Fungal Diversity (2011) 51:249–277
DOI 10.1007/s13225-011-0141-x
A molecular, morphological and ecological re-appraisal
of Venturiales―a new order of Dothideomycetes
Ying Zhang & Pedro W. Crous & Conrad L. Schoch &
Ali H. Bahkali & Liang Dong Guo & Kevin D. Hyde
Received: 5 October 2011 / Accepted: 6 October 2011 / Published online: 2 November 2011
# Kevin D. Hyde (outside the USA) 2011
Abstract The Venturiaceae was traditionally assigned to
Pleosporales although its diagnostic characters readily
distinguish it from other pleosporalean families. These
include a parasitic or saprobic lifestyle, occurring on leaves
or stems of dicotyledons; small to medium-sized ascomata,
often with setae; deliquescing pseudoparaphyses; 8-spored,
broadly cylindrical to obclavate asci; 1-septate, yellowish,
greenish or pale brown to brown ascospores; and hyphomycetous anamorphs. Phylogenetically, core genera of
Venturiaceae form a monophyletic clade within Dothideomycetes, and represent a separate sister lineage from current
orders, thus a new order—Venturiales is introduced. A new
family, Sympoventuriaceae, is introduced to accommodate
taxa of a well-supported subclade within Venturiales, which
contains Sympoventuria, Veronaeopsis simplex and Fusicladium-like species. Based on morphology and DNA
sequence analysis, eight genera are included in Venturiaceae, viz. Acantharia, Apiosporina (including Dibotryon),
Caproventuria, Coleroa, Pseudoparodiella, Metacoleroa,
Tyrannosorus and Venturia. Molecular phylogenetic information is lacking for seven genera previously included in
Venturiales, namely Arkoola, Atopospora, Botryostroma,
Lasiobotrys, Trichodothella, Trichodothis and Rhizogenee
and these are discussed, but their inclusion in Venturiaceae
is doubtful. Crotone, Gibbera, Lineostroma, Phaeocryptopus, Phragmogibbera, Platychora, Polyrhizon, Rosenscheldiella, Uleodothis and Xenomeris are excluded from
Venturiales, and their ordinal placement needs further
Y. Zhang
Mushroom Research Foundation,
128 Moo3, Bahn Pa Dheng, T. Pa Pae, A. Mae Taeng Chiang Mai
50150, Thailand
K. D. Hyde
International Fungal Research & Development Centre,
The Research Institute of Resource Insects,
Chinese Academy of Forestry, Kunming,
Yunnan, People’s Republic of China 650034
P. W. Crous
CBS-KNAW Fungal Biodiversity Centre,
P.O. Box 85167, 3508 AD Utrecht, The Netherlands
C. L. Schoch
National Center for Biotechnology Information,
National Library of Medicine, National Institutes of Health,
45 Center Drive, MSC 6510,
Bethesda, MD 20892-6510, USA
A. H. Bahkali : K. D. Hyde
Botany and Microbiology Department, College of Science,
King Saud University,
Riyadh 11442, Saudi Arabia
L. D. Guo
State Key Laboratory of Mycology, Institute of Microbiology,
Chinese Academy of Sciences,
Beijing 100101, People’s Republic of China
Y. Zhang : K. D. Hyde (*)
Institute of Excellence in Fungal Research, School of Science,
Mae Fah Luang University,
Tasud( Muang( Chiang Rai 57100, Thailand
e-mail: kdhyde3@gmail.com
P. W. Crous
Microbiology, Department of Biology, Utrecht University,
Padualaan 8,
3584 CH Utrecht, The Netherlands
P. W. Crous
Wageningen University and Research Centre (WUR),
Laboratory of Phytopathology,
Droevendaalsesteeg 1,
6708 PB Wageningen, The Netherlands
250
investigation. Zeuctomorpha is treated as a synonym of
Acantharia.
Keywords Fusicladium . Generic type .
Sympoventuriaceae . Taxonomy . Venturiaceae
Introduction
The name Venturiaceae was first introduced by Müller and
von Arx (1950), and a systematic generic key given by von
Arx (1952) includes 12 genera, i.e. Atopospora, Coleroa,
Gibbera, Lasiobotrys, Neogibbera, Parodiella, Phaeocryptopus, Pseudoparodia, Stigmatea, Trichodothella, Trichodothis and Venturia. Further detailed studies and additions
to the family have been made (von Arx 1954; Menon 1956;
Müller 1958; Müller and Menon 1955; Müller and von Arx
1962; Nüesch 1960; Petrak 1950, 1953, 1954; Shoemaker
1963). The first valid description of Venturiaceae was
provided by Barr (1979) who considered setose ascomata
and hyaline, olive to greenish brown, obovate to oblong,
generally 1-septate ascospores as the most important
diagnostic characters. Based on these morphological characters, 12 genera were included, i.e. Acantharia, Apiosporina, Coleroa, Gibbera, Metacoleroa, Phaeocryptopus,
Platychora, Protoventuria, Pyrenobotrys, Trichodothis,
Venturia and