Australia
P.W. Crous
JX901701
JX902280
JX902034
JX901911
GQ852770
Pseudocercosporella capsellae
CBS 127.29
–
–
K. Togashi
KF253273
KF252801
KF252330
KF251830
KF251326
CBS 112032
Brassica sp.
UK
R. Evans
KF253267
KF252797
KF252324
KF251824
KF251320
CBS 112033
Brassica sp.
UK
R. Evans
KF253254
KF252785
KF252311
KF251810
KF251306
CBS 118412
Brassica sp.
New Zealand
C.F. Hill
KF253272
KF252800
KF252329
KF251829
KF251325
“Pella.” magnusiana
CBS 114735
Geranium silvaticum
Sweden
E. Gunnerbeck
KF253274
KF252802
–
KF251831
KF251327
Pella. pastinacae
CBS 114116
Laserpitium latifolium
Sweden
L. Holm
KF253275
KF252803
KF252331
KF251832
KF251328
Pseudoseptoria collariana
CBS 135104; CPC 18119
Bambusoideae sp.
Iran
A. Mirzadi Gohari
KF253174
KF252707
KF252223
KF251721
KF251218
Pseudos. obscura
CBS 135103; CPC 18118
Bambusoideae sp.
Iran
A. Mirzadi Gohari
KF253175
KF252708
KF252224
KF251722
KF251219
Ramularia endophylla
CBS 113265
Quercus robur
Netherlands
G.J.M. Verkley
KF253176
KF252709
KF252225
KF251723
KF251220
Ram. eucalypti
CBS 120726
Eucalyptus grandis var.
grandilora Maiden
Italy
W. Gams
KF253177
KF252710
KF252226
KF251724
KF251221
Ram. lamii
CPC 11312
Leonurus sibiricus
South Korea
H.D. Shin
KF253178
KF252711
KF252227
KF251725
KF251222
Ram. pratensis
CPC 11294
Rumex crispus
South Korea
–
KF253179
KF252712
KF252228
KF251726
KF251223
Ramularia sp.
CBS 115913
Cerastium semidecandrum
Netherlands
A. Aptroot
KF253180
–
KF252229
KF251727
KF251224
Readeriella angustia
CBS 124998
Eucalyptus delegatensis
Australia
B.A. Summerel
KF253181
KF252713
KF252230
KF251728
KF251225
Rea. eucalypti
CPC 13401
Eucalyptus sp.
Portugal
P.W. Crous
KF253173
–
KF252222
KF251720
KF251217
Sizing up Septoria
313
CBS 135475; CPC 19487
Pseudocercospora chiangmaiensis
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Rea. readeriellophora
CPC 12920
Eucalyptus sp.
Australia
A. Carnegie
KF253114
KF252652
KF252163
KF251658
KF251154
Ruptoseptoria unedonis
CBS 355.86
Arbutus unedo
France
H.A. van der Aa
–
KF252715
KF252233
KF251731
KF251228
CBS 755.70
Arbutus unedo
Croatia
J.A. von Arx
–
KF252716
KF252234
KF251732
KF251229
Sclerostagonospora phragmiticola
CBS 338.86
Phragmites australis
France
H.A. van der Aa
KF253184
KF252717
KF252235
KF251733
KF251230
Septoria abei
CBS 128598
Hibiscus syriacus
South Korea
H.D. Shin
KF253280
KF252805
KF252336
KF251837
KF251333
Sep. “agropyrina”
CBS 387.64
–
Japan
–
KF302392
KF302387
KF302398
KF302410
KF302404
Sep. anthrisci
CBS 109020
Anthriscus sp.
Austria
G.J.M. Verkley
KF253286
KF252811
KF252340
KF251843
KF251339
Sep. anthurii
CBS 346.58
Anthurium scherzerianum
Germany
R. Schneider
KF253288
KF252813
KF252342
KF251845
KF251341
Sep. apiicola
CBS 400.54
Apium graveolens
Netherlands
J.A. von Arx
KF253292
KF252817
KF252346
KF251849
KF251345
“Sep.” arundinacea
CBS 133.68
Phragmites australis
Netherlands
H.A. van der Aa
KF253185
KF252718
KF252236
KF251734
KF251231
GenBank accession no.2
CBS 281.72
Phragmites australis
Netherlands
J.W. Veenbaas-Rijks
KF253186
KF252719
KF252237
KF251735
KF251232
Sep. astericola
CBS 128593
Aster yomena
South Korea
H.D. Shin
KF253294
KF252819
KF252348
KF251851
KF251347
Sep. astragali
CBS 109116
Astragalus sp.
Austria
G.J.M. Verkley
KF253298
KF252823
KF252352
KF251855
KF251351
KF251350
CBS 123878
Astragalus glycyphyllos
Czech Republic G.J.M. Verkley
KF253297
KF252822
KF252351
KF251854
Sep. atropurpurea
CBS 348.58
Aster canus
Germany
R. Schneider
KF253299
KF252824
KF252353
KF251856
KF251352
Sep. bothriospermi
CBS 128599
Bothriospermum tenellum
South Korea
H.D. Shin
KF253301
KF252826
KF252355
KF251858
KF251354
Sep. bupleuricola
CBS 128603
Bupleurum falcatum
South Korea
H.D. Shin
KF253303
KF252828
KF252357
KF251860
KF251356
Sep. calendulae
CBS 349.58
Calendula arvensis
Italy
R. Schneider
KF253304
KF252829
KF252358
KF251861
KF251357
Sep. callistephi
CBS 128590
Callistephus chinensis
South Korea
H.D. Shin
KF253305
KF252830
KF252359
KF251862
KF251358
Sep. campanulae
CBS 128604
Campanula takesimana
South Korea
H.D. Shin
KF253308
KF252833
KF252362
KF251865
KF251361
Sep. cerastii
CBS 128612
Cerastium holosteoides
South Korea
H.D. Shin
KF253311
KF252836
KF252365
KF251868
KF251364
Sep. cf. agrimoniicola
CBS 128585
Agrimonia pilosa
South Korea
H.D. Shin
KF253283
KF252808
KF252337
KF251840
KF251336
CBS 128602
Agrimonia pilosa
South Korea
H.D. Shin
KF253284
KF252809
KF252338
KF251841
KF251337
Sep. cf. rubi
CBS 128646
Rubus crataegifolius
South Korea
H.D. Shin
KF253314
KF252839
KF252368
KF251871
KF251367
Sep. cf. stachydicola
CBS 128668
Stachys riederi var. japonica
South Korea
H.D. Shin
KF253512
KF253033
KF252558
KF252070
KF251565
Sep. chelidonii
CBS 128607
Chelidonium majus
South Korea
H.D. Shin
KF253319
KF252844
KF252373
KF251876
KF251372
Sep. chromolaenae
CBS 113373
Chromolaena odorata
Cuba
S. Neser
KF253321
KF252846
KF252375
KF251878
KF251374
Sep. chrysanthemella
CBS 128622
Chrysanthemum boreale
South Korea
H.D. Shin
KF253323
KF252848
KF252377
KF251880
KF251376
CBS 128716
–
South Africa
E. Oh
KF253325
KF252850
KF252379
KF251882
KF251378
Sep. cirsii
CBS 128621
Cirsium setidens
South Korea
H.D. Shin
KF253328
KF252853
KF252382
KF251885
KF251381
Sep. citricola
CBS 356.36
Citrus sinensis
Italy
G. Ruggieri
KF253329
KF252854
KF252383
KF251886
KF251382
Sep. clematidis
CBS 108983
Clematis vitalba
Germany
G.J.M. Verkley
KF253330
KF252855
KF252384
KF251887
KF251383
Sep. codonopsidis
CBS 128620
Codonopsis lanceolata
South Korea
H.D. Shin
KF253333
KF252858
KF252387
KF251890
KF251386
Quaedvlieg et al.
314
Table 1. (Continued).
Table 1. (Continued).
www.studiesinmycology.org
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Sep. convolvuli
CBS 128627
Calystegia soldanella
South Korea
H.D. Shin
KF253336
KF252861
KF252390
KF251893
KF251389
Sep. coprosma
CBS 113391
Coprosma robusta
New Zealand
G.J.M. Verkley
KF253255
KF252787
KF252313
KF251812
KF251308
Sep. crepidis
CBS 128608
Youngia japonica
South Korea
H.D. Shin
KF253337
KF252862
KF252391
KF251894
KF251390
GenBank accession no.2
CBS 128619
Youngia japonica
South Korea
H.D. Shin
KF253338
KF252863
KF252392
KF251895
KF251391
Sep. cretae
CBS 135095; CPC 651
Nerium oleander
Greece
U. Damm
–
KF252720
KF252238
KF251736
KF251233
Sep. cruciatae
CBS 123747
Galium odoratum
Czech Republic G.J.M. Verkley
KF253340
KF252865
KF252394
KF251897
KF251393
Sep. cucubali
CBS 102386
Saponaria oficinalis
Netherlands
G.J.M. Verkley
KF253344
KF252869
KF252398
KF251901
KF251397
Sep. cucurbitacearum
CBS 178.77
Cucurbita maxima
New Zealand
H.J. Boesewinkel
KF253346
–
KF252400
KF251903
KF251399
Sep. dearnessii
CBS 128624
Angelica dahurica
South Korea
H.D. Shin
KF253347
KF252871
KF252401
KF251904
KF251400
Sep. digitalis
CBS 391.63
Digitalis lanata
Czech Republic V. Holubová
KF253349
KF252873
KF252403
KF251906
KF251402
Sep. dysentericae
CBS 131892; CPC 12328
Inula britannica
South Korea
H.D. Shin
KF253353
KF252877
KF252406
KF251910
KF251406
Sep. epambrosiae
CBS 128629
Ambrosia triida
South Korea
H.D. Shin
KF253356
KF252880
KF252407
KF251913
KF251409
Sep. epilobii
CBS 109084
Epilobium leischeri
Austria
G.J.M. Verkley
KF253358
KF252882
KF252409
KF251915
KF251411
CBS 109085
Epilobium leischeri
Austria
G.J.M. Verkley
KF253359
KF252883
KF252410
KF251916
KF251412
CBS 186.93
Erigeron annuus
Italy
M. Vurro
KF253364
KF252887
KF252537
KF252048
KF251543
CBS 109094
Erigeron annuus
Austria
G.J.M. Verkley
KF253360
KF252884
KF252411
KF251917
KF251413
CBS 131893; CPC 12340
Erigeron annuus
South Korea
H.D. Shin
KF253363
KF252888
KF252414
KF251920
KF251416
Sep. eucalyptorum
CBS 118505
Eucalyptus sp.
India
W. Gams
KF253365
KF252889
KF252415
KF251921
KF251417
Sep. exotica
CBS 163.78
Hebe speciosa
New Zealand
H.J. Boesewinkel
KF253366
KF252890
KF252416
KF251922
KF251418
Sep. galeopsidis
CBS 191.26
Galeopsis sp.
–
C. Killian
KF253370
KF252894
KF252420
KF251926
KF251422
CBS 102314
Galeopsis tetrahit
Netherlands
G.J.M. Verkley
KF253371
KF252895
KF252421
KF251927
KF251423
CBS 102411
Galeopsis tetrahit
Netherlands
G.J.M. Verkley
KF253372
KF252896
KF252422
KF251928
KF251424
Sep. gentianae
CBS 128633
Gentiana scabra
South Korea
H.D. Shin
KF253374
KF252898
KF252424
KF251930
KF251426
“Sep.” gladioli
CBS 121.20
–
–
W.J. Kaiser
KF253375
KF252899
KF252425
KF251931
KF251427
Sep. erigerontis
–
Netherlands
J.C. Went
KF253376
KF252900
KF252426
KF251932
KF251428
CBS 128618
Glycine max
South Korea
H.D. Shin
KF253378
KF252902
KF252427
KF251934
KF251430
Sep. helianthi
CBS 123.81
Helianthus annuus
–
M. Muntañola
KF253379
KF252903
KF252428
KF251935
KF251431
Sep. hibiscicola
CBS 128615
Hibiscus syriacus
South Korea
H.D. Shin
KF253382
KF252906
KF252431
KF251938
KF251434
Sep. hippocastani
CBS 411.61
Aesculus hippocastanum
Germany
W. Gerlach
KF253383
KF252907
KF252432
KF251939
KF251435
CPC 23103; MP11
Aesculus sp.
Netherlands
S.I.R. Videira
KF253510
KF253031
KF252556
KF252068
KF251563
Sep. justiciae
CBS 128625
Justicia procumbens
South Korea
H.D. Shin
KF253385
KF252909
KF252434
KF251941
KF251437
Sep. lactucae
CBS 352.58
Lactuca sativa
Germany
G. Sörgel
KF253388
KF252912
KF252437
KF251944
KF251440
Sizing up Septoria
315
CBS 353.29
Sep. glycinicola
Isolate no.1
host
location
collector
CBS 108943
Lactuca sativa
Netherlands
P. Grooteman
Sep. lamiicola
CBS 123884
Lamium sp.
Sep. lepidiicola
CBS 128635
Lepidium virginicum
Sep. leptostachyae
CBS 128613
CBS 128628
Sep. leucanthemi
Species
GenBank accession no.2
EF-1α
Btub
rPB2
lsu
ITS
KF253387
KF252911
KF252436
KF251943
KF251439
Czech Republic G.J.M. Verkley
KF253397
KF252921
KF252446
KF251953
KF251449
South Korea
H.D. Shin
KF253398
KF252922
KF252447
KF251954
KF251450
Phryma leptostachya
South Korea
H.D. Shin
KF253399
KF252923
KF252448
KF251955
KF251451
Phryma leptostachya
South Korea
H.D. Shin
KF253400
KF252924
KF252449
KF251956
KF251452
CBS 109090
Chrysanthemum
leucanthemum
Austria
G.J.M. Verkley
KF253403
KF252927
KF252452
KF251959
KF251455
Sep. limonum
CBS 419.51
Citrus limonum
Italy
G. Goidánich
KF253407
KF252931
KF252456
KF251963
KF251459
Sep. linicola
CBS 316.37
Linum usitatissimum
–
H.W. Hollenweber
KF253408
KF252932
KF252457
KF251964
KF251460
Sep. lycoctoni
CBS 109089
Aconitum vulparia
Austria
G.J.M. Verkley
KF253409
KF252933
KF252458
KF251965
KF251461
Sep. lycopersici
CBS 128654
Lycopersicon esculentum
South Korea
H.D. Shin
KF253410
KF252934
KF252459
KF251966
KF251462
Sep. lycopicola
CBS 128651
Lycopus ramosissimus
South Korea
H.D. Shin
KF253412
KF252936
KF252461
KF251968
KF251464
Sep. lysimachiae
CBS 102315
Lysimachia vulgaris
Netherlands
G.J.M. Verkley
KF253413
KF252937
KF252462
KF251969
KF251465
CBS 123795
Lysimachia sp.
Czech Republic G.J.M. Verkley
KF253417
KF252941
KF252466
KF251973
KF251469
Sep. malagutii
CBS 106.80
Solanum sp.
Peru
G.H. Boerema
KF253418
–
KF252467
KF251974
KF251470
Sep. matricariae
CBS 109001
Matricaria discoidea
Netherlands
G.J.M. Verkley
KF253420
KF252943
KF252469
KF251976
KF251472
Sep. mazi
CBS 128755
Mazus japonicus
South Korea
H.D. Shin
KF253422
KF252945
KF252471
KF251978
KF251474
Sep. melissae
CBS 109097
Melissa oficinalis
Netherlands
H.A. van der Aa
KF253423
KF252946
KF252472
KF251979
KF251475
Sep. napelli
CBS 109105
Aconitum napellus
Austria
G.J.M. Verkley
KF253426
KF252949
KF252474
KF251982
KF251478
Sep. obesa
CBS 354.58
Chrysanthemum indicum
Germany
R. Schneider
KF253431
–
KF252479
KF251987
KF251483
CBS 128588
Artemisia lavandulaefolia
South Korea
H.D. Shin
KF253428
KF252951
KF252476
KF251984
KF251480
CBS 128623
Chrysanthemum indicum
South Korea
H.D. Shin
KF253429
KF252952
KF252477
KF251985
KF251481
Sep. oenanthicola
CBS 128649
Oenanthe javanica
South Korea
H.D. Shin
KF253187
KF252721
KF252239
KF251737
KF251234
Sep. oenanthis
CBS 128667
Cicuta virosa
South Korea
H.D. Shin
KF253432
KF252953
KF252481
KF251989
KF251485
Sep. orchidearum
CBS 457.78
Listera ovata
France
H.A. van der Aa
KF253435
KF252956
KF252483
KF251991
KF251487
CBS 128631
Cyclamen fatrense
South Korea
H.D. Shin
KF253434
KF252955
KF252482
KF251990
KF251486
Sep. pachyspora
CBS 128652
Zyathoxylum schinifolium
South Korea
H.D. Shin
KF253437
KF252958
KF252485
KF251993
KF251488
Sep. paridis
CBS 109108
Viola sp.
Austria
G.J.M. Verkley
KF253440
KF252961
KF252488
KF251996
KF251491
CBS 109111
Paris quadrifolia
Austria
G.J.M. Verkley
KF253438
KF252959
KF252486
KF251994
KF251489
Sep. passilorae
CBS 102701
Passilora edulis
New Zealand
C.F. Hill
KF253442
KF252963
KF252490
KF251998
KF251493
Sep. perillae
CBS 128655
Perilla frutescens
South Korea
H.D. Shin
KF253444
KF252965
KF252491
KF252000
KF251495
Sep. petroselini
CBS 182.44
Petroselinum sativum
Netherlands
S.D. de Wit
KF253446
KF252967
KF252493
KF252002
KF251497
Sep. phlogis
CBS 128663
Phlox paniculata
South Korea
H.D. Shin
KF253448
KF252969
KF252495
KF252004
KF251499
Quaedvlieg et al.
316
Table 1. (Continued).
Table 1. (Continued).
www.studiesinmycology.org
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Sep. polygonorum
CBS 347.67
Polygonum persicaria
Netherlands
H.A. van der Aa
KF253455
KF252976
KF252502
KF252011
KF251506
CBS 109834
Polygonum persicaria
Netherlands
G.J.M. Verkley
KF253453
KF252974
KF252500
KF252009
KF251504
Sep. posoniensis
CBS 128645
Chrysosplenium japonicum
South Korea
H.D. Shin
KF253456
KF252977
KF252503
KF252012
KF251507
Sep. protearum
CBS 177.77
Fragaria sp.
New Zealand
H.J. Boesewinkel
KF253463
KF252984
KF252509
KF252019
KF251514
CBS 390.59
Ligustrum vulgare
Italy
M. Ribaldi
KF253467
KF252987
KF252513
KF252023
KF251518
CBS 566.88
Hedera helix
France
H.A. van der Aa
KF253470
KF252990
KF252515
KF252026
KF251521
CBS 778.97
Protea cynaroides
South Africa
L. Viljoen
KF253472
KF252992
KF252517
KF252028
KF251523
KF251524
GenBank accession no.2
CBS 135477; CPC 19675
Zantedeschia aethiopica
South Africa
P.W. Crous
KF253473
KF252993
KF252518
KF252029
Sep. pseudonapelli
CBS 128664
Aconitum pseudolaeve var.
erectum
South Korea
H.D. Shin
KF253475
KF252995
KF252520
KF252031
KF251526
Sep. putrida
CBS 109088
Senecio nemorensis
Austria
G.J.M. Verkley
KF253477
KF252997
KF252522
KF252033
KF251528
Sep. rumicum
CBS 503.76
Rumex acetosa
France
H.A. van der Aa
KF253478
KF252998
KF252523
KF252034
KF251529
Sep. saccardoi
CBS 128756
Lysimachia vulgaris
South Korea
H.D. Shin
KF253479
KF252999
KF252524
KF252035
KF251530
Sep. scabiosicola
CBS 102334
Knautia arvensis
Netherlands
G.J.M. Verkley
KF253481
KF253001
KF252526
KF252037
KF251532
CBS 102336
Knautia arvensis
Netherlands
G.J.M. Verkley
KF253483
KF253003
KF252528
KF252039
KF251534
KF251535
Knautia arvensis
Germany
G.J.M. Verkley
KF253484
KF253004
KF252529
CBS 109093
Knautia dipsacifolia
Austria
G.J.M. Verkley
KF253487
KF253007
KF252532
KF252043
KF251538
CBS 102366
Senecio luviatilis
Netherlands
G.J.M. Verkley
KF253492
KF253012
KF252538
KF252049
KF251544
CBS 102381
Senecio luviatilis
Netherlands
G.J.M. Verkley
KF253493
KF253013
KF252539
KF252050
KF251545
CBS 128659
Siegesbeckia glabrescens
South Korea
H.D. Shin
KF253494
KF253014
KF252540
KF252051
KF251546
CBS 128661
Siegesbeckia pubescens
South Korea
H.D. Shin
KF253495
KF253015
KF252541
KF252052
KF251547
Sep. sii
CBS 102370
Berula erecta
Netherlands
G.J.M. Verkley
KF253497
KF253017
KF252543
KF252054
KF251549
Sep. sisyrinchii
CBS 112096
Sysirinchium sp.
New Zealand
C.F. Hill
KF253499
KF253019
KF252545
KF252056
KF251551
Septoria sp.
CBS 128650
Taraxacum oficinale
South Korea
H.D. Shin
KF253504
KF253024
KF252550
KF252061
KF251556
CBS 128658
Chrysosplenium japonicum
South Korea
H.D. Shin
KF253505
KF253025
KF252551
KF252062
KF251557
CBS 128757
Sonchus asper
South Korea
H.D. Shin
KF253500
KF253020
KF252546
KF252057
KF251552
CBS 135472; CPC 19304
Vigna unguiculata ssp.
sesquipedalis
Austria
P.W. Crous
KF253506
KF253026
KF252552
KF252063
KF251558
CBS 135474; CPC 19485
Conyza canadensis
Brazil
R.W. Barreto
KF253507
KF253027
KF252553
KF252064
KF251559
CBS 135478; CPC 19716
Eucalyptus sp.
India
W. Gams
KF253188
KF252722
KF252240
KF251738
KF251235
CBS 135479; CPC 19793
Syzygium cordatum
South Africa
P.W. Crous
–
KF253029
KF252555
KF252066
KF251561
CPC 19976
Feijoa sellowiana
Italy
G. Polizzi
KF253509
KF253030
–
KF252067
KF251562
Sep. senecionis
Sep. siegesbeckiae
317
Sizing up Septoria
CBS 108981
KF252040
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
CPC 21105
Cluvia sp.
South Africa
P.W. Crous
–
–
KF302396
KF302408
KF302402
CPC 23104
–
Italy
E. van Agtmaal
KF253511
KF253032
KF252557
KF252069
KF251564
CBS 347.58
Aster canus
Germany
R. Schneider
KF253295
KF252820
KF252349
KF251852
KF251348
CBS 102326
Stachys sylvatica
Netherlands
G.J.M. Verkley
KF253514
KF253035
KF252560
KF252072
KF251567
CBS 109115
Campanula glomerata
Austria
G.J.M. Verkley
KF253502
KF253022
KF252548
KF252059
KF251554
CBS 109127
Stachys sylvatica
Austria
G.J.M. Verkley
KF253517
KF253038
KF252563
KF252075
KF251570
Sep. stellariae
CBS 102376
Stellaria media
Netherlands
G.J.M. Verkley
KF253521
KF253042
KF252567
KF252079
KF251574
“Sep.” steviae
CBS 120132
Stevia rebaudiana
Japan
J. Ishiba
KF253191
–
KF252243
KF251741
KF251238
“Sep.” tanaceti
CBS 358.58
Tanacetum vulgare
Germany
R. Schneider
KF253192
–
KF252244
KF251742
KF251239
Sep. taraxaci
CBS 567.75
Taraxacum sp.
Armenia
H.A. van der Aa
KF253524
KF253045
KF252570
KF252082
KF251577
Sep. tinctoriae
CBS 129154
Serratula coronata
South Korea
H.D. Shin
KF253525
KF253046
KF252571
KF252083
KF251578
Sep. tormentillae
CBS 128643
Potentilla fragarioides
South Korea
H.D. Shin
KF253526
KF253047
KF252572
KF252084
KF251579
CBS 128647
Potentilla fragarioides
South Korea
H.D. Shin
KF253527
KF253048
KF252573
KF252085
KF251580
CBS 102316
Glechoma hederacea
Netherlands
G.J.M. Verkley
KF253528
KF253049
KF252574
KF252086
KF251581
Species
Sep. stachydis
Sep. urticae
GenBank accession no.2
CBS 102375
Urtica dioica
Netherlands
G.J.M. Verkley
KF253530
KF253051
KF252576
KF252088
KF251583
Sep. verbascicola
CBS 102401
Verbascum nigrum
Netherlands
G.J.M. Verkley
KF253531
KF253052
KF252577
KF252089
KF251584
Sep. verbenae
CBS 113438
Verbena oficinalis
New Zealand
G.J.M. Verkley
KF253532
KF253053
KF252578
KF252090
KF251585
Sep. villarsiae
CBS 514.78
Nymphoides peltata
Netherlands
H.A. van der Aa
KF253534
KF253055
KF252580
KF252092
KF251587
Sep. violae-palustris
CBS 128644
Viola selkirkii
South Korea
H.D. Shin
KF253537
KF253058
KF252583
KF252095
KF251590
CBS 128660
Viola yedoensis
South Korea
H.D. Shin
KF253538
KF253059
KF252584
KF252096
KF251591
CBS 134910; CPC 19500
Tibouchina herbacea
Brazil
D.F. Parreira
KF302391
KF302386
KF302397
KF302409
KF302403
KF251240
septoria-like sp.
CBS 135471; CPC 19294
Corymbia gummifera
Australia
P.W. Crous
KF253193
KF252725
KF252245
KF251743
CBS 135473; CPC 19311
Phragmites sp.
USA
–
KF253194
KF252726
KF252246
KF251744
KF251241
CBS 135481; CPC 22154;
S672
Polygonatum sp.
Netherlands
U. Damm
–
–
KF252247
KF251745
KF251242
Septorioides pini-thunbergii
CBS 473.91
Pinus thunbergii
Japan
S. Kaneko & Y. Zinno
–
KF252727
KF252248
KF251746
KF251243
Setophoma chromolaenae
CBS 135105; CPC 18553
Chromolaena odorata
Brazil
R.W. Barreto
KF253195
KF252728
KF252249
KF251747
KF251244
Setop. sacchari
CBS 333.39
Saccharum oficinarum
Brazil
A.A. Bitancourt
–
–
KF252250
KF251748
KF251245
Setop. terrestris
CBS 335.29
Allium sativum
USA
H.N. Hansen
KF253196
KF252729
KF252251
KF251749
KF251246
CBS 335.87
Allium cepa
Senegal
–
KF253197
KF252730
KF252252
KF251750
KF251247
CBS 377.52
Allium cepa
–
R.H. Larson
KF253198
KF252731
KF252253
KF251751
KF251248
CBS 135470; CPC 18417
Zea mays
South Africa
S. Lamprecht
KF253189
KF252723
KF252241
KF251739
KF251236
Quaedvlieg et al.
318
Table 1. (Continued).
Table 1. (Continued).
www.studiesinmycology.org
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Setoseptoria phragmitis
CBS 114802
Phragmites australis
Hong Kong
K.D. Hyde
KF253199
KF252732
KF252254
KF251752
KF251249
CBS 114966
Phragmites australis
Hong Kong
K.D. Hyde
KF253200
KF252733
KF252255
KF251753
KF251250
Sphaerulina abeliceae
CBS 128591
Zelkova serrata
South Korea
H.D. Shin
KF253539
–
KF252585
KF252097
KF251592
Sph. aceris
CBS 687.94
Acer pseudoplatanus
Netherlands
G.J.M. Verkley
KF253542
KF253061
KF252588
KF252100
KF251595
Sph. amelanchier
CBS 102063
Actinidia deliciosa
New Zealand
C.F. Hill
KF253581
KF253096
KF252627
KF252140
KF251635
CBS 135110; MP8
Amelanchier sp.
Netherlands
S.I.R. Videira
KF253543
KF253062
KF252589
KF252101
KF251596
CPC 23105; MP22
Quercus sp.
Netherlands
S.I.R. Videira
KF253544
KF253063
KF252590
KF252102
KF251597
CPC 23106; MP7
Castanea sp.
Netherlands
S.I.R. Videira
KF253545
KF253064
KF252591
KF252103
KF251598
CPC 23107; MP9
Betula sp.
Netherlands
S.I.R. Videira
KF253583
KF253098
KF252626
KF252139
KF251634
CBS 352.49
Rhododendron sp.
Belgium
J. van Holder
KF253547
KF253066
KF252593
KF252105
KF251600
CBS 128605
Rhododendron sp.
South Korea
H.D. Shin
KF253546
KF253065
KF252592
KF252104
KF251599
Sph. berberidis
CBS 324.52
Berberis vulgaris
Switzerland
E. Müller
KF253548
KF253067
KF252594
KF252106
KF251601
Sph. betulae
CBS 116724
Betula pubescens
Netherlands
S. Green
KF253549
KF253068
KF252595
KF252107
KF251602
CBS 128600
Betula platyphylla var. japonica
South Korea
H.D. Shin
KF253552
KF253071
KF252598
KF252110
KF251605
CBS 501.50
Cercis siliquastrum
Netherlands
G. van den Ende
KF253556
KF253075
KF252601
KF252113
KF251608
CBS 118910
Eucalyptus sp.
France
P.W. Crous
KF253553
KF253072
KF252602
KF252114
KF251609
CBS 128634
Cercis siliquastrum
Argentina
H.D. Shin
KF253554
KF253073
KF252599
KF252111
KF251606
CBS 129151
Cercis siliquastrum
Argentina
H.D. Shin
KF253555
KF253074
KF252600
KF252112
KF251607
CBS 102324
Cornus sp.
Netherlands
A. van Iperen
KF253557
KF253076
KF252603
KF252115
KF251610
CBS 102332
Cornus sp.
Netherlands
A. van Iperen
KF253558
KF253077
KF252604
KF252116
KF251611
Sph. frondicola
CBS 391.59
Populus pyramidalis
Germany
R. Schneider
KF253572
–
KF252617
KF252130
KF251625
Sph. gei
CBS 102318
Geum urbanum
Netherlands
G.J.M. Verkley
KF253560
KF253079
KF252605
KF252118
KF251613
Sph. azaleae
Sph. cercidis
Sph. cornicola
GenBank accession no.2
Geum japonicum
South Korea
H.D. Shin
KF253562
KF253081
KF252607
KF252120
KF251615
CBS 102313
Hypericum sp.
Netherlands
G.J.M. Verkley
KF253563
KF253082
KF252608
KF252121
KF251616
Sph. menispermi
CBS 128666
Menispermum dauricum
South Korea
H.D. Shin
KF253564
KF253083
KF252609
KF252122
KF251617
CBS 128761
Menispermum dauricum
South Korea
H.D. Shin
KF253565
KF253084
KF252610
KF252123
KF251618
Sph. musiva
CBS 130570
Populus deltoides
Canada
J. LeBoldus
JX901725
JX902304
JX902058
JX901935
JX901812
Sph. myriadea
CBS 124646
Quercus dentata
Japan
K. Tanaka
KF253201
KF252734
KF252256
KF251754
KF251251
Sph. oxyacanthae
CBS 135098; S654
Crataegus sp.
Netherlands
W. Quaedvlieg
KF253202
KF252735
KF252257
KF251755
KF251252
Sph. patriniae
CBS 128653
Patrinia scabiosaefolia
South Korea
H.D. Shin
KF253570
KF253087
KF252615
KF252128
KF251623
Sph. populicola
CBS 100042
Populus trichocarpa
USA
G. Newcombe
KF253573
–
KF252618
KF252131
KF251626
Sph. pseudovirgaureae
CBS 135109; S669
Solidago gigantea
Netherlands
S.I.R. Videira
KF253203
KF252736
KF252258
KF251756
KF251253
Sizing up Septoria
319
CBS 128632
Sph. hyperici
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Sph. quercicola
CBS 663.94
Quercus robur
Netherlands
H.A. van der Aa
KF253577
KF253092
KF252622
KF252135
KF251630
CBS 109009
Quercus rubra
Netherlands
G.J.M. Verkley
KF253574
KF253089
KF252619
KF252132
KF251627
CBS 115016
Quercus robur
Netherlands
G.J.M. Verkley
KF253575
KF253090
KF252620
KF252133
KF251628
CBS 115136
Quercus robur
Netherlands
G.J.M. Verkley
KF253576
KF253091
KF252621
KF252134
KF251629
CBS 115137
Quercus robur
Netherlands
G.J.M. Verkley
KF302390
KF302385
KF302394
KF302406
KF302400
CBS 355.58
Rosa sp.
–
–
KF253579
KF253094
KF252624
KF252137
KF251632
CBS 357.58
Chrysanthemum leucanthemum Germany
R. Schneider
KF253580
KF253095
KF252625
KF252138
KF251633
CBS 109017
Rubus idaeus
Austria
G.J.M. Verkley
KF253584
KF253099
KF252629
KF252142
KF251637
Sph. socia
Sph. tirolensis
GenBank accession no.2
CBS 109018
Rubus idaeus
Austria
G.J.M. Verkley
KF253585
KF253100
KF252630
KF252143
KF251638
Sph. viciae
CBS 131898
Vicia amurense
South Korea
H.D. Shin
KF253586
KF253101
KF252631
KF252144
KF251639
Sph. westendorpii
CBS 117478
Rubus fruticosus
Netherlands
G.J.M. Verkley
KF253589
KF253104
KF252634
KF252147
KF251642
Stagonospora cf. paludosa
CBS 130005
Carex sp.
Russia
–
KF253204
KF252737
KF252259
KF251757
KF251254
Sta. duoseptata
CBS 135093; S618
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253205
KF252738
KF252260
KF251758
KF251255
“Sta.” foliicola
CBS 110111
Phalaris arundinacea
USA
N. O’Neil
KF253206
KF252739
KF252261
KF251759
KF251256
Sta. paludosa
CBS 135088; S601
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253207
KF252740
KF252262
KF251760
KF251257
Sta. perfecta
CBS 135099; S656
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253208
–
KF252263
KF251761
KF251258
Sta. pseudocaricis
CBS 135132; S610
Carex acutiformis
France
A. Gardiennet
KF253210
KF252742
KF252265
KF251763
KF251260
CBS 135414; S609
Carex acutiformis
France
A. Gardiennet
–
KF302383
KF302395
KF302407
KF302401
CBS 135094; S620
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253211
KF252743
KF252266
KF251764
KF251261
S602
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253212
KF252744
KF252267
KF251765
KF251262
Stagonospora sp.
CBS 135096; 652
Carex acutiformis
France
A. Gardiennet
–
–
KF252268
KF251766
KF251263
Sta. uniseptata
CBS 135090; S611
Carex acutiformis
Netherlands
W. Quaedvlieg
–
KF252745
KF252269
KF251767
KF251264
CPC 22150; S608
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253214
KF252747
KF252271
KF251769
KF251266
CPC 22151; S607
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253213
KF252746
KF252270
KF251768
KF251265
CBS 516.74
Triticum aestivum
Brazil
Y.R. Mehta
KF253215
KF252748
KF252272
KF251770
KF251267
CBS 135482; CPC 22155;
S526
Poa sp.
Netherlands
W. Quaedvlieg
KF253216
KF252749
KF252273
KF251771
KF251268
CBS 135483; CPC 22157;
S617
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253217
KF252750
KF252274
KF251772
KF251269
S619
Carex acutiformis
Netherlands
W. Quaedvlieg
KF253218
KF252751
KF252275
KF251773
KF251270
CBS 102322
Castanea sativa
Netherlands
G.J.M. Verkley
KF253219
KF252752
KF252276
KF251774
KF251271
CBS 102377
Castanea sativa
Netherlands
G.J.M. Verkley
KF253220
KF252753
KF252277
KF251775
KF251272
CBS 111149
Eucalyptus cladocalyx
South Africa
P.W. Crous
KF253221
KF252754
KF252278
KF251776
KF251273
Sta. pseudovitensis
stagonospora-like sp.
Stromatoseptoria castaneicola
Teratosphaeria juvenalis
Quaedvlieg et al.
320
Table 1. (Continued).
Table 1. (Continued).
www.studiesinmycology.org
Species
Isolate no.1
host
location
collector
EF-1α
Btub
rPB2
lsu
ITS
Ter. molleriana
CBS 111164
Eucalyptus globulus
Portugal
M.J. Wingield
KF253222
KF252755
KF252279
KF251777
KF251274
Ter. parva
CBS 119901
Eucalyptus globulus
Ethiopia
A. Gezahgne
KF253223
KF252756
KF252280
KF251778
KF251275
Ter. pseudoeucalypti
CBS 124577
Eucalyptus grandis ×
E. camaldulensis
Australia
V. Andjic
KF253224
KF252757
KF252281
KF251779
KF251276
Ter. suberosa
CPC 13106
Eucalyptus dunnii
Australia
A.J. Carnegie
KF253183
–
KF252232
KF251730
KF251227
Ter. toledana
CBS 113313
Eucalyptus sp.
Spain
P.W. Crous & G. Bills
KF253225
KF252758
KF252282
KF251780
KF251277
Vrystaatia aloeicola
CBS 135107; CPC 20617
Aloe maculata
South Africa
P.W. Crous & W.J. Swart
–
KF252759
KF252283
KF251781
KF251278
Xenobotryosphaeria calamagrostidis
CBS 303.71
Calamagrostis sp.
Italy
G.A. Hedjaroude
KF253226
KF252760
KF252284
KF251782
KF251279
Xenoseptoria neosaccardoi
CBS 120.43
Cyclamen persicum
Netherlands
Roodenburg
KF253227
KF252761
KF252285
KF251783
KF251280
CBS 128665
Lysimachia vulgaris var.
davurica
South Korea
H.D. Shin
KF253228
KF252762
KF252286
KF251784
KF251281
Zasmidium anthuriicola
CBS 118742
Anthurium sp.
Thailand
C.F. Hill
KF253229
KF252763
KF252287
KF251785
FJ839626
Zas. citri
CPC 13467
Eucalyptus sp.
Thailand
W. Himaman
KF253182
KF252714
KF252231
KF251729
KF251226
Zas. lonicericola
CBS 125008
Lonicera japonica
South Korea
H.D. Shin
KF253231
KF252765
KF252289
KF251787
KF251283
Zas. nocoxi
CBS 125009
Twig debris
USA
P.W. Crous
KF253232
KF252766
KF252290
KF251788
KF251284
Zas. scaevolicola
CBS 127009
Scaevola taccada
Australia
R.G. Shivas & P.W Crous
KF253233
KF252767
KF252291
KF251789
KF251285
Zymoseptoria brevis
CBS 128853
Phalaris minor
Iran
–
JQ739777
JF700968
JF700799
JQ739833
JF700867
CPC 18109
Phalaris paradoxa
Iran
–
JQ739779
JF700970
JF700801
JQ739835
JF700869
GenBank accession no.2
CPC 18112
Phalaris paradoxa
Iran
–
JQ739782
JF700973
JF700804
JQ739838
JF700872
Zym. halophila
CBS 128854; CPC 18105
Hordeum glaucum
Iran
M. Razavi
KF253592
–
JF700808
KF252150
KF251645
Zym. passerinii
CBS 120384
Hordeum vulgare
USA
S. Ware
JQ739788
JF700878
JF700979
JQ739844
JF700810
CBS 120385
Hordeum vulgare
USA
S. Ware
JQ739789
JF700980
JF700811
JQ739845
JF700879
Zym. pseudotritici
CBS 130976
Dactylis glomerata
Iran
M. Javan-Nikkhah
JQ739772
JN982484
JN982482
JQ739828
JN982480
Zym. tritici
CPC 18117
Avena sp.
Iran
–
JQ739801
JF700986
JF700817
JQ739857
JF700885
CBS: CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands; CPC: Culture collection of Pedro Crous, housed at CBS; IMI: International Mycological Institute, CABI-Bioscience, Egham, Bakeham Lane, U.K.; MP: Working collection of Sandra
Videira; S: Working collection of William Quaedvlieg.
1
2
Btub: β-tubulin; EF-1α: Translation elongation factor 1-alpha; ITS: internal transcribed spacers and intervening 5.8S nrDNA; LSU: 28S large subunit of the nrRNA gene; RPB2: RNA polymerase II second largest subunit.
Sizing up Septoria
321
Quaedvlieg et al.
0.8
0.96
0.98
0.95
0.58
0.1
1 Septoria
Mycosphaerellaceae
0.56
Septoria galeopsidis CBS 102314
Septoria calendulae CBS 349.58
Septoria epilobii CBS 109084
Septoria epilobii CBS 109085
Septoria galeopsidis CBS 102411
Septoria galeopsidis CBS 191.26
Septoria melissae CBS 109097
Septoria orchidearum CBS 457.78
Septoria verbascicola CBS 102401
Septoria taraxaci CBS 567.75
Septoria stachydis CBS 109115
Septoria stachydis CBS 109127
Septoria stachydis CBS 347.58
Septoria orchidearum CBS 128631
Septoria siegesbeckiae CBS 128659
Septoria siegesbeckiae CBS 128661
Septoria stachydis CBS 102326
Septoria cerastii CBS 128612
Septoria violae-palustris CBS 128644
Septoria chelidonii CBS 128607
Septoria digitalis CBS 391.63
Septoria sp. CPC 23104
Septoria leptostachyae CBS 128613
1 Septoria leptostachyae CBS 128628
Septoria codonopsidis CBS 128620
Septoria urticae CBS 102316
Septoria urticae CBS 102375
Septoria crepidis CBS 128619
1
Septoria crepidis CBS 128608
Septoria tormentillae CBS 128643
1
Septoria tormentillae CBS 128647
Septoria callistephi CBS 128590
Septoria convolvuli CBS 128627
Septoria perillae CBS 128655
Septoria dysentericae CPC 12328
Septoria pachyspora CBS 128652
Septoria sp. CBS 128650
Septoria glycinicola CBS 128618
Septoria villarsiae CBS 514.78
Septoria phlogis CBS 128663
Septoria polygonorum CBS 109834
Septoria polygonorum CBS 347.67
Septoria epambrosiae CBS 128629
Septoria cf. stachydicola CBS 128668
Septoria saccardoi CBS 128756
Septoria exotica CBS 163.78
Septoria posoniensis CBS 128645
Septoria chrysanthemella CBS 128622
Septoria cirsii CBS 128621
Septoria lycoctoni CBS 109089
Septoria napelli CBS 109105
Septoria violae-palustris CBS 128660
Septoria lamiicola CBS 123884
1 Septoria senecionis CBS 102366
Septoria senecionis CBS 102381
Septoria leucanthemi CBS 109090
Fig. 1. A Bayesian 50 % majority rule RPB2/LSU consensus tree containing all Septoria and septoria-like taxa available at the CBS, which cluster in or near the Mycosphaerellaceae.
Bayesian posterior probabilities support values for the respective nodes are displayed in the tree. A stop rule (set to 0.01) for the critical value for the topological convergence
diagnostic was used for the Bayesian analysis. The tree was rooted to Phaeosphaeria nodorum (CBS 259.49). The scalebar indicates 0.1 expected changes per site.
322
Sizing up Septoria
Septoria obesa CBS 128588
Septoria obesa CBS 128623
Septoria obesa CBS 354.58
Septoria chrysanthemella CBS 128716
Septoria pseudonapelli CBS 128664
Septoria putrida CBS 109088
Septoria lycopicola CBS 128651
Septoria paridis CBS 109111
Septoria paridis CBS 109108
Septoria sp. CBS 128658
Septoria malagutii CBS 106.80
1
Septoria lycopersici CBS 128654
Septoria cucurbitacearum CBS 178.77
Septoria apiicola CBS 400.54
Septoria petroselini CBS 182.44
Septoria anthrisci CBS 109020
Septoria astericola CBS 128593
Septoria cf. rubi CBS 128646
0.56
Septoria cf. agrimoniicola CBS 128602
Septoria cf. agrimoniicola CBS 128585
Septoria tinctoriae CBS 129154
Septoria bothriospermi CBS 128599
Septoria erigerontis CBS 109094
1
Septoria erigerontis CBS 186.93
Septoria erigerontis CPC 12340
Septoria lysimachiae CBS 102315
Septoria lysimachiae CBS 123795
Septoria helianthi CBS 123.81
Septoria matricariae CBS 109001
Septoria atropurpurea CBS 348.58
Septoria sp. CPC 19976
Septoria protearum CBS 177.77
Septoria protearum CBS 390.59
1 Septoria limonum CBS 419.51
Septoria protearum CBS 778.97
Septoria protearum CBS 135477
0.83
Septoria sp. CPC 21105
Septoria citricola CBS 356.36
Septoria justiciae CBS 128625
Septoria linicola CBS 316.37
1
Septoria
cretae CBS 135095
0.59
Septoria cucubali CBS 102386
Septoria sp. CPC 19793
0.74
Septoria sp. CPC 19304
Septoria protearum CBS 566.88
Septoria lepidiicola CBS 128635
Septoria cruciatae CBS 123747
0.71
Septoria verbenae CBS 113438
Septoria sisyrinchii CBS 112096
0.98
0.76
Septoria chromolaenae CBS 113373
1 Septoria anthurii CBS 346.58
0.67
Septoria passiflorae CBS 102701
1 Septoria abei CBS 128598
Septoria hibiscicola CBS 128615
Septoria eucalyptorum CBS 118505
1
Mycosphaerellaceae
0.1
1 Septoria (continued)
Fig. 1. (Continued).
www.studiesinmycology.org
323
Quaedvlieg et al.
Septoria oenanthis CBS 128667
Septoria sii CBS 102370
Septoria mazi CBS 128755
Septoria lactucae CBS 108943
1 Septoria lactucae CBS 352.58
Septoria sp. CBS 128757
Septoria gentianae CBS 128633
0.86
Septoria oenanthicola CBS 128649
Septoria coprosma CBS 113391
0.64
Septoria campanulae CBS 128604
Septoria sp. CPC 19485
Septoria dearnessii CBS 128624
Septoria
hippocastani CPC 23103
1
Septoria hippocastani CBS 411.61
0.73
1 Septoria astragali CBS 109116
1
Septoria astragali CBS 123878
0.85
Septoria rumicum CBS 503.76
0.99
Septoria stellariae CBS 102376
Septoria scabiosicola CBS 102336
1 Septoria scabiosicola CBS 108981
Septoria scabiosicola CBS 109093
Septoria scabiosicola CBS 102334
“Pseudocercosporella” magnusiana CBS 114735
Septoria bupleuricola CBS 128603
Septoria clematidis CBS 108983
Septoria sp. CPC 19716
Sphaerulina amelanchier CPC 23106
Sphaerulina amelanchier CBS 135110
1
Sphaerulina amelanchier CPC 23107
Sphaerulina amelanchier CPC 23105
0.97
Sphaerulina amelanchier CBS 102063
Sphaerulina pseudovirgaureae CBS 135109
0.98
Sphaerulina gei CBS 102318
1
Sphaerulina gei CBS 128632
0.55
Sphaerulina viciae CBS 131898
Sphaerulina patriniae CBS 128653
0.84
Sphaerulina cercidis CBS 129151
Sphaerulina cercidis CBS 501.50
Sphaerulina cercidis CBS 128634
Sphaerulina cercidis CBS 118910
1 Sphaerulina menispermi CBS 128761
1 Sphaerulina menispermi CBS 128666
0.94
Sphaerulina hyperici CBS 102313
Sphaerulina azaleae CBS 128605
1
Sphaerulina azaleae CBS 352.49
Sphaerulina berberidis CBS 324.52
1 Sphaerulina tirolensis CBS 109018
0.53
Sphaerulina tirolensis CBS 109017
1 Sphaerulina socia CBS 355.58
Sphaerulina socia CBS 357.58
Sphaerulina quercicola CBS 109009
Sphaerulina quercicola CBS 663.94
Sphaerulina quercicola CBS 115137
1
Sphaerulina quercicola CBS 115136
Sphaerulina quercicola CBS 115016
0.55
Sphaerulina populicola CBS 100042
1
0.97
Sphaerulina musiva CBS 130570
Sphaerulina frondicola CBS 391.59
0.55
Sphaerulina aceris CBS 687.94
1 Sphaerulina betulae CBS 116724
1
Sphaerulina betulae CBS 128600
0.98
0.91
Fig. 1. (Continued).
324
2 Sphaerulina
Mycosphaerellaceae
0.1
1 Septoria (continued)
Sizing up Septoria
Sphaerulina oxyacanthae CBS 135098
Sphaerulina abeliceae CBS 128591
1 Sphaerulina cornicola CBS 102332
Sphaerulina cornicola CBS 102324
Sphaerulina westendorpii CBS 117478
Sphaerulina myriadea CBS 124646
Caryophylloseptoria lychnidis CBS 109099
1 Caryophylloseptoria lychnidis CBS 109102
Caryophylloseptoria lychnidis CBS 109098
0.75
Caryophylloseptoria lychnidis CBS 109101
1 Caryophylloseptoria silenes CBS 109100
0.57
Caryophylloseptoria silenes CBS 109103
Caryophylloseptoria spergulae CBS 397.52
1
1
Caryophylloseptoria spergulae CBS 109010
Caryophylloseptoria pseudolychnidis CBS 128614
1
Caryophylloseptoria pseudolychnidis CBS 128630
Caryophylloseptoria pseudolychnidis CBS 128630
Pseudocercosporella capsellae CBS 112032
Pseudocercosporella capsellae CBS 112033
1
Pseudocercosporella capsellae CBS 118412
Pseudocercosporella capsellae CBS 127.29
0.98
Mycosphaerella brassicicola CBS 228.32
Mycosphaerella brassicicola CBS 267.53
0.94
Mycosphaerella sp. CPC 11677
0.98
Passalora depressa CPC 14915
Pseudocercosporella pastinacae CBS 114116
Cercospora zebrina CBS 118790
1
Cercospora zebrina CBS 137.56
Cercospora zebrina IMI 262766
0.82
Cercospora capsici CBS 118712
1
Cercospora capsici CBS 118712
1 Cercospora beticola CBS 124.31
Cercospora beticola CPC 5070
Phloeospora ulmi CBS 101564
Phloeospora ulmi CBS 109835
1
Phloeospora ulmi CBS 344.97
Phloeospora ulmi CBS 613.81
1 ‘Septoria’ gladioli CBS 353.29
‘Septoria’ gladioli CBS 121.20
1 Passalora dioscoreae CPC 10855
Passalora dioscoreae CPC 11513
Neoseptoria caricis CBS 135097
Pseudocercospora eucalyptorum CBS 116303
Pseudocercospora eucalyptorum CPC 13816
0.58
1
Pseudocercospora robusta CBS 111175
0.55
Pseudocercospora natalensis CBS 111069
Pseudocercospora norchiensis CBS 120738
1
Pseudocercospora chiangmaiensis CBS 123244
1
0.99
Pseudocercospora schizolobii CBS 120029
1
Pseudocercospora madagascariensis CBS 124155
Pseudocercospora tereticornis CPC 13299
Zymoseptoria brevis CBS 128853
1 Zymoseptoria brevis CPC 18112
1
Zymoseptoria brevis CPC 18109
Zymoseptoria pseudotritici CBS 130976
0.69
1
Zymoseptoria tritici CPC 18117
Zymoseptoria passerinii CBS 120385
1 Zymoseptoria passerinii CBS 120384
Zymoseptoria halophila CPC 18105
Ramularia eucalypti CBS 120726
0.96
Ramularia
pratensis CPC 11294
0.99
Ramularia lamii CPC 11312
1
Ramularia sp. CBS 115913
Ramularia endophylla CBS 113265
0.59
1
1
1
3 Caryophylloseptoria
4 pseudocercosporella-like
5 Cercospora
6 Phloeospora
7 septoria-like
8 passalora-like
9 Neoseptoria
10 Pseudocercospora
11 Zymoseptoria
Mycosphaerellaceae
0.1
2 Sphaerulina (continued)
12 Ramularia
Fig. 1. (Continued).
www.studiesinmycology.org
325
Quaedvlieg et al.
1
1
8x
0.98
1
1
Mycosphaerellaceae
0.1
Dothistroma pini CBS 116484
Dothistroma pini CBS 116485
1
Dothistroma pini CBS 116487
Dothistroma pini CBS 121005
1
Dothistroma pini CBS 121011
Dothistroma septosporum CPC 16799
1
1
1
Dothistroma septosporum CBS 383.74
Dothistroma septosporum CPC 16798
1 Stromatoseptoria castaneicola CBS 102322
Stromatoseptoria castaneicola CBS 102377
L. acicola CBS 322.33
L. acicola CBS 133791
1
L. guatamalensis IMI 281598
1
L. longispora CBS 133602
0.66
L. brevispora CBS 133601
1
1 Ph. eugeniae CPC 15143
Ph. eugeniae CPC 15159
Cy. martiniana CBS 135102
Z. citri CPC 13467
0.51
0.92
Z. scaevolicola CBS 127009
1
Z. anthuriicola CBS 118742
Z. lonicericola CBS 125008
1
1
Z. nocoxi CBS 125009
Po. terminaliae CBS 135475
1
Po. terminaliae CBS 135106
Po. tabebuiae-serratifoliae CBS 112650
1 Ruptoseptoria unedonis CBS 355.86
Ruptoseptoria unedonis CBS 755.70
D. commune CPC 12397
Readeriella eucalypti CPC 13401
0.95
1
Readeriella readeriellophora CPC 12920
1
Readeriella angustia CBS 124998
T. suberosa CPC 13106
Teratosphaeria parva CBS 119901
Teratosphaeria molleriana CBS 111164
0.91
Teratosphaeria toledana CBS 113313
1
Teratosphaeria juvenalis CBS 111149
Teratosphaeria pseudoeucalypti CBS 124577
septoria-like sp. CBS 134910
Cylindroseptoria ceratoniae CBS 477.69
0.73
Cylindroseptoria pistaciae CBS 471.69
Pseudoseptoria obscura CBS 135103
1
Pseudoseptoria collariana CBS 135104
Phaeosphaeria “nodorum” CBS 259.49
13 Dothistroma
14 Stromatoseptoria
15 Lecanosticta
16 Phaeophleospora
17 Cytostagonospora
18 Zasmidium
19 Polyphialoseptoria
20 Ruptoseptoria
21 Dissoconium
Dissoconiaceae
22 Readeriella
Teratosphaeriaceae
23 Teratosphaeria
24 septoria-like
25 Cylindroseptoria
Incertae sedis
26 Pseudoseptoria
Dothioraceae
Dothideaceae
4x
Fig. 1. (Continued).
Table 2. Primer combinations used during this study for generic ampliication and sequencing.
locus
Translation elongation factor-1α
β-tubulin
Primer
Primer sequence 5’ to 3’
Annealing
temperature (°c)
orientation
reference
EF1-728F
CATCGAGAAGTTCGAGAAGG
52
Forward
Carbone & Kohn (1999)
EF-2
GGARGTACCAGTSATCATGTT
52
Reverse
O’Donnell et al. (1998)
T1
AACATGCGTGAGATTGTAAGT
52
Forward
O’Donnell & Cigelnik (1997)
β-Sandy-R
GCRCGNGGVACRTACTTGTT
52
Reverse
Stukenbrock et al. (2012)
RNA polymerase II second largest
subunit
fRPB2-5F
GAYGAYMGWGATCAYTTYGG
49
Forward
Liu et al. (1999)
fRPB2-414R
ACMANNCCCCARTGNGWRTTRTG
49
Reverse
Quaedvlieg et al. (2011)
LSU
LSU1Fd
GRATCAGGTAGGRATACCCG
52
Forward
Crous et al. (2009a)
LR5
TCCTGAGGGAAACTTCG
52
Reverse
Vilgalys & Hester (1990)
ITS
ITS5
GGAAGTAAAAGTCGTAACAAGG
52
Forward
White et al. (1990)
ITS4
TCCTCCGCTTATTGATATGC
52
Reverse
White et al. (1990)
326
Sizing up Septoria
Table 3. Ampliication success, phylogenetic data and the substitution models used in the phylogenetic analysis, per locus.
locus
rPB2
lsu
Ampliication succes (%)
99.20 %
100 %
Number of characters
327
792
Unique site patterns
197
216
Substitution model used
GTR-I-gamma
GTR-I-gamma
Number of generations (1000×)
2575
Total number of trees (n)
5152
Sampled trees (n)
3864
which 26 contained species belonging to the Septoria (-like) complex.
These 47 resolved clades belong to a multitude of different families
within the Dothidiomycetes ranging from the Mycosphaerellaceae in
the Capnodiales to the Lentitheciaceae in the Pleosporales. It is still
unclear within the Dothidiomycetes where the phylogenetic family
borders are located, or even how many phylogenetically substainable
families there actually are. The family annotation in the phylogenetic
trees (Figs 1, 2) is therefore based on the closest LSU neighbour that
was available in GenBank, with clades treated as incertae sedis if no
closer relationship than 97 % could be found.
Septoria and septoria-like genera
In addition to Septoria s. str., numerous septoria-like genera
(pycnidial/acervular/stromatic conidioma with iliform conidia) have
since been described. Although the majority of these have no extype culture available for DNA analysis, many have type material
deposited in herbaria, which were available for morphological
examination. A summary of these genera is provided below.
Pycnidial forms
Cytostagonospora Bubák, Ann. Mycol. 14: 150. 1916. Fig.
3.
Mycelium immersed, dark brown, branched, septate. Conidiomata
pycnidial, amphigenous, separate, globose, dark brown to black,
immersed, unilocular, thick-walled, clypeate; walls of dark brown,
thick-walled textura angularis to textura globulosa, becoming
hyaline towards the conidiogenous region, extending in the upper
part to become a circular clypeus of similar thickness to the wall.
Ostiole central, circular, papillate to shortly rostrate, depressed,
situated immersed within the clypeus. Conidiophores reduced to
conidiogenous cells. Conidiogenous cells holoblastic, determinate,
discrete, lageniform, hyaline, smooth, formed from the inner cells of
the pycnidial wall. Conidia hyaline, 0–2-euseptate, not constricted
at septa, base truncate, apex obtuse, thin-walled, eguttulate,
smooth, iliform, often curved (Sutton 1980).
Type species: C. photiniicola Bubák, Ann. Mycol. 14(3–4): 150.
1916.
Notes: Von Arx (1983) and Sutton (1980) disagreed about the link
of Cytostagonospora to Septoria. Von Arx treated it as a synonym
of Septoria, while Sutton retained it as a separate genus.
www.studiesinmycology.org
Dearnessia Bubák, Hedwigia 58: 25. 1916.
Mycelium hyaline to brown, branched, septate. Conidiomata
pycnidial, amphigenous, separate, globose, immersed, brown;
wall of thin-walled textura angularis. Ostiole central, circular,
papillate. Setae ostiolar, approximately straight, unbranched,
tapered towards apex, dark brown, smooth, thin-walled, septate.
Conidiogenous cells holoblastic, determinate, discrete, doliiform
to ampulliform, hyaline, smooth and formed from the inner layer
of the pycnidial wall. Conidia cylindrical to irregular, hyaline,
1–multi-transversely euseptate, rarely with 1–2 longitudinal
eusepta, continuous or constricted, often tapered at the apex,
base truncate, thin-walled, smooth, guttulate or not (Sutton 1980).
Type species: D. apocyni Bubák, Hedwigia 58: 25. 1916.
Dearnessia apocyni Bubák, Hedwigia 58: 25. 1916. Figs 4,
5.
Leaf spots amphigenous, irregular, feathery to angular, dark brown,
3–6 mm diam, surrounded by a wide chlorotic zone up to 3 mm
diam. Conidiomata epiphyllous, pycnidial, erumpent, up to 150
µm diam, with central ostiole; wall of 3–6 layers of brown textura
angularis. Conidiogenous cells doliiform, globose to subcylindrical,
hyaline, smooth, thin-walled, mode of proliferation obscure, 5–10 ×
4–6 µm. Conidia hyaline, smooth, subcylindrical to obclavate, apex
obtuse, base truncate to subobtuse, straight to irregular (lateral
swellings?), 1–4-septate, 16–33 × 5–8 µm.
Specimen examined: canada, Ontario, London, on leaves of Apocynum
androsaemifolium (Apocynaceae), 11 Aug. 1910, J. Dearness, holotype F43227.
Notes: Because the specimen is in poor condition, no deinite
conclusion could be reached about its potential relationships.
However, D. apocyni does appear septoria-like in general
morphology.
Jahniella Petr., Ann. Mycol. 18: 123. 1921. [1920]. Figs 6, 7.
Mycelium branched, immersed, septate, brown. Conidiomata
pycnidial, supericial on epidermis, immersed, separate, globose,
papillate, dark brown, thick-walled, sclerenchymatic; wall consisting
of an outer layer of dark brown, thick-walled textura angularis,
a middle layer of 8 cells thick, of hyaline to pale brown, thickwalled cells, and an inner layer of thin-walled, hyaline, irregular
cells. Ostiole single, circular, with a distinct channel and hyaline
327
Quaedvlieg et al.
Parastagonospora avenae CBS 289.69
Parastagonospora avenae CBS 290.69
Parastagonospora caricis CBS 135671
0.99
Parastagonospora nodorum CBS 110109
1
Phaeosphaeria nigrans CBS 307.79
0.84
Parastagonospora poae CBS 135089
1
Parastagonospora poae CBS 135091
1
Parastagonospora “nodorum” CBS 259.49
1
“Septoria” agropyrina CBS 387.64
“Stagonospora” foliicola CBS 110111
1
“Septoria” arundinacea CBS 133.68
0.96
Neostagonospora elegiae CBS 135101
0.83
Neostagonospora caricis CBS 135092
0.91
phaeosphaeria-like sp. CBS 135469
1
0.94
Chaetosphaeronema hispidulum CBS 216.75
Phaeosphaeria caricicola CBS 603.86
1
Phaeosphaeria juncicola CBS 110108
0.79
Phaeosphaeriopsis glaucopunctata CBS 653.86
stagonospora-like sp. CBS 135483
1
1
stagonospora-like sp. S619
“Phaeosphaeria” vagans CBS 604.86
0.66
“Phaeosphaeria”
pontiformis CBS 117487
1
“Septoria” arundinacea CBS 281.72
0.70
Leptosphaeria albopunctata CBS 254.64
1
Sclerostagonospora phragmiticola CBS 338.86
“Phaeosphaeria” phragmiticola CBS 459.84
0.77
phaeosphaeria-like sp. CBS 135466
0.78
1
phaeosphaeria-like sp. CPC 12130
Phaeosphaeria sp. CBS 206.87
0.98
1
Phaeosphaeria papayae CBS 135416
0.99
Phaeosphaeria oryzae CBS 110110
0.97
stagonospora-like sp. CBS 135482
0.94
Phaeosphaeria sp. CBS 135465
stagonospora-like sp. CBS 516.74
phaeosphaeria-like sp. CBS 123.76
1
0.96
phaeosphaeria-like sp. CBS 135461
Neosetophoma
samarorum CBS 139.96
1
Neosetophoma
samarorum CBS 568.94
0.93
1
0.55
Neosetophoma samarorum CBS 138.96
“Phaeosphaeria” typharum CBS 296.54
1
“Phaeosphaeria” alpina CBS 456.84
Paraphoma chrysanthemicola CBS 172.70
1
Paraphoma chrysanthemicola CBS 522.66
0.98
Paraphoma radicina CBS 111.79
1
0.59
Paraphoma
radicina CBS 102875
0.86
Paraphoma dioscoreae CPC 11361
1
Paraphoma dioscoreae CBS 135100
0.71
Paraphoma dioscoreae CPC 11355
Paraphoma fimeti CBS 170.70
1
1
Paraphoma fimeti CBS 368.91
Xenoseptoria neosaccardoi CBS 120.43
0.98
1
Xenoseptoria neosaccardoi CBS 128665
Vrystaatia aloeicola CBS 135107
Setophoma terrestris CBS 135470
Setophoma terrestris CBS 335.87
1
Setophoma terrestris CBS 377.52
Setophoma terrestris CBS 335.29
1
Setophoma sacchari CBS 333.39
1
Setophoma chromolaenae CBS 135105
0.83
1
28 Neostagonospora
29 Phaeosphaeriopsis
30 Incertae sedis
31 Phaeosphaeria
32 Neosetophoma
33 Paraphoma
34 Xenoseptoria
Phaeosphaeriaceae
0.01
27 Parastagonospora
35 Vrystaatia
1
36 Setophoma
Fig. 2. A Bayesian 50 % majority rule RPB2/LSU consensus tree containing all Septoria and septoria-like taxa available at the CBS, which cluster in or near the
Phaeosphaeriaceae. Bayesian posterior probabilities support values for the respective nodes are displayed in the tree. A stop rule (set to 0.01) for the critical value
for the topological convergence diagnostic was used for the Bayesian analysis. The tree was rooted to Dothistroma pini (CBS 121005). The scalebar indicates 0.01
expected changes per site.
328
Sizing up Septoria
Coniothyrium carteri CBS 101633
Coniothyrium carteri CBS 105.91
37
0.82
Coniothyrium glycinicola CBS 124141
0.93
Coniothyrium sidae CBS 135108
Xenobotryo. calamagrostidis CBS 303.71
38
“Septoria” steviae CBS 120132
0.97
1
39
Boeremia telephii CBS 135415
Phoma
herbarum
CBS
615.75
0.59
40
Acicuseptoria rumicis CBS 522.78
Stagonospora pseudocaricis CBS 135132
1
Stagonospora pseudocaricis CBS 135414
1
Stagonospora paludosa CBS 135088
Stagonospora cf. paludosa CBS 130005
0.62
Stagonospora pseudovitensis S602
1
1 Stagonospora pseudovitensis CBS 135094
41
0.94
Stagonospora perfecta CBS 135099
0.89
Stagonospora sp. CBS 135096
0.97
Stagonospora duoseptata CBS 135093
Stagonospora uniseptata CPC 22151
1
1
Stagonospora uniseptata CPC 22150
Stagonospora uniseptata CBS 135090
0.95
42
Corynespora leucadendri CBS 135133
Setoseptoria
phragmitis
CBS
114966
1
43
1
Setoseptoria phragmitis CBS 114802
septoria-like sp. CBS 135473
44
Septorioides pini-thunbergii CBS 473.91
Phlyctema vincetoxici CBS 123727
1
Phlyctema vincetoxici CBS 123726
45
1
Phlyctema vincetoxici CBS 123743
septoria-like sp. CBS 135481
septoria-like sp. CBS 135471
“Septoria” tanaceti CBS 358.58
Kirstenboschia
diospyri CBS 134911
1
46
Kirstenboschia diospyri CPC 19870
Phlogicylindrium eucalyptorum CBS 111680 45
1
Phlogicylindrium eucalyptorum CBS 111689
Dothistroma pini CBS 121005
0.54
1
1.6x
0.93
1.4x
0.99
1
1
3.8x
3x
1.2x
1
Coniothyrium
Xenobotryosphaeria
Phoma
Coniothyriaceae
Pleosporales
Didymellaceae
Acicuseptoria
Leptosphaeriaceae
Stagonospora
Massarinaceae
Corynespora
Corynesporascaceae
Setoseptoria
Lentitheciaceae
Septorioides
Botryosphaeriaceae
Phlyctema
Dermateaceae
Incertae sedis
Kirstenboschia
Phlogicylindrium
Incertae sedis
Sordariomycetes
incertae sedis
0.01
Fig. 2. (Continued).
periphysoid cells. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells holoblastic, determinate, discrete, hyaline,
ampulliform, lining the wall of the pycnidium. Conidia straight or
slightly curved, hyaline, thin-walled, smooth, 3–4-euseptate,
eguttulate, truncate at the base, slightly tapered to the apex (Sutton
1980).
Type species: J. bohemica Petr., Ann. Mycol. 18(4–6): 123. 1921.
[1920]
Specimen examined: czech republic, Bohemia, on stems of Scrophularia nodosa
(Scrophulariaceae), 18 Mar. 1916, J. Jahn, holotype K(M) 180917, slides ex BPI.
Note: The specimen correlates closely with the description provided
by Sutton (1980), except that the conidiomata are supericial, not
immersed in the epidermis.
Megaloseptoria Naumov, Morbi Plantarum 14: 144. 1925.
Figs 8, 9.
Mycelium immersed, branched, septate, brown. Conidiomata
pycnidial, separate, globose, slightly papillate, dark brown to
www.studiesinmycology.org
black, supericial, sessile, often aggregated in groups, unilocular,
thick-walled; wall of several cell layers of brown textura angularis,
more darkly pigmented on the outside. Ostiole single, circular.
Conidiophores hyaline, branched, septate (mainly at the base),
smooth, straight or irregular, formed from the inner cells of the
pycnidial wall. Conidiogenous cells enteroblastic, determinate,
discrete or integrated, doliiform, ampulliform or irregularly
cylindrical, hyaline, smooth, collarette evident, channel wide,
periclinal thickening present. Conidia hyaline to pale brown with
several transverse eusepta, continuous, tapered near the obtuse
apex and truncate base, thin-walled, smooth, cylindrical, straight
or slightly curved, often with 2 guttules in each cell (Sutton 1980).
Type species: M. mirabilis Naumov, Morbi Plant. Script. Sect.
Phytopath. Hort. Bot. Prince. USSR 14: 144. 1925.
Megaloseptoria mirabilis Naumov, Morbi Plantarum 14:
144. 1925.
Conidiomata aggregated in a black stroma at the ends of
branchlets, globose, black, smooth, with central ostiole, up to
600 µm diam, papillate; wall of 3–8 layers of dark brown textura
329
Quaedvlieg et al.
Fig. 3. Conidia and conidiogenous cells of Cytostagonospora photiniicola (redrawn from Sutton 1980). Scale bar = 10 µm.
Fig. 4. Conidia and conidiogenous cells of Dearnessia apocyni (F43227). Scale bars = 10 µm.
Fig. 5. Dearnessia apocyni (F43227). A. Leaf spot. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
330
Sizing up Septoria
Fig. 6. Conidia and conidiogenous cells of Jahniella bohemica (redrawn from Sutton 1980). Scale bar = 10 µm.
Fig. 7. Jahniella bohemica [K(M) 180917]. A. Vertical section through conidioma. B. Ostiolar region with loose cells. C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
Fig. 8. Conidia and conidiogenous cells of Megaloseptoria mirabilis (MA-Fungi 6978-1). Scale bars = 10 µm.
www.studiesinmycology.org
331
Quaedvlieg et al.
Fig. 9. Megaloseptoria mirabilis (MA-Fungi 6978-1). A. Conidiomata on host tissue. B. Conidiogenous cells. C. Conidia. Scale bars = 10 µm.
angularis. Conidiogenous cells lining the cavity, subcylindrical
to ampulliform, hyaline, smooth, 7–15 × 4–8 µm; proliferating
percurrently near apex. Conidia solitary, scolecosporous, variously
curved, subcylindrical, tapering in upper third to obtuse apex, base
truncate, 3–4 µm diam, transversely 30–40-septate, (170–)200–
250 × (5–)6(–7) µm.
Specimen examined: Switzerland, Zürich, St. Schnach., on branchlets of Pinus
pungens var. glauba (Pinaceae), 10 July 1951, E. Müller, holotype MA-Fungi 69781.
Note: Megaloseptoria differs from Septoria in that the conidiomata
are aggregated in a black stroma, which is not the case in Septoria
s. str.
Phaeoseptoria Speg., Revista Mus. La Plata 15(2): 39.
1908.
Leaf spots angular-subcircular, 0.5–3 mm diam, becoming conluent.
Conidiomata pycnidial, epiphyllous, subepidermal, black, 60–90 µm
diam. Conidiogenesis cells hyaline, smooth, holoblastic (?). Conidia
iliform, obclavate, smooth, 1–3-euseptate, medium brown, 30 × 3 µm
(Saccardo & Trotter 1913, Walker et al. 1992, Crous et al. 1997).
Type species: P. papayae Speg., Revista Mus. La Plata 15(2): 39.
1908.
Notes: Phaeoseptoria papayae was originally described from
leaf spots on Carica papaya collected in the São Paulo Botanical
Garden, Brazil. Presently there are numerous clades that contain
isolates conforming to this morphology, and this matter can only be
resolved once fresh material of P. papayae has been recollected to
clarify its phylogeny (see below).
Pseudoseptoria Speg., Ann. Mus. Nac. B. Aires, Ser. 3 13:
388. 1910.
Mycelium immersed, branched, septate, pale brown. Conidiomata
pycnidial, solitary or linearly aggregated, immersed, brown, globose,
unilocular; walls thin, of pale brown textura angularis. Ostiole
distinct, central, circular. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells discrete, determinate or indeterminate,
hyaline, smooth, ampulliform with a prominent cylindrical papilla
with several percurrent proliferations at the apex. Conidia falcate,
fusoid, acutely rounded at each end, hyaline, aseptate, guttulate,
smooth, thin-walled (Sutton 1980).
332
Type species: P. donacicola Speg., Ann. Mus. Nac. B. Aires, Ser. 3
13: 388. 1910.
Note: Species of Pseudoseptoria are plant pathogenic to members
of Poaceae.
Rhabdospora (Durieu & Mont. ex Sacc.) Sacc., Syll. Fung.
(Abellini) 3: 578. 1884. nom. cons.
Basionym: Septoria sect. Rhabdospora Durieu & Mont., in Durieu,
Expl. Sci. Alg. 1 (livr. 15): 592. 1849. [1846–1849].
Type species: R. oleandri Durieu & Mont., in Durieu, Expl. Sci. Alg.
1 (livr. 15): 593. 1849 [1846–1849].
Notes: Rhabdospora is a poorly deined genus, originally
established to accommodate septoria-like species occurring on
stems (Priest 2006). Of the 11 species treated by Sutton (1980),
most are currently placed in Septoria. This genus is in need of
revision pending the recollection of fresh material (on Nerium
oleander from Algeria).
Sclerostagonospora Höhn., Hedwigia 59: 252. 1917.
Conidiomata pycnidial, immersed, separate, dark brown to black,
globose, unilocular; walls thin, composed of thick-walled, dark
brown textura angularis; ostiole single, circular, central, papillate.
Conidiophores reduced to conidiogenous cells. Conidiogenous cells
holoblastic, determinate, discrete, hyaline, smooth, ampulliform to
irregular, formed from the inner cells of the pycnidial wall. Conidia
subcylindrical, pale brown, thin-walled, minutely verruculose,
3-euseptate, sometimes slightly constricted at the septa (from
Sutton 1980).
Type species: S. heraclei (Sacc.) Höhn., Hedwigia 59: 252. 1917.
Note: Sclerostagonospora differs from Stagonospora in having
pigmented conidia.
Septoria (Sacc.) Sacc., Syll. Fung 3: 474. 1884. nom. cons.
Figs 10, 11.
= Septaria Fr., Novit. Fl. Svec. 5: 78. 1819. nom. rejic.
Mycelium slow-growing, pale brown, septate, immersed.
Conidiomata pycnidial, immersed, separate or aggregated (but
not conluent), globose, papillate (or not), brown, wall of thin, pale
Sizing up Septoria
Conidiomata pycnidial, immersed, unilocular, globose, separate,
ostiolate; walls of dark brown, thick-walled textura angularis, and
on the inside of hyaline, thin-walled, lattened cells. Conidiophores
reduced to conidiogenous cells. Conidiogenous cells doliiform,
hyaline, with several percurrent proliferations at the apex, formed
from the inner cells of the pycnidial wall. Conidia hyaline, smooth to
inely verruculose, 1–multiseptate, cylindrical or fusoid-ellipsoidal,
straight or slightly curved, often guttulate, constricted or not at
septa.
Type species: S. paludosa (Sacc. & Speg.) Sacc., Syll. Fung.
(Abellini) 3: 453. 1884.
Fig. 10. Conidia and conidiogenous cells of Septoria cytisi (BPI USO 378994). Scale
bars = 10 µm.
brown textura angularis, inner layer of lattened, hyaline textura
angularis, frequently somewhat darker and more thick-walled
around the ostiole. Ostiole single, circular, central. Conidiophores
reduced to conidiogenous cells. Conidiogenous cells holoblastic,
either determinate or indeterminate, proliferating sympodially
and/or percurrently, hyaline, smooth, ampulliform, dolliform or
lageniform to short cylindrical; scars unthickened. Conidia hyaline,
multiseptate, iliform, smooth, continuous or constricted at septa.
Sexual states are mycosphaerella-like.
Type species: S. cytisi Desm., Ann. Sci. Nat. Bot. 8: 24. 1847.
Specimen examined: Slovakia, Muehlthal near Bratislava (Pressburg), on leaves
of Laburnum anagyroides (Leguminosae), 1884, J.A. Baeumler, BPI USO 378994.
Note: The ITS and LSU sequences of this specimen were published
respectively under GenBank accession numbers JF700932 and
JF700954.
Stagonospora (Sacc.) Sacc., Syll. Fung. (Abellini) 3: 445.
1884. nom. cons.
Basionym: Hendersonia subgen. Stagonospora Sacc., Michelia 2
(no. 6): 8. 1880.
Stenocarpella Syd. & P. Syd., Ann. Mycol. 15(3–4): 258.
1917. Fig. 12.
Mycelium immersed, brown, branched, septate. Conidiomata
pycnidial, separate or sometimes conluent, globose or elongated,
dark brown, subepidermal, unilocular, thick-walled; walls
composed of dark brown, thick-walled textura angularis. Ostiole
single, circular, papillate, protruding. Conidiophores usually absent.
Conidiogenous cells cylindrical, hyaline, determinate, discrete,
phialidic, with collarette and minute periclinal thickening, lining the
inner layer of the pycnidial wall. Conidia subcylindrical, straight or
curved, fusiform, apex obtuse, base tapered, truncate, thick-walled,
smooth-walled, granular, pale to medium brown, 0–3-euseptate.
Beta conidia hyaline, scolecosporous, curved (Crous et al. 2006,
Lamprecht et al. 2011).
Type species: S. zeae Syd. & P. Syd., Ann. Mycol. 15(3–4): 258.
1917. [= S. macrospora (Earle) B. Sutton]
Specimens examined: South Africa, KwaZulu-Natal, Hlabisa, rain-damaged Bt Zea
mays hybrid (Poaceae), 2003-04 season, J. Rheeder (ex-epitype, CBS 117560 =
MRC 8615, designated in Crous et al. 2006); KwaZulu-Natal, Zea mays kernels,
2005, P. Caldwell, CPC 11863 = CBS 128560.
Notes: Stenocarpella presently contains two species, S. macrospora
and S. maydis, both causing “Diplodia ear rot of maize”. These
two taxa were previously assigned to Diplodia and Macrodiplodia,
respectively (Petrak & Sydow 1927, Sutton 1964). Several years
later, Sutton re-examining these taxa and placed them in their own
genus, Stenocarpella (Sutton 1977, 1980). Recent phylogenetic
studies conirmed that these taxa indeed cluster by themselves
Fig. 11. Septoria cytisi (BPI USO 378994). A. Leaf with symptoms. B. Close-up of leaf spot with conidiomata. C, D. Conidiogenous cells giving rise to conidia. E. Conidia. Scale
bars = 10 µm.
www.studiesinmycology.org
333
Quaedvlieg et al.
Type species: Z. tritici (Desm.) Quaedvlieg & Crous, Persoonia 26:
67. 2011.
Notes: Zymoseptoria was split off from Septoria s. str. and
redescribed by Quaedvlieg et al. (2011) based on LSU sequence
data when said authors delimitated Septoria s. str. by sequencing
the ITS and LSU sequences out of S. cytisi herbarium material.
Phylogenetic analysis showed that Zymoseptoria species cluster
within a distinct clade inside the Mycosphaerellaceae that is closely
related to Ramularia, but located distant from Septoria s. str.
Acervular forms
Asteromidium Speg., Ann. Soc. cient. argent. 26(1): 66.
1888. Figs 13, 14.
Fig. 12. Stenocarpella maydis (top) and S. macrospora (bottom) (redrawn from
Sutton 1980). Scale bars = 10 µm.
within the Diaporthales (Crous et al. 2006, Lamprecht et al. 2011),
supporting the decision of Sutton (1980).
Trichoseptoria Cavara, Atti Ist. Bot. Univ. Lab. Crittog. Pavia
2: 40. 1892.
Type species: T. alpei Cavara, Atti Ist. Bot. Univ. Lab. Crittog. Pavia
2: 40. 1892.
Notes: Not much is known about this septoria-like genus, except
that it is distinguished from Septoria by having setae on its pycnidia
with 1–2-septate, hyaline conidia. This genus is in further need of
revision once fresh material has been recollected (Citrus vulgaris,
Belgiojoso, Alps).
Mycelium immersed, branched, septate, hyaline. Conidiomata
acervular, subcuticular, separate or conluent, pulvinate to doliiform,
at the base, composed of hyaline to pale brown, thin-walled textura
angularis which extends laterally, inally with separate cells dispersed
in a mucilaginous matrix to form the overlying wall; cuticle discoloured
and occasionally pseudoparenchymatous, walls adjacent to the upper
epidermal wall also discoloured; dehiscence irregular. Conidiogenous
cells holoblastic, discrete, indeterminate, ± cylindrical, hyaline, smooth,
with 1–2 sympodial proliferations, scars unthickened, lat, formed from
the basal and lateral walls. Conidia cylindrical to fusoid, gently tapered
at each end, apex obtuse, base truncate, thin-walled, guttulate to
granular, hyaline, 3-septate (Sutton 1980).
Type species: A. imperspicuum Speg., Ann. Soc. cient. argent.
26(1): 66. 1888.
Specimen examined: Paraguay, on leaves of Sapindaceae, 1883, isotype K(M)
180228, ex B. Balansa Pl. du Paraguay No. 4085.
Notes: This genus has to be recollected (Sapindaceae, Paraguay)
to allow for a molecular comparison to other existing genera in this
Zymoseptoria Quaedvlieg & Crous, Persoonia 26: 64. 2011.
Conidiomata pycnidial, semi-immersed to erumpent, dark brown
to black, subglobose, with central ostiole; wall of 3–4 layers of
brown textura angularis. Conidiophores hyaline and smooth,
1–2-septate, or reduced to conidiogenous cells, lining the inner
cavity. Conidiogenous cells are tightly aggregated and ampulliform
to doliiform or subcylindrical, phialidic with periclinal thickening,
or with 2–3 inconspicuous, percurrent proliferations at the apex.
Conidia (Type I) solitary, hyaline, smooth, guttulate, narrowly
cylindrical to subulate, tapering towards acutely rounded apex, with
bluntly rounded to truncate base, transversely euseptate; hila not
thickened nor darkened. On OA and PDA media plates the aerial
hyphae disarticulate into phragmospores (Type II conidia) that
again give rise to Type I conidia via microcyclic conidiation; yeastlike growth and microcyclic conidiation (Type III conidia) common
on agar media (Quaedvlieg et al. 2011).
334
Fig. 13. Conidia and conidiogenous cells of Asteromidium imperspicuum (redrawn
from Sutton 1980). Scale bar = 10 µm.
Sizing up Septoria
Fig. 14. Asteromidium imperspicuum [K(M) 180228]. A. Conidiomata on host surface. B. Section through conidioma. C, D. Conidiogenous cells and conidia. Scale bars: B =
75 µm, all others = 10 µm.
complex. The morphology of the specimen examined correlates
well with the description provided by Sutton (1980).
Ciferriella Petr., Ann. Mycol. 28(5/6): 409. 1930.
Type species: C. domingensis Petr. & Cif., Ann. Mycol. 28(5/6):
409. 1930.
= Pseudocercospora Speg., Anales Mus. Nac. Hist. Nat. B. Aires, Ser. 3,
20: 437. 1910.
Pseudocercospora domingensis (Petr. & Cif.) Quaedvlieg,
Verkley & Crous, comb. nov. MycoBank MB804401. Figs 15,
16.
Basionym: Ciferriella domingensis Petr. & Cif., Ann. Mycol. 28(5/6):
409. 1930.
Leaf spots amphigenous, subcircular, medium brown with dark purple
margin, 1.5–6 mm diam. Sporulation hypophyllous, fasciculate to
sporodochial, brown, arising from a brown stroma, up to 50 µm diam.
Conidiophores medium brown, smooth, subcylindrical, 0–2-septate,
straight to once geniculate, 15–20 × 3–5 µm. Conidiogenous
cells terminal, brown, smooth to inely verruculose, ampulliform to
subcylindrical, proliferating sympodially or percurrently, tapering
to a truncate apex, 2 µm diam, 10–15 × 3–4 µm. Conidia brown,
smooth, straight to slightly curved, obclavate, apex subobtuse, base
obconically truncate, 0–3-septate, 35–60 × 3–4 µm.
Fig. 15. Conidia and conidiogenous cells of Pseudocercospora domingensis (NY
No 01048475). Scale bars = 10 µm.
the upper cells of the acervulus. Conidiogenous cells integrated or
discrete, indeterminate, cylindrical or doliiform, with several percurrent
proliferations at apex. Conidia hyaline to pale brown, 0-multiseptate,
straight, curved or irregular, truncate at the base, obtuse at the apex,
usually thin-walled, smooth, guttulate or not.
Specimen examined: dominican republic, on Vitex umbrosa (Lamiaceae), 26 May
1929, coll. R. Ciferri, det. F. Petrak, holotype ex N.Y. Bot. Gard. No 01048475.
Type species: C. dalbergiae (S. Ahmad) Petr., Sydowia 7: 369.
1953. [= C. sissoo (Syd.) B. Sutton, Mycol. Pap. 97: 14. 1964.]
Notes: The dimensions of the conidia and conidiophores correlate
with the observations of Sutton (1980). However, the conidiomata
are sporodochial to fasciculate, and not acervular. Ciferriella
domingensis is a typical Pseudocercospora sensu Crous et al.
(2013). Based on the species presently known from Vitex (Crous
& Braun 2003), it appears to represent a distinct taxon, for which a
new combination in Pseudocercospora is proposed.
Notes: The exact taxonomic position of Colletogloeum was unclear
for a long time as it included many species that appear to represent
asexual morphs of Teratosphaeria. Crous et al. (2009a–c) used ITS
sequence data from a specimen representative of C. sissoo (IMI
119162) to demonstate that the type of Colletogloeum clustered near
the Pseudocercospora complex within the Mycosphaerellaceae.
Colletogloeum Petr., Sydowia 7: 368. 1953.
Cylindrosporium Grev., Scott. crypt. l. (Edinburgh) 1: pl.
27. 1822.
= Cylindrodochium Bonord., Handb. Allgem. mykol. (Stuttgart): 132. 1851.
Mycelium immersed, branched, septate, hyaline to pale brown.
Conidiomata acervular, epidermal to subepidermal, separate,
occasionally conluent, composed of hyaline to pale brown, thin-walled
textura angularis. Conidiophores hyaline to pale brown, sparsely
branched, septate, smooth, cylindrical or slightly irregular, formed from
www.studiesinmycology.org
Mycelium immersed, branched, septate, hyaline. Conidiomata
acervular, white, slimy, subcuticular, separate or conluent,
formed of pale brown to hyaline, thin-walled textura angularis;
dehiscence irregular. Conidiophores hyaline, parallel, branched
335
Quaedvlieg et al.
Fig. 16. Pseudocercospora domingensis (NY No 01048475). A. Leaf spot. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
only at the base, 1–2-septate, smooth, formed from the upper
pseudoparenchyma. Conidiogenous cells enteroblastic, phialidic,
integrated, cylindrical, hyaline, smooth. Conidia straight or
slightly curved, aseptate, cylindrical, thin-walled, smooth, hyaline,
eguttulate (Sutton 1980).
Type species: C. concentricum Unger, Exanth. Planzen (Wien) 2:
9. 1833.
Notes: Sutton (1980), Von Arx (1983), Deighton (1987) and Braun
(1990) could not agree on the taxonomic status of this genus,
which is associated with light leaf spot of oil seed rape (sexual
morph Pyrenopeziza brassicae). This genus is in need of revision,
awaiting the recollection of fresh material of C. concentricum (on
Pulmonaria oficinalis, Germany).
Phloeospora Wallr., Fl. Crypt. Germ. (Norimbergae) 2: 176.
1833.
Fig. 17. Conidia and conidiogenous cells of Phloeosporella ceanothi (redrawn from
Sutton 1980). Scale bar = 10 µm.
Mycelium immersed, septate, hyaline. Conidiomata acervular,
subepidermal, circular, discrete or conluent, composed of hyaline
to pale brown, thin-walled textura angularis; dehiscence irregular.
Conidiophores reduced to conidiogenous cells or with one or two
supporting cells, branched at base or not. Conidiogenous cells
holoblastic, annellidic, occasionally also sympodial, discrete,
indeterminate hyaline, smooth, cylindrical, with several apical
inconspicuous annellations, formed from the upper cells of the
acervuli. Conidia hyaline, septate, smooth, guttulate or not,
cylindrical, curved, attenuated towards the apices, apex obtuse to
subobtuse, base truncate, with minute marginal frill.
to pale brown, thin-walled textura angularis. Conidiogenous cells
holoblastic, sympodial, discrete, indeterminate, hyaline, smooth,
lageniform to cylindrical, with 1–2 broad, lat unthickened apical
scars, formed from the upper pseudoparenchyma. Conidia hyaline,
2-euseptate, thin-walled, smooth, guttulate, straight, curved or
irregular, tapered gradually to an obtuse apex and abruptly to a
truncate base (Sutton 1980).
Type species: P. ulmi (Fr.) Wallr., Fl. Crypt. Germ. (Norimbergae)
2: 177. 1833.
Type species: P. ceanothi (Ellis & Everh.) Höhn., Ann. Mycol. 22(1–
2): 201. 1924.
Notes: Sexual morphs of Phloeospora have been linked to genera
that resemble the concepts of Mycosphaerella, Didymella and
Sphaerulina. Verkley & Priest (2000) already noted that this genus
is heterogeneous and in need of revision. The phylogenetic analysis
performed in this study conirmed that Phloeospora (based on P.
ulmi) clusters close to, but separate from Septoria s. str. (Fig. 1).
Notes: Not much is known of the sexual state of this genus, but
P. padi has been linked to Blumeriella jaapii (Sutton 1980). A
phylogenetic analysis performed on available isolates (unpubl.
data) indicated that Phloeosporella is polyphyletic. However, as the
type is not known from culture (on Ceanothus, California, USA),
this matter could not be resolved.
Phloeosporella Höhn., Ann. Mycol. 22: 201. 1924. Fig. 17.
Septogloeum Sacc., Michelia 2(6): 11. 1880.
Mycelium immersed, branched, septate, hyaline. Conidiomata
acervular, subepidermal, ± circular, discrete, composed of hyaline
Mycelium immersed, branched, septate, hyaline. Conidiomata
acervular, epidermal to subepidermal, separate or conluent, formed
336
Sizing up Septoria
of pale brown thin-walled pseudoparenchyma. Conidiophores
short, stout, 1–2-septate, hyaline, smooth, branched at the base,
formed from the upper pseudoparenchyma. Conidiogenous cells
phialidic, discrete or integrated, determinate, cylindrical, doliiform to
obpyriform, hyaline, smooth, with minute collarette and prominent
periclinal thickening. Conidia hyaline, 1–3-euseptate, thin-walled,
smooth, eguttulate, base truncate, apex obtuse, straight or curved,
constricted, obovoid (Sutton 1980).
Type species: S. carthusianum (Sacc.) Sacc., Michelia 2(6): 11.
1880.
Notes: Although more than 120 species of Septogloeum have been
described, the genus was reduced to just two species by Sutton &
Pollack (1974). Sexual morphs have been linked to Pleuroceras in
the Diaporthales (Monod 1983). The genus is in need of revision
pending fresh collections.
Xenocylindrosporium Crous & Verkley, Fungal Planet 44.
2009.
Conidiomata immersed, black, opening by irregular rupture,
acervuloid, up to 300 μm diam; wall consisting of 3–4 layers of
pale brown textura angularis. Conidiophores hyaline, smooth,
subcylindrical, branched, septate, or reduced to ampulliform
conidiogenous cells. Conidiogenous cells hyaline, smooth,
ampulliform to subcylindrical, terminal or lateral on septate
conidiophores, monophialidic with minute periclinal thickening.
Conidia solitary, hyaline, smooth, curved, widest in middle, tapering
to acutely rounded apex and truncate base, 0 –1-septate.
Type species: X. kirstenboschense Crous & Verkley, Fungal Planet
44. 2009.
Stromatic forms
Dothistroma Hulbary, Bull. Ill. Nat. Hist. Surv. 21: 235. 1941.
Mycelium immersed, branched, septate, pale brown to hyaline.
Conidiomata sometimes acervular, initially subepidermal later
erumpent, composed of pale brown, thin-walled textura angularis,
sometimes eustromatic, multilocular and of darker brown, thickwalled tissue. Stromata are strongly erumpent and inally pulvinate.
Conidiogenous cells holoblastic, discrete, determinate, ampulliform,
hyaline, smooth, non-proliferating, formed from the upper cells of
stroma or from inner cells of the locular walls. Conidia hyaline,
straight or curved, iliform, 1–5-euseptate, continuous, thin-walled
and smooth (Barnes et al. 2004).
Type species: D. pini Hulbary, Bull. Ill. Nat. Hist. Surv. 21: 235.
1941.
Notes: Dothistroma sexual morphs are mycosphaerella-like (Evans
1984), and the two species of Dothistroma that have been subjected
to DNA sequencing (D. septosporum and D. pini) cluster together
in the “Dothistroma clade” as described by Crous et al. (2009a, c).
Because of a lack of recognisable morphological characteristics,
it is virtually impossible to discriminate between D. septosporum
and D. pini without molecular tools (Barnes et al. 2004). Multiple
morphological varieties of both D. septosporum and D. pini have
www.studiesinmycology.org
Fig. 18. Conidia and conidiogenous cells of Phlyctaeniella humuli (IMI 202260)
(redrawn from Sutton 1980). Scale bar = 10 µm.
been described based on differences in conidia length alone (e.g.
D. septosporum var. keniense). However, controversy exists as
to whether spore size represents an adequate characteristic
to distinguish among these Dothistroma varieties, as since the
introduction of molecular tools only D. septosporum and D. pini
have been conirmed as distinct species.
Phlyctaeniella Petr., Ann. Mycol. 20: 323. 1922. Fig. 18.
Mycelium immersed, branched, septate, hyaline. Conidiomata
eustromatic, separate, immersed, pale brown, globose, unilocular,
scarcely erumpent; side wall and base of several cell layers of
hyaline, thin-walled textura angularis, above of larger pale brown
tissue. Ostiole indistinct, and dehiscence by rupture of the upper
wall. Conidiophores hyaline, smooth, septate, irregularly branched,
especially at the base, formed from the inner cells of the stroma wall.
Conidiogenous cells phialidic, integrated or discrete, determinate,
hyaline, markedly tapered at the apices, smooth, with apical or
lateral apertures, collarette minute, with periclinal thickening;
only rarely becoming percurrent. Conidia hyaline, smooth, thinwalled, irregularly guttulate, iliform, straight, curved or irregular,
multiseptate (Sutton 1980).
Type species: P. polonica Petr., Ann. Mycol. 20: 323. 1922.
Note: Fresh material needs to be collected of this taxon (on Aruncus
silvestris, Austria), before its taxonomy can be resolved.
Septocyta Petr., Ann. Mycol. 25: 330. 1927. Figs 19, 20.
Mycelium immersed, branched, septate, hyaline to pale brown.
Conidiomata eustromatic, immersed, separate, erumpent, dark
brown to black, inally opening widely, unilocular, multilocular or
convoluted, thick-walled; wall of pale brown, thin-walled textura
angularis except in the dehiscent region which is darker brown and
more thick-walled. Ostiole absent, dehiscence by breakdown of the
upper wall. Conidiogenous cells are holoblastic, sympodial with 1–3
337
Quaedvlieg et al.
Specimen examined: Germany, Brandenberg, on Rubus fructicosus (Rosaceae),
7 June 1923, coll. P. Sydow, det. H. Sydow, Sydow Mycoth. Germ. PDD 51271.
Notes: Septocyta ramealis, the type of Septocyta, has a long list
of synonyms. The specimen examined here (PDD 51271), differs
somewhat from the description provided by Sutton (1980), and
appears to represent a species of Septoria s. str., as the mode
of conidiogenesis is not that different. Presently there is a single
ITS sequence labelled as S. ruborum available on GenBank
(JN133277.1), placing it in the middle of Septoria s. str. As no
type material of S. ramealis could be located, this matter remains
unresolved.
Septopatella Petr., Ann. Mycol. 23: 128. 1925.
Fig. 19. Conidia and conidiogenous cells of Septocyta ramealis (PDD 51271). Scale
bars = 10 µm.
apical, scarcely protruding, unthickened denticles, indeterminate,
discrete, ampulliform to lageniform, hyaline, smooth, formed from
the inner cells of the locular walls. Conidia hyaline, 1–3 euseptate,
smooth, straight or slightly curved, acicular, apex obtuse, base
truncate, often with minute guttules associated with septa (Sutton
1980).
Type species: S. ramealis (Roberge ex Desm.) Petr., Ann. Mycol.
25: 330. 1927.
Septocyta ramealis (Roberge ex Desm.) Petr., Ann. Mycol.
25: 330. 1927.
Conidiomata eustromatic to pycnidial, black, up to 160 µm diam,
aggregated in clusters, erumpent through ruptures in epidermis,
convulated; wall of 3–8 layers of brown textura angularis.
Conidiophores lining the inner cavity, reduced to conidiogenous
cells, or one or two supporting cells. Conidiogenous cells hyaline,
smooth, ampulliform, proliferating sympodially and percurrently
near apex, also with lateral denticle-like protrusions, 6–12 × 2.5–4
µm. Conidia hyaline, smooth, guttulate, (9–)20–30(–35) × 1.5(–2)
µm, 1(–3)-septate, irregularly curved, subcylindrical, apex obtuse,
base tapering slightly to truncate hilum, 0.5 µm diam.
Mycelium immersed, branched, septate, hyaline to subhyaline.
Conidiomata supericial, often subtended by a supericial, pale
brown, septate, branched mycelium, pulvinate, separate to
occasionally aggregated, dark brown to black, inally opening widely,
cupulate; basal wall of small-celled, brown, thin-walled textura
angularis, becoming textura porrecta as it merges into the periclinal
walls; a hypostroma attaches the conidioma to the substrate;
Ostiole absent. Conidiophores hyaline, septate, branched at the
base, thin-walled, cylindrical, formed from the gelatinized basal
wall of the conidioma. Conidiogenous cells holoblastic, sympodial,
integrated, indeterminate, cylindrical, hyaline, smooth, produced as
2–3 branches from the apex of the conidiophores. Conidia hyaline,
3–4-euseptate, thin-walled, smooth, minutely guttulate, straight
or curved, occasionally irregularly iliform (Dyko & Sutton 1979,
Sutton 1980).
Type species: S. septata (Jaap) Petr., Ann. Mycol. 23: 129. 1925.
Note: Not much is known about this genus, and as no cultures
of S. septata are presently available (on Pinus montana, Czech
Republic) this matter cannot be resolved.
Stictosepta Petr., Sydowia 17: 230. 1964. [1963]. Fig. 21.
Mycelium immersed, branched, septate, hyaline. Conidiomata
eustromatic, immersed, globose to collabent, papillate, unilocular,
often convoluted, hyaline; walls thick, of hyaline, thin-walled
Fig. 20. Septocyta ramealis (PDD 51271). A. Conidiomata on host tissue. B, C. Conidiogenous cells. D. Conidia. Scale bar = 10 µm.
338
Sizing up Septoria
to verruculose-echinulate; hila distinct, slightly to conspicuously
thickened, darkened, refractive; conidial secession schizolytic.
Ascomata immersed to supericial, uniloculate, globose to
subglobose with papillate, central, periphysate ostiole, dark brown
to black, scattered or gregarious. Peridium of 3–6 layers of thin- to
thick-walled textura angularis, dark brown to black. Hamathecium
dissolves at maturity, and no stromatic tissue remains between the
asci. Asci bitunicate, issitunicate, 8-spored, cylindrical to cylindricclavate, ovoid to ampulliform or saccate, sessile to subsessile, apex
rounded with distinct or indistinct ocular chamber. Ascospores bi- to
tri- or multiseriate, ellipsoid-fusoid to obclavate or subcylindrical,
hyaline, medianly 1-septate, often constricted at the septum,
smooth-walled, granular to guttulate, mostly lacking any sheath.
Type species: Ramularia pusilla Unger, Exanth. Planzen (Wien):
169. 1833.
Fig. 21. Conidia and conidiogenous cells of Stictosepta cupularis (redrawn from
Sutton 1980). Scale bar = 10 µm.
textura intricata. Ostiole central and circular, single, furfuraceous.
Conidiophores hyaline, septate, branched, anastomosing, formed
from the inner cells of the locular wall. Conidiogenous cells
sympodial or synchronous, integrated, indeterminate, hyaline,
thin-walled, with usually two small, unthickened, apical, slightly
protuberant conidiogenous loci. Conidia hyaline, thin-walled,
smooth, multiseptate, slightly constricted at the septa, each cell
medianly guttulate, straight or curved, base truncate, apex obtuse
(Sutton 1980).
Type species: S. cupularis Petr., Sydowia 17: 230. 1964. [1963].
Note: Not much is known about this genus, but as no isolate of
S. cupularis is presently available (on stems of Fraxinus, Czech
Republic), it will not be treated here.
Sexual morphs linked to Septoria
Several sexual genera have been linked to Septoria and allied
genera in literature, but very few have been conirmed in culture.
Most sexual states cluster in the Mycosphaerella complex.
Mycosphaerella Johanson, Öfvers. K. Svensk. Vetensk.Akad. Förhandl. 41(no. 9): 163. 1884.
= Ramularia Unger, Exanth. Planzen (Wien): 119. 1833.
Mycelium immersed to supericial, septate, hyaline, branched.
Caespituli usually whitish to greyish on host tissue. Conidiophores
fasciculate to synnematal, rarely solitary, or forming small
sporodochia, emerging through stomata, from inner hyphae
or stromata; conidiophores straight, subcylindric to geniculatesinuous, aseptate or septate, hyaline, occasionally branched,
smooth, rarely rough. Conidiogenous cells integrated, terminal,
polyblastic, elongating sympodially, apex more or less straight
to geniculate-sinuous or strongly curved, cicatrized, conidial
scars hardly to conspicuously thickened, but always darkened,
refractive. Conidia solitary to catenate, sometimes in branched
chains, 0–4(–multi)-septate, hyaline, ellipsoid-ovoid to cylindricalfusoid, rarely iliform, occasionally constricted at the septa, smooth
www.studiesinmycology.org
Notes: Species of Ramularia (including the Mycosphaerella sexual
morph) have evolved over a broad developmental and physiological
adaptation range that includes endophytes, saprophytes and
symbionts. However, for a major part Ramularia consists of a wide
range of narrow host range, foliicolous plant pathogens which are
the cause of signiicant economical losses in both temperate and
tropical crops worldwide (Crous et al. 2001). Verkley et al. (2004)
showed that Mycosphaerella s. str. (linked to M. punctiformis) was
in fact restricted to species with Ramularia anamorphs, leaving
many “Mycosphaerella” species to be disposed to other genera.
In employing the one fungus = one name concept (Hawksworth
et al. 2011, Wingield et al. 2012), the choice is to use Ramularia
over Mycosphaerella, as the former is monophyletic and recently
monographed (Braun 1995, 1998), while Mycosphaerella is polyand paraphyletic, and consists of more than 40 genera, many as
yet untreated (Crous et al. 2009c)
Sphaerulina Sacc., Michelia 1(no. 4): 399. 1878.
Ascomata pseudothecial, immersed, subepidermal, erumpent at
the top, single to clustered, globose, papillate. Ostiole central, with
hyaline periphyses; wall of textura angularis, composed of 2–4
layers of brown cells. Hamathecium dissolving at maturity. Asci
bitunicate, issitunicate, clustered, cylindrical to obclavate, rounded
at apex, with or without a shallow apical chamber, short-stipitate
or sessile, with 8 biseriate to triseriate ascospores. Ascospores
subcylindrical to fusiform, rounded at ends, slightly tapered,
straight or slightly curved, 1–3-septate, with a primary septum
nearly median, hyaline, smooth, without sheath or appendages.
Type species: Sphaerulina myriadea (DC.) Sacc., Michelia 1(no.
4): 399. 1878.
Notes: The genus Sphaerulina was chiely separated from
Mycosphaerella on the basis of ascospore septation (Crous et
al. 2011). Sphaerulina myriadea, which occurs on hosts in the
Fagaceae, appears to be a species complex. Results in this
paper show that Sphaerulina myriadea clusters together with
many septoria-like species in a clade that is distinct, but very
closely related to Septoria s. str. The septoria-like species in this
Sphaerulina clade were subsequently rediscribed in Sphaerulina.
Species including ones with 1-septate ascospores and septorialike asexual morphs are treated below and by Verkley et al. (2013).
339
Quaedvlieg et al.
Treatment of phylogenetic clades
Based on the phylogenetic data generated in this study, we
were able to delineate several clades in the Septoria complex.
Recognised clades, as well as novel species and genera, are
described and discussed below. Taxa with descriptions that are
freely available online in MycoBank or open access journals, are
not repeated here.
clade 1: Septoria
Description: See above.
Type species: S. cytisi Desm., Ann. Sci. Nat. Bot. 8: 24. 1847.
Septoria cf. agrimoniicola Bondartsev, Mater. mikol.
obslêed. Ross. 2: 6. 1921.
Leaf spots on the upper leaf surface, distinct, scattered, brown
with purplish margin, circular to angular, sometimes vein-limited,
discrete lesions 2–4 mm diam, reaching 10 mm wide when
conluent, inally the center becoming pale colored to nearly whitish;
on the lower leaf surface similar but discoloured (Shin & Sameva
2004). On sterile Carex leaves on WA. Conidiomata pycnidial,
separate but frequently aggregated and linked by brown stromatic
tissue in a stroma; globose, black, exuding a creamy conidial mass
via a central ostiole; conidiomata up to 350 µm diam; wall of 6–12
layers of dark brown, thick-walled textura angularis. Conidiophores
reduced to conidiogenous cells or 1–2 supporting cells, hyaline,
subcylindrical, lining the inner layer of conidioma. Conidiogenous
cells hyaline, smooth, subcylindrical to ampulliform, 10–17 × 3–4
µm; proliferating sympodially but also percurrently near apex.
Conidia hyaline, smooth, guttulate, iliform, apex subobtuse, base
long obconically truncate, 1–4-septate, (20–)25–35(–40) × 1.5–2(–
2.5) µm; microcyclic conidiation observed.
Culture characteristics: Colonies on PDA lat, undulate with
sparse, white aerial mycelium, surface olivaceous-black,
reverse olivaceous-black, after 14 d, 3.5 cm diam; on MEA with
sparse white aerial mycelium, surface olivaceous-black, reverse
olivaceous-black, after 14 d, 5 cm diam; on OA with sparse white
aerial mycelium, surface olivaceous, reverse olivaceous, after 14
d, 3 cm diam.
conluent, inally the center becoming paler or nearly whitish; on
the lower leaf surface similar but discoloured (Shin & Sameva
2004). On OA. Conidiomata solitary to aggregated, black, globose,
becoming somewhat papillate, up to 250 µm diam, opening by
means of central ostiole, up to 40 µm diam; wall of 6–8 layers
of thick-walled, brown textura angularis; exuding a creamy
conidial mass. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells lining the inner wall layer, hyaline, discrete,
ampulliform to lageniform, 4–10 × 3–5 µm, proliferating sympodially
or percurrently with inconspicuous proliferations. Conidia iliform,
curved or lexuous, rarely straight, (60–)65–75(–90) × 1.5–2(–3)
µm, hyaline, guttulate, 4–7(–11)–septate, apex subobtuse, slightly
tapering from basal septum to truncate base, 1.5–2 µm.
Culture characteristics: Colonies on PDA erumpent, with feathery
margin, with sparse white aerial mycelium, surface greenish-black,
reverse olivaceous-black, after 14 d, 2.5 cm diam; on MEA with
sparse white aerial mycelium, surface cinnamon to olivaceousblack in the younger patches, reverse cinnamon to olivaceousblack in patches, after 14 d, 4 cm diam; on OA with sparse white
aerial mycelium, surface greenish-black, reverse fuscous-black,
after 14 d, 3 cm diam.
Specimen examined: South Korea, Incheon, leaf of Stachys riederi var. japonica
(Lamiaceae), 14 Aug. 2008, H.D. Shin (CBS H-21278, culture CBS 128668 = KACC
44796 = SMKC 24663).
Note: The Korean collection was originally identiied as Septoria
stachydicola, which its the original description provided for this
taxon (Shin & Sameva 2004). However, authentic European
material is required for a comparison to conirm this identiication,
as we suspect S. stachydicola may be restricted to Europe.
Septoria cretae Quaedvlieg, Verkley & Crous, sp. nov.
MycoBank MB804402. Figs 22, 23.
Etymology: Named after Crete, the island from where it was
collected.
On sterile Carex leaves on WA. Conidiomata up to 250 µm diam,
brown, immersed, subepidermal, pycnidial, subglobose with central
Specimen examined: South Korea, Guri, on leaves of Agrimonia pilosa (Rosaceae),
11 Jul. 2009, H.D. Shin (CBS H-21279, culture CBS 128602 = KACC 44644 = SMKC
24292).
Notes: This fungus was irst reported from Korea by Shin & Sameva
(2002) as S. agrimoniicola, and its well with the original description
of this European taxon. However, fresh European collections and
cultures are required for comparison, as S. agrimoniicola may well
be restricted to Europe.
Septoria cf. stachydicola Hollós, Mathem. Természettud.
Közlem. Magg. Tudom. Akad. 35(1): 60. 1926.
Leaf spots on the upper leaf surface distinct, scattered, brown
with purplish margin, circular to angular, sometimes vein-limited,
discrete lesions 2–4 mm diam, reaching 10 mm wide when
340
Fig. 22. Conidia and conidiogenous cells of Septoria cretae (CBS 135095). Scale
bar = 10 µm.
Sizing up Septoria
Fig. 23. Septoria cretae (CBS 135095). A. Colony sporulating in culture. B–F. Conidiophores and conidiogenous cells giving rise to conidia. G. Conidia. Scale bars = 10 µm.
ostiole, exuding creamy conidial mass; wall of 2–3 layers of brown
textura angularis. Conidiophores reduced to conidiogenous cells, or
with a supporting cell that gives rise to several conidiogenous cells.
Conidiogenous cells phialidic, hyaline, smooth, aggregated, lining
the inner cavity, ampulliform to subcylindrical, straight to curved,
proliferating sympodially near apex, 10–20 × 2–3.5 µm. Conidia
hyaline, smooth, thin-walled, subcylindrical to narrowly obclavate,
granular, with subobtuse apex and obconically truncate to truncate
base, 1–3-septate, (8–)15–22(–27) × 2(–3) µm.
Culture characteristics: Colonies on PDA erumpent, with feathery
margin, lacking aerial mycelium, surface fuscous-black, reverse
olivaceous-black, after 14 d, 3.5 cm diam; on MEA surface fuscousblack, reverse olivaceous-black, after 14 d, 4 cm diam; on OA
surface fuscous-black, reverse fuscous-black, after 14 d, 3.5 cm
diam.
Specimen examined: Greece, Crete, on leaves of Nerium oleander (Apocynaceae),
7 Jul. 2012, U. Damm, (holotype CBS H-21277, culture ex-type CBS 135095).
Notes: Several species of Septoria are known on Nerium oleander,
namely S. juliae [conidia 1–6(–7)-septate, 26–54 × 2.5–5.5 µm], S.
neriicola (conidia 1-septate, 30–40 × 0.7–1 µm), S. oleandriicola
[conidia 1–3-septate, 12.5–22.5–37.5(–40) × 2.5–3(–4.5) µm], S.
oleandrina (conidia 0–1-septate, 9–19 × 1–1.5 µm), and S. rollhansenii (conidia 0–4-septate, 25–39 × 3–4 µm) (Bedlan 2011),
which differ from S. cretae based on conidial dimensions and
septation.
Septoria glycinicola Quaedvlieg, H.D. Shin, Verkley &
Crous, sp. nov. MycoBank MB804403. Fig. 24.
Etymology: Named after the host genus on which it was collected,
Glycine.
On OA. Conidiomata forming in concentric circles, pycnidial,
separate, black, globose, up to 150 µm diam, opening by a
central ostiole, up to 30 µm diam, exuding a creamy conidial
mass; wall consisting of 3–6 layers of brown textura angularis.
Conidiophores reduced to conidiogenous cells. Conidiogenous
cells lining the inner cavity, hyaline, smooth, ampulliform, 10–16
× 2.5–3.5 µm, proliferating sympodially near apex, holoblastic.
Fig. 24. Septoria glycinicola (CBS 128618). A, B. Colonies sporulating on PDA. C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
www.studiesinmycology.org
341
Quaedvlieg et al.
Conidia hyaline, smooth, guttulate to granular, subcylindrical to
narrowly obclavate, irregularly to gently curved, apex subobtuse,
base long obconically truncate, 3–6-septate, (33–)45–55(–65) ×
(1.5–)2 µm.
Culture characteristics: Colonies on PDA lat, circular, with
sparse black aerial mycelium with black tufts, surface patches of
olivaceous-black to fawn in the younger parts, reverse with patches
of olivaceous-black in the older parts to mouse-grey and pale
purplish grey in the younger mycelium, after 14 d, 6.5 cm diam,
pinkish exudate; on OA lobate, with sparse white aerial mycelium,
surface patches of vinaceous to olivaceous-black, reverse fuscousblack to vinaceous-buff; after 14 d, 8.5 cm diam, pinkish exudate;
on MEA with radial lobes, very short white aerial mycelium, surface
fuscous-black, reverse olivaceous-black; after 14 d, 4.5 cm diam.
Specimen examined: South Korea, Namyangju, on leaves of Glycine max
(Fabaceae), 22 Sep. 2008, H.D. Shin (holotype CBS H-21270, culture ex-type CBS
128618 = KACC 43091 = SMKC 22879).
Notes: Septoria glycines is the common Septoria species
associated with brown spot of soybeans. Septoria glycinicola is
distinct from S. glycines (conidia 1–4 septate, 21–45 × 1.5–2 µm)
in that it has larger conidia.
Septoria oenanthicola Quaedvlieg, H.D. Shin, Verkley &
Crous, sp. nov. MycoBank MB804405. Fig. 25.
Etymology: Named after the host genus from which it was collected,
Oenanthe.
On sterile Carex leaves on WA. Conidiomata pycnidial, separate
but aggregated, black, globose, up to 200 µm diam, opening by
central ostiole, up to 20 µm diam, exuding a creamy conidial mass;
wall consisting of dark brown, thickened, 6–10 layers of textura
angularis. Conidiophores reduced to conidiogenous cells or to one
supporting cell. Conidiogenous cells hyaline, smooth, 3–5 × 3–7
µm, ampulliform, proliferating sympodially near apex, holoblastic.
Conidia hyaline, smooth, guttulate, subcylindrical to narrowly
obclavate, apex subobtuse, base long obconically truncate,
1–6-septate, (17–)25–45(–55) × (2–)2.5(–3) µm.
Culture characteristics: Colonies on PDA lat, undulate with sparse,
white aerial mycelium, surface olivaceous-grey, reverse olivaceous,
after 14 d, 2.5 cm diam; on MEA with sparse, white aerial mycelium,
surface olivaceous-grey, reverse olivaceous-black, after 14 d, 5 cm
diam; on OA with sparse white aerial mycelium, surface olivaceousgrey, reverse olivaceous, after 14 d, 3 cm diam.
Specimen examined: South Korea, Yangpyeong, on leaves of Oenanthe javanica
(Apiaceae), 25 May 2006, H.D. Shin (holotype CBS H-21281, culture ex-type CBS
128649 = KACC 42394 = SMKC 21807).
Notes: This fungus was originally recorded from Korea by Shin
(1998) as Septoria oenanthis. However, conidia of Korean
specimens (30–60 ×1.5–2.5 µm; Shin & Sameva 2004) are much
larger than that of the American type collection (20–35 × 1.5–2
µm; Saccardo 1895), and therefore better treated as a separate
taxon.
Septoria pseudonapelli Quaedvlieg, H.D. Shin, Verkley &
Crous, sp. nov. MycoBank MB804404. Fig. 26.
Etymology: Named after its morphological similarity to Septoria
napelli.
Leaf spots on the upper leaf surface, scattered to conluent, distinct,
angular to irregular, usually vein-limited, small to large, up to 30 mm
when conluent, at irst appearing small angular brown discoloration,
later turning blackish brown with or without distinct border line, inally
central area becoming blackish and surrounded by pale greenish
margin; on the lower leaf surface similar but discoloured (Shin
Fig. 25. Septoria oenanthicola (CBS 128649). A. Colony sporulating on MEA. B. Section through conidiomata. C–G. Conidiogenous cells. H. Conidia. Scale bars: B = 200 µm,
all others = 10 µm.
342
Sizing up Septoria
Fig. 26. Septoria pseudonapelli (CBS 128664). A. Colony sporulating on PDA. B. Section through conidioma. C–E. Conidiogenous cells. F. Conidia. Scale bars: B = 125 µm,
all others = 10 µm.
& Sameva 2004). On sterile Carex leaves on WA. Conidiomata
pycnidial, separate, black, globose, papillate with short neck (at times
1–2 necks develop), up to 250 µm wide, 500 µm high with central
ostiole; wall of 5–7 layers of brown textura angularis. Conidiophores
reduced to conidiogenous cells. Conidiogenous cells ampulliform,
lining the inner cavity, hyaline, smooth, with sympodial or apical
percurrent proliferation, 10–13 × 5–7 µm. Conidia iliform, curved to
lexuous, (50–)75–90(–100) × (2.5–)3(–3.5) µm, hyaline, guttulate,
4–10-septate, apex subobtuse, base obconically truncate, 2 µm
diam.
Culture characteristics: Colonies on PDA lat, undulate with sparse,
white aerial mycelium, surface olivaceous-black, reverse olivaceousblack, after 14 d, 2 cm diam; on MEA with sparse white aerial mycelium,
surface olivaceous-black, reverse olivaceous-black, after 14 d, 4 cm
diam; on OA with sparse white aerial mycelium, surface olivaceous,
reverse olivaceous, after 14 d, 2 cm diam.
Specimen examined: South Korea, Chuncheon, on leaves of Aconitum pseudolaeve
var. erectum (Ranunculaceae), 4 Sep. 2008, H.D. Shin (holotype CBS H-21280,
culture ex-type CBS 128664 = KACC 43952 = SMKC 23638).
(Fagaceae), J.E. Vize [Microfungi Brit. Ex. No. 195] (ex IMI 57186, K(M) 167735).
uSA, California: Sequoia National Park. alt. 2590 m, on leaves of Castanopsis
sempervirens, 18 Jun. 1931, H.E. Parks (BPI 623686); Lake Co., Hoberg’s Resort,
on leaves of Q. kelloggii, 15 May 1943, V. Miller (BPI 623707); Maryland, Marlboro,
on leaves of Q. alba, 26 Apr. 1929, C.L. Shear ( BPI 623705); Texas, Houston, on
leaves of Q. alba, 8 Apr. 1869, H.W. Ravenel (BPI 623704).
Notes: Sivanesan (1984) linked Sphaerulina to Septoria,
Cercospora and Cercosporella asexual morphs, though these
were never conirmed based on DNA data. The latter two
genera have since been shown to be distinct (Crous et al. 2013,
Groenewald et al. 2013; this volume), which leaves septoria-like
asexual morphs such as Sphaerulina rubi Demaree & Wilcox
(linked to Cylindrosporium rubi Ellis & Morgan), and S. rehmiana
(linked to Septoria rosae), which conirms the results obtained
here (Fig. 1).
Sphaerulina abeliceae (Hiray.) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804406.
Basionym: Septoria abeliceae Hiray., Mem. Col. Agr. Kyoto. Imp.
Univ. 13(3): 33. 1931.
Notes: This taxon was originally reported as Septoria napelli from
Korea by Shin & Sameva (2004), and broadly corresponds with the
original description provided for this taxon (Petrak 1957). However,
we have examined European material authentic for the name (see
Verkley et al. 2013, this issue), from which the Korean fungus is
genetically different. Based on these observations we describe the
Korean collection as new.
Sphaerulina amelanchier Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804407. Figs 27, 28.
clade 2: Sphaerulina
Etymology: Named after the host genus from which it was collected,
Amelanchier.
Sphaerulina Sacc., Michelia 1(no. 4): 399. 1878.
Description: See above.
Type species: Sphaerulina myriadea (DC.) Sacc., Michelia 1(no.
4): 399. 1878.
Specimens examined: Germany, Driesen, Lasch [Rabenhorst, Fungi Eur. no. 149]
(L). Japan, Aomori, Tsugaru, Kidukuri, Bense-marsh (40°51′53″ N, 140°17′42″E),
on leaves of Q. dentata, 21 Apr. 2007, K. Tanaka 2243 (HHUF 29940; single
ascospore culture CBS 124646 = JCM 15565). uK, on leaves of Quercus robur
www.studiesinmycology.org
Specimen examined: South Korea, Jeonju, on leaves of Zelkova serrata
(Ulmaceae), 29 Oct. 2006, H.D. Shin, CBS 128591 = KACC 42626.
On sterile Carex leaves on WA. Conidiomata pycnidial, brown,
separate, immersed, globose, up to 150 µm diam, exuding a
creamy conidial mass via central ostiole; wall of 3–6 layers of brown
textura angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells hyaline, smooth, subcylindrical, irregularly
curved, branched to once geniculate-sinuous, 5–20 × 3–4 µm;
proliferating sympodially. Conidia hyaline, smooth, guttulate,
iliform, narrowly obclavate, apex subacutely rounded, base long
obconically truncate, 1–8-septate, (25–)40–55(–60) × (1.5–)2(–2.5)
µm; microcyclic conidiation common. Ascomata globose, brown,
343
Quaedvlieg et al.
Fig. 27. Conidia, conidiogenous cells, ascospore and ascus of Sphaerulina amelanchier (CBS 135110). Scale bars = 10 µm.
Fig. 28. Sphaerulina amelanchier (CBS 135110). A. Colony on PDA. B. Conidiogenous cells. C. Ascomata on host tissue. D. Germinating ascospore. E, F. Asci. G. Ascospores.
H. Conidia. Scale bars = 10 µm.
separate, immersed to erumpent, up to 150 µm diam. Asci broadly
ellipsoid to obclavate, 22–35 × 7–9 µm; apical chamber visible,
1–1.5 µm diam. Ascospores fusoid-ellipsoid, hyaline, smooth,
granular, not to slightly constricted at median septum, widest just
above septum, prominently curved, (13–)17–20(–25) × (2.5–)3(–
3.5) µm. Ascospores germinating from both ends, with germ tubes
parallel to the long axis, developing lateral branches and becoming
constricted at septum, 3–4 µm diam.
Culture characteristics: Colonies on PDA radially striate with lobate
edge, sparse white aerial mycelium, surface fuscous-black to buff
for the younger tissue, reverse cinnamon to olivaceous-black, after
344
14 d, 3 cm diam; on MEA surface patches of hazel to fawm to
fuscous-black, reverse sepia to olivaceous-black, after 14 d, 4.5
cm diam; on OA surface pale-vinaceous to fuscous-black, reverse
cinnamon to fuscous-black, after 14 d, 3 cm diam.
Specimen examined: Netherlands, Houten, on leaf litter of Amelanchier sp.
(Rosaceae), 28 Mar. 2012, S. Videira (holotype CBS H-21282, culture ex-type CBS
135110 = MP8 = S544).
Note: Presently there are no known species of septoria-like
fungi known from Amelanchier. Phylogenetically, it is similar
to Sphaerulina rhabdoclinis (conidia 8–30 × 1.5–2 µm), which
infects needles of Pseudotsuga menziesii. Phylogenetically similar
Sizing up Septoria
isolates occur on Betula, Castanea and Quercus. More isolates
and molecular data are required to resolve this complex.
Sphaerulina menispermi (Thüm.) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804412.
Basionym: Septoria menispermi Thüm., Pilzlora Siber.: no. 818. 1880.
Sphaerulina azaleae (Voglino) Quaedvlieg, Verkley & Crous,
comb. nov. MycoBank MB804408.
Basionym: Septoria azaleae Voglino, Syll. Fung. (Abellini) 14(2):
976. 1899.
Specimens examined: South Korea, Chuncheon, on leaves of Menispermum
dauricum (Menispermaceae), 16 Jun. 2008, H.D. Shin, KACC 43848 = CBS
128761; Pyeongchang, on leaves of M. dauricum, 23 Sep. 2008, H.D. Shin, KACC
43968 = CBS 128666.
≡ Phloeospora azaleae (Voglino) Priest, Fungi of Australia: 224. 2006.
Specimens examined: Belgium, on leaves of Rhododendron sp. (Ericaceae), J. van
Holder, CBS 352.49. South Korea, Hongcheon, on leaves of Rhododendron sp., 18
Oct. 2009, H.D. Shin, KACC 44865 = CBS 128605.
Sphaerulina berberidis (Niessl) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804409.
Basionym: Septoria berberidis Niessl, in Rabenhorst, Bot. Ztg. 24:
411. 1866.
= Sphaerella berberidis Auersw., in Gonnermann & Rabenhorst, Mycol. eur.
Abbild. Sämmtl. Pilze Eur. 5-6: 3. 1869 (nom. nov. for Sphaeria berberis
Nitschke ex Fuckel).
≡ Mycosphaerella berberidis (Auersw.) Lindau, in Engler & Prantl, Nat.
Planzenfam., Teil. I (Leipzig) 1(1): 424. 1897.
Description in vitro (CBS 116724): Colonies on OA 16–20 mm diam
after 14 d, with an even, colourless margin; colonies spreading to
restricted, somewhat elevated in the centre, the surface covered
by a dense mat of pure white, woolly aerial mycelium; reverse in
the centre dark brick to brown vinaceous, surrounded by cinnamon
tinges; small amounts of a yellow to greenish pigment diffusies into
the surrounding medium. Colonies on MEA 8–10 mm diam after 14
d, with an even to slighlty rufled vinaceous buff margin; colonies
restricted, pustulate, the surface ochraceous or darker, with diffuse
to locally more dense inely felted grey aerial mycelium; reverse
brown vinaceous to vinaceous buff. Culture remained sterile.
Specimen examined: Switzerland, Kt. Graubünden, Rodels-Realta, on Berberis
vulgaris (Berberidaceae), 2 Jun. 1951, E. Müller, specimen CBS-H4984, culture
CBS 324.52.
Sphaerulina betulae (Pass.) Quaedvlieg, Verkley & Crous,
comb. nov. MycoBank MB804410.
Basionym: Septoria betulae Pass., Primo Elenc. Funghi Parm.: no.
52. 1867.
Specimens examined: Netherlands, Olst, leaves of Betula pubescens (Betulaceae),
Sep. 2004, S. Green, CBS 116724. South Korea, Hongcheon, leaves of B.
platyphylla var. japonica, 27 May 2008, H.D. Shin, CBS 128600 = KACC 43769.
Sphaerulina musiva (Peck) Quaedvlieg, Verkley & Crous,
comb. nov. MycoBank MB804413.
Basionym: Septoria musiva Peck, Ann. Rep. N.Y. St. Mus. Nat.
Hist. 35: 138. 1883 [1881]
= Mycosphaerella populorum G.E. Thomps., Phytopathology 31: 246. 1941.
≡ Davidiella populorum (G.E. Thomps.) Aptroot, CBS Diversity Ser.
(Utrecht) 5: 164. 2006.
= Cylindrosporium oculatum Ellis & Everh., J. Mycol. 5(3): 155. 1889.
Specimen examined: canada, Quebec, leaf spot of Populus deltoids (Salicaceae),
J. LeBoldus, CBS 130570.
Sphaerulina oxyacanthae (Kunze & J.C. Schmidt)
Quaedvlieg, Verkley & Crous, comb. nov. MycoBank
MB804414. Figs 29, 30.
Basionym: Septoria oxyacanthae Kunze & J.C. Schmidt, Myk.
Hefte (Leipzig) 2: 108. 1823.
≡ Phloeospora oxyacanthae (Kunze & J.C. Schmidt) Wallr., Fl. Crypt.
Germ. (Norimbergae) 2: 117. 1833.
Leaf spots amphigenous, medium to dark brown, subcircular
to angular, 1–6 mm diam, with dark brown border. Conidiomata
epiphyllous, up to 150 µm diam, brown, immersed, subepidermal,
opening by irregular rupture of upper layer, with 3–4 apical laps,
exuding a long crystalline lame-like cirrhus of conidia; wall
3–8 layers of brown textura angularis. On sterile Carex leaves
on WA. Conidiophores reduced to conidiogenous cells, or with
one supporting cell that can become fertile, forming a lateral
conidiogenous locus just below the septum, 10–20 × 2.5–4 µm.
Conidiogenous cells hyaline, smooth, aggregated, lining the inner
cavity, terminal and lateral, ampulliform, 5–10 × 2.5–3.5 µm;
proliferating several times percurrently near apex. Conidia hyaline,
smooth, guttulate, 6–12-septate, falcate, widest in lower third of
conidium, lexuous, apical cell tapering to subacute apex, forming a
curved apical appendage-like elongation, 10–17 µm long, median
cells are 5–10 µm long, basal cell forming an eccentric appendage
that tapers to a subacutely rounded base, scar approximately 2–4
Sphaerulina cercidis (Fr.) Quaedvlieg, Verkley & Crous,
comb. nov. MycoBank MB804411.
Basionym: Septoria cercidis Fr., in Léveillé, Ann. Sci. Nat., Bot.,
Sér. 3 9: 251. 1848.
= Septoria provencialis Crous, Stud. Mycol. 55: 127. 2006.
Specimens examined: Argentina, La Plata, on Cercis siliquastrum
(Caesalpiniaceae), 12 Feb. 2008, H.D. Shin, KACC 43596 = CBS 129151; on
C. siliquastrum, 1 Sep. 2007, H.D. Shin, KACC 44497 = CBS 128634. France,
Provence, Cheval Blanc camping site, on leaves of Eucalyptus sp., 29 Jul. 2005,
P.W. Crous, holotype of S. provincialis, CBS H-19701, culture ex-type CBS 118910.
Netherlands, on C. siliquastrum, Sep. 1950, G. van den Ende, CBS 501.50.
www.studiesinmycology.org
Fig. 29. Conidia and conidiogenous cells of Sphaerulina oxyacanthae (CBS
135098). Scale bars = 10 µm.
345
Quaedvlieg et al.
Fig. 30. Sphaerulina oxyacanthae (CBS 135098). A. Leaves with leaf spots. B. Close-up of conidiomata. C. Section though conidioma. D–F. Conidiogenous cells. G. Conidia
(note appendages). Scale bars: C = 150 µm, all others = 10 µm.
µm below basal septum; basal cell (incl. appendage) 11–20 µm
long, conidia (60–)75–90(–100) × 2(–2.5) µm.
Culture characteristics: Colonies on PDA umbonate with undulate
edge and sparse, white aerial mycelium, surface isabelline, reverse
greyish sepia, after 14 d, 3 cm diam; similar on MEA and PDA.
Specimen examined: Netherlands, Wageningen, 51°57’50.43”N 5°41’0.41”E, on
leaves of Crataegus sp. (Rosaceae), Sep. 2012, W. Quaedvlieg (CBS H-21291,
culture CBS 135098 = S654).
Notes: Several septoria-like species have been described from
leaves of Crataegus (Farr & Rossman 2013). The present
collection matches the description of Septoria oxyacanthae (leaf
spots on Crataegus oxyacantha in Germany, conidia 8–12-septate;
conidial dimensions not given). Unfortunately we have been unable
to locate type material of this species.
Sphaerulina patriniae (Miura) Quaedvlieg, Verkley & Crous,
comb. nov. MycoBank MB804415.
Basionym: Septoria patriniae Miura, Flora of Manchuria and East
Mongolia, III Cryptogams, Fungi (Industr. Contr. S. Manch. Rly 27)
3: 465. 1928.
Specimen examined: South Korea, Pocheon, on leaves of Patrinia scabiosaefolia
(Valerianaceae), 20 Aug. 2006, H.D. Shin, KACC 42518 = CBS 128653.
Sphaerulina populicola (Peck) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804416.
Basionym: Septoria populicola Peck, Ann. Rep. N.Y. St. Mus. 40:
59. 1887.
= Septoria populicola House, Bull. N.Y. St. Mus.: 59. 1920. (nom. illegit.)
= Mycosphaerella populicola C.H. Thomps., Phytopathology 31: 251. 1941.
Specimen examined: uSA, Washington, Puyallup, on Populus trichocarpa
(Salicaceae), 2 May 1997, G. Newcombe, CBS 100042.
Fig. 31. Conidia, conidiogenous loci on a hypha, and conidiogenous cells of
Sphaerulina pseudovirgaureae (CBS 135109). Scale bars = 10 µm.
Sphaerulina pseudovirgaureae Quaedvlieg, Verkley &
Crous, sp. nov. MycoBank MB804417. Figs 31, 32.
Etymology: Named after its similarity to Septoria virgaureae.
Conidiomata pycnidial, separate, erumpent, globose, up to 120 µm
diam, dark brown, exusing a creamy conidial cirrhus through central
ostiole, somewhat papillate; wall of 2–3 laters of brown textura
angularis. Conidiophores reduced to conidiogenous cells or with
one supporting cell, subcylindrical, 0–1-septate, branched below
or not, pale brown at base, 10–20 × 3–5 µm. Conidiogenous cells
integrated, hyaline, but pale brown at base, smooth, proliferating
sympodially near apex, 7–17 × 2–3 µm. Conidia solitary,
hyaline, smooth, guttulate, subcylindrical to narrowly obclavate,
scolecosporous, irregularly curved, apex subobtuse, base truncate
or narrowly obconically truncate, 3–10-septate, (30–)40–60(–80) ×
2.5(–3) µm.
Culture characteristics: Colonies spreading, erumpent with sparse
aerial mycelium and smooth, lobate margin and folded surface;
reaching 13 mm diam after 2 wk. On MEA surface saffron with
346
Sizing up Septoria
Fig. 32. Sphaerulina pseudovirgaureae (CBS 135109). A. Conidiomata forming in culture. B. Conidiogenous cells. C. Microcyclic conidiation. D. Conidia. Scale bars = 10 µm.
patches of dirty white, reverse saffron to orange; on PDA surface
and reverse saffron; on OA surface saffron.
Specimen examined: Netherlands, Nijmegen, de Duffelt, on leaves of Solidago
gigantea (Asteraceae), Aug. 2012, S. Videira (holotype CBS H-21327, culture extype CBS 135109 = S669).
Notes: Several septoria-like species have been recorded on
Solidago (Farr & Rossman 2013). Of these taxa Sphaerulina
pseudovirgaureae is most similar to Septoria virguareae (conidia
80–100 × 1.5 µm) except that its conidia are shorter and wider.
Sphaerulina quercicola (Desm.) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804419. Figs 33, 34.
Basionym: Septoria incondita var. quercicola Desm., Ann. Sci. nat.,
Sér. 3, Bot. 20: 95. 1853.
≡ Septoria quercicola (Desm.) Sacc., Michelia 1: 174. 1879.
≡ Phleospora quercicola (Desm.) Sacc., in P. A. Saccardo & D. Saccardo,
1906. Syll. Fung. 18: 490. 1906.
= Septoria quercina Fautr., in Fautrey & Lambotte, Revue Mycol. 17: 170.
1895 (nom. illeg., art. 53; non Desmazières, 1847). Nom. nov. pro Septoria
quercicola f. macrospora Roum., Revue Mycol. 13: 80. 1891.
Description in vivo. Symptoms deinite, small hologenous leaf
spots, scattered or in clusters, in the centre orange brown, pale
yellowish brown to white, usually delimited by a blackened,
somewhat elevated zone, the surrounding leaf tissues becoming
red or yellow. Conidiomata pycnidial or acervuloid, one to a few
in each leafspot, scattered, semi-immersed, predominantly
hypophyllous, pale to dark brown, lenticular to globose, 100–200
µm diam; ostiolum often not well-developed, initially circular,
central, soon opening widely, lacking distinctly differentiated cells;
conidiomatal wall composed of textura angularis without distinctly
differentiated layers and sometimes only well-developed in the
lower part of the conidioma, mostly 10–15 µm thick, the outer cells
with brown, somewhat thickened walls and 4.5–8 µm diam, the
inner cells hyaline, thin-walled, 3–8 µm diam. Conidiogenous cells
hyaline, discrete or integrated in simple, short, (1–)3–5-septate
conidiophores which may be branched at the base, doliiform,
cylindrical, or ampuliform, hyaline, holoblastic, proliferating
percurrently with one to several, more or less distinct annellations,
or sympodially, sometimes both types of proliferation occurring in
a single conidiogenous cell, 4.5–16(–22.5) × 3–4.5 µm. Conidia
cylindrical, curved or lexuous, broadly rounded at the apex
which is provided with a cap of mucilaginous material, attenuated
www.studiesinmycology.org
Fig. 33. Ascospores and asci of Sphaerulina quercicola (CBS 113266). Scale bar
= 10 µm.
gradually to a broadly or more narrowly truncate base which often
is also provided with an amorphous mass of mucilaginous material,
hyaline, (0–)1–3-septate, constricted around the septa, sometimes
at one or more septa also some amorphous mucilaginous material
may be present, contents with numerous small oil droplets,
(32.5–)38–50(–65) × 3–4 µm. Ascomata not clearly associated
with leaf spots, pseudothecial, predominantly hypophyllous, black,
subepidermal, erumpent to supericial, globose, 100–150 µm
diam; apical ostiole 5–10 µm wide; wall consisting of 2–3 layers of
medium brown textura angularis. Asci aparaphysate, fasciculate,
bitunicate, subsessile, broadly ellipsoidal to subcylindrical, straight
to slightly curved, 8-spored, 35–50 × 9–12 µm. Ascospores tri- to
347
Quaedvlieg et al.
Fig. 34. Sphaerulina quercicola (CBS 663.94). A. Leaves with leaf spots. B. Close-up of lesion. C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
Fig. 35. Sphaerulina rhabdoclinis (CBS 102195). A. Conidiomata forming in culture. B. Sporulation on PDA. C. Conidia. Scale bar = 10 µm.
multiseriate, overlapping, hyaline, guttulate, thin-walled, curved,
rarely straight, fusoid-ellipsoidal with obtuse ends, widest at septum
or just above, medianly 1-septate, not constricted at the septum,
tapering towards both ends, (13–)15–18(–20) × (3.5–)4–4.5(–5)
µm (av. 17 × 4.5 µm).
Culture characteristics: Colonies on OA reaching 5–7 mm diam
in 21 d, with an even to undulating, colourless margin; colonies
restricted, irregularly pustulate, immersed mycelium appearing
dark greyish to olivaceous black, rosy buff near the margin,
covered mostly with a dense mat of woolly, pure white or greyish
aerial mycelium; reverse in the centre brown vinaceous or more
greyish black, surrounded by brick to rosy buff. Pycnidia developing
on the agar surface in the centre, releasing droplets of rosy-buff
conidial slime. Colonies on MEA reaching 4–6(–8) mm diam in 21
d, with an even, to irregularly undulating margin which is mostly
hidden under the aerial mycelium; colonies restricted, irregularly
pustulate, the surface mostly blackish or very dark grey, covered by
dense to diffuse, inely felted, white aerial mycelium; reverse mostly
olivaceous black, near the margin cinnamon to buff. Numerous
single and aggregated pycnidia developing on the colony surface
in the centre, releasing milky white to rosy buff conidial slime.
Conidia as in planta (CBS 663.94) though on average considerably
longer, 51.5–74.5 × 3–4(–4.5) µm (OA), the apex, base and area
around septa normally both provided with mucilaginous material as
described above, (0–)1–3(–5)-septate.
Specimens examined: Austria, endophyte culture ex twig of Quercus petraea
(Fagaceae), Aug. 1991, E. Halmschlager 212 (H. A. van der Aa 10986), CBS 456.91.
France, loc. unknown, on leaves of Quercus sp. (“divers Chênes”), distributed in
348
Desmazières, Pl. crypt. Fr., Fasc. 43, no. 2193 (PC, type of Septoria incondita var.
quercicola Desm.). Netherlands, Utrecht, Baarn, on living leaves of Q. robur, 11
Aug. 1994, G. Verkley 225 (CBS H-21188), living culture CBS 663.94; prov. Utrecht,
Soest, De Stompert, on living leaves of Q. rubra, 15 Aug. 1995, G. Verkley 310
(CBS H-21189), CBS 791.95; Same loc., dead fallen leaves of Q. robur, Apr. 2003,
G. Verkley s.n., single ascospore-isolate CBS 113266 (‘Crous 3’); Same loc., G.
Verkley & I. van Kempen, endophyte isolates ex green leaves of Q. robur CBS
115016, 115136, 115137; Prov. Gelderland, Amerongen, Park Kasteel Amerongen,
leaf spot of Q. rubra, 11 Jul. 2000, G. Verkley 973 (CBS H-21231), living culture CBS
109009; Prov. Utrecht, Amelisweerd, on dead leaves of Q. robur, 25 Apr. 2005, G.
Verkley 3108A, culture CBS 117803, CPC 12097.
Sphaerulina rhabdoclinis (Butin) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804420. Fig. 35.
Basionym: Dothistroma rhabdoclinis Butin, For. Path. 30: 196.
2000.
Specimen examined: Germany, Wolfenbüttel, on needles of Pseudotsuga menziesii
(Pinaceae), 24 May 1998, H. Butin, culture ex-type CBS 102195.
Note: Sphaerulina rhabdoclinis is phylogenetically closely related to
S. amelanchier, which appears to be a species complex occurring
on unrelated hosts (see Verkley et al. 2013).
Sphaerulina viciae Quaedvlieg, H.D. Shin, Verkley & Crous,
sp. nov. MycoBank MB804418. Figs 36, 37.
Etymology: Named after the host genus from which it was collected,
Vicia.
Sizing up Septoria
On Anthriscus stem. Conidiomata pycnidial, solitary, erumpent,
brown, globose, up to 150 µm diam, with central ostiole; wall
of 3–6 layers of textura angularis. Conidiophores reduced
to conidiogenous cells. Conidiogenous cells lining the inner
cavity, hyaline, smooth, subcylindrical, tapering and proliferating
sympodially at apex, 5–10 × 3–4 µm. Conidia hyaline, smooth,
guttulate, subcylindrical, irregularly curved, apex obtuse, base
truncate, (3–)6–multiseptate, not or slightly constricted at septa
(especially constricted on SNA, OA and MEA), (45–)55–75(–110)
× (2.5–)3(–3.5) µm.
Culture characteristics: Colonies erumpent, spreading with folded
surface and sparse aerial mycelium, and smooth, lobate margin;
reaching 12 mm diam after 2 wk. On MEA and PDA surface and
reverse olivaceous-grey. On OA surface pale olivaceous-grey.
Specimen examined: South Korea, on leaves of Vicia amurense (Fabaceae), 12
Aug. 2004, H.D. Shin (holotype CBS H-21283, culture ex-type CPC 11414, 11416,
11415 = CBS 131898).
Notes: Several septoria-like species are known from Vicia (Farr
& Rossman 2013). Of these, Sphaerulina viciae is most similar to
Septoria viceae (conidia 30–60 × 2.5 µm), but distinct in having
longer and wider conidia.
Clade 3: Caryophylloseptoria
Description: See Verkley et al. (2013)
Type species: Caryophylloseptoria lychnidis (Desm.) Verkley,
Quaedvlieg & Crous.
Caryophylloseptoria pseudolychnidis Quaedvlieg, H.D.
Shin, Verkley & Crous, sp. nov. MycoBank MB804481. Fig.
38.
Etymology: Named after its morphological similarity to Septoria
lychnidis.
Fig. 36. Conidia and conidiogenous cells of Sphaerulina viciae (CBS 131898). Scale
bars = 10 µm.
Leaf spots on the upper leaf surface, scattered to conluent,
distinct, circular, angular to irregular, usually very large, reaching
up to 20 mm diam, often surrounded with yellow halo, lacking
concentric rings, initially dark brown with pale green border,
becoming brown to dark brown, inally turning greyish brown to
pallid in the centre; on the lower leaf surface greyish brown to
brown with yellowish margin (Shin & Sameva 2004). On sterile
Carex leaves on WA. Conidiomata pycnidial, globose, up to 250
µm diam, black with central ostiole, but frequently splitting open
at maturity, appearing acervular; wall of 6–8 layers of dark brown
textura angularis. Conidiophores subcylindrical, lining the inner
cavity, hyaline, smooth, reduced to conidiogenous cells, or with
1–2 supporting cells, frequently branched at base, 10–25 × 3–5
µm. Conidiogenous cells subcylindrical to ampulliform, 7–15 × 3–5
µm; proliferating sympodially or percurrently near apex. Conidia
Fig. 37. Sphaerulina viciae (CBS 131898). A. Conidiomata forming in culture. B, C, E. Conidiogenous cells. D, F. Conidia. Scale bars = 10 µm.
www.studiesinmycology.org
349
Quaedvlieg et al.
Fig. 38. Caryophylloseptoria pseudolychnidis (CBS 128630). A. Colony sporulating on MEA. B. Vertical section through conidiomata. C, D. Conidiogenous cells. E. Conidia.
Scale bar: B = 250 µm, others = 10 µm.
hyaline, smooth, guttulate, cylindrical, apex obtuse to subobtuse,
base truncate, 3–3.5 µm; 1–3(–5)-septate, (25–)32–45(–50) ×
(2–)2.5–3(–3.5) µm.
Culture characteristics: Colonies on PDA lat, undulate, very
sparse, mixed grey and white aerial mycelium, surface isabelline
to fuscous-black, reverse olivaceous-black to isabelline for the
younger tissue, after 14 d, 3 cm diam; on MEA umbonate, striate,
undulate, surface fuscous-black to honey for the younger tissue
after 14 d 3.5 cm diam; on OA surface dark-mouse-grey, reverse
iron-grey to mouse-grey.
Specimen examined: South Korea, Yangpyeong, Jungmi mountain, on leaves
of Lychnis cognata (Caryophyllaceae), 27 May 2007, H.D. Shin (holotype CBS
H-21292, culture ex-type CBS 128630 = KACC 43866 = SMKC 23519).
Notes: Shin (1995) recorded this species for the irst time in
Korea, while Shin & Sameva (1999) provided a full morphologial
description. Although it compared well with the original description
of this European taxon, its conidia tend to be smaller than those of
S. lychnidis (50–70 × 2.5–3 µm), of which we have also examined
European material (see Verkley et al. 2013, this issue).
Clade 4: pseudocercosporella-like
Note: See Frank et al. (2010).
Clade 5: Cercospora
Note: See Groenewald et al. (2013).
Clade 6: Phloeospora
Description: See above.
Type species: P. ulmi (Fr.) Wallr., Fl. Crypt. Germ. (Norimbergae)
2: 177. 1833.
Phloeospora ulmi (Fr.) Wallr., Fl. Crypt. Germ. (Norimbergae)
2: 177. 1833. Figs 39, 40.
≡ Septoria ulmi Fr. [as ‘Septaria’], Novit. Fl. Svec. 5(cont.): 78. 1819.
350
Fig. 39. Conidia and conidiogenous cells of Phloeospora ulmi (CBS 613.81). Scale
bars = 10 µm.
≡ Septogloeum ulmi (Fr. & Kunze) Died., Krypt. Fl. Brandenburg (Leipzig)
9: 836. 1915.
≡ Cylindrosporium ulmi (Fr.) Vassiljevsky, Fungi Imperfecti Parasitici 2:
580. 1950.
= Mycosphaerella ulmi Kleb., Z. PlKrankh. 12: 257. 1902.
= Sphaerella ulmi (Kleb.) Sacc. & D. Sacc., Syll. Fung. (Abellini) 17: 642. 1905.
Leaf spots angular, vein limited, separate, becoming somewhat
conluent, initially small yellow-green spots that inally turn brown.
Conidiomata acervular, hypophyllous, separate, subepidermal,
composed of thin-walled, medium brown textura angularis, up to
200 µm diam, opening by irregular rupture, and exuding a prominent
cirrhus of orange to yellow-orange conidia. Conidiophores reduced
to conidiogenous cells, or with 1–2 supporting cells, branched
below or not, subcylindrical, 10–30 × 4–5 µm. Conidiogenous
cells hyaline, smooth, subcylindrical, straight to once geniculate,
with numerous prominent percurrent proliferations at apex, 10–15
× 4–5 µm. Conidia solitary, hyaline, smooth, straight to curved,
guttulate or not, fusiform, tapering towards an obtuse or subobtuse
apex, and truncate base, 2–3 µm diam, with minute marginal frill,
Sizing up Septoria
Fig. 40. Phloeospora ulmi (CBS 613.81). A, B, D, E. Conidiomata bursting through host tissue. G, H. Microconidiogenous cells. K. Spermatia. C, F, I, J, L. Macroconidiogenous
cells (arrows denote percurrent proliferation). M. Conidia. Scale bars = 10 µm.
3–5-septate, (20–)30–50(–60) × (3.5–)4–5(–6) µm. Leaf spots also
contain black spermatogonia and ascomata.
Specimens examined: Austria, Innsbruck, near Hungerburg, on leaves of Ulmus sp.
(Ulmaceae), 21 Sep. 1981, H.A. van der Aa, CBS H-14740, H-14861, culture CBS
613.81; Innsbruck, road to Hungerburg, on leaves of Ulmus glabra, 20 Oct. 1996, W.
Gams, CBS 344.97. Netherlands, Baarn, garden of CBS, Oosterstraat 1, on leaves
of Ulmus sp., 26 Aug. 1998, H.A. van der Aa, CBS H-14739, culture CBS 101564.
unknown, on leaves of Ulmus pedunculata, 15 Jul. 1901, A. van Luijk, CBS H-920.
Note: Distinct from Septoria s. str. by having acervuli, and
conidiogenous cells with prominent percurrent proliferation.
Clade 7: septoria-like
Septoria gladioli Pass., in Rabenhorst, Fungi europ. exsicc.:
no. 1956. 1875. Passerini, Atti Soc. crittog. ital. 2: 41. 1879.
Descripton in vitro (18 ºC, NUV). CBS 121.20: Colonies on OA 15–
18 mm diam after 21 d, with an even to slightly rufled, colourless
margin; colonies plane, immersed mycelium olivaceous black,
fading over amber towards the margin, aerial mycelium absent;
www.studiesinmycology.org
reverse concolorous. No sporulation observed. Colonies on MEA
10–15 mm diam after 21 d, with an even, pale luteous to amber
margin; colonies restricted, irregularly pustulate to cerebriform,
immersed mycelium ochreous to salmon, covered by diffuse, inely
felted, white aerial mycelium; reverse in the centre rust, fading
towards the margin over apricot to pale luteous. No sporulation
observed. CBS 353.29: Colonies on OA 16–20 mm diam after
21 d, with an even to slightly rufled, colourless margin; colonies
plane, immersed mycelium rosy buff mixed with some olivaceous
grey, aerial mycelium absent; reverse mainly pale purplish grey
to pale mouse grey. No sporulation observed. Colonies on MEA
14–22(–26) mm diam after 21 d, with an even to lobed, buff margin;
colonies restricted, elevated towards the centre, radially striate,
immersed mycelium greenish olivaceous fading to ochreous or buff
salmon, the central part mostly covered by diffuse, inely felted,
white aerial mycelium; reverse in the centre dark brick to isabelline
or hazel, fading towards the margin over pale cinnamon to buff. No
sporulation observed.
Specimen examined: Netherlands, Mar. 1929, J.C. Went, CBS 353.29. Unknown
location and host, 1920, W.J. Kaiser, CBS 121.20.
351
Quaedvlieg et al.
Notes: Priest (2006) provided a complete description of S. gladioli
on host material, based on observations of an isotype in MEL, and
several specimens on Gladiolus cultivars collected in Australia.
The two strains available from the CBS are old and sterile, and
show some differences that also seem to be relected in the DNA
data obtained. Septoria gladioli is the only species of septorioid
fungi described from the genus Gladiolus. An unusual feature of
the species is that it overwinters as “sclerotia”, that cause leaf
infections in the next season (Priest 2006). The conidiogenous
cells are holoblastic and very distinctly proliferate percurrently to
form subsequent conidia, but no sympodial proliferation has been
reported. Based on the multilocus phylogeny, the aforementioned
isolates should be placed in their own genus, with the genus
Phloeospora as its closest relative. Recollecting material will be
required to determine the generic disposition, the delimitation of the
taxa (as there seem to be at least two) and to which of these taxa
the name Septoria gladioli should be applied.
Clade 8: passalora-like
Passalora dioscoreae (Ellis & G. Martin) U. Braun & Crous,
in Crous & Braun, CBS Biodiversity Ser. (Utrecht) 1: 162.
2003.
mass; wall of 2–3 layers of brown textura angularis. Conidiophores
0–2-septate, subcylindrical, hyaline to pale brown at base, smooth,
straight to geniculate-sinuous. Conidiogenous cells phialidic,
hyaline, smooth, aggregated, lining the inner cavity, subcylindrical
to ampulliform, straight to geniculate-sinuous; proliferating
several times percurrently near apex, rarely sympodially. Conidia
scolecosporous, hyaline, smooth, lexuous, rarely straight, granular,
thin-walled, narrowly obclavate, apex subobtuse, base long
obconically truncate, tapering to a truncate hilum, 3–multiseptate.
Type species: Neoseptoria caricis Quaedvlieg, Verkley & Crous.
Note: The genus Neoseptoria is morphologically similar to Septoria,
but distinct in having mono- to polyphialidic conidiogenous cells
that proliferate percurrently at the apex.
Neoseptoria caricis Quaedvlieg, Verkley & Crous, sp. nov.
MycoBank MB804422. Figs 41, 42.
Etymology: Named after the host genus on which it occurs, Carex.
Specimen examined: South Korea, on leaves of Dioscorea tokoro (Dioscoreaceae),
24 Oct. 2003, H.D. Shin (CPC 10855); ibid., on leaves of Dioscorea tenuipes, 1 Jan.
2004, H.D. Shin (CPC 11513).
Notes: Passalora dioscoreae is not congeneric with the type
species of the genus, P. bacilligera. The taxonomy of Passalora
and its relatives will be treated in a future publication (Videira et
al., in prep.).
Clade 9: Neoseptoria
Neoseptoria Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804421.
Etymology: Resembling the genus Septoria.
Foliicolous. Conidiomata black, immersed, subepidermal,
pycnidial, subglobose with central ostiole, exuding creamy conidial
Fig. 41. Conidia and conidiogenous cells of Neoseptoria caricis (CBS 135097).
Scale bars = 10 µm.
Fig. 42. Neoseptoria caricis (CBS 135097). A, B. Conidiomata developing in culture. C, D. Conidiogenous cells. E, F. Conidia. Scale bars = 10 µm.
352
Sizing up Septoria
On sterile Carex leaves on WA. Conidiomata up to 150 µm diam,
black, immersed, subepidermal, pycnidial, subglobose with central
ostiole, exuding creamy conidial mass; wall of 2–3 layers of brown
textura angularis. Conidiophores reduced to conidiogenous cells, or
0–2-septate, subcylindrical, hyaline to pale brown at base, smooth,
straight to geniculate-sinuous, 10–30 × 2.5–3.5 µm. Conidiogenous
cells phialidic, hyaline, smooth, aggregated, lining the inner cavity,
subcylindrical to ampulliform, straight to geniculate-sinuous, 8–15 ×
2.5–3 µm; proliferating several times percurrently near apex, rarely
sympodially. Conidia scolecosporous, hyaline, smooth, lexuous, rarely
straight, granular, thin-walled, narrowly obclavate, apex subobtuse,
base long obconically truncate, tapering to a truncate hilum, 1.5–2 µm
diam, 3(–5)-septate, (40–)55–68(–80) × (2.5–)3(–3.5) µm.
Culture characteristics: Colonies on PDA erumpent, undulate,
lacking aerial mycelium, reverse iron-grey, after 14 d, 3 cm diam;
on MEA reverse greyish sepia, after 14 d, 3 cm diam, with ine,
pale pink to orange aerial mycelium; on OA similar to MEA, but with
pinkish tufts of aerial mycelium.
Specimen examined: Netherlands, Wageningen, on leaves of Carex acutiformis
(Cyperaceae), Aug. 2012, W. Quaedvlieg (holotype CBS H-21293, culture ex-type
CBS 135097 = S653).
Notes: Several septoria-like species have been described from
Carex (Farr & Rossman 2013). Of these, N. caricis is most similar
to S. caricicola (conidia 25–55 × 4 µm; (6–)7(–8)-septate), but
distinct in having longer and narrower conidia with less septa.
Clade 10: Pseudocercospora
Note: See Crous et al. (2013)
clade 11: Zymoseptoria
Note: See Quaedvlieg et al. (2011).
clade 12: Ramularia
Note: See Crous et al. (2009a, c).
Clade 13: Dothistroma
Note: See Barnes et al. (2004).
Clade 14: Stromatoseptoria
Stromatoseptoria Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804423.
Etymology: Stroma = referring to central stoma in pycnidium that
gives rise to conidiophores; Septoria = septoria-like morphology.
Foliicolous, plant pathogenic. Conidiomata pycnidial,
hypophyllous, subglobose to lenticular, very pale brown to
dark brown, immersed to erumpent, exuding conidia in white
cirrhus; ostiolum central, circular, surrounding cells concolorous;
conidiomatal wall composed of a homogenous tissue of hyaline
to very pale brown, angular to irregular cells. Conidiophores
subcylindrical, branched, hyaline, septate. Conidiogenous cells
hyaline, discrete or integrated, cylindrical or narrowly ampulliform,
holoblastic, often also proliferating percurrently. Conidia
cylindrical, slightly to distinctly curved, broadly rounded apex,
attenuated towards a truncate base, transversely euseptate,
mostly constricted at septa.
Type species: Stromatoseptoria castaneicola (Desm.) Quaedvlieg,
Verkley & Crous.
Notes: Stromatoseptoria is distinguished from Septoria based on
the central cushion or stroma that gives rise to its conidiophores
(sensu Coniella and Pilidiella; van Niekerk et al. 2004), and conidia
that tend to be olivaceous-brown in mass, and also turn olivaceous
and verruculose with age.
Stromatoseptoria castaneicola (Desm.) Quaedvlieg,
Verkley & Crous, comb. nov. MycoBank MB804424. Fig. 43.
Basionym: Septoria castaneicola Desm., Ann. Sci. Nat., Sér. 3, Bot.
8: 26. 1847.
≡ (?) Phleospora castanicola (Desm.) D. Sacc., Mycoth. Ital., Cent. 1-2,
no. 173.
= Septoria gilletiana Sacc., Michelia 1: 359. 1878.
? = Septoria castaneae Lév., Ann. Sci. Nat., Sér. 3, Bot. 5: 278. 1846.
≡ Cylindrosporium castaneae Krenner, Bot. Közl. 41(3-4): 126. 1944.
Description in vivo. Leaf spots numerous, small, angular, and often
merging to irregular patterns, visible on both sides of the leaf,
initially pale yellowish brown, later reddish brown with a narrow,
darker border; Conidiomata pycnidial, hypophyllous, several in each
Fig. 43. Stromatoseptoria castaneicola (CBS 102320). A. Colony sporulating on MEA. B. Stroma giving rise to conidiogenous cells. C, D. Conidiogenous cells. E. Conidia. Scale
bars: B = 200 µm, all others = 10 µm.
www.studiesinmycology.org
353
Quaedvlieg et al.
leaf spot, subglobose to lenticular, very pale brown to dark brown,
usually fully immersed, 80–150(–200) µm diam, releasing conidia
in white cirrhi; ostiolum not well-differentiated, central, circular,
18–50 µm wide, surrounding cells concolorous; conidiomatal
wall about 10–17 µm thick, composed of a homogenous tissue of
hyaline to very pale brown, angular to irregular cells 4–10 µm diam;
Conidiophores subcylindrical, branched at base, hyaline, smooth,
1–2-septate; base frequently brown, verruculose. Conidiogenous
cells hyaline, discrete or integrated in conidiophores cylindrical
or narrowly ampulliform, holoblastic, often also proliferating
percurrently with up to 3 closely positioned annellations, 7–17(–
20) × 3–4(–5) µm. Conidia cylindrical, slightly to distinctly curved,
irregularly bent or lexuous, with a relatively broadly rounded apex,
attenuated towards a truncate base, basal and apical cell often
both wider than intermediate cells, (0–)2–3(–4)-septate, mostly
constricted around the septa in the living state, hyaline, contents
with several oil-droplets and granular material in each cell in the
living state, with granular contents in the rehydrated state, 30–
46 × 3–4 µm ("T"; rehydrated, "NT" 2–3 µm wide). Conidia are
olivaceous-brown in mass, and older conidia also turn olivaceous
and verruculose, and at times anastomose in culture.
Notes: According to the original diagnosis that Desmazières
published in 1847 based on material on Castanea collected in
autumn, the conidia are elongated, thin and curved, and about
40 µm in length. No further details like conidial septa were
given. The material PC0084574 is the only collection received
from PC that antidates the publication and assumedly is the
type. It consists of several leaves with numerous pycnidia in leaf
spots, some of which belong to Septoria castaneicola with the
characteristic conidia, but most are a spermatial state of most
likely the Mycosphaerella punctiformis complex (= Ramularia,
Verkley et al. 2004).
Teterevnikova-Babayan (1987) treated S. castaneicola Desm.
as a synonym of S. castaneae Lév., and both originally were
described from the same host, Castanea sativa (syn. C. vesca).
Teterevnikova-Babayan (1987) described the conidia as 3-septate,
25–40 × 2.5–4.5 µm, which is in fairly good agreement with present
observations. The type of S. castanaea Lév. could not be studied
and the name remains doubtful. Even though Léveillé described
symptoms that match those of S. castaneicola fairly well, he
described the conidia as aseptate, and failed to give information
about their size.
Culture characteristics: Colonies (CBS 102322) on OA reaching
4–8 mm diam in 25 d (9–12 mm in 33 d), with an even, glabrous,
buff margin; colonies restricted, up to 1 mm high, immersed
mycelium homogeneously buff, where conidiomatal complexes
develop dark brick to black, in part covered by pure white, dense,
appressed and woolly aerial mycelium, later a salmon haze occurs
in the immersed mycelium; reverse buff, locally cinnamon to sepia.
Colonies on CMA reaching (4–)7–11 mm diam in 25 d (8–12 mm
in 33 d), as on OA, but with a halo of reddish to salmon, diffusing
pigment, which becomes more intense after 33 d, and immersed
mycelium in the centre darker, and aerial mycelium more strongly
developed, later becoming locally salmon or citrine; reverse brick
and dark brick, surrounded by a reddish to salmon zone. Colonies
on MEA reaching 6.5–9 mm diam in 25 d (9–11.5 mm in 33 d),
with an even, buff to cinnamon margin, entirely hidden under the
aerial mycelium, with a very faint halo of diffusing pigment; colonies
restricted, up to 4 mm high, hemispherical to irregularly pustulate,
entirely covered by a dense mat of felted aerial mycelium, which,
especialy in the centre, attains a rosy buff or primrose to citrine
haze; reverse cinnamon to hazel, around a brick to dark brick
centre. Colonies on CHA reaching 7–9 mm diam in 25 d (9–11 mm
in 33 d), as on MEA, but no diffusing pigment observed around
the colonies. Conidiomata on OA developing after 10–15 d, black,
globose, single or merged to complexes up to 250 µm diam,
releasing milky white conidial slime. Conidiogenous cells as in
planta. Conidia as in planta, mostly 3-septate, 30–45 × 3.5–4.5 µm
(CBS 102320, OA, "T"; "NT" 3 µm wide).
Clade 15: Lecanosticta
Specimens examined: Austria, Tirol, Klausen, on leaves of Castanea vesca
(Fagaceae), Aug., distributed in F. von Höhnel, Krypt. exsicc. no. 415, (PC0084576,
PC0084583). France, Lébisey, Aug. and Sep. 1843, M. Roberge, ‘Coll.
Desmazières 1863, no. 8’, on leaves of Castanea sativa (PC0084574, type of
Septoria castanicola Desm.); same substr., Meudon, 1 Aug. 1849 (PC0084571,
PC0084589, PC0084590, PC0084591) and Jul. 1852 (PC0084572); same substr.,
loc. and date unknown, ‘Coll. Desmazières 1863, no. 8’ (PC0084570); Seine-etMarne, Fontainebleau, Sep 1881, distributed in Roumeguère, Fungi Gallici exsicc.
no. 2029 (PC0084575). Netherlands, prov. Utrecht, Baarn, Lage Vuursche, on
living leaves of Castanea sativa, 29 Aug. 1999, G. Verkley 912 (CBS H-21200),
cultures CBS 102320–102322; same substr., prov. Limburg, St. Jansberg, 9 Sep.
1999, G. Verkley 932 (CBS H-21214), culture CBS 102377; same substr., prov.
Limburg, Molenhoek, Heumense Schans (46-12-55), 23 Aug. 2004, G. Verkley & M.
Starink 3040, culture CBS 116464.
354
Note: See Quaedvlieg et al. (2012).
Clade 16: Phaeophleospora
Note: See Crous et al. (2009b, c).
Clade 17: Cytostagonospora
Cytostagonospora Bubák, Ann. Mycol. 14: 150. 1916.
Description: See above.
Type species: Cytostagonospora photiniicola
“photinicola”], Ann. Mycol. 14: 150. 1916.
Bubák
[as
Cytostagonospora martiniana (Sacc.) B. Sutton & H.J.
Swart, Trans. Br. mycol. Soc. 87: 99. 1986. Figs 44, 45.
Basionym: Septoria martiniana Sacc., Syll. Fung. (Abellini) 10: 351.
1892.
= Septoria phyllodiorum Cooke & Massee, Grevillea 19(90): 47. 1890, non S.
phyllodiorum Sacc., Hedwigia 29: 156. 1890.
On sterile Carex leaves on WA. Leaf spots amphigenous, circular,
grey to brown with raised dark brown border, 1–3 mm diam.
Conidiomata immersed, subepidermal, epiphyllous, solitary to
aggregated with stromatic tissue, with central ostiolar opening
exuding a creamy to white conidial mass, rupturing at maturity
(pycnidial to acervular), brown, globose, up to 400 µm diam; wall
of 3–6 layers of brown textura angularis. Conidiophores hyaline,
smooth, subcylindrical, 0–5-septate, branched or not, 10–15(–50)
× 3–4 µm, giving rise to terminal and lateral conidiogenous cells.
Conidiogenous cells hyaline, smooth, subcylindrical or ampulliform,
4–8 × 3–4 µm, polyphialidic, with apical and lateral loci, with visible
periclinal thickening, at times also proliferating percurrently (both
modes can also be present on the same conidiogenous cell).
Conidia hyaline, smooth, granular, irregularly curved, subcylindrical
Sizing up Septoria
to narrowly obclavate, apex subobtuse, base long, obconically
truncate, (1–)3-septate, (18–)32–45(–50) × (1.5–)2(–3) µm; base
not thickened, 0.5–1 µm diam.
Culture characteristics: Colonies on PDA convex, erumpent with
feathery margin, lacking aerial mycelium, surface fuscous-black,
reverse olivaceous-black, after 14 d, 4 cm diam, with a beautifull
purple exudate at the outer edges; on MEA, after 14 d, 3.5 cm
diam, lacking any exudate; on OA surface fuscous-black, reverse
olivaceous-grey, after 14 d, 4 cm diam, purplish-red coloured
exudate.
Specimen examined: Australia, Warneet close to Melbourne, S38º13’37.8”
E145º18’25.4”, on leaves of Acacia pycnantha (Mimosaceae), 21 Oct. 2009, P.W.
Crous (specimen CBS H-21297, culture CBS 135102 = CPC 17727).
Notes: The present collection matches the description of
Cytostagonospora martiniana provided by Sutton & Swart (1986).
As discussed by the authors, this genus is distinct from Septoria
s. str. based on its conidiomata aggregated in stromatic tissue,
and unique mode of conidiogenesis. In culture conidiogenous cells
exhibited a mixture of sympodial proliferation, or were polyphialidic
with periclinal thickening, but also proliferated percurrently. Species
of Septoria occurring on Acacia were treated by Sutton & Pascoe
(1987).
Clade 18: Zasmidium
Note: See Crous et al. (2007a, b, 2009c).
Clade 19: Polyphialoseptoria
Polyphialoseptoria Quaedvlieg, R.W. Barreto, Verkley &
Crous, gen. nov. MycoBank MB804425.
Etymology: Polyphialo = polyphialides; Septoria = septoria-like.
Foliicolous, plant pathogenic. Conidiomata brown, erumpent,
pycnidial (acervular in culture), globose, brown; wall of 3–6
layers of pale brown textura angularis. Conidiophores reduced
to conidiogenous cells. Conidiogenous cells hyaline, smooth,
subcylindrical to ampulliform; proliferating sympodially at apex,
forming polyphialides with minute periclinal thickening, or as
solitary loci on supericial mycelium in culture. Conidia hyaline,
smooth, granular to guttulate, scolecosporous, irregularly curved,
apex subobtuse, base long obconically truncate, transversely multieuseptate, in older cultures disarticulating at septa; microcyclic
conidiation also common in older cultures.
Fig. 44. Conidia and conidiogenous cells of Cytostagonospora martiniana (CBS
135102). Scale bars = 10 µm.
Type species: Polyphialoseptoria terminaliae Quaedvlieg, R.W.
Barreto, Verkley & Crous.
Fig. 45. Cytostagonospora martiniana (CBS 135102). A. Leaf spot. B. Conidiomata forming in culture. C–F. Conidiogenous cells. G. Conidia. Scale bars = 10 µm.
www.studiesinmycology.org
355
Quaedvlieg et al.
Polyphialoseptoria tabebuiae-serratifoliae Quaedvlieg,
Alfenas & Crous, sp. nov. MycoBank MB804427. Figs 46,
47.
Polyphialoseptoria tabebuiae-serratifoliae is distinct from species
of Septoria known from Tabebuia based on its conidial morphology.
Etymology: Named after its host, Tabebuia serratifolia.
Polyphialoseptoria terminaliae Quaedvlieg, R.W. Barreto,
Verkley & Crous, sp. nov. MycoBank MB804426. Fig. 48.
Leaf spots variable in number on mature leaves; initially as small
spots or purple-brown areas, with the inner part becoming greywhite with age, surrounded by a purple-brown halo. Conidiomata
developing on sterile barley leaves on WA, pale cream in colour,
erumpent, globose, up to 180 µm diam; wall of 2–3 layers of
pale brown textura angularis. Conidiophores hyaline, smooth,
cylindrical, septate, branched, 10–35 × 1.5 µm. Conidiogenous
cells terminal and lateral, cylindrical, hyaline, smooth, proliferating
sympodially, 10–15 × 1.5 µm. Conidia solitary, hyaline, smooth,
granular, irregularly curved, subcylindrical, apex subobtuse, base
truncate, (0–)1–3(–4)-septate, (15–)25–35(–55) × 1.5(–2) µm.
Culture characteristics: Colonies lat, spreading, with sparse aerial
mycelium and smooth, even margins, reaching 40 mm diam after
2 wk. On OA surface dirty pink; on PDA surface and reverse dirty
white. On MEA surface folded, dirty white, reverse cinnamon.
Specimen examined: Brazil, Minas Gerais, Viçosa, on leaves of Tabebuia serratifolia
(Bignoniaceae), 1999, A.C. Alfenas (holotype CBS H-21299, culture ex-type CBS
112650).
Notes: Inácio & Dianese (1998) described Septoria tabebuiaeimpetiginosae on T. impetiginosa (conidia 25–67 × 2–4 µm,
2–6-septate), and also compared this species to S. tabebuiae
(18–40 × 1.7–2.5 µm, aseptate conidia) on T. berteroi, and S.
cucutana (34–40 × 0.8–1 µm) on T. pentaphylla and T. spectabilis.
Furthermore, they also referred to an undescribed species Ferreira
(1989) mentioned on T. serratifolia in Viçosa, Minas Gerais,
which is named as S. tabebuiae-serratifoliae in the present study.
Etymology: Named after the host genus from which it was collected,
Terminalia.
Leaf spots irregular to subcircular, amphigenous, mostly aggregated
along leaf veins, pale brown, 3–8 mm diam, surrounded by a
prominent, wide, red-purple border. On sterile Carex leaves on
WA. Conidiomata brown, erumpent, pycnidial (acervular in culture),
up to 600 µm diam, globose, brown, exuding a crystalline cirrhus
of conidia; wall of 3–6 layers of pale brown textura angularis.
Conidiophores reduced to conidiogenous cells. Conidiogenous
cells hyaline, smooth, subcylindrical to ampulliform, 5–10 × 3–4
µm; proliferating sympodially at apex, forming polyphialides
with minute periclinal thickening, or as solitary loci on supericial
mycelium in culture. Conidia hyaline, smooth, granular to guttulate,
scolecosporous, irregularly curved, apex subobtuse, base long
obconically truncate (1–1.5 µm diam), multiseptate (–16), in
older cultures disarticulating at septa; microcyclic conidiation also
common in older cultures, (40–)75–120(–140) × 2–3(–3.5) µm.
Culture characteristics: Colonies on PDA erumpent with feathery
margin, lacking aerial mycelium, surface fuscous-black, reverse
olivaceous-black to buff in the younger tissue, after 14 d, 1 cm
diam; on MEA surface and reverse isabelline to greyish-sepia; on
OA surface pale-vinaceous, reverse rosy-buff to buff.
Specimen examined: Brazil, Minas Gerais, Viçosa, on leaves of Terminalia catappa
(Combretaceae), 18 May 2010, R.W. Barreto (holotype CBS H-21298, culture extype CBS 135106 = CPC 19611); ibed., (CBS 135475 = CPC 19487)
Notes: As far as we could establish there are presently no species
of Septoria described from Terminalia, and as this taxon is distinct
from all taxa in GenBank, we herewith describe it as a novel species.
A Septoria sp. has been reported on leaves of Terminalia sp. in
Florida and Venezuela (Farr & Rossman 2013). Polyphialoseptoria
is distinct from Septoria based on the presence of polyphialides.
Neoseptoria also has phialides as observed in Polyphialoseptoria,
but these tend to chiely be monophialides.
Clade 20: Ruptoseptoria
Fig. 46. Conidia and conidiogenous loci on hypha of Polyphialoseptoria tabebuiaeserratifoliae (CBS 112650). Scale bars = 10 µm.
Ruptoseptoria Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804428.
Fig. 47. Polyphialoseptoria tabebuiae-serratifoliae (CBS 112650). A. Conidiomata forming in culture. B. Conidiogenous cells. C. Conidia. Scale bars = 10 µm.
356
Sizing up Septoria
Fig. 48. Polyphialoseptoria terminaliae (CBS 135106). A. Leaves with leaf spots. B, C. Conidiomata sporulating in culture. D–F. Conidiogenous cells and loci. G. Conidia. Scale
bars = 10 µm.
Etymology: Rupto = irregular rupture of conidiomata; Septoria =
septoria-like.
Foliicolous, plant pathogenic. Conidiomata black, appressed,
elongated, pycnidial, but opening via irregular rupture, convulated;
exuding a creamy white conidial mass; outer wall dark brown,
crusty, consisting of 6–8 layers of dark brown textura angularis;
giving rise to 2–3 inner layers of pale brown to hyaline textura
angularis. Conidiophores lining the inner cavity, hyaline, smooth
or pale brown, verruculose at base, branched below, septate,
subcylindrical. Conidiogenous cells integrated, terminal,
subcylindrical, smooth; proliferating sympodially at apex, or apex
phialidic with minute periclinal thickening. Conidia solitary, hyaline,
smooth, guttulate, subcylindrical to narrowly obclavate, gently
to irregularly curved, apex subobtuse, base truncate to narrowly
obovoid, transversely septate.
Type species: Ruptoseptoria unedonis (Roberge ex Desm.)
Quaedvlieg, Verkley & Crous.
Ruptoseptoria unedonis (Roberge ex Desm.) Quaedvlieg,
Verkley & Crous, comb. nov. MycoBank MB804429. Figs 49,
50.
Basionym: Septoria unedonis Roberge ex Desm., Ann. Sci. Nat.,
Bot., Sér. 3(8): 20. 1847.
= Sphaerella arbuticola Peck, Bull. Torrey Bot. Club 10(7): 75. 1883.
≡ Mycosphaerella arbuticola (Peck) Jaap, Ann. Mycol. 14(1/2): 13. 1916.
≡ Mycosphaerella arbuticola (Peck) House, Contr. Univ. Mich. Herb. 9(8):
587. 1972.
Leaf spots numerous, small, amphigenous, irregular to subcircular,
whitish in the middle, with very broad, purple borders. Conidiomata
black, appressed, elongated, pycnidial, but opening via irregular
rupture, convulated, up to 450 µm diam, exuding a creamy white
conidial mass; outer wall dark brown, crusty, consisting of 6–8
layers of dark brown textura angularis; giving rise to 2–3 inner
www.studiesinmycology.org
Fig. 49. Conidia and conidiogenous cells of Ruptoseptoria unedonis (CBS 355.86).
Scale bars = 10 µm.
layers of pale brown to hyaline textura angularis. Conidiophores
lining the inner cavity, hyaline, smooth or pale brown, verruculose
at base, branched below, 1–2-septate, subcylindrical, 10–15 ×
2–4 µm. Conidiogenous cells integrated, terminal, subcylindrical,
smooth, 6–12 × 2.5–3.5 µm; proliferating sympodially at apex, or
apex phialidic with minute periclinal thickening. Conidia solitary,
hyaline, smooth, guttulate, subcylindrical to narrowly obclavate,
gently to irregularly curved, apex subobtuse, base truncate to
narrowly obovoid, 1–3(–6)-septate, (25–)30–47(–56) × 2(–3) um.
357
Quaedvlieg et al.
Fig. 50. Ruptoseptoria unedonis (CBS 355.86). A, C. Conidiomata forming in culture. B, D. Conidiogenous cells. E. Conidia. Scale bars: A = 450 µm, C = 110 µm, all others =
10 µm.
Culture characteristics: Colonies on OA spreading with moderate
aerial mycelium and smooth, even margins; surface olivaceousgrey in outer region, centre dirty white to pale pink, reverse iron
grey; on MEA surface dark-mouse-grey to mouse-grey, reverse
greenish-black; on PDA surface mouse-grey to dark-mouse-grey,
reverse greenish-black.
Specimen examined: France, Seignosse le Penon, Lamdes, Forest communale de
Seignosse, on leaves of Arbutus unedo (Ericaceae), Aug. 1986, H.A. van der Aa
(CBS H-14645, culture CBS 355.86).
Notes: Mycosphaerella arbuticola (CBS 355.86) is a species
pathogenic to Arbutus menziesii in California (Aptroot 2006),
clusters with “Septoria” unedonis (CBS 755.70, CBS H-18192),
which is associated with leaf spots on Arbutus unedo in Croatia, and
elsewhere in Europe. Based on these results, the sexual-asexual link
between these two names is conirmed. Morphologically, however,
Ruptoseptoria is similar to Septoria, and can only be distinguished
based on its conidiomata that are convulated, opening by irregular
rupture, and conidiogenous cells that are frequently phialidic.
Clade 25: Cylindroseptoria
Cylindroseptoria Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804430.
Etymology: Cylindro = cylindrical conidia; Septoria = septoria-like.
Conidiomata pycnidial with central ostiole, or cupulate, separate,
brown, short-stipitate, tapering towards base; rim with elongated
brown, thick-walled cells with obtuse ends; rim covered with mucoid
layer that lows over from conidiomatal cavity, illed with conidial
mass; wall of 3–4 layers of medium brown textura angularis,
becoming hyaline towards inner region. Conidiogenous cells
hyaline, smooth, ampulliform, lining inner cavity, with prominent
periclinal thickening at apex. Conidia solitary, hyaline, smooth,
granular or not, cylindrical with obtuse apex, tapering at base to
truncate scar, aseptate.
Type species: Cylindroseptoria ceratoniae Quaedvlieg, Verkley &
Crous.
clade 21: Dissoconium (Dissoconiaceae)
Note: See Li et al. (2012).
Cylindroseptoria ceratoniae Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804431. Figs 51, 52.
clade 22: Readeriella (Teratosphaeriaceae)
Note: See Crous et al. (2007a, 2009a–c).
Clade 23: Teratosphaeria
Note: See Crous et al. (2007, 2009c).
Clade 24: septoria-like
Specimen examined: Brazil, Nova Friburgo, on leaves of Tibouchina herbacea
(Melastomataceae), 15 Dec. 2007, D.F. Parreira (CBS 134910 = CPC 19500).
Note: The taxonomy of this species could not be resolved, as
isolate CPC 19500 proved to be sterile.
358
Etymology: Named after the host genus on which it occurs,
Ceratonia.
Conidiomata separate, brown, cupulate, short-stipitate, rim up to
300 µm diam, 100–180 µm tall, tapering towards base, 20–50 µm
diam (on Anthriscus sylvestris stems, not on OA or PDA, where
they appear more lattened with agar surface); rim with elongated
brown, thick-walled cells with obtuse ends, 5–12 × 4–5 µm; rim
covered with mucoid layer that lows over from conidiomatal cavity,
illed with conidial mass; wall of 3–4 layers of medium brown textura
angularis, becoming hyaline towards inner region. Conidiogenous
cells hyaline, smooth, ampulliform, lining inner cavity, 7–12 × 4–6
µm; apex 2 µm diam, with prominent periclinal thickening. Conidia
solitary, hyaline, smooth, granular or not, cylindrical with obtuse
Sizing up Septoria
apex, tapering at base to truncate scar 1 µm diam, aseptate, (10–)
12–14(–16) × 3(–3.5) µm.
Culture characteristics: Colonies spreading, reaching 28 mm diam
after 2 wk, with sparse aerial mycelium and even, lobate margins.
On MEA surface iron-grey, reverse olivaceous-grey. On OA surface
olivaceous-grey. On PDA surface and reverse iron-grey.
Specimen examined: Spain, Mallorca, Can Pastilla, on leaves of Ceratonia siliqua
(Caesalpinaceae), 24 May 1969, H.A. van der Aa (holotype CBS H-21300, culture
ex-type CBS 477.69).
Notes: Cylindroseptoria ceratoniae is quite distinct in that it
has cup-shaped acervuli, ampilliform conidiogenous cells with
periclinal thickening, and hyaline, aseptate, cylindrical conidia.
Cylindroseptoria needs to be compared with Satchmopsis
(infundibular conidiomata), Cornucopiella (tubular conidiomata) and
Thaptospora (cylindrical / lageniform / campanulate conidiomata),
but the combination of cupulate conidiomata and cylindrical, and
aseptate conidia is distinct.
Conidiomata pycnidial, erumpent, globose, black, separate,
with black crusty outer layer of cells, up to 200 µm diam, with
central ostiole; wall of 3–6 layers of brown textura angularis.
Conidiophores reduced to conidiogenous cells. Conidiogenous
cells phialidic (mostly monophialidic, but a few observed to also be
polyphialidic), lining the inner cavity, hyaline, smooth, ampulliform,
5–8 × 3–4 µm, proliferating percurrently (inconspicuous) or with
periclinal thickening at apex (also occurring as solitary loci on
supericial hyphae surrounding pycnidia). Conidia hyaline, smooth,
cylindrical, mostly straight, rarely slightly curved, apex subobtuse,
base truncate, guttulate, aseptate, (9–)11–13(–18) × 2.5–3(–3.5)
µm.
Culture characteristics: Colonies on PDA lat, circular, lacking
aerial mycelium, surface fuscous-black, reverse olivaceous-black,
after 14 d, 3.5 cm diam; on MEA surface fuscous-black, reverse
olivaceous-black, after 14 d, 4.5 cm diam; on OA similar to PDA.
Specimen examined: Spain, Mallorca, El Arenal, on leaves of Pistacia lentiscus
(Anacardiaceae), 25 May 1969, H.A. van der Aa (holotype CBS H-21301, culture
CBS 471.69).
Etymology: Named after the host genus on which it occurs, Pistacia.
Notes: Cylindroseptoria pistaciae is tentatively placed in
Cylindroseptoria, as it has pycnidial rather than cupulate
conidiomata. However, synapomorphies with Cylindroseptoria
include phialides with periclinal thickening, and cylindrical, aseptate
conidia. Further collections are required to determine if conidiomatal
anatomy is more important than conidiogenesis and conidial
morphology. For the present, however, the generic circumscription
Fig. 51. Conidia and conidiogenous cells of Cylindroseptoria ceratoniae (CBS
477.69). Scale bar = 10 µm.
Fig. 53. Conidia and conidiogenous cells of Cylindroseptoria pistaciae (CBS
471.69). Scale bars = 10 µm.
Cylindroseptoria pistaciae Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804432. Figs 53, 54.
Fig. 52. Cylindroseptoria ceratoniae (CBS 477.69). A, B. Conidiomata forming in culture. C, D. Conidiogenous cells giving rise to conidia. E. Conidia. Scale bars: B = 45 µm,
all others = 10 µm.
www.studiesinmycology.org
359
Quaedvlieg et al.
Fig. 54. Cylindroseptoria pistaciae (CBS 471.69). A, B. Conidiomata sporulating in culture. C, D. Intercalary chains of chlamydospore-like cells. E, F. Conidiogenous cells. G,
H. Conidia. Scale bars = 10 µm.
of Cylindroseptoria has been widened to include taxa with pycnidial
conidiomata. Cylindroseptoria pistaciae could be confused with
Septoria pistaciae, though conidia of the latter are 20–30 × 1.6 µm,
and are 1(–3)-septate (Chitzanidis & Michaelides 2002).
and inconspicuous. Conidia fusiform, lunate or irregular, curved,
unicellular, colourless, smooth-walled with or without an excentric
basal appendage, continuous with conidium body, plectronoid to
podiform, or with a blunt or spathulate distal end.
Clade 26: Pseudoseptoria
Type species: P. donacicola Speg., Ann. Mus. Nac. B. Aires, Ser. 3
13: 388. 1910. [= P. donacis (Pass.) B. Sutton].
Pseudoseptoria Speg., Ann. Mus. Nac. B. Aires, Ser. 3 13:
388. 1910.
= Aphanofalx B. Sutton, Trans. Brit. Mycol. Soc. 86: 21. 1986.
Caulicolous and foliicolous, plant pathogenic or saprobic.
Conidiomata stromatic, pycnidioid, unilocular, glabrous, black,
ostiolate; wall of textura angularis, in some cases cells in the upper
wall larger and darker than cells in the lower wall. Conidiophores
reduced to conidiogenous cells lining the cavity of the conidioma.
Conidiogenous cells discrete or integrated, cylindrical or lageniform,
colourless, smooth-walled, invested in mucus, with a prominent
cylindrical papilla with several percurrent proliferations at the
apex; collarette prominent and extanding past conidia, or reduced
Pseudoseptoria collariana Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804433. Fig. 55.
Etymology: Named after its prominently lared collarettes, forming
a sleeve.
On sterile Carex leaves on WA. Conidiomata immersed to erumpent,
globose, dark brown, up to 400 µm diam, unilocular, opening via
central ostiole; wall of 6–10 layers of brown textura angularis.
Conidiophores reduced to conidiogenous cells, or branched at
the base with one supporting cell that is dark brown, encased
Fig. 55. Pseudoseptoria collariana (CBS 135104). A, B. Colonies sporulating in culture. C–F. Conidiogenous cells with prominent collarettes. G, H. Conidia. Scale bars: A = 400
µm, all others = 10 µm.
360
Sizing up Septoria
Fig. 56. Pseudoseptoria obscura (CBS 135103). A, B. Colony sporulating in culture. C. Chlamydospore-like cells developing. D, E. Conidiogenous cells. F–H. Conidia. Scale
bars: B = 250 µm, all others = 10 µm.
in a mucilaginous matrix. Conidiogenous cells subcylindrical to
ampulliform, hyaline, smooth to pale brown, inely verruculose,
18–35 × 3.5–8 µm; apical region with numerous conspicuous
percurrent proliferations, with long, prominent collarettes that
completely enclose and extend above young, developing conidia,
but disintegrating into a mucoid mass with age. Conidia fusiform,
lunate, curved, aseptate, hyaline, smooth, tapering to an subobtuse
to spathulate apex, base truncate (1 µm diam), with a single,
unbranched, eccentric basal appendage, 2–4 µm long; conidia
(from apex to hilum) (24–)26–28(–30) × (2.5–)3 µm.
Culture characteristics: Colonies on PDA lat, round with feathery
margins, lacking aerial mycelium, surface olivaceous-black to rosybuff for younger tissue, reverse olivaceous-black, to rosy-buff for
younger tissue, after 14 d 1.5 cm diam; on MEA surface olivaceousblack to buff for younger tissue, reverse olivaceous-black to brick
for younger tissue, after 14 d, 2 cm diam; on OA similar to MEA.
Specimen examined: Iran, Golestan Province, on leaves of Bamboo (Poaceae), 12
May 2009, A. Mirzadi Gohari (holotype CBS H-21302, culture ex-type CBS 135104
= CPC 18119).
Pseudoseptoria obscura Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804434. Fig. 56.
Etymology: Named after the obscure basal appendage that occurs
on some conidia.
On sterile Carex leaves on WA. Conidiomata immersed to
erumpent, globose, dark brown, up to 250 µm diam (smaller than in
18119), unilocular, opening via central ostiole; wall of 3–6 layers of
brown textura angularis. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells subcylindrical to doliiform, hyaline,
smooth to pale brown, inely verruculose, 6–12 × 2–5 µm; apical
region with numerous inconspicuous to conspicuous percurrent
proliferations; collarettes absent to prominent. Conidia fusiform,
www.studiesinmycology.org
lunate, curved, aseptate, hyaline, smooth, tapering to an subobtuse
apex; base truncate, rarely with a single, unbranched, eccentric
basal appendage, 1–2 µm long; conidia (from apex to hilum) (8–)
12–14(–15) × (2–)2.5(–3) µm.
Culture characteristics: Colonies on PDA lat, undulate with
feathery margins, lacking aerial mycelium, surface concentric rings
of fuscous-black to pale purplish grey to fuscous-black, reverse
concentric rings of greyish-sepia to fawn to fuscous-black, after 14
d, 2 cm diam; on MEA similar to PDA; OA lat, undulate, lacking
aerial mycelium, surface fuscous-black to purplish grey for the
younger tissue, reverse greyish-sepia to vinaceous-buff for the
younger tissue.
Specimen examined: Iran, Golestan Province, on leaves of Bamboo (Poaceae), 12
May 2009, A. Mirzadi Gohari (holotype CBS H-21303, culture ex-type CBS 135103
= CPC 18118).
Notes: Species of the genus Aphanofalx occur on members of
Poaceae, presumably as saprobes. The genus is characterised
by having taxa with pycnidial conidiomata, and percurrently
proliferating conidiogenous cells, and hyaline, aseptate conidia
with a basal, excentric appendage. In contrast, species of
Pseudoseptoria are known to occur on members of Poaceae
as plant pathogens. The genus is also characterised by having
taxa with pycnidial conidiomata, and percurrently proliferating
conidiogenous cells, and hyaline, aseptate conidia that lack basal
appendages. During this study we also investigated three strains
identiied as P. donasis (CBS 291.69, 313.68 and 417.51), the
type species of Pseudoseptoria. Much to our surprise they formed
a monophyletic lineage (results not shown) with the two strains
described here (which have basal appendages), suggesting that
Pseudoseptoria represents an older name for Aphanofalx, and that
the basal appendage is a species-speciic character, as also found
in other groups of coelomycetes (Crous et al. 2012b).
Aphanofalx is presently known from two species, A. mali (conidia
26–33 × 2–2.5 µm), and A. irregularis (conidia 12–28(–31) × (2–)2.5–
361
Quaedvlieg et al.
3(–3.5) µm (Nag Raj 1993). Pseudoseptoria collariana [conidia (24–)
26–28(–30) × (2.5–)3 µm] and P. obscura [conidia (8–)12–14(–15) ×
(2–)2.5(–3) µm] are easily distinguished from these taxa based on
their conidial dimensions. The three species of Pseudoseptoria treated
by Sutton (1980), namely P. donacis (conidia 20–23 × 2–2.5 µm), P.
stromaticola (conidia 16–18.5 × 2 µm) and P. bromigena (conidia 20–
23 × 2–2.5 µm) can be distinguished from P. collorata and P. obscura
by conidial dimensions, and lacking basal conidial appendages.
Clade 27: Parastagonospora
Specimens examined: Germany, Kiel-Kitzeberg, on Lolium multilorum, 1968, U.G.
Schlösser, CBS 290.69, CBS 289.69.
Notes: Although the oldest epithet for this taxon is Pleospora
tritici (1874), “avenae” has been well established in literature, and
accepted by the community. We thus recommend that this epithet
be retained for this pathogen. Parastagonospora avenae leaf blotch
of barley and rye (f.sp. tritici), appears distinct from the pathogen on
oats (f.sp. avenaria) (Cunfer 2000), and further research is required
to resolve this issue.
Parastagonospora Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804435.
Parastagonospora caricis Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804437. Figs 57, 58.
Etymology: Resembling the genus Stagonospora.
Etymology: Named after the host genus from which it was collected,
Carex.
Foliicolous, plant pathogenic. Ascocarps immersed, globose,
becoming depressed, medium brown to black; wall of 3–6 layers
of thick-walled, brown textura angularis; ostiole slightly papillate.
Asci clavate, cylindrical or curved, shortly stipitate, 8-spored;
ascus wall thick, bitunicate. Ascospores fusoid, subhyaline to
pale brown, transversely euseptate (–3), constricted at the septa,
penultimate cell swollen. Pseudoparaphyses iliform, hyaline,
septate. Conidiomata black, immersed, subepidermal, pycnidial,
subglobose with central ostiole, exuding creamy conidial mass;
wall of 2–3 layers of brown textura angularis. Conidiophores
reduced to conidiogenous cells. Conidiogenous cells phialidic,
hyaline, smooth, aggregated, lining the inner cavity, ampulliform
to subcylindrical, with percurrent proliferation near apex. Conidia
hyaline, smooth, thin-walled, cylindrical, granular to multi-guttulate,
with obtuse apex and truncate base, transversely euseptate.
Type species: Parastagonospora nodorum (Berk.) Quaedvlieg,
Verkley & Crous.
Notes: The genus Parastagonospora is introduced to accommodate
several serious cereal pathogens that were formerly accommodated
in either Septoria/Stagonospora, or Leptosphaeria/Phaeosphaeria.
As shown previously, Septoria is not available for these fungi
(Quaedvlieg et al. 2011), and neither is Leptosphaeria (de Gruyter
et al. 2013). Furthermore, in the present study we also clarify the
phylogenetic positions of Stagonospora and Phaeosphaeria, which
cluster apart from this group of cereal pathogens, which are best
accommodated in their own genus, Parastagonospora.
Parastagonospora is distinguished from Stagonospora in that
Stagonospora has conidiogenous cells that proliferate percurrently,
or via phialides with periclinal thickening, and conidia that are
subcylindrical to fusoid-ellipsoidal. Sexual morphs known for
species of Parastagonospora are phaeosphaeria-like, whereas
those observed for Stagonospora s. str. are didymella-like.
On sterile Carex leaves on WA. Conidiomata up to 250 µm diam,
black, immersed, subepidermal, pycnidial, subglobose with central
ostiole, exuding pale pink conidial cirrhus; wall of 2–3 layers of
brown textura angularis. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells phialidic, hyaline, smooth, aggregated,
lining the inner cavity, ampulliform, 8–15 × 4–6 µm, with percurrent
proliferation at apex. Conidia hyaline, smooth, thin-walled,
scolecosporous, subcylindrical, with subobtuse apex and truncate
base, 7–15-septate, (50–)60–70(–75) × (5–)6 µm.
Culture characteristics: Colonies on PDA lat, undulate, with short,
white aerial mycelium, surface olivaceous-black in the older parts,
vinaceous-buff in the younger mycelium, reverse olivaceous-black in
the older parts, brick in the younger mycelium, after 14 d, 4 cm diam;
on MEA convex, imbriate, surface fawn to hazel, reverse fusceousblack to cinnamon, after 14 d, 3 cm diam; on OA similar to MEA.
Specimen examined: Netherlands, Veenendaal, de Blauwe Hel, on leaves of Carex
acutiformis (Cyperaceae), 25 Jul. 2012, W. Quaedvlieg (holotype CBS H-21304,
culture ex-type CBS 135671 = S615).
Note: Conidia of P. caricis are larger than those of P. avenae, which
are (1–)3(–7)-septate, 17–46 × 2.5–4.5 µm (Bissett 1982), and
narrower than those of Stagonospora gigaspora, which are 58–84
× 10–14 µm (Ellis & Ellis 1997).
Parastagonospora avenae (A.B. Frank) Quaedvlieg,
Verkley & Crous, comb. nov. MycoBank MB804436.
Basionym: Septoria avenae A.B. Frank, Ber. Dt. Bot. Ges. 13: 64.
1895.
≡ Stagonospora avenae (A.B. Frank) Bissett [as ‘avena’], Fungi
Canadenses, Ottawa 239: 1. 1982
= Leptosphaeria avenaria G.F. Weber, Phytopath. 12: 449. 1922.
≡ Phaeosphaeria avenaria (G.F. Weber) O.E. Erikss., Ark. Bot., Ser. 2
6: 408. 1967.
= Pleospora tritici Garov., Arch. Triennale Lab. Bot. Crittog. 1: 123. 1874.
362
Fig. 57. Conidia and conidiogenous cells of Parastagonospora caricis (CBS
H-21304). Scale bars = 10 µm.
Sizing up Septoria
Fig. 58. Parastagonospora caricis (CBS H-21304). A. Colony sporulating in culture. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
Fig. 59. Parastagonospora nodorum (CBS H-13909). A, C. Ascomata and conidiomata forming in culture. B, D, F. Asci with ascospores. E, G. Conidia. Scale bars = 10 µm.
Parastagonospora nodorum (Berk.) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804438. Fig. 59.
Basionym: Depazea nodorum Berk., Gard. Chron., London: 601.
1845.
≡ Septoria nodorum (Berk.) Berk., Gard. Chron., London: 601. 1845.
≡ Stagonospora nodorum (Berk.) E. Castell. & Germano, Annali Fac. Sci.
Agr. Univ. Torino 10: 71. 1977. [1975–76]
= Leptosphaeria nodorum E. Müll., Phytopath. J. 19: 409. 1952.
≡ Phaeosphaeria nodorum (E. Müll.) Hedjar., Sydowia 22: 79. 1969.
[1968]
Specimen examined: denmark, on Lolium perenne, Feb. 2002, M.P.S. Câmara,
CBS 110109.
Notes: Parastagonospora nodorum blotch is an important disease
of cereals, having been reported from barley and wheat in most
countries where these crops are cultivated (Cunfer 2000). Recent
studies have also indicated that P. nodorum probably resembles a
species complex, awaiting further morphological characterisation
(McDonald et al. 2013).
www.studiesinmycology.org
Parastagonospora poae Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804439. Figs 60, 61.
Etymology: Named after the host genus from which it was collected,
Poa.
On sterile Carex leaves on WA. Conidiomata up to 250 µm diam,
black, immersed, subepidermal, pycnidial, subglobose with central
ostiole, exuding creamy conidial mass; wall of 2–3 layers of brown
textura angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells phialidic, hyaline, smooth, aggregated, lining
the inner cavity, ampulliform to subcylindrical, with percurrent
proliferation near apex, 6–10 × 3–4(–5) µm. Conidia hyaline,
smooth, thin-walled, cylindrical, granular, with obtuse apex and
truncate base, medianly 1-septate, (20–)25–27(–32) × (2–)2.5(–
2.5) µm; ends becoming swollen and guttulate with age.
Culture characteristics: Colonies on PDA lat, circular, with sparse,
white aerial mycelium, surface dark-mouse-grey, reverse black,
363
Quaedvlieg et al.
after 14 d, 8.5 cm diam; on MEA surface hazel, reverse dark-brick
to sepia; OA similar to MEA.
Type species: Neostagonospora caricis Quaedvlieg, Verkley &
Crous.
Specimens examined: Netherlands, Wageningen, on leaves of Poa sp. (Poaceae),
2 Aug. 2012, S. Videira J (holotype CBS H-21305, culture ex-type CBS 135089 =
S606); Wageningen, on leaves of Poa sp., 2 Aug. 2012, S. Videira CBS 135091 =
S613).
Note: Neostagonospora is similar to Stagonospora by having
pycnidial conidiomata with euseptate, hyaline, fusoid-ellipsoidal
to subcylindrical conidia, but distinct in having conidiogenous cells
that are phialidic, with prominent periclinal thickening.
Note: Conidia of P. poae are narrower than those of P. nodorum,
which are (0–)1–3-septate, 13–28 × 2.8–4.6 µm (Bissett 1982).
Clade 28: Neostagonospora
Neostagonospora Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804440.
Etymology: Resembling the genus Stagonospora.
Foliicolous. Conidiomata immersed, pycnidial, globose, exuding a
pale luteous to creamy conidial mass; wall of 2–3 layers of pale
brown textura angularis. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells phialidic, hyaline, smooth, aggregated,
lining the inner cavity, ampulliform to doliiform, tapering at apex with
prominent periclinal thickening. Conidia hyaline, smooth, granular,
thin-walled, narrowly fusoid-ellipsoidal to subcylindrical, apex
subobtusely rounded, base truncate, widest in middle, transversely
euseptate, becoming constricted with age.
Fig. 60. Conidia and conidiogenous cells of Parastagonospora poae (CBS 135091).
Scale bars = 10 µm.
Neostagonospora caricis Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804441. Figs 62, 63.
Etymology: Named after the host genus on which it occurs, Carex.
On sterile Carex leaves on WA. Conidiomata immersed,
pycnidial, globose, up to 200 µm diam, exuding a pale luteous
to creamy conidial mass; wall of 2–3 layers of pale brown textura
angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells phialidic, hyaline, smooth, aggregated, lining
the inner cavity, ampulliform to doliiform, 5–7 × 5–7 µm; tapering
at apex with prominent periclinal thickening. Conidia hyaline,
smooth, granular, thin-walled, narrowly fusoid-ellipsoidal, apex
subobtusely rounded, base truncate, widest in middle, 1-septate,
becoming constricted with age, (10–)13–16(–19) × (3–)3.5(–4)
µm.
Fig. 62. Conidia and conidiogenous cells of Neostagonospora caricis (CBS 135092).
Scale bars = 10 µm.
Fig. 61. Parastagonospora poae (CBS 135091). A, B. Conidiomata forming in culture. C–E. Conidiogenous cells. F, G. Conidia. Scale bars = 10 µm.
364
Sizing up Septoria
Fig. 63. Neostagonospora caricis (CBS 135092). A. Conidioma forming in culture. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
Culture characteristics: Colonies on PDA lat, undulate, with
sparse, powdery white aerial mycelium, surface greyish-sepia to
isabelline, reverse olivaceous-grey to pale olivaceous-grey, after
14 d, 8.5 cm diam; on MEA erumpent, circular, with ine white
aerial mycelium, surface honey, reverse cinnamon, after 14 d,
6 cm diam; on OA similar to PDA but surface honey, reverse
cinnamon.
Specimen examined: Netherlands, Veenendaal, de Blauwe Hel, on leaves of Carex
acutiformis (Cyperaceae), Aug. 2012, W. Quaedvlieg (holotype CBS H-21306,
culture ex-type CBS 135092 = S616).
Note: Neostagonospora caricis is similar to Septoria caricis
(conidia 1-septate, 20–35 × 2.5–3 µm; Ellis & Ellis 1997), although
its conidia are shorter.
Fig. 64. Conidia and conidiogenous cells of Neostagonospora elegiae (CBS
135101). Scale bars = 10 µm.
Neostagonospora elegiae Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804442. Figs 64, 65.
Etymology: Named after the host genus from which it was collected,
Elegia.
On Anthriscus stem. Conidiomata pycnidial, up to 150 µm diam,
erumpent, globose, brown, opening by a central ostiole, exuding
a crystalline conidial mass; wall consisting of 3–6 layers of pale
brown textura angularis. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells phialidic, lining the inner cavity,
hyaline, smooth, ampulliform, 4–7 × 4–6 µm; apex with prominent
periclinal thickening. Conidia hyaline, smooth, guttulate to granular,
scolecosporous, irregularly curved, subcylindrical, apex subobtuse,
base truncate (slight taper from apical septum to apex and basal
septum to hilum visible in some conidia), (0–)3-septate, (20–)50–
65(–70) × (2.5–)3 µm.
Culture characteristics: Colonies spreading, erumpent with
moderate aerial mycelium and smooth, even margins; reaching 35
mm diam after 2 wk. On OA pale luteous. On MEA dirty white on
surface, luteous in reverse. On PDA dirty white on surface, pale
luteous in reverse.
Specimen examined: South Africa, Western Cape Province, Harold Porter
Botanical Garden, on leaves of Elegia cuspidata (Restionaceae), 30 Nov. 2001, S.
Lee (holotype CBS H-21307, culture ex-type CBS 135101 = CPC 16977).
www.studiesinmycology.org
Notes: No septoria-like fungi are presently known from Elegia (Lee
et al. 2004). Neostagonospora elegiae is distinguished from N.
caricis based on its conidial morphology.
Clade 29: Phaeosphaeriopsis
Phaeosphaeriopsis M.P.S. Câmara, M.E. Palm & A.W.
Ramaley, Mycol. Res. 107: 519. 2003.
Saprobic or plant pathogenic. Ascomata solitary or aggregated,
immersed, subepidermal to erumpent, pushing up laps of the
epidermis, globose to pyriform, often papillate, solitary or gregarious
in a stroma of scleroplectenchyma or dark brown textura angularis,
often surrounded by septate, brown hyphae extending into the host
tissues. Asci 8-spored, bitunicate, cylindrical to broadly fusoid, short
stipitate, with visible apical chamber. Ascospores uni- to triseriate,
cylindrical, broadly rounded at apex, tapering to narrowly rounded
base, 4–5-septate, irst septum submedian, often constricted,
medium brown, echinulate, punctate or verrucose. Asexual
morph coniothyrium-like or phaeostagonospora-like. Conidiomata
pseudoparenchymatous, sometimes of scleroplectenchyma.
Conidiogenous cells lining locule, ampulliform, hyaline, proliferating
percurrently, resulting in inconspicuous annellations. Conidia
cylindrical, with bluntly rounded ends, 0–3-septate, yellowish
brown, punctate (Câmara et al. 2003, Zhang et al. 2012).
365
Quaedvlieg et al.
Fig. 65. Neostagonospora elegiae (CBS 135101). A. Conidioma forming in culture. B–D. Conidiogenous cells. E. Conidia. Scale bars: A = 150 µm, all others = 10 µm.
Type species: Phaeosphaeriopsis glaucopunctata (Grev.) M.P.S.
Câmara, M.E. Palm & A.W. Ramaley, Mycol. Res., 107: 519. 2003.
Phaeosphaeriopsis glaucopunctata (Grev.) M.P.S.
Câmara, M.E. Palm & A.W. Ramaley, Mycol. Res. 107: 519.
2003. Figs 66, 67.
Basionym: Cryptosphaeria glaucopunctata Grev., Fl. Edin.: 362.
1824.
≡ Paraphaeosphaeria glaucopunctata (Grev.) Shoemaker & C. E. Babc.,
Can. J. Bot. 63: 1286. 1985.
= Sphaeria rusci Wallr., Fl. Crypt. Germ. 2: 776. 1833.
≡ Leptosphaeria rusci (Wallr.) Sacc., Syll. Fung. 2: 74. 1883.
≡ Paraphaeosphaeria rusci (Wallr.) O. E. Erikss., Ark. Bot., Ser. 2 6: 406.
1967.
Ascomata scattered or aggregated, immersed, globose to
subglobose, up to 250 µm diam; peridium up to 25 µm wide, of
thick-walled textura angularis; hamathecium of dense, wide, cellular
pseudoparaphyses, 3–5 μm diam. Asci 8-spored, bitunicate,
cylindrical to broadly fusoid, with a short pedicel and small apical
chamber, 50–110 × 10–16 μm. Ascospores uni- to triseriate,
cylindrical, medium brown, 4(−5)-septate, without constriction
or slightly constricted at the basal septum, the forth cell from the
apex usually slightly inlated, the basal cell often longer, 14–28 ×
(3.5–)5–7.5 μm. Conidiomata pycnidial, immersed, scattered or
aggregated, dark brown, subglobose, ostiolate, up to 200 μm diam.
Conidiophores reduced to conidiogenous cells. Conidiogenous cells
lining the inner cavity, ampulliform, hyaline, smooth, 5–10 × 3–6
µm; proliferating percurrently at apex. Conidia aseptate, smooth
to inely verruculose, medium brown, subcylindrical, straight to
reniform with obtuse ends, (5–)7–9(–10) × (2.5–)3(–5) μm.
Culture characteristics: On PDA colonies lat, spreading, with
sparse aerial mycelium and smooth, lobate, even margins, surface
primrose, reverse olivaceous-buff, On OA buff with patches of
isabelline due to sporulating conidiomata. On MEA dirty white on
surface, isabelline in reverse (centre), cinnamon in outer region.
Specimen examined: Switzerland, Kt. Basel-Stadt, Park Basel, on Ruscus aculeatus
(Ruscaceae), 25 Sep. 1980, A. Leuchtmann (CBS H-21308, culture CBS 653.86).
366
Fig. 66. Conidia and conidiogenous cells of Phaeosphaeriopsis glaucopunctata
(CBS 653.86). Scale bar = 10 µm.
Notes: The genus Phaeosphaeriopsis is characterised by having
uni- or multiloculate stromata and 4–5-septate ascospores.
It presently contains species with coniothyrium-like, and
phaeostagonospora-like asexual morphs (e.g. P. musae;
Arzanlou & Crous 2006). The type species, Phaeosphaeriopsis
glaucopunctata, is associated with leaf spot and necrosis on Ruscus
aculeatus (Câmara et al. 2003, Golzar & Wang 2012). The fact that
an isolate identiied as Chaetosphaeronema hispidulum (lectotype
of Chaetosphaeronema) clusters in this clade is puzzling. The
genus Chaetosphaeronema is characterised by setose, dark brown
pycnidia with thick-walled outer cell layers, producing hyaline,
1-septate conidia (Sutton 1980). Isolate CBS 216.75 proved to be
sterile, however, so this matter could unfortunately not be resolved.
Clade 30: Sclerostagonospora
Description: See above.
Type species: S. heraclei (Sacc.) Höhn., Hedwigia 59: 252. 1917.
Sclerostagonospora phragmiticola Quaedvlieg, Verkley &
Crous, sp. nov. MycoBank MB804443. Fig. 68.
Sizing up Septoria
Fig. 67. Phaeosphaeriopsis glaucopunctata (CBS 653.86). A. Colony on MEA. B. Colony on OA. C–F. Conidiogenous cells giving rise to conidia. G. Conidia. Scale bars = 10 µm
Fig. 68. Sclerostagonospora phragmiticola (CBS 338.86). A. Colony sporulating in culture. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
Etymology: Named after the host genus from which it was collected,
Phragmites.
On sterile Carex leaves on WA. Conidiomata pycnidial, brown,
globose, immersed to erumpent, up to 400 µm diam with central
ostiole; wall of 6–8 layers of brown textura angularis. Conidiophores
reduced to conidiogenous cells. Conidiogenous cells lining the
inner cavity of conidioma, hyaline to pale olivaceous, smooth,
subcylindrical to doliiform, 6–15 × 3–4 µm, proliferating several
times percurrently at apex. Conidia brown, smooth, subcylindrical,
apex obtuse, base truncate, straight to gently curved,
(1–)3(–5)-euseptate, older conidia swelling, becoming widest in
second or third cell from base, (15–)20–25(–27) × (3–)3.5(–4) µm.
Specimen examined: France, Landes, Seignosse, Étang d’Hardy, on leaves of
Phragmites australis (Poaceae), 11 June 1986, H.A. van der Aa (holotype CBS
H-21309, culture ex-type CBS 338.86).
Notes: Sclerostagonospora caricicola its the concept of
Sclerostagonospora by having pycnidial conidiomata that give rise
to hyaline conidiogenous cells that proliferate percurrently, and
subcylindrical, pigmented conidia. Until fresh material of the type
species, S. heraclei has been recollected and subjected to DNA
analysis, the application of this generic name will remain tentative.
Several other species cluster in this clade, suggesting that the
sexual morph is phaeosphaeria-like.
Clade 31: Phaeosphaeria
Phaeosphaeria I. Miyake, Bot. Mag., Tokyo 23: 93. 1909.
= Phaeoseptoria Speg., Revta Mus. La Plata 15: 39. 1908.
Foliicolous. Ascomata immersed, subepidermal, ellipsoidal to
globose, glabrous; ostiole central, devoid of periphyses; wall
of 2–3 layers of brown textura angularis. Pseudoparaphyses
transversely septate, guttulate, encased in mucous. Asci stipitate,
clavate to cylindrical, stalked, biseriate. Ascospores brown,
narrowly fusiform, straight or slightly curved, transversely septate,
smooth to verruculose, enclosed in a mucoid sheath or not.
Conidiomata pycnidial, immersed, becoming erumpent, brown,
with central ostiole; wall of 2–3 layers of brown textura angularis.
Conidiophores reduced to conidiogenous cells. Conidiogenous
cells hyaline, ampulliform to subcylindrical or doliiform; proliferating
inconspicuously percurrently near apex. Conidia solitary, pale
brown, smooth, guttulate, subcylindrical to narrowly obclavate,
apex obtuse, base truncate, straight to curved, transversely
euseptate, at times slightly constricted at septa; hilum not darkened
nor thickened.
Type species: P. oryzae I. Miyake, Bot. Mag. Tokyo, 23(266): 93.
1909.
Notes: Phaeosphaeria (1909; based on P. oryzae) is congeneric
with Phaeoseptoria (1908; based on P. papayae). We choose to
www.studiesinmycology.org
367
Quaedvlieg et al.
use the sexual name Phaeosphaeria, as it is well established, and
less confused than Phaeoseptoria, which has become a confused
concept applied to numerous septoria-like taxa with pigmented
conidia (see Walker et al. 1992).
Phaeosphaeria oryzae I. Miyake, Bot. Mag. Tokyo, 23(266):
93. 1909. Figs 69, 70.
≡ Pleospora oryzae (I. Miyake) Hara, J. Agric. Soc. Japan 31(361): 17.
1927.
≡ Trematosphaerella oryzae (I. Miyake) Padwick, A manual of rice
diseases: 153. 1950.
≡ Leptosphaerella oryzae (I. Miyake) Hara, A monograph of rice diseases:
53. 1959.
≡ Leptosphaerulina oryzae (I. Miyake) Karan, Mycopath. Mycol. Appl. 24:
88. 1964.
= Phaeoseptoria oryzae I. Miyake, J. Coll. Agric. Imp. Univ. Tokyo 2(4): 260.
1910.
Ascomata immersed, subepidermal, ellipsoidal to globose,
glabrous, up to 150 µm diam, ostiole central, up to 20 µm diam,
devoid of periphyses; wall of 2–3 layers of brown textura angularis.
Pseudoparaphyses 2–3 µm diam, transversely septate, guttulate,
encased in mucous. Asci stipitate, cylindrical, 30–55 × 7–9 µm,
stalked, biseriate. Ascospores brown, narrowly fusiform, straight or
slightly curved, (15–)17–20(–23) × 4(–5) µm, 3-septate, uniformly
verruculose, enclosed in a mucoid sheath; after discharge,
ascospores become prominently swollen, up to 33 µm long and
8 µm wide.
Specimens examined: Japan, No. 196178, on 2, Prov. Susuya Shizuoka, Sep.
1907, ex Herb. Sydow, ex S., as Leptosphaeria oryzae Hori = Phaeosphaeria oryzae
I. Miyake, slides prepared by O. Eriksson, lectotype (UPS). Korea, on leaf of Oryza
sativa (Poaceae), intercepted at Port San Francisco, CA, 29 Dec. 1997, coll. L.
Hausch, det. M.E. Palm, epitype designated here as BPI 744438, culture ex-epitype
CBS 110110 (MBT175330).
Notes: Several detailed accounts of this species are available
(Eriksson 1967, Shoemaker & Babcock 1989, Fukuhara 2002). The
epitype chosen here closely matches the lectotype in morphology.
Phaeosphaeria papayae (Speg.) Quaedvlieg, Verkley &
Crous, comb. nov. MycoBank MB804444. Figs 71, 72.
Basionym: Phaeoseptoria papayae Speg., Revta Mus. La Plata:
39. 1908.
Fig. 69. Asci and ascospores of Phaeosphaeria oryzae (BPI 744438). Scale bars
= 10 µm.
Leaf spots associated with infections of Asperisporium caricae,
amphigenous, pale brown to grey-white, subcircular to angular,
1–5 mm diam, with red-purple margin; conidiomata developing
Fig. 70. Phaeosphaeria oryzae (BPI 744438). A. Ascomata on host tissue. B–G. Asci. H. Ascospores. Scale bars = 10 µm.
368
Sizing up Septoria
and sporulating on leaves when incubated in moist chambers,
with white, luffy mycelium erumpting from lesions. Conidiomata
amphigenous, pycnidial, brown, globose, up to 120 µm diam,
with central ostiole, exuding a brown conidial cirrhus; wall of
3–4 layers of brown textura angularis. Conidiophores reduced
to conidiogenous cells. Conidiogenous cells lining the inner
cavity, hyaline, smooth, ampulliform to subcylindrical or doliiform,
5–12 × 4–6 µm; proliferating inconspicuously percurrently near
apex (conidiogenous cells disintegrating at maturity). Conidia
solitary, pale brown, smooth, guttulate, subcylindrical to narrowly
obclavate, apex obtuse, base truncate, (1–)3(–4)-septate, at times
slightly constricted at septa, straight to slightly curved, (15–)26–
32(–35) × (2.5–)3 µm; hilum not darkened nor thickened, 2 µm
diam. Ascomata developed after 4 wk in culture on sterile nettle
stems: aggregated in black clusters, globose, up to 150 µm diam,
with central ostiole; wall of 2–3 layers of brown textura angularis.
Asci bitunicate, curved to straight, fasciculate, short stipitate with
ocular chamber, 40–60 × 8–11 µm. Pseudoparaphyses hyaline,
smooth, 2–3 µm, septate, constricted at septa, not anastomosing,
hypha-like with obtuse ends, distributed among asci. Ascospores
tri to multiseriate, fusoid, curved to straight, brown, verruculose
throughout, somewhat constricted at septa with age, second cell
from apex swollen, (18–)24–26(–29) × (3–)4(–5) µm.
Culture characteristics: Colonies with abundant aerial mycelium,
covering dish within 2 wk at 24 ºC, fast growing, olivaceous-grey on
MEA (surface and reverse); margins smooth, even, sterile on MEA,
PDA and OA, as well as on SNA with sterile barley leaves.
Specimens examined: Brazil, São Paulo, Botanical Garden, on leaves of Carica
papaya (Caricaceae), Sep. 1908, IMI 246301, slide ex-holotype; Minas Gerais,
Viçosa, UFV campus, on leaves of Carica papaya, Mar. 2013, A.C. Alfenas, epitype
designated here as CBS H-21310, culture ex-epitype CBS 135416 (MBT175331).
Fig. 71. Conidia, ascospores and ascus of Phaeosphaeria papayae (CBS H-21310).
Scale bars = 10 µm.
Notes: It is interesting to note that Walker et al. (1992) also
observed Phaeoseptoria papayae to co-occur with Asperisporium
Fig. 72. Phaeosphaeria papayae (CBS H-21310). A. Leaf spot. B. Conidioma with ostiole (arrow). C–E. Conidiogenous cells. F. Conidia. G–K. Asci and ascospores. Scale bars
= 10 µm.
www.studiesinmycology.org
369
Quaedvlieg et al.
caricae on the holotype specimen (noted by Spegazzini as
Cercospora caricae), suggesting that the co-occurrence of these
two pathogens is quite common. The fresh collection obtained in
this study enabled us to elucide the conidiogenesis of the fungus
(not observed by Walker et al. 1992), and also designate an epitype
specimen. Phylogenetically it is closely related to Phaeosphaeria
oryzae, which has Phaeoseptoria oryzae as asexual morph.
Clade 32: Neosetophoma
Neosetophoma Gruyter, Aveskamp & Verkley, Mycologia
102(5): 1075. 2010.
Foliicolous, plant pathogenic. Conidiomata pycnidial, solitary
to conluent, on upper surface of agar, globose to irregular, with
mycelial outgrowths, or conluent, with papillate ostioles, sometimes
developing long necks, honey to olivaceous or olivaceous-black,
with up to 10 layers of pseudoparenchymatal cells. Conidiogenous
cells hyaline, monophyalidic. Conidia slightly yellowish,
0–1(–3)-septate, ellipsoidal to cylindrical, usally attenuate at one
end, often guttulate.
Type species: N. samarorum Gruyter, Aveskamp & Verkley,
Mycologia 102(5): 1075. 2010.
Type species: P. radicina (McAlpine) Morgan-Jones & J.F. White,
Mycotaxon 18: 60. 1983.
Paraphoma dioscoreae Quaedvlieg, H.D. Shin, Verkley &
Crous, sp. nov. MycoBank MB804445. Figs 73, 74.
Etymology: Named after the host genus from which it was collected,
Dioscorea.
On Anthriscus stem. Conidiomata pycnidial, separate, immersed
becoming erumpent, globose, with papillate neck and central
ostiole exuding a crystalline conidial mass; conidiomata up to 350
µm diam, neck up to 150 µm diam, of darker brown cells than
body, which is pale brown; wall of 3–6 layers of pale brown textura
angularis. Conidiophores hyaline, smooth, subcylindrical, reduced to
conidiogenous cells, 1–5-septate, irregularly branched, 5–20 × 3–5
µm. Conidiogenous cells phialidic, hyaline, smooth, ampulliform to
subcylindrical (long, elongated neck on Anthriscus stem, but not on
MEA), 5–15 × 2–3 µm; apex with prominent periclinal thickening, or
with several percurrent prolferations (especially on conidiogenous
cells with elongated necks). Conidia solitary, straight to slightly
curved, hyaline, smooth, aseptate, cylindrical with obtuse ends and
a guttule at each end, (5–)6(–7) × 2(–2.5) µm.
Note: The fact that several strains with a phaeosphaeria-like
morphology cluster in this clade, suggests that sexual states do
exist for species of Neosetophoma.
Clade 33: Paraphoma
Paraphoma Morgan-Jones & J.F. White, Mycotaxon 18: 58.
1983.
Mycelium consisting of branched, septate, subhyaline to pale
brown, smooth hyphae. Conidiomata pycnidial, solitary to
aggregated, supericial to immersed, dark brown, globose to
subglobose, papillate, uniloculate, setose; ostiole circular, single;
wall of 3–6 layers of brown textura angularis. Setae copious, straight
to lexuous, smooth to verruculose, thick-walled, septate, pale
brown to brown. Conidiogenous cells lageniform, monophalidic,
formed from inner layer of conidiomatal wall, hyaline to subhyaline,
discrete. Conidia ellipsoid, aseptate, hyaline, smooth, guttulate.
Chlamydospores if present unicellular.
Fig. 73. Conidia and conidiogenous cells of Paraphoma dioscoreae (CBS 135100).
Scale bar = 10 µm.
Fig. 74. Paraphoma dioscoreae (CBS 135100). A. Conidioma forming in culture. B–E. Conidiogenous cells. F. Conidia. Scale bars: B = 350 µm, all others = 10 µm.
370
Sizing up Septoria
Culture characteristics: Colonies lat, spreading with sparse aerial
mycelium and even, smooth margins; after 2 wk reaching 30 mm
diam on MEA, 40 mm on PDA and 50 mm on OA. On PDA dark
brick, reverse fuscous-black. On OA dark brick with patches of
sienna and ochreous. On MEA surface dirty white (due to aerial
mycelium), also somewhat sectored, reverse umber.
Specimen examined: South Korea, on leaves of Dioscorea tokoro (Dioscoreaceae),
24 Oct. 2003, H.D. Shin (holotype CBS H-21311, culture ex-type CPC 11357 = CBS
135100).
Note: Paraphoma dioscoreae is phylogenetically distinct from the
three other species presently known in the genus (de Gruyter et
al. 2010).
Clade 34: Xenoseptoria
Xenoseptoria Quaedvlieg, H.D. Shin, Verkley & Crous, gen.
nov. MycoBank MB804446.
Xenoseptoria neosaccardoi Quaedvlieg, H.D. Shin, Verkley
& Crous, sp. nov. MycoBank MB804447. Figs 75, 76.
Etymology: Resembling Septoria saccardoi, but morphologically
distinct.
Leaf spots on the upper leaf surface, scattered, distinct, circular,
2–4 mm diam, initially appearing as reddish brown discolouration,
later turning brown to reddish brown without a distinct border
line, inally central area becoming greyish brown to dull grey and
surrounded by reddish to dark brown margin, reddish pigments
may diffuse outward to form a halo; on the lower leaf surface
initially showing reddish discolouration, later becoming brown with
distinct border line, center greyish brown to grey with indistinct
border (Shin & Sameva 2004). On sterile Carex leaves on WA.
Conidiomata separate, pycnidial, immersed becoming erumpent,
globose, up to 350 µm diam, brown, becoming ostiolate, developing
1–3 papillate necks, exuding a pink to orange conidial mass; wall
of 4–8 layers of brown textura angularis. Conidiophores hyaline,
Etymology: Similar to the genus Septoria s. str., but distinct.
Foliicolous, plant pathogenic. Conidiomata separate, pycnidial,
immersed becoming erumpent, globose, brown, developing 1–3
papillate necks, exuding a pink to orange conidial mass; wall of
4–8 layers of brown textura angularis. Conidiophores hyaline,
smooth, reduced to conidiogenous cells or septate, branched
below. Conidiogenous cells lining the inner cavity, hyaline, smooth,
ampulliform to doliiform or subcylindrical, mono- to polyphialidic,
with prominent periclinal thickening, but also with percurrent
proliferation. Conidia hyaline, smooth, guttulate, scolecosporous,
straight to irregularly curved, cylindrical to obclavate, transversely
euseptate, tapering to subobtuse apex, base obtuse.
Type species: Xenoseptoria neosaccardoi Quaedvlieg, Verkley &
Crous.
Fig. 75. Conidia and conidiogenous cells of Xenoseptoria neosaccardoi (CBS
128665). Scale bars = 10 µm.
Fig. 76. Xenoseptoria neosaccardoi (CBS 128665). A, B. Pycnidia forming in culture. C–E. Conidiogenous cells. F, G. Conidia. Scale bars: B = 170 µm, all others = 10 µm.
www.studiesinmycology.org
371
Quaedvlieg et al.
smooth, reduced to conidiogenous cells or 1–2-septate, branched
below, 10–20 × 4–6 µm. Conidiogenous cells lining the inner cavity,
hyaline, smooth, ampulliform to doliiform or subcylindrical, monoto polyphialidic, with prominent periclinal thickening, but also with
percurrent proliferation, 5–15 × 3–5 µm. Conidia hyaline, smooth,
guttulate, scolecosporous, straight to irregularly curved, cylindrical
to obclavate, (1–)3-septate, (23–)33–45(–48) × (2.5-)3(–4) µm,
tapering to subobtuse apex, base obtuse, 2–2.5 µm diam.
Culture characteristics: Colonies lat, spreading, with sparse aerial
mycelium and lobate, feathery mergins, reaching 30 mm after 2 wk.
On PDA surface iron-grey, reverse olivaceous-grey; on OA surface
olivaceous-grey; on MEA surface folded, bay, reverse umber.
Specimen examined: South Korea, Pyeongchang, on leaves of Lysimachia vulgaris
var. davurica (Primulaceae), 30 May 2007, H.D. Shin (holotype CBS H-21312,
culture ex-type CBS 128665 = KACC 43962 = SMKC 23666).
Notes: An isolate of Septoria saccardoi (CBS 128756) clusters in
Septoria s. str., thus well apart from this taxon, which was collected
in Korea. The Korean collection closely matches that of the original
description of Septoria saccardoi (on Lysimachia vulgaris in Italy),
having 3-septate, curved, cylindrical conidia, 38–40 × 3.5 µm,
3-septate (Saccardo & Saccardo 1906). Xenoseptoria is however
distinct from Septoria s. str. in forming pycnidia with multiple papillate
necks, and having conidiogenous cells that are mono- or polyphialidic.
wall of 6–8 layers of pale brown textura angularis; exuding cirrhus
of orange conidia. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells lining the inner cavity of conidioma, globose
to ampulliform, rarely allantoid, hyaline, smooth; with prominent
periclinal thickening, or proliferating several times percurrently near
apex, giving rise to macro- and microconidia. Macroconidia solitary,
hyaline, smooth, guttulate, subcylindrical to narrowly obclavate
or acicular, apex obtuse to subobtuse, base truncate to long
obconically truncate, conidia widest at or just above basal septum,
transversely euseptate. Microconidia hyaline, smooth, aseptate,
pear-shaped to globose or ellipsoid, apex obtuse, base truncate.
Type species: Vrystaatia aloeicola Quaedvlieg, Verkley, W.J. Swart
& Crous.
Vrystaatia aloeicola Quaedvlieg, Verkley, W.J. Swart &
Crous, sp. nov. MycoBank MB804449. Figs 77, 78.
Etymology: Named after the host genus from which it was collected,
Aloe.
Clade 35: Vrystaatia
Vrystaatia Quaedvlieg, W.J. Swart, Verkley & Crous, gen.
nov. MycoBank MB804448.
Etymology: Named after the Free State Province in South Africa,
“Vrystaat” in Afrikaans, where this fungus was collected.
Foliicolous. Conidiomata black, globose, pycnidial with central,
dark brown ostiolar area, substomatal on host, erumpent in culture;
Fig. 77. Macro- and microconidia and conidiogenous cells of Vrystaatia aloeicola
(CBS 135107). Scale bars = 10 µm.
Fig. 78. Vrystaatia aloeicola (CBS 135107). A. Conidiomata sporulating on PDA, with characteristic orange conidial cirrhi. B–D. Conidiogenous cells. E, F. Conidia. Scale bars
= 10 µm.
372
Sizing up Septoria
On sterile Carex leaves on WA. Conidiomata black, globose, pycnidial
with central, dark brown ostiolar area, substomatal on host, erumpent
in culture; wall of 6–8 layers of pale brown textura angularis; exuding
cirrhus of orange conidia. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells lining the inner cavity of conidioma,
globose to ampulliform, rarely allantoid, hyaline, smooth, 5–12 ×
4–6 µm; with prominent periclinal thickening, or proliferating several
times percurrently near apex, 2–2.5 µm diam, giving rise to macroand microconidia. Macroconidia solitary, hyaline, smooth, guttulate,
subcylindrical to narrowly obclavate or acicular, apex obtuse to
subobtuse, base truncate to long obconically truncate, conidia widest
at or just above basal septum, (1–)3-septate, (30–)40–52(–65) × (2.5–)
3(–3.5) µm. Microconidia hyaline, smooth, aseptate, pear-shaped to
globose or ellipsoid, apex obtuse, base truncate, 4–6 × 3–3.5 µm.
Culture characteristics: On MEA colonies spreading fast, with
moderate aerial mycelium and smooth, even margin, reaching 30
mm diam after 2 wk; surface with concentric zones of umber and
apricot; reverse umber, produces brown exudates; on PDA round
lobate margins, lacking aerial mycelium, reaching 20 mm diam after
2 wk, surface fuscous-black to greyish-sepia for younger mycelium,
reverse fuscous-black to greyish-sepia for younger mycelium; on
OA round, lobate, lacking aerial mycelium, reaching 30 mm diam
after 2 wk, surface vinaceous-grey, reverse greyish sepia.
Clade 36: Setophoma
Setophoma Gruyter, Aveskamp & Verkley, Mycologia 102:
1077. 2010.
Conidiomata pycnidial, solitary to conluent, supericial or
submerged in agar, globose to subglobose, setose, with papillate
ostioles, honey to olivaceous to olivaceous-black, with 2–7(–11)
layers of pseudoparenchymatal cells. Conidiogenous cells hyaline,
monophyalidic. Conidia aseptate, ellipsoidal to subcylindrical to
subfusoid, guttulate.
Type species: S. terrestris (H.N. Hansen) Gruyter, Aveskamp &
Verkley, Mycologia 102: 1077. 2010.
Setophoma chromolaenae Quaedvlieg, Verkley, R.W.
Barreto & Crous, sp. nov. MycoBank MB804450. Figs 79,
80.
Specimen examined: South Africa, Orange Free State, Bloemfontein, Free State
National Botanical Garden, on dead leaf tips of Aloe maculata (Aloaceae), 7 May
2012, P.W. Crous & W.J. Swart (holotype CBS H-21313, culture ex-type CBS
135107 = CPC 20617).
Notes: Vrystaatia is distinct from Septoria s. str. in that it has phialidic
conidiogenous cells that proliferate percurrently or with prominent
periclinal thickening, and form macro- as well as microconidia in
culture, which is not typical of Septoria. Rhabdospora aloetica was
described from stems of Aloe sp. in Portugal, with aseptate conidia,
12–16 × 1.5 µm (Saccardo & Saccardo 1906); it is likely this is
an asexual morph of Diaporthe. As far as we could establish, no
septoria-like fungi have thus far been described from Aloe.
Fig. 79. Conidia and conidiogenous cells of Setophoma chromolaenae (CBS
135105). Scale bar = 10 µm.
Fig. 80. Setophoma chromolaenae (CBS 135105). A. Conidiomata forming on OA. B, C, F. Conidiomata with setae. D, E. Conidiogenous cells. G. Conidia. Scale bars: B = 22
µm, C, F = 45 µm, all others = 10 µm.
www.studiesinmycology.org
373
Quaedvlieg et al.
Etymology: Named after the host genus from which it was collected,
Chromolaena.
Conidiomata pycnidial, brown, globose, separate, erumpent, up to
90 µm diam; outer surface covered in brown setae, up to 80 µm
long, brown, thick-walled, 3–5 µm diam, 1–4-septate, with slight
apical taper to obtuse apex; conidial wall of 3–6 layers of brown
textura angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells lining the inner cavity, ampulliform, hyaline,
smooth, 4–6 × 3–6 µm, with prominent periclinal thickening at
apex. Conidia hyaline, smooth, subcylindrical, somewhat narrowly
ellipsoid when old, with two prominent guttules at ends, (4.5–)5–6
(–7) × (2–)2.5(–3) µm.
Culture characteristics: On MEA spreading, with sparse aerial
mycelium, folded surface, margin smooth, lobate; surface umber
with patches of apricot and dirty white, reverse ochreous. On PDA
surface iron-grey, reverse olivaceous-grey. On OA surface irongrey, surrounded by orange to apricot diffuse pigment layer in agar;
reaching 55 mm diam after 2 wk.
Specimen examined: Brazil, Rio de Janeiro, Fazenda Santa Rosa, Ponte das
Laranjeiras, on leaves of Chromolaena odorata (Asteraceae), 6 Apr. 2010, R.W.
Barreto (holotype CBS H-21314, culture ex-type CBS 135105 = CPC 18553).
Note: Setophoma chromolaenae is phylogenetically distinct from S.
sacchari and S. terrestris, the two other species presently known
from the genus (de Gruyter et al. 2010).
Clade 37: Coniothyrium (Coniothyriaceae)
Coniothyrium Corda, Icon. Fung. (Prague) 4: 38. 1840.
Mycelium immersed, consisting of septate, hyaline to brown,
branched hyphae. Conidiomata pycnidial, separate, globose, pale
to dark brown, immersed, unilocular, thin-walled; wall of brown,
thick-walled textura angularis. Ostiole circular, central, papillate or
not. Conidiophores reduced to conidiogenous cells. Conidiogenous
cells lining the inner cavity, phialidic, annellidic, indeterminate,
discrete, doliiform to cylindrical, hyaline to pale brown, smooth,
several annellations at apex. Conidia subcylindrical, spherical,
ellipsoid or broadly clavate, brown, thick-walled, 0(–1)-euseptate,
smooth to verruculose, apex obtuse, base truncate, at times with
minute marginal frill (Sutton 1980).
Type species: C. palmarum Corda, Icon. Fung. (Prague) 4: 38.
1840.
Coniothyrium sidae Quaedvlieg, Verkley, R.W. Barreto &
Crous, sp. nov. MycoBank MB804451. Figs 81, 82.
Etymology: Named after the host genus from which it was collected,
Sida.
Conidiomata pycnidial, globose, immersed becoming erumpent, up
to 200 µm diam; wall consisting of 3–4 layers of subhyaline to pale
brown textura angularis. Ostiole central, papillate, dark brown, up
to 30 µm diam, surrounded by a whorl of brown setae, smooth,
thick-walled, 4–8-septate, straight to curved, tapering to subobtuse
apices, up to 130 µm long, 5–8 µm diam at base. Conidiogenous
cells hyaline, smooth, lining the inner cavity, ampulliform to
374
Fig. 81. Conidia and conidiogenous cells of Coniothyrium sidae (CBS 135108).
Scale bar = 10 µm.
globose, 4–7 × 4–6 µm; apex with prominent periclinal thickening.
Conidia solitary, hyaline, smooth, aseptate, granular (in Shear’s
medium, prominently guttulate in lactic acid), fusoid-ellipsoidal,
straight to slightly curved, apex obtuse, base truncate to bluntly
rounded, (9–)10–12(–13) × (2.5–)3 µm. Ascomata developing
after several weeks on MEA, separate, pseudothecial, erumpent,
uniloculate, papillate, brown, up to 300 µm diam; wall of 4–8
layers of brown textura angularis. Asci fasciculate, 8-spored,
short papillate, hyaline, smooth, subcylindrical, bitunicate, with
well-developed apical chamber, 2 µm diam, 55–65 × 8–11 µm.
Ascospores bi- to triseriate, brown, smooth, guttulate, straight to
slightly curved, (3–)5-septate, apical cell obtusely rounded, basal
cell somewhat elongated and subobtuse; in ascospores that are
4-septate, the second cell from the apex is markedly swollen,
in 5-septate ascospores the third cell from the apex is markedly
swollen, (18–)20–24(–26) × (4–)5(–5.5) µm. Pseudoparaphyses
hyaline, smooth, intermingled among asci, anastomosing, cellular,
constricted at septa, up to 80 µm long, 2–4 µm diam.
Culture characteristics: Colonies erumpent, spreading, moderate
aerial mycelium even, lobate margins. On MEA surface olivaceousgrey, reverse umber. On OA suface olivaceous-grey with diffuse
umber pigment in agar. On PDA surface and reverse olivaceousgrey.
Specimen examined: Brazil, Rio de Janeiro, Nova Friburgo, Riograndina, along
roadside on Sida sp. (Malvaceae), 24 Feb. 2008, R.W. Barreto (holotype CBS
H-21315, culture ex-type CPC 19602 = RWB 866 = CBS 135108).
Note: De Gruyter et al. (2013) placed several phoma-like species
with a similar morphology in the genus Coniothyrium, to which
C. sidae is allied. Of interest is the paraphaeosphaeria-like
sexual morph that developed in culture, which is newly linked
here to Coniothyrium. The genus Paraphaeosphaeria is linked to
Paraconiothyrium (Verkley et al. 2004).
Clade 38: Xenobotryosphaeria
Xenobotryosphaeria Quaedvlieg, Verkley & Crous, gen.
nov. MycoBank MB804452.
Etymology: Resembling the genus Botryosphaeria, but distinct.
Sizing up Septoria
Fig. 82. Coniothyrium sidae (CBS 135108). A–E. Conidiomata forming in culture, showing setae. F, G. Conidiogenous cells. H. Conidia. I–K. Asci and ascospores. Scale bars:
B, D, E = 100 µm, all others = 10 µm.
Ascomata brown, globose, smooth, ostiolate, supericial on stems;
wall of 3–4 layers of brown textura angularis. Asci clavate, hyaline,
smooth, short stipitate, fasciculate, bitunicate, thin-walled, apical
chamber not visible, 6–8-spored. Ascospores multiseriate, hyaline,
smooth and thin-walled, granular, broadly ellipsoid, ends obtuse,
aseptate. Pseudoparaphyses not seen.
Type species: Xenobotryosphaeria calamagrostidis Quaedvlieg,
Verkley & Crous.
Xenobotryosphaeria calamagrostidis Quaedvlieg, Verkley
& Crous, sp. nov. MycoBank MB804453. Figs 83, 84.
Etymology: Named after the host genus from which it was collected,
Calamagrostis.
On Anthriscus stem. Ascomata brown, globose, smooth, supericial on
stems, ostiolate, up to 180 µm diam; wall of 3–4 layers of brown textura
angularis. Asci clavate, hyaline, smooth, short stipitate, fasciculate,
bitunicate, thin-walled, apical chamber not visible, 6–8-spored, 60–80 ×
30–40 µm. Ascospores multiseriate, hyaline, smooth and thin-walled,
granular, broadly ellipsoid, ends obtuse, aseptate, (17–)18–20(–24) ×
(11–)12–13(–14) µm. Pseudoparaphyses not seen.
Culture characteristics: Colonies lat, spreading, with sparse to no
aerial mycelium. On PDA surface and reverse dirty white; on MEA
concolorous with agar; on OA pale pink on surface.
Specimen examined: Italy, Bergamo Vigolo, on Calamagrostis sp. (Poaceae), 20
Jun. 1967, G.A. Hedjaroude (holotype CBS H-21316, culture ex-type CBS 303.71).
Notes: Hedjaroude (1968) studied the specimen (ETH 7131; as
Phaeosphaeria silvatica), but obviously the incorrect fungus was
cultivated, as X. calamagrostidis is quite distinct from P. silvatica,
which has cylindrical-fusoid, brown, 6–8-septate ascospores,
18–18 × 4–5 µm. Xenobotryosphaeria is reminiscent of genera in
the Botryosphaeriales, but is phylogenetically distinct (Crous et al.
2006, Phillips et al. 2008, Liu et al. 2012). It also resembles species
of Muyocopron (Muyocopronaceae), but the latter genus differs
in that it has circular, lattened ascomata, as well as prominent
pseudoparaphyses, which are absent in Xenobotryosphaeria.
Clade 39: Phoma
Fig. 83. Ascospores and asci of Xenobotryosphaeria calamagrostidis (CBS 303.71).
Scale bars = 10 µm.
www.studiesinmycology.org
Note: See Aveskamp et al. (2010), de Gruyter et al. (2009, 2013).
375
Quaedvlieg et al.
Fig. 84. Xenobotryosphaeria calamagrostidis (CBS 303.71). A, C. Ascomata forming in culture. E, G. broken wall with asci. B, D, F. Asci. H. Ascospores. Scale bars: C = 45
µm, all others = 10 µm.
Clade 40: Acicuseptoria
Acicuseptoria Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804454.
to conidiogenous cells. Conidiogenous cells hyaline, smooth,
ampulliform; proliferating inconspicuously and percurrently at apex,
or simply appearing holoblastic. Conidia solitary, hyaline, granular,
acicular, straight to gently curved, tapering towards apex that is
acutely rounded, base truncate, transversely euseptate.
Etymology: Acicu- from acicular (conidia), and Septoria = septorialike.
Type species: Acicuseptoria rumicis Quaedvlieg, Verkley & Crous.
Conidiomata pycnidial, erumpent, brown, globose, with central
ostiole, exuding a cream conidial mass; wall consisting of 3–6
layers of thin, brown textura angularis. Conidiophores reduced
Acicuseptoria rumicis Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804455. Fig. 85.
Fig. 85. Acicuseptoria rumicis (CBS 522.78). A. Conidiomata sporulating in culture. B–E. Conidiogenous cells. F, G. Conidia. Scale bars = 10 µm.
376
Sizing up Septoria
Etymology: Named after the host genus from which it was collected,
Rumex.
On sterile Carex leaves on WA. Conidiomata pycnidial, erumpent,
brown, globose, up to 300 µm diam, with central ostiole, exuding
a cream conidial mass; wall consisting of 3–6 layers of thin, brown
textura angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells hyaline, smooth, ampulliform, 7–15 × 5–7 µm;
proliferating inconspicuously and percurrently at apex, or simply
appearing holoblastic. Conidia solitary, hyaline, granular, acicular,
straight to gently curved, tapering towards apex that is acutely
rounded, base truncate, 1.5–2 µm diam, up to 8-septate, (32–)40–
60(–70) × 2(–2.5) µm.
Culture characteristics: Colonies lobate, lat with little appressed,
white aerial mycelium. On MEA surface olivaceous-grey, reverse
umber. On OA suface olivaceous-grey. On PDA surface and
reverse olivaceous-grey.
Specimen examined: France, Haute Savoie, Mt. Beaudin, 2000 m alt., stem
of Rumex alpinus (Polygonaceae), Oct. 1978, H.A. van der Aa (holotype CBS
H-18163, culture ex-type CBS 522.78).
Notes: Acicuseptoria rumicis was originally deposited as Septoria
rumicum, but is distinct from the latter in having acicular, narrower
conidia. Acicuseptoria is distinct from Septoria s. str. in having
acicular conidia.
Clade 41: Stagonospora
Stagonospora (Sacc.) Sacc., Syll. Fung. (Abellini) 3: 445.
1884.
Fig. 86. Conidia and conidiogenous cells of Stagonospora duoseptata (CBS
135093). Scale bars = 10 µm.
On sterile Carex leaves on WA. Conidiomata dark brown,
immersed, subepidermal, pycnidial, globose, up to 400 µm
diam, exuding a short, hyaline cirrhus of conidia; wall of 3–4
layers of medium brown textura angularis. Conidiophores
hyaline, smooth, lining inner cavity, 0–1-septate, subcylindrical,
10–20 × 4–5 µm. Conidiogenous cells phialidic, hyaline,
smooth, aggregated, lining the inner cavity, subcylindrical to
ampulliform or doliiform, 6–8 × 3–4 µm; phialidic with several
apical percurrent proliferations. Conidia hyaline, smooth, thinwalled, granular, fusoid-ellipsoidal, 2-septate, with septa 4–6
µm inwards from both obtuse conidial ends; conidia widest in
middle, (18–)20–23(–25) × (5–)6(–7) µm.
Culture characteristics: Colonies on PDA lattened, circular with
lobate edges, and ine grey aerial mycelium, surface mouse-grey,
reverse olivaceous-black, after 14 d, 4 cm diam; on MEA after 14 d,
4.5 cm diam; on OA similar to MEA.
Description: See above.
Type species: S. paludosa (Sacc. & Speg.) Sacc., Syll. Fung.
(Abellini) 3: 453. 1884.
Stagonospora duoseptata Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804459. Figs 86, 87.
Etymology: Named after the fact that conidia are 2-septate.
Specimen examined: Netherlands, Nijmegen, de Duffelt, on leaves of a Carex
acutiformis (Cyperaceae), 29 Jul. 2012, W. Quaedvlieg (holotype CBS H-21321,
culture ex-type CBS 135093 = S618).
Notes: Stagonospora duoseptata is distinct from other species
occurring on Carex in that it has fusoid-ellipsoidal, 2-septate
conidia, (18–)20–23(–25) × (5–)6(–7) µm, with septa positioned
4–6 µm inwards from its obtuse conidial ends. Stagonospora
biseptata (occurring on Carex lanuginosa, Wisconsin, USA) has
conidia that are larger, (35–)40–50(–55) × (2–)10–11(–13) µm
(Greene 1961).
Fig. 87. Stagonospora duoseptata (CBS 135093). A. Conidiomata forming in culture. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
www.studiesinmycology.org
377
Quaedvlieg et al.
Stagonospora paludosa (Sacc. & Speg.) Sacc., Syll. Fung.
(Abellini) 3: 453. 1884. Figs 88, 89.
Basionym: Hendersonia paludosa Sacc. & Speg., Michelia 1(no.
3): 353. 1878.
On sterile Carex leaves on WA. Conidiomata black, immersed,
subepidermal, pycnidial, globose, up to 400 µm diam, exuding a
short, hyaline cirrhus of conidia; wall of 3–4 layers of medium brown
textura angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells phialidic, hyaline, smooth, aggregated, lining
the inner cavity, ampulliform to doliiform, 5–10 × 5–10 µm; tapering
at apex with prominent periclinal thickening or 1–2 inconspicuous
percurrent proliferations visible at apex. Conidia hyaline, smooth,
thin-walled, granular, or each cell with a large central guttule,
subcylindrical to fusoid, apex subobtusely to obtusely rounded, base
truncate (4–7 µm diam), (6–)7–8-septate (becoming constricted at
septa with age), (45–)55–63(–65) × (9–)10–11 µm.
Culture characteristics: Colonies on PDA lat, circular, with grey
aerial mycelium, reverse olivaceous-black to buff at the margins,
after 14 d, 8.5 cm diam; on MEA umbonate, round, with appressed,
grey aerial mycelium, with white patches; OA similar to PDA, but
reverse buff with iron-grey patches at the outer region.
Specimens examined: Italy, on Carex riparia (Cyperaceae), Feb. 1878, holotype
(presumably lost). Netherlands, Utrecht, Veenendal, de Blauwe Hel, Carex
acutiformis (Cyperaceae), 23 Jul. 2012, W. Quaedvlieg (neotype designated here
CBS H-21317, culture ex-type S601 = CBS 135088) (MBT175339).
Fig. 88. Conidia and conidiogenous cells of Stagonospora paludosa (CBS 135088).
Scale bars = 10 µm.
Notes: For more than a century, Stagonospora was confused
with Septoria. The introduction of molecular techniques around
the turn of the century made it possible to deinitively establish
that Stagonospora was not linked to Septoria, and that it in fact
clusters with other important plant pathogenic genera like Phoma
and Leptosphaeria in the Pleosporales (Cunfer & Ueng 1999,
Solomon et al. 2006). The type of Stagonospora (S. paludosa)
was recollected from a Carex during this study and phylogenetic
analyses showed that this species clustered separately from most
other known “Stagonospora” spp. (mostly isolated from Poaceae),
but together with several other Stagonospora species that were also
collected from Carex. This led to the conclusion that Stagonospora
s. str. was limited to Carex, and that other commercially important
stagonospora-like species on Poaceae (e.g. S. avenae and S.
nodorum) in fact belonged to different genera.
Stagonospora perfecta Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804458. Figs 90, 91.
Etymology: Named after the fact that both sexual and asexual
morphs of the fungus developed in culture.
On sterile Carex leaves on SNA. Ascomata developing on SNA,
solitary, globose, brown, erumpent, up to 300 µm diam, with
central ostiole; wall of 3–4 layers of brown textura angularis.
Pseudoparaphyses intermingled among asci, hyaline, smooth,
guttulate, multi-septate, constricted at septa, branched, hyphallike, 4–6 µm diam, filling entire cavity. Asci stipitate, hyaline,
smooth, clavate to fusoid-ellipsoidal, bitunicate, with prominent
apiculus, 1.5–2.5 µm diam, 8-spored, 45–100 × 12–18 µm.
Ascospores hyaline, smooth, 3- to multi-seriate in ascus,
Fig. 90. Conidia, conidiogenous cells and ascus with ascospores of Stagonospora
perfecta (CBS 135099). Scale bars = 10 µm.
Fig. 89. Stagonospora paludosa (CBS 135088). A, B. Conidiomata forming in culture. C, D. Conidiogenous cells. E, F. Conidia. Scale bars: B = 400 µm, all others = 10 µm.
378
Sizing up Septoria
Fig. 91. Stagonospora perfecta (CBS 135099). A. Conidiomata forming in culture. B. Ascomata forming in culture. C–F, I, J. Asci and pseudoparaphyses. G, H. Conidiogenous
cells. K. Conidia. Scale bars: B = 300 µm, all others = 10 µm.
fusoid-ellipsoidal with median septum, prominently constricted
at septum, tapering towards subobtuse apices, with 1–2 large
guttules per cell, thin-walled, widest just above septum in
upper cell, (20–)23–25(–27) × (5–)6–7(–8) µm. Conidiomata
up to 300 µm diam, brown, immersed, subepidermal, pycnidial,
subglobose with central ostiole, exuding crystalline to creamy
conidial mass; wall of 2–3 layers of brown textura angularis.
Conidiophores reduced to conidiogenous cells. Conidiogenous
cells phialidic, hyaline, smooth, aggregated, lining the inner
cavity, ampulliform to doliiform or subcylindrical, with several
percurrent proliferations near apex, 5–12 × 4–6 µm. Conidia
hyaline, smooth, thin-walled, subcylindrical to narrowly fusoidellipsoidal, with obtuse apex and bluntly rounded base,
2–3-septate, slightly constricted at septa, with 1–2 large guttules
per cell, (19–)25–29(–32) × (6–)7(–8) µm.
Culture characteristics: Colonies on PDA lattened, convex, circular,
with white aerial mycelium, surface fuscous-black, reverse irongrey to black, after 14 d, 8.5 cm diam; on MEA surface fuscousblack, reverse olivaceous-black; on OA surface isabelline, reverse
fuscous-black.
Specimen examined: Netherlands, Limburg, Weert, Moerselpeel, on leaves
of Carex acutiformis (Cyperaceae), Sep. 2012, W. Quaedvlieg (holotype CBS
H-21320, culture ex-type CBS 135099 = S656).
Notes: Stagonospora perfecta is the irst species with a conirmed
sexual state in the genus Stagonospora. Of interest is the fact that it is
didymella-like, rather than phaeosphaeria-like in morphology, which
also explains it clustering in the Didymellaceae. Morphologically S.
perfecta resembles S. vitensis (18–32 × 4–6 µm, 2–3(–4)-septate;
Ellis & Ellis 1997), but conidia are wider. Stagonospora perfecta is
closely related to S. pseudovitensis, though in the latter conidia are
www.studiesinmycology.org
slightly longer, more fusoid-ellipsoidal in shape, and lack a sexual
morph in culture.
Stagonospora pseudocaricis Quaedvlieg, Verkley,
Gardiennet & Crous, sp. nov. MycoBank MB804456. Figs
92, 93.
Etymology: Named after the species that it resembles,
Stagonospora caricis.
On sterile Carex leaves on WA. Conidiomata black, immersed,
subepidermal, pycnidial, globose, up to 400 µm diam, exuding a
short, hyaline cirrhus of conidia; wall of 3–4 layers of medium brown
textura angularis. Conidiophores reduced to conidiogenous cells.
Conidiogenous cells phialidic, hyaline, smooth, aggregated, lining
the inner cavity, ampulliform to doliiform, 5–9 × 5–8 µm; tapering
at apex with prominent periclinal thickening or 1–2 inconspicuous
percurrent proliferations visible at apex. Conidia hyaline, smooth,
thin-walled, granular, or each cell with a large central guttule,
subcylindrical to fusoid, apex subobtusely to obtusely rounded,
base truncate, (5–)6(–7)-septate, (35–)42–48(–50) × (6–)7–8 µm.
Culture characteristics: Colonies on PDA lat, circular, with appressed,
grey aerial mycelium, surface sepia, reverse olivaceous-black to buff,
after 14 d, 8.5 cm diam; on MEA umbonate, round, with appressed,
grey aerial mycelium with white patches, surface greyish sepia,
reverse fuscous-black to olivaceous-black; OA similar to PDA.
Specimens examined: France, Foncegrive, Rive de la Venelle, on Carex acutiformis
(Cyperaceae), Oct. 2012, A. Gardiennet (holotype CBS H-21318, culture ex-type
CBS 135132 = S610); ibed., S609 = CBS 135414).
379
Quaedvlieg et al.
Note: Conidia of S. pseudocaricis closely resemble those of S.
caricis (25–45 × 4–8 µm, 5–7-septate; Ellis & Ellis 1997), but are
longer.
Stagonospora pseudovitensis Quaedvlieg, Verkley &
Crous, sp. nov. MycoBank MB804457. Figs 94, 95.
Etymology: Named after the species that it resembles,
Stagonospora vitensis.
On sterile Carex leaves on WA. Conidiomata black, immersed,
subepidermal, pycnidial, globose with central ostiole, up to 180 µm
diam; wall of 3–4 layers of pale brown textura angularis. Conidiophores
reduced to conidiogenous cells. Conidiogenous cells phialidic,
hyaline, smooth, aggregated, lining the inner cavity, ampulliform
to doliiform, 5–7 × 4–5 µm; tapering at apex with inconspicuous
periclinal thickening or percurrent proliferation. Conidia hyaline,
smooth, thin-walled, granular, subcylindrical with obtuse apex and
truncate to bluntly rounded base, 3–4 µm diam, 3-septate, with large
central guttule in each cell, (25–)28–33(–36) × (6–)7(–8) µm.
Fig. 92. Conidia of Stagonospora pseudocaricis (CBS 135132). Scale bar = 10 µm.
Culture characteristics: Colonies on PDA lat, circular, aerial
mycelium consisting of some grey tufts, surface pale mouse-grey,
reverse olivaceous-black, after 14 d, 8.5 cm diam; on MEA similar
to PDA, but with appressed, white aerial mycelium, and with some
grey tufts; OA similar to MEA, but reverse olivaceous-grey.
Specimens examined: Netherlands, Veenendaal, de Blauwe Hel, on leaves of
Carex acutiformis (Cyperaceae), 23 Jul. 2012, W. Quaedvlieg (holotype CBS
H-21319, culture ex-type CBS 135094 = S620); ibed., S602.
Note: Conidia of S. pseudovitensis differ from that of S. vitensis
(18–32 × 4–6 µm, 2–3(–4)-septate; Ellis & Ellis 1997), by having
consistently 3-septate, wider conidia.
Stagonospora uniseptata Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804460. Figs 96, 97.
Etymology: Named after the fact that conidia are 1-septate.
On sterile Carex leaves on WA. Conidiomata up to 150 µm diam,
black, immersed, subepidermal, pycnidial, globose with central
ostiole, exuding yellow conidial masses; wall of 3–4 layers of redbrown textura angularis. Conidiophores reduced to conidiogenous
cells. Conidiogenous cells phialidic, hyaline, smooth, aggregated,
lining the inner cavity, ampulliform to subcylindrical, 5–8 × 3–4 µm,
with percurrent proliferation at apex. Conidia hyaline, smooth, thinwalled, fusoid-ellipsoidal, with obtuse apex and truncate to bluntly
rounded base (2 µm diam), medianly 1-septate, prominently
constricted at septum, straight to irregularly curved, widest in
middle of either apical or basal cell, granular, including yellowgreen relective guttules, (13–)16–20(–22) × (5–)5.5(–6) µm.
Fig. 94. Conidia and conidiogenous cells of Stagonospora pseudovitensis (CBS
135094). Scale bars = 10 µm.
Fig. 93. Stagonospora pseudocaricis (CBS 135132). A. Conidiomata forming in culture. B, C. Conidia. Scale bars = 10 µm.
380
Sizing up Septoria
Fig. 95. Stagonospora pseudovitensis (CBS 135094). A. Conidiomata forming in culture. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
Fig. 96. Conidia and conidiogenous cells of Stagonospora uniseptata (CBS 135090). Scale bars = 10 µm.
Fig. 97. Stagonospora uniseptata (CBS 135090). A. Conidiomata sporulating in culture. B. Conidiogenous cells. C. Conidia. Scale bars = 10 µm.
Culture characteristics: Colonies on PDA appressed, circular,
with short, greyish-white aerial mycelium, surface fusous-black,
reverse olivaceous-black to hazel, after 14 d, 8.5 cm diam; on
MEA surface hazel, reverse cinnamon; on OA with patches of
white aerial mycelium, surface isabelline, reverse olivaceous to
fuscous-black.
Specimens examined: Netherlands, Nijmegen, de Duffelt, on leaves of a Carex
acutiformis (Cyperaceae), 29 Jul. 2012, W. Quaedvlieg, (holotype CBS H-21322,
culture ex-type CBS 135090 = S611); ibed., S607, S608 = CPC 22151 and CPC 22150.
Notes: Of the Stagonospora and Septoria species occurring on
Carex, Stagonospora uniseptata is most similar to Septoria caricis
(conidia 20–35 × 2.5–3 µm, 1-septate; Ellis & Ellis 1997), but
distinct in that conidia are shorter and wider.
www.studiesinmycology.org
Clade 42: Corynespora
Corynespora Güssow, Z. PlKrankh. PlPath. PlSchutz 16:
10. 1906.
Mycelium immersed or supericial. Stroma present in some species.
Setae and hyphopodia absent. Conidiophores macronematous,
mononematous, straight or lexuous, unbranched, brown or
olivaceous brown, smooth. Conidiogenous cells monotretic,
integrated, terminal, percurrent, cylindrical or doliiform. Conidia
solitary or catenate, dry, acrogenous, simple, obclavate, rarely
cylindrical, subhyaline, pale to dark brown or olivaceous brown
or straw-coloured, euseptate or distoseptate, smooth, rarely
verruculose (Ellis 1971).
381
Quaedvlieg et al.
Type species: C. mazei Güssow, Consp. Regni Veget. (Leipzig) 16:
13. 1906. [= C. cassiicola (Berk. & M.A. Curtis) C.T. Wei, Mycol.
Pap. 34: 5. 1950.]
Corynespora leucadendri Quaedvlieg, Verkley & Crous,
sp. nov. MycoBank MB804461. Figs 98, 99.
Etymology: Named after the host genus from which it was collected,
Leucadendron.
On MEA and PDA after 2 wk. Mycelium consisting of creeping,
branched, septate, hyaline, smooth, 3–4(–5) µm diam hyphae
that become brown close to conidiophores; stroma lacking.
Conidiophores subcylindrical, erect, medium brown, 100–300 µm
tall, 4–6(–7) µm diam, thick-walled, transversely multiseptate,
with several swollen nodes of conidiophore rejuvenation (up to
12 µm diam). Conidiogenous cells terminal, cylindrical, medium
brown, smooth, ends swollen or not, central locus somewhat
darkened or inconspicuous, 15–40 × 5–6(–7) µm. Conidia
medium brown, obclavate to subcylindrical, straight to slightly
curved, thick-walled, (3–)4–6(–10)-distoseptate, basal locus
thickened, darkened, protruding, 2–3 µm diam, (35–)70–110(–
170) × (6–)7–8(–11) µm.
Culture characteristics: Colonies erumpent, spreading with moderate
aerial mycelium and smooth, even margin; reaching 25 mm diam
after 2 wk. On MEA surface dirty white, reverse cinnamon. On PDA
surface dirty white, reverse buff to rosy buff with diffuse rosy buff
pigment. On OA surface dirty white with diffuse rosy buff pigment
in agar.
Specimen examined: South Africa, Western Cape Province, Helderberg Nature
Reserve, from the leaves of Leucadendron sp. (Proteaceae), 14 Aug. 2000, S. Lee
(holotype CBS H-21323, culture ex-type CBS 135133 = CPC 19345).
Notes: This species was not treated by Marincowitz et al. (2008),
and presently no species of Corynespora are known from
Leucadendron. Furthermore, based on conidial morphology, none
of the species treated by Ellis (1971, 1976) resemble C. leucadendri,
nor is it similar to any Corynespora sequence presently deposited
in GenBank. For these reasons we thus introduce C. leucadendri
as a new taxon.
Clade 43: Setoseptoria
Setoseptoria Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804462.
Etymology: Named after its conidiomata which are septoria-like,
but setose.
Conidiomata pycnidial, brown, immersed, globose with central
ostiole, somewhat papillate, apical erumpent part at times with
brown, verruculose to warty setae; wall of 6–8 layers of brown
textura angularis; inner layer of 6–10 layers of hyaline textura
angularis. Conidiophores lining the inner cavity, reduced to
conidiogenous cells, or with one supporting cell. Conidiogenous
cells hyaline, smooth, subcylindrical to doliiform; apical region with
several inconspicuous percurrent proliferations, or with periclinal
thickening; collarette inconspicuous, or prominent, lared. Conidia
hyaline, smooth, becoming somewhat olivaceous and verruculose
in older cultures, subcylindrical, tapering in apical part to obtuse or
subobtuse apex, base truncate, transversely euseptate, straight to
somewhat curved, mostly with one large central guttule per cell,
older conidia becoming constricted at septa, disarticulating into
phragmospores.
Fig. 98. Conidia and conidiogenous loci of Corynespora leucadendri (CBS 135133).
Scale bar = 10 µm.
Type species: Setoseptoria phragmites Quaedvlieg, Verkley &
Crous.
Fig. 99. Corynespora leucadendri (CBS 135133). A–C. Conidiogenous cells giving rise to conidia. D. Conidia. Scale bars = 10 µm.
382
Sizing up Septoria
Fig. 100. Setoseptoria phragmitis (CBS 114802). Conidioma sporulating in culture. B. Setae. C, D. Conidiogenous cells. E. Conidia. Scale bars = 10 µm.
Setoseptoria phragmitis Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804463. Fig. 100.
Etymology: Named after the host genus from which it was collected,
Phragmites.
On sterile Carex leaves on WA. Conidiomata pycnidial, brown,
immersed, globose with central ostiole, up to 30 µm diam,
somewhat papillate, up to 200 µm diam, apical erumpent part at
times with brown, verruculose to warty setae; wall of 6–8 layers
of brown textura angularis; inner layer of 6–10 layers of hyaline
textura angularis. Conidiophores lining the inner cavity, reduced to
conidiogenous cells, or with one supporting cell. Conidiogenous
cells hyaline, smooth, subcylindrical to doliiform, 7–12 × 3–4 µm;
apical region with several inconspicuous percurrent proliferations,
or with periclinal thickening; collarette inconspicuous, or prominent,
lared. Conidia hyaline, smooth, becoming somewhat olivaceous
and verruculose in older cultures, subcylindrical, (1–)3-septate,
(19–)25–35(–38) × (3.5–)4 µm, tapering in apical part to obtuse
or subobtuse apex, base truncate, 1.5–2.5 µm diam, straight to
somewhat curved, mostly with one large central guttule per cell,
older conidia becoming constricted at septa, disarticulating into
phragmospores.
Culture characteristics: Colonies on PDA umbonate, round, luffy
grey white aerial mycelium on the younger parts with longer grey
blackish tufts on the older parts, surface olivaceous-black to buff at
the younger mycelium, reverse olivaceous-black at the older parts
to buff at the younger mycelium, after 14 days 6 cm diam; on MEA
similar toPDA but after 14 d, 7 cm diam; on OA similar to PDA.
µm), S. arundinacea (conidia 6–7-septate, 60–70 × 5–6 µm), S.
curva (conidia 14–20 × 3.5–4.5 µm), and S. graminum (conidia
multiseptate, 55–75 × 1–1.3 µm), all of which appear to differ from
Setoseptoria phragmitis based on its conidial morphology.
Clade 44: Septorioides
Septorioides Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804464.
Etymology: Resembling the genus Septoria.
Foliicolous. Conidiomata black, unilocular, globose, lattened,
opening by means of irregular rupture; wall consisting of 6–10 layers
of dark brown textura irregularis to angularis, exuding a crystal
conidial mass. Paraphyses intermingled among conidiophores,
hyaline, cylindrical, branched at base, septate with obtuse ends.
Microconidia hyaline, smooth, cylindrical, mostly straight, apex
obtuse, base truncate. Conidiophores reduced to conidiogenous
cells or with a supporting cell. Conidiogenous cells lining the inner
cavity in basal layer, hyaline, smooth, subcylindrical to ampulliform,
giving rise to macro- and microconidia. Spermatia formed in
conidiomata, cylindrical, hyaline, smooth, straight to curved.
Macroconidia hyaline, smooth, guttulate, subcylindrical, straight to
irregularly curved, tapering in apical cell to subobtuse apex, base
truncate, transversely euseptate.
Type species: Septorioides pini-thunbergii (S. Kaneko) Quaedvlieg,
Verkley & Crous.
Specimens examined: hong Kong, Mai Po Mangrove, from the leaves of
Phragmites australis (Poaceae), 12 Mar. 1998, K.D. Hyde (holotype CBS H-21324,
culture ex-type CBS 114802 = HKUCC 2689); ibid., 3 Feb. 2000, K.D. Hyde (CBS
114966 = HKUCC 6029).
Septorioides pini-thunbergii (S. Kaneko) Quaedvlieg,
Verkley & Crous, comb. nov. MycoBank MB804465. Fig.
101.
Notes: Setoseptoria needs to be compared to Dearnessia and
Trichoseptoria (see above). The genus Trichoseptoria is poorly
known, and details about its conidiogenesis is lacking, and thus
it cannot be compared until it has been recollected. Setoseptoria
is distinct from Dearnessia in that it has conidiogenous cells with
prominent percurrent proliferation, and conidia that tend to become
olivaceous and verruculose in older cultures, and disarticulate into
phragmospores. Several Septoria species have been described
from Phragmites, including S. phragmitis (conidia 20–30 × 1.5–2
Associated with needle blight, or isolated as endophyte. On PDA.
Conidiomata black, unilocular, globose, lattened, up to 400 µm
diam, opening by means of irregular rupture; wall consisting of 6–10
layers of dark brown textura irregularis to angularis, exuding a crystal
conidial mass. Paraphyses intermingled among conidiophores,
hyaline, cylindrical, branched at base, septate with obtuse ends,
2–2.5 µm diam, up to 80 µm long. Microconidia hyaline, smooth,
www.studiesinmycology.org
Basionym: Septoria pini-thunbergii S. Kaneko, Trans. Mycol. Soc.
Japan 30(4): 463. 1989.
383
Quaedvlieg et al.
Fig. 101. Septorioides pini-thunbergii (CBS 473.91). A. Colony sporulating on PDA. B. Spermatia. C–E. Conidiogenous cells. F. Conidia. Scale bars = 10 µm.
cylindrical, mostly straight, apex obtuse, base truncate, 5–15 ×
2–2.5 µm. Conidiophores reduced to conidiogenous cells or with
a supporting cell. Conidiogenous cells lining the inner cavity in
basal layer, hyaline, smooth, subcylindrical to ampulliform, 10–15
× 4–6 µm, giving rise to macro- and microconidia. Spermatia
formed in conidiomata, cylindrical, hyaline, smooth, straight to
curved, 3–7 × 2 µm. Macroconidia hyaline, smooth, guttulate,
subcylindrical, straight to irregularly curved, tapering in apical cell
to subobtuse apex, base truncate, (60–)70–80(–110) × 3.5(–4) µm,
(1–)3–6(–10)-septate.
Specimen examined: Japan, Akita Prefecture, Tenno-cho, on needles of Pinus
thunbergii (Pinaceae), Aug. 1984, S. Kaneko & Y. Zinno, culture ex-type of Septoria
pini-thunberghii (CBS 473.91).
Note: Septorioides is distinguished from Septoria by having
conidiomata that open by means of an irregular split (acervular),
and having paraphyses intermingled among its conidiophores.
Septorioides pini-thunbergii was originally described from blighted
needles of Pinus thunbergii in Japan (Kaneko et al. 1989). It was
also recently isolated as endophyte from needles of P. densilora in
Korea (Yoo & Eom 2012).
Clade 45: Phlyctema
hyaline conidiophores, and phialidic conidiogenous cells that give
rise to hyaline, aseptate, fusiform, straight to curved conidia. The
genus has more than 80 names, and is in need of revision. . The
type species is linked to a sexual morph known as Neofabraea alba
(Verkley 1999).
Phlyctema vincetoxici Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804466. Figs 102, 103.
Etymology: Named after the host genus from which it was collected,
Vincetoxicum.
Conidiomata immersed, separate, eustromatic, unilocular,
convulated, opening by irregular rupture, becoming acervular
to sporodochial, up to 450 µm diam; wall of 3–6 layers of brown
textura angularis; outer surface covered in brown, warty hyphae.
Conidiophores hyaline, smooth, subcylindrical, lining the inner
layer, branched, 1–4-septate, 15–50 × 4–5 µm. Conidiogenous
cells phialidic, hyaline, smooth, subcylindrical to cymbiform or
doliiform, with apical periclinal thickening and minute, non-laring
collarette, 7–18 × 3.5–5 µm. Conidia hyaline, smooth, guttulate,
aseptate, fusiform, curved, tapering to subobtuse apex and truncate
base, (27–)33–37(–40) × 3(–3.5) µm.
Phlyctema Desm., Ann. Sci. Nat., Sér. 3, 8: 16. 1847.
= Allantozythia Höhn., Mykol. Unters. 3: 322. 1923.
Mycelium immersed, branched, septate, hyaline. Conidiomata
eustromatic, immersed, erumpent, sporodochial, separate, yellowish
brown, pulvinate, circular, unilocular but convoluted, thick-walled;
wall of textura angularis, darker brown and thicker-walled at base
than at the sides. Ostiole absent, dehiscence by irregular rupture.
Conidiophores hyaline, septate, branched irregularly, cylindrical to
iliform, formed from the wall lining the conidiomata. Conidiogenous
cells enteroblastic, phialidic, integrated or discrete, determinate,
hyaline, with minute collarette and periclinal thickening. Conidia
hyaline, aseptate, fusiform, eguttulate, straight to slightly curved or
irregular (Sutton 1980).
Type species: P. vagabunda Desm., Ann. Sci. Nat., Bot., Sér. 3, 8:
16. 1847.
Notes: Phlyctema is characterised by having eustromatic,
convulated, pulvinate to sporodochial conidiomata, branched,
384
Fig. 102. Conidia and conidiogenous cells of Phlyctema vincetoxici (CBS 123727).
Scale bar = 10 µm.
Sizing up Septoria
Fig. 103. Phlyctema vincetoxici (CBS 123727). A. Colonies forming on OA. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 µm.
Culture characteristics: Colonies on PDA lat, circular, with sparse,
white aerial mycelium, surface dark-brick, reverse greyish sepia,
after 14 d, 7 cm diam; on MEA undulate, lacking aerial mycelium,
after 14 d, 6 cm diam; on OA lat, circular, lacking aerial mycelium,
after 14 d, 8.5 cm diam.
Kirstenboschia diospyri Quaedvlieg, Verkley & Crous, sp.
nov. MycoBank MB804468. Figs 104, 105.
Specimen examined: czech republic, Moravia, Podyji National Park, Masovice,
Klinka area, on leaves of Vincetoxicum oficinale (Asclepiadaceae), 17 Sep. 2008,
G. Verkley (holotype CBS H-21325, culture ex-type CBS 123727 = V6015.2).
Conidiomata erumpent, sporodochial, up to 300 µm diam, separate,
appearing creamy to pale yellow when sporulating on SNA with
barley leaves, with slightly raised outer margin of 3–10 layers of
textura intricata. Conidiophores lining the inner cavity, hyaline,
smooth, 0–4-septate, subcylindrical, branched below and above,
5–15 × 2–4 µm. Conidiogenous cells 5–10 × 2–3 µm, terminal and
lateral, hyaline, smooth, ampulliform to subcylindrical, proliferating
sympodially, apical loci truncate, at times appearing subdenticulate,
1 µm diam. Conidia solitary, hyaline, scolecosporous, smooth,
granular, thin-walled, acicular to narrowly obclavate with subobtuse
apex and truncate to long obconically truncate base, 3-septate,
irregularly curved, (40–)60–70(–75) × (1.5–)2 µm.
Notes: No species of Phlyctema has thus far been described on
Vincetoxicum. Septoria vincetoxici (conidia 30–50 × 1–1.5 µm;
Saccardo 1884) has somewhat longer, narrower conidia. Phlyctema
vincetoxici was found sporulating in leaf spots showing numerous
hypophyllous teleospore sori of the rust fungus Cronartium
laccidum (identiied by H.A. van der Aa).
Clade 46: Kirstenboschia
Kirstenboschia Quaedvlieg, Verkley & Crous, gen. nov.
MycoBank MB804467.
Etymology: Kirstenbosch National Botanical Garden is one of the
most acclaimed botanical gardens of the world, set against the foot
of Cape Town’s Table Mountain. With more than 7000 plant species,
it has also proven to be a source of numerous undescribed fungal
species. Kirstenbosch was established in 1913, and to celebrate its
centenary (2013), the fungal genus Kirstenboschia is named after
this beautiful garden.
Etymology: Named after the host genus from which it was collected,
Diospyros.
Culture characteristics: Colonies on PDA erumpent, with moderate
aerial mycelium, and smooth, lobate margin; surface and reverse
dirty white. On OA dirty white with diffuse brown pigment in agar.
On MEA surface folded, irregular, strongly erumpent, dirty white,
reverse sienna.
Foliicolous. Conidiomata erumpent, sporodochial, separate, with
slightly raised outer margin of 3–10 layers of textura intricata.
Conidiophores lining the inner cavity, hyaline, smooth, septate,
subcylindrical, branched below and above. Conidiogenous cells
terminal and lateral, hyaline, smooth, ampulliform to subcylindrical,
proliferating sympodially, apical loci truncate, at times appearing
subdenticulate. Conidia solitary, hyaline, scolecosporous, smooth,
granular, thin-walled, acicular to narrowly obclavate with subobtuse
apex and truncate to long obconically truncate base, 3-septate,
irregularly curved.
Type species: K. diospyri Quaedvlieg, Verkley & Crous.
Fig. 104. Conidia and conidiogenous cells of Kirstenboschia diospyri (CBS 134911).
Scale bars = 10 µm.
www.studiesinmycology.org
385
Quaedvlieg et al.
Fig. 105. Kirstenboschia diospyri (CBS 134911). A. Conidiomata forming in culture. B, C. Conidiogenous cells. D. Conidia. Scale bars: A = 300 µm, all others = 10 µm.
Specimen examined: South Africa, Western Cape Province, Kirstenbosch Botanical
Garden, on leaves of Diospyros whyteana (Ebenaceae), 9 Aug. 2011, P.W. Crous
(holotype CBS H-21326, culture ex-type CBS 134911 = CPC 19869).
Note: Kirstenboschia is distinguished from Septoria s. str. and
allied genera based on its distinctive, sporodochial conidiomata,
and conidiogenous cells that proliferate sympodially, but at times
are subdenticulate.
Clade 47: Phlogicylindrium
Phlogicylindrium Crous, Summerb. & Summerell, Fungal
Diversity 23: 340. 2006.
Foliicolous. Conidiomata synnematal to sporodochial, pale brown.
Macroconidiophores arising from a brown stroma of 3–6 layers
of textura angularis, giving rise to subcylindrical, hyaline (dark
brown at the base), smooth, frequently branched conidiophores,
0–2(–6)-septate. Macroconidiogenous cells hyaline, smooth,
subcylindrical, proliferating sympodially and percurrently near
apex. Macroconidia hyaline, smooth, subcylindrical, transversely
septate, apex obtusely rounded, base truncate, slightly
curved. Microconidia formed in acervular conidiomata together
with macroconidia. Microconidiophores intermingled among
macroconidiophores, hyaline, smooth, subcylindrical, branched,
1–4-septate. Microconidiogenous cells terminal and lateral,
hyaline, smooth, ampulliform, phialidic, solitary or in penicillate
clusters. Microconidia hyaline, smooth, hamate, curved, apex
subobtuse, base truncate, widest in upper third, aseptate
(Summerell et al. 2006).
subcylindrical, 10–15 × 2–4 μm, proliferating sympodially
and percurrently near apex. Macroconidia hyaline, smooth,
subcylindrical, 1(–3)-septate, apex obtusely rounded, base
truncate, slightly curved, (27–)40–50(–55) × 2–2.5(–3) μm.
Microconidia formed in acervular conidiomata together with
macroconidia. Microconidiophores intermingled among
macroconidiophores, hyaline, smooth, subcylindrical, branched,
1–4-septate, 20–40 × 2–2.5 µm. Microconidiogenous cells
terminal and lateral, hyaline, smooth, ampulliform, phialidic,
5–16 × 2–2.5 µm, solitary or in penicillate clusters of up to 3.
Microconidia hyaline, smooth, hamate, curved, apex subobtuse,
base truncate, widest in upper third, aseptate, (16–)17–20(–24)
1.5(–2) µm.
Specimens examined: Australia, Victoria, Otway Ranges, (near Gellibrand),
latitude: -38.568412, longitude: 143.539586, elevation: 175 m, on leaves of
Eucalyptus globulus (Myrtaceae), Sep. 2005, I. Smith, holotype CBS H-19771,
cultures ex-type CPC 12429 = CBS 120221; New South Wales, on leaves of E.
nitens, 22 Nov. 1996, P.W. Crous (CBS 111689 = CPC 1547 = STE-U 1547).
Notes: The present strain represents the second collection of this
fungus. Isolates from this collection formed a microconidial state
not observed in the type (Crous et al. 2007c), and novel for species
of Phlogicylindrium.
Type species: P. eucalypti Crous, Summerb. & Summerell, Fungal
Diversity 23: 340. 2006.
Phlogicylindrium eucalyptorum Crous, Fungal Planet 20.
2007. Figs 106, 107.
On OA. Conidiomata synnematal to sporodochial, pale
brown up to 300 μm diam. Macroconidiophores arising from
a brown stroma of 3–6 layers of textura angularis, giving rise
to subcylindrical, hyaline (dark brown at the base), smooth,
frequently branched conidiophores, 0–2(–6)-septate, 15–25(–
45) × 3–4 μm. Macroconidiogenous cells hyaline, smooth,
386
Fig. 106. Macro- and microconidia and conidiogenous cells of Phlogicylindrium
eucalyptorum (CBS 111689). Scale bars = 10 µm.
Sizing up Septoria
Fig. 107. Phlogicylindrium eucalyptorum (CBS 111689). A. Colony on OA. B, E. Microcyclic conidiation with macro- and macroconidia. C. Macroconidiogenous cells. D.
Microconidia. F. Macroconidia. Scale bars = 10 µm.
dIScuSSIoN
The main question considered in the present study was: what is
Septoria? To address this we included 370 isolates representing
170 species, sampled from six continents. Furthermore, we
also generated several phylogenetic datasets based on partial
sequences of the ITS, LSU, Btub, RPB2 and EF-1α loci. In the
inal analysis, it was clear that Septoria is a well-deined genus
and phylogenetic clade, with pycnidial, ostiolate conidiomata,
conidiophores reduced to conidiogenous cells that proliferate
sympodially, and hyaline, iliform conidia with transverse eusepta,
itting the original concept of Sutton (1980). However, when host
material has been incubated for a while, several pycnidial species
tend to form acervuli (also not clearly deined when studied in
culture on normal agar media), and conidiogenous cells could
have a combination of sympodial and percurrent proliferation (as
observed in Pseudocercospora; Crous et al. 2013).
The present study, including that of Verkley et al. (2013)
deined an additional 15 genera that were formerly treated as
“septoria” in the widest sense. Although it has recently been shown
that Phoma is a generic complex representing many morphologic
and phylogenetic genera (Aveskamp et al. 2010, de Gruyter et al.
2010, 2013), this was not expected to also be the case for Septoria.
Furthermore, many of the septoria-like genera discussed earlier in
this paper are presently still not known from sequence, and thus
their phylogeny remains to be resolved, meaning that they could
add futher entities to the list of acknowledged septoria-like genera.
Although Septoria s. str. is a genus in the Mycosphaerellaceae
(Capnodiales), several of the septoria-like genera clustered outside
this family. Species of Septoria are morphologically conserved,
and in the past many taxa were identiied based on host, which
has been shown to be unreliable (see Verkley et al. 2013), as
several taxa have wide host ranges. Another complication revealed
in the present study is that many septoria-like genera cluster in
different phylogenetic clades, but have still retained the Septoria
morphological characters, which means that as in Phoma, future
www.studiesinmycology.org
identiications in this complex will also have to rely on DNA
sequence data to support morphological conclusions.
The genus Stagonospora has always been separated from
Septoria on the basis that Septoria has conidiogenous cells with
sympodial proliferation, whereas in Stagonospora they proliferate
percurrently. As shown in the present study, however, conidiogenesis
is far too broad a feature to deine all genera that express these modes
of proliferation in their conidiogenous cells. Stagonospora, which is
based on S. paludosa, was epitypiied in this study, and shown to
cluster apart from Septoria s. str. Another major surprise lies in the fact
that Septoria nodorum blotch, caused by “Stagonospora” nodorum,
clusters in a distinct genus, unrelated to Stagonospora s. str., and
also separate from Phaeosphaeria s. str. A repercussion from these
indings is the fact that the common cereal pathogens, which are
neither Stagonospora, Septoria, Phaeosphaeria or Leptosphaeria
(see de Gruyter et al. 2013), now have to be accommodated in
a new genus, Parastagonospora. Furthermore, it appears that
Stagonospora s. str. occurs on Poaceae, but has thus far only been
conirmed from Carex, though further sampling will undoubtedly
extend the host range of this genus. Parastagonospora is thus a
novel, distinct stagonospora-like genus, which has sexual morphs
that are phaeosphaeria-like in morphology, thus quite unlike those of
Stagonospora s. str., which are more didymella-like in morphology.
The genus Phaeosphaeria is based on P. oryzae (asexual
morph Phaeoseptoria oryzae), for which we could designate
an epitype in this study. Furthermore, we also recollected the
type species of Phaeoseptoria, P. papayae, for which we also
designated an epitype. As expected, Phaeoseptoria clusters with
Phaeosphaeria, for which we choose the name of the sexual
morph, Phaeosphaeria, on the basis that it is clearly resolved,
and well established in literature. In contrast, Phaeoseptoria has
in recent years become a muddled concept harbouring unrelated
coelomycetes with pigmented conidia.
Obtaining a culture of Cytostagonospora martiniana clariied
the phylogenetic position of the genus as distinct from Septoria,
resolving the difference of opinion between von Arx (1983), who
regarded it as synonym of Septoria, versus Sutton (1980), who
387
Quaedvlieg et al.
retained it as separate genus. Of interest is the unique mode of
conidiogenesis, ranging from holoblastic sympodial to polyphialides
with periclinal thickening to percurrent proliferation. It should be
noted, however, that although this is a distinct genus, C. mariniana
is not the type of Cytostagonospora, and C. photiniicola (occurring
on Photinia serrulata, Austria) will have to be recollected to conirm
that these two fungi are congeneric.
The genus Phloeospora (based on P. ulmi) has for long been
assumed to be a synonym of Septoria based on morphology. It
is thus good to inally see it resolved as separate phylogenetic
lineage, which is also supported morphologically based on its
acervular conidiomata and conidiogenous cells with prominent
percurrent proliferation. In spite of resolving 21 genera, several
lineages remain unresolved, and are simply treated as “septorialike” awaiting the recollection of additional material.
It is surprising that so many of the cereal pathogens actually
have a confused taxonomy. Eyespot disease of wheat, formely
treated as Tapesia (Ramulispora asexual states), was shown to
represent a distinct genus Oculimacula (Helgardia asexual states)
(Crous et al. 2003), while Quaedvlieg et al. (2011) determined that
Septoria tritici blotch, caused by “Septoria” tritici, is in fact better
accommodated in a new genus, Zymoseptoria, which appears
to be restricted to members of Poaceae. The present study also
resolved the phylogenetic position of Septoria nodorum blotch, which
proved to not represent a member of Septoria, Stagonospora, or
Phaeosphaeria, but to represent a distinct genus, described here
as Parastagonospora. Clearly more attention should be directed
towards resolving the taxonomy of the pathogens of agricultural
crops of major economic importance in future, as these indings
also have implications for genomic studies, where organisms from
different genera, and even families get compared to one another,
and new evolutionary hypotheses are proposed on the assumption
that these taxa are congeneric. To clarify the taxonomy of well-known
plant pathogens, however, many species will have to be recollected,
and epitypiied, so that authentic cultures and DNA barcodes will
become available to ix the genetic application of these names.
General conclusions
The genus Septoria is deined by having pycnidial to acervular
conidiomata, and hyaline conidiophores that give rise to
conidiogenous cells that proliferate sympodially and percurrently,
forming hyaline, iliform conidia with transverse eusepta. Many
species have wide host ranges, and host occurrence should not be
used as primary character for identiication (see Verkley et al. 2013,
this issue). Although species of Septoria and several of the novel
genera introduced here have mycosphaerella-like sexual states,
the name Mycosphaerella is restricted to the genus Ramularia, and
is unavailable for species of Septoria and related genera.
aCKNoWlEdGEMENTs
We thank the technical staff, Arien van Iperen (cultures), and Marjan Vermaas
(photographic plates), for their invaluable assistance. The research leading to
these results has received funding from the European Community’s Seventh
Framework Program (FP7/2007–2013)/grant agreement no. 226482 (Project: QBOL
- Development of a new diagnostic tool using DNA barcoding to identify quarantine
organisms in support of plant health) by the European Commission under the theme
“Development of new diagnostic methods in support of Plant Health policy” (no.
KBBE-2008-1-4-01). Special thanks also go to Dr Ellen van Agtmaal who prepared
the line drawings included in this paper from photomicrographs and published
materials (Sutton 1980) using Adobe Photoshop CS3.
388
rEFErENCEs
Aptroot A (2006). Mycosphaerella and its anamorphs. 2, Conspectus of
Mycosphaerella. CBS Biodiversity Series 5. CBS-KNAW Fungal Biodiversity
Centre, Utrecht, The Netherlands.
Arx JA von (1983). Mycosphaerella and its anamorphs. Proceedings of the
Koninklijke Nederlandse Akademie van Wetenschappen Series C-Biological
and Medical Sciences 86(1): 15–54.
Arzanlou M, Crous PW (2006). Phaeosphaeriopsis musae. Fungal Planet 9. CBSKNAW Fungal Biodiversity Centre, Utrecht, The Netherlands.
Aveskamp M, Gruyter H de, Woudenberg J, Verkley G, Crous PW (2010). Highlights
of the Didymellaceae: A polyphasic approach to characterise Phoma and
related pleosporalean genera. Studies in Mycology 65: 1–60.
Barnes I, Crous PW, Wingield BD, Wingield MJ (2004). Multigene phylogenies
reveal that red band needle blight of Pinus is caused by two distinct species of
Dothistroma, D. septosporum and D. pini. Studies in Mycology 50: 551–565.
Beach WS (1919). Biologic specialization in the genus Septoria. American Journal
of Botany 6: 1–32.
Bedlan G (2011). Septoria juliae sp. nov. – a new Septoria species on Nerium
oleander. Journal für Kulturplanzen 63: 430–431.
Bissett J (1982). Stagonospora avenae. Fungi Canadenses 239. National
Mycological Herbarium, Biosystematics Research Institute, Agriculture
Canada, Ottawa.
Braun U (1990). Taxonomic problems of the Ramularia / Cercosporella complex.
Studies in Mycology 32: 65–75.
Braun U (1995). A monograph of Cercosporella, Ramularia and allied genera
(Phytopathogenic Hyphomycetes). Vol. 1. IHW-Verlag, Eching.
Braun U (1998). A monograph of Cercosporella, Ramularia and allied genera
(Phytopathogenic Hyphomycetes). Vol. 2. IHW-Verlag, Eching.
Câmara MPS, Ramaley AW, Castlebury LA, Palm ME (2003). Neophaeosphaeria
and Phaeosphaeriopsis , segregates of Paraphaeosphaeria. Mycological
Research 107: 516–522.
Carbone I, Kohn LM (1999). A method for designing primer sets for speciation
studies in ilamentous ascomycetes. Mycologia 91: 553–556.
Cheewangkoon R, Crous PW, Hyde KD, Groenewald JZ, To-anan C (2008). Species
of Mycosphaerella and related anamorphs on Eucalyptus leaves from Thailand.
Persoonia 21: 77–91.
Constantinescu O (1984). Taxonomic revision of Septoria-like fungi parasitic on
Betulaceae. Transactions of the British Mycological Society 83: 383–398.
Crous PW (1998). Mycosphaerella spp. and their anamorphs associated with leaf
spot diseases of Eucalyptus. Mycologia Memoir 21. APS Press, MN, USA.
Crous PW, Braun U (2003). Mycosphaerella and its anamorphs: 1. Names published
in Cercospora and Passalora. CBS Biodiversity Series 1. CBS-KNAW Fungal
Biodiversity Centre, Utrecht, The Netherlands.
Crous PW, Braun U, Groenewald JZ (2007a). Mycosphaerella is polyphyletic.
Studies in Mycology 58: 1–32.
Crous PW, Braun U, Hunter GC, Wingield MJ, Verkley GJM, et al. (2013).
Phylogenetic lineages in Pseudocercospora. Studies in Mycology 75: 37–114.
Crous PW, Braun U, Schubert K, Groenewald JZ (2007b). Delimiting Cladosporium
from morphologically similar genera. Studies in Mycology 58: 33–56.
Crous PW, Ferreira FA, Sutton BC (1997). A comparison of the fungal genera
Phaeophleospora and Kirramyces (coelomycetes). South African Journal of
Botany 63: 111–115.
Crous PW, Groenewald JZ, Gams W (2003). Eyespot of cereals revisited: ITS
phylogeny reveals new species relationships. European Journal of Plant
Pathology 109: 841–850.
Crous PW, Groenewald JZ, Smith IW (2007c). Phlogicylindrium eucalyptorum.
Fungal Planet 20. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The
Netherlands.
Crous PW, Kang JC, Braun U (2001). A phylogenetic redeinition of anamorph
genera in Mycosphaerella based on ITS rDNA sequence and morphology.
Mycologia 93: 1081–1101.
Crous PW, Schoch CL, Hyde KD, Wood AR, Gueidan C, et al. (2009a). Phylogenetic
lineages in the Capnodiales. Studies in Mycology 64: 17–47.
Crous PW, Shivas RG, Wingield MJ, Summerell BA, Rossman AY, et al. (2012a).
Fungal Planet description sheets 128–127. Persoonia 29: 138–153.
Crous PW, Slippers B, Wingield MJ, Rheeder J, Marasas WFO, et al. (2006).
Phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology 55:
235–253.
Crous PW, Summerell BA, Carnegie AJ, Wingield MJ, Groenewald JZ (2009b).
Novel species of Mycosphaerellaceae and Teratosphaeriaceae. Persoonia 23:
119–146.
Crous PW, Summerell BA, Carnegie AJ, Wingield MJ, Hunter GC, et al. (2009c).
Unravelling Mycosphaerella: do you believe in genera? Persoonia 23: 99–118.
Crous PW, Tanaka K, Summerell BA, Groenewald JZ (2011). Additions to the
Mycosphaerella complex. IMA Fungus 2: 49–64.
Sizing up Septoria
Crous PW, Verkley GJM, Christensen M, Castañeda-Ruiz RF, Groenewald JZ
(2012b). How important are conidial appendages? Persoonia 28: 126–137.
Crous PW, Verkley GJM, Groenewald JZ, Samson RA (2009d). CBS Laboratory
Manual Series 1. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The
Netherlands.
Crous PW, Wingield MJ, Park RF (1991). Mycosphaerella nubilosa a synonym of M.
molleriana. Mycological Research 95: 628–632.
Cunfer BM (2000). Stagonospora and Septoria diseases of barley, oat, and rye.
Canadian Journal of Plant Pathology 22: 332–348.
Cunfer BM, Ueng PP (1999). Taxonomy and identiication of Septoria and
Stagonospora species on small-grain cereals. Annual Review of Phytopathology
37: 267–284.
Deighton FC (1987). New species of Pseudocercospora and Mycovellosiella, and
new combinations into Pseudocercospora and Phaeoramularia. Transactions
of the British Mycological Society 88: 365–391.
Demaree JB, Wilcox MS (1943). The fungus causing the so-called “Septoria leafspot disease” of raspberry. Phytopathology 33: 986–1003.
Desmazières JBHJ (1847). Quatorzième notice sur les plantes cryptogames
récemment découvertes en France. Annales des Sciences Naturelles
Botanique, Série 3, 8: 9–37, 172–193.
Donk MA (1964). Nomina conervana proposita. Deuteromycetes. Regnum
Vegetable 34: 7–15.
Dyko BJ, Sutton BC (1979). Two new and unusual deuteromycetes. Transactions of
the British Mycological Society 72: 411–417.
Ellis MB (1971). Dematiaceous Hyphomycetes. Commonwealth Mycological
Institute, Kew, Surrey, UK.
Ellis MB (1976). More Dematiaceous Hyphomycetes. Commonwealth Mycological
Institute, Kew, Surrey, UK.
Ellis MB, Ellis JP (1997). Microfungi on Land Plants – An Identiication Handbook.
Richmond Publishing, England.
Eriksson OE (1967). On graminicolous pyrenomycetes from Fennoscandia I, II, Ill.
Phragmosporous and scolecosporous species. Arkiv för Botanik Series 2, 6:
381–440.
Evans HC (1984). The genus Mycosphaerella and its anamorphs Cercoseptoria,
Dothistroma and Lecanosticta on pines. Mycological Papers 153: 1–102.
Eyal Z, Sharen AL, Prescott JM, Ginkel M van (1987). The Septoria diseases of
wheat: concepts and methods of disease management. Mexico, DF, CIMMYT.
Farr DF (1991). Septoria species on cornus. Mycologia 83: 611–623.
Farr DF (1992). Species of Septoria on the Fabaceae, subfamily Faboidae, tribe
Genistae. Sydowia 44: 13–31.
Farr DF, Rossman AY (2013). Fungal Databases, Systematic Mycology and
Microbiology Laboratory, ARS, USDA. Retrieved May 3, 2013, from http://
nt.ars-grin.gov/fungaldatabases/
Feau N, Hamelin RC, Bernier L (2006). Attributes and congruence of three molecular
data sets: Inferring phylogenies among Septoria related species from woody
perennial plants. Molecular Phylogenetics and Evolution 40: 808–829.
Ferreira FA (1989). Patologia Florestal. Principais Doenças Florestais No Brasil.
Sociedade de Investigaçoes Florestais, Viçosa, MG, Brasil.
Frank J, Crous PW, Groenewald JZ, Oertel B, Hyde KD, et al. (2010). Microcyclospora
and Microcyclosporella: novel genera accommodating epiphytic fungi causing
sooty blotch on apple. Persoonia 24: 93–105.
Fukuhara M (2002). Three Phaeosphaeria species and Paraphaeosphaeria michotii
isolated from Phragmites leaves in Osaka, Japan. Mycoscience 43: 275–382.
Golzar H, Wang C (2012). First report of Phaeosphaeriopsis glaucopunctata as the
cause of leaf spot and nectrosis on Ruscus aculeatus in Australia. Australasian
Plant Disease Notes 7: 13–15.
Goodwin SB (2004). Minimum phylogenetic coverage: An additional criterion to
guide the selection of microbial pathogens for initial genomic sequencing
efforts. Phytopathology 94: 800–804.
Greene HC (1961). Notes on Wisconsin parasitic fungi. XXVII. Wisconsin Academy
of Sciences, Arts and Letters 50: 141–161.
Groenewald JZ, Nakashima C, Nishikawa J, Shin H-D, Park J-H, et al. (2013).
Species concepts in Cercospora: spotting the weeds among the roses. Studies
in Mycology 75: 115–170.
Gruyter J de, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous
PW (2010). Systematic reappraisal of species in Phoma section Paraphoma,
Pyrenochaeta and Pleurophoma. Mycologia 102: 1066–1081.
Gruyter J de, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ,
Crous PW (2013). Redisposition of Phoma-like anamorphs in Pleosporales.
Studies in Mycology 75: 1–36.
Hall TA (1999). BioEdit: A user-friendly biological sequence alignment editor and
analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:
95–98.
Hawksworth DL, Crous PW, Redhead SA, Reynolds DR, Samson RA, et al. (2011).
The Amsterdam Declaration on Fungal Nomenclature. IMA Fungus 2: 105–112.
Huelsenbeck JP, Ronquist F (2001). MRBAYES: Bayesian inference of phylogenetic
trees. Bioinformatics 17: 754–755.
www.studiesinmycology.org
Inácio CA, Dianese JC (1998). Some foliicolous fungi on Tabebuia species.
Mycological Research 102: 695–708.
Jørstad I (1965). Septoria and septoroid fungi on dicotyleones in Norway. Oslo
University Press, Oslo.
Jørstad I (1967). Septoria and Septoroid fungi on Gramineae in Norway. Oslo
University Press, Oslo.
Kaneko S, Fujioka H, Zinno Y (1989). A new species of Septoria on Japanese black
pine. Transactions of the Mycological Society of Japan 30: 463–466.
Katoh K, Misawa K, Kuma K, Miyata T (2002). MAFFT: a novel method for rapid
multiple sequence alignment based on fast Fourier transform. Nucleic Acids
Research 30: 3059–3066.
Lamprecht SC, Crous PW, Groenewald JZ, Tewoldemedhin YT, Marasas WFO
(2011). Diaporthaceae associated with root rot of maize. IMA Fungus 2: 13–24.
Lee S, Mel’nik V, Taylor JE, Crous PW (2004). Diversity of saprobic hyphomycetes
on Proteaceae and Restionaceae from South Africa. Fungal Diversity 17:
91–114.
Li HY, Sun GY, Zhai XR, Batzer JC, Mayield DA, et al. (2012). Dissoconiaceae
associated with sooty blotch and lyspeck on fruits in China and the United
States. Persoonia 28: 113–125.
Liu JK, Phookamsak R, Mingkhuan M, Wikee S, Li YM, et al. (2012) Towards a
natural classiication of Botryosphaeriales. Fungal Diversity 57: 149–210.
Liu Y, Whelen S, Hall B (1999). Phylogenetic relationships among ascomycetes:
evidence from an RNA polymerse II subunit. Molecular Biology and Evolution
16: 1799–1808.
Lombard L, Crous PW, Wingield BD, Wingield MJ (2010). Species concepts in
Calonectria (Cylindrocladium). Studies in Mycology 66: 1–13.
Marincowitz S, Crous PW, Groenewald JZ, Wingield MJ (2008). Microfungi
occurring on Proteaceae in the fynbos. CBS Biodiversity Series 7. CBS-KNAW
Fungal Biodiversity Centre, Utrecht, The Netherlands.
Mason-Gamer RJ, Kellogg EA (1996). Testing for phylogenetic conlict among
molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology 45:
524–545.
McDonald MC, Razavi M, Friesen TL, Brunner PC, McDonald BA (2012).
Phylogenetic and population genetic analyses of Phaeosphaeria nodorum and
its close relatives indicate cryptic species and an origin in the Fertile Crescent.
Fungal Genetics and Biology 49: 882–895.
Michaelides T, Morgan DP, Doster MA (1995). Foliar and fruit fungal diseases. In:
Pistachio Production (L Ferguson, ed). Center for Fruit and Nut Crop Research
and Information, Pomology Department, University of California, Davis CA.:
148–159.
Monod M (1983). Monographie taxonomique des gnomoniacées ascomycètes de
l’ordre des Diaporthales. Sydowia 9: 1–315.
Nag Raj TR (1993). Coelomycetous anamorphs with appendage-bearing conidia.
Mycologue Publications, Waterloo, Ontario.
Niekerk JM van, Groenewald JZ, Verkley GJM, Fourie PH, Wingield MJ, Crous PW
(2004). Systematic reappraisal of Coniella and Pilidiella, with speciic reference
to species occurring on Eucalyptus and Vitis in South Africa. Mycological
Research 108: 283–303.
Nylander JAA (2004). MrModeltest v2. Program distributed by the author.
Evolutionary Biology Centre Uppsala University 2: 1–2.
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998). Multiple evolutionary origins
of the fungus causing Panama disease of banana: Concordant evidence from
nuclear and mitochondrial gene genealogies. Proceedings of the National
Academy of Sciences of the United States of America 95: 2044–2049.
Petrak F (1957). Über die auf Aconitum vorkommenden Arten der gattung Septoria.
Sydowia 11: 375–379.
Petrak F, Sydow H (1927). Die Gattungen der Pyrenomyzeten, Sphaeropsideen
und Melanconieen. 1. Teil. Die phaeosporen Sphaeropsideen und die Gattung
Macrophoma. Repertorium specierum novarum regni vegetabilis, Beihefte Bd
42.
Phillips AJL, Alves A, Pennycook SR, Johnston PR, Ramaley A, et al. (2008).
Resolving the phylogenetic and taxonomic status of dark-spored teleomorph
genera in the Botryosphaeriaceae. Persoonia 21: 29–55.
Priest MJ (2006). Fungi of Australia: Septoria. ABRS, Canberra: CSIRO publishing,
Melbourne, Australia.
Punithalingam E (1976). Septoria chrysanthemella. CMI Descriptions of Pathogenic
Fungi and Bacteria 669. Commonwealth Mycological Institute, Kew, UK
Quaedvlieg W, Groenewald JZ, de Jesús Yáñez-Morales M, Crous PW (2012). DNA
barcoding of Mycosphaerella species of quarantine importance to Europe.
Persoonia 29: 101–115.
Quaedvlieg W, Kema GHJ, Groenewald JZ, Verkley GJM, Seifbarghi S, et al. (2011).
Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species
occurring on graminicolous hosts. Persoonia 26: 57–69.
Rayner RW (1970). A mycological colour chart. CMI and British Mycological Society.
Kew, UK.
Rogers DP (1949). Nomina conservanda proposita and nomina confusa – Fungi:
Nomina conservanda. Farlowia 3: 425–493.
389
Quaedvlieg et al.
Saccardo PA (1884). Sylloge Fungorum: Sylloge Sphaeropsidearum et
Melanconiearum 3: 542. Padova, Italy.
Saccardo PA (1895). Sylloge Fungorum: Supplementum Universale, Pars III 11:
542. Padova, Italy.
Saccardo PA, Saccardo D (1906). Sylloge Fungorum: Supplementum Universale,
Pars VII 18: 1–828. Padova, Italy.
Saccardo PA, Trotter A (1913). Sylloge Fungorum: Supplementum Universale, Pars
IX 22: 1–1612. Padova, Italy.
Shin HD (1995). New fungal diseases of economic resource plants in Korea (II).
Korean Journal of Plant Pathology 11: 120–131.
Shin HD, Sameva EF (2002). Taxonomic notes on the genus Septoria in Korea (II).
Mycotaxon 83: 287–300.
Shin HD, Sameva EF (2004). Septoria in Korea. National Institute of Agricultural
Science and Technology, Republic of Korea.
Shoemaker RA, Babcock CE (1989). Phaeosphaeria. Canadian Journal of Botany
67: 1500–1599.
Sivanesan A (1984). The Bitunicate Ascomycetes and their anamorphs. J. Cramer,
Vaduz, Germany.
Solomon PS, Lowe RGT, Tan KC, Waters ODC, Oliver RP (2006). Stagonospora
nodorum: cause of stagonospora nodorum blotch of wheat. Molecular Plant
Pathology 7: 147–156.
Stukenbrock EH, Quaedvlieg W, Javan-Nikhah M, Zala M, Crous PW, McDonald
BA (2012). Zymoseptoria ardabilia and Z. pseudotritici, two progenitor species
of the septoria tritici leaf blotch fungus Z. tritici (synonym: Mycosphaerella
graminicola). Mycologia 104: 1397–1407.
Summerell BA, Groenewald JZ, Carnegie AJ, Summerbell RC, Crous PW (2006).
Eucalyptus microfungi known from culture. 2. Alysidiella, Fusculina and
Phlogicylindrium genera nova, with notes on some other poorly known taxa.
Fungal Diversity 23: 323–350.
Sutton B, Pollack F (1974). Microfungi on Cercocarpus. Mycopathologia 52: 331–
351.
Sutton BC, Pascoe IG (1987). Septoria species on Acacia. Transactions of the
British Mycological Society 89: 521–532.
Sutton BC, Pascoe IG (1989). Some Septoria species on native Australian plants.
Studies in Mycology 31: 177–186.
Sutton BC, Swart HJ (1986). Australian leaf-inhabiting fungi XXIII. Colletogloeum
species and similar fungi on Acacia. Transactions of the British Mycological
Society 87: 93–102.
Sutton BC (1964). Coelomycetes III. Annellolacinia gen. nov., Aristastoma,
Phaecytostroma, Seimatosporium, etc. Mycological Papers 64. Commonwealth
Mycological Institute, Kew, UK.
Sutton BC (1977). Coelomycetes VI. Nomenclature of generic names proposed for
Coelomycetes. Mycological Papers 141. Commonwealth Mycological Institute,
Kew, UK.
390
Sutton BC (1980). The coelomycetes. Fungi imperfecti with pycnidia, acervuli and
stromata. Commonwealth Mycological Institute, Kew, UK.
Teterevnikova-Babayan DN (1987). Fungi of the genus Septoria in the U.S.S.R.
Akademiya Nauk Armyanskoi SSR, Yerevan.
Verkley GJM (1999). A monograph of the genus Pezicula and its anamorphs.
Studies in Mycology 44: 1–180.
Verkley GJM, Priest MJ (2000). Septoria and similar coelomycetous anamorphs of
Mycosphaerella. Studies in Mycology 45: 123–128.
Verkley GJM, Crous PW, Groenewald JZ, Braun U, Aptroot A (2004a). Mycosphaerella
punctiformis revisited: morphology, phylogeny, and epitypiication of the type
species of the genus Mycosphaerella (Dothideales, Ascomycota). Mycological
Research 108: 1271–1282.
Verkley GJM, Silva da M, Wicklow DT, Crous PW (2004b). Paraconiothyrium, a new
genus to accommodate the mycoparasite Coniothyrium minitans, anamorphs of
Paraphaeosphaeria, and four new species. Studies in Mycology 50: 323–335.
Verkley GJM, Starink-Willemse M, van Iperen A, Abeln ECA (2004c). Phylogenetic
analyses of Septoria species based on the ITS and LSU-D2 regions of nuclear
ribosomal DNA. Mycologia 96: 558–571.
Verkley GJM, Quaedvlieg W, Shin HD, Crous PW (2013). A new approach to species
delimitation in Septoria. Studies in Mycology 75: 213–305.
Vilgalys R, Hester M. 1990. Rapid genetic identiication and mapping of
enzymatically ampliied ribosomal DNA from several Cryptococcus species.
Journal of Bacteriology 172: 4238–4246.
Wakeield EM (1940). Nomina generica conservanda. Transactions of the British
Mycological Society 24: 282–293.
Walker J, Sutton BC, Pascoe IG (1992). Phaeoseptoria eucalypti and similar fungi
on Eucalyptus, with description of Kirramyces gen. nov. (Coelomycetes).
Mycological Research 96: 911–924.
White TJ, Bruns T, Lee S, Taylor J (1990). Ampliication and direct sequencing of
fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: a guide to
methods and applications (Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds).
Academic Press, San Diego, California: 315–322.
Wingield MJ, De Beer ZW, Slippers B, Wingield BD, Groenewald JZ, et al. (2012).
One fungus, one name promotes progressive plant pathology. Molecular Plant
Pathology 13: 604–613.
Yoo J-J, Eom A-H (2012). Molecular identiication of endophytic fungi isolated
from needle leaves of conifers in Bohyeon Mountain, Korea. Mycobiology 40:
231–235.
Zhang Y, Crous PW, Schoch CL, Hyde KD (2012). Pleosporales. Fungal Diversity
53: 1–221.
Wijnand Swart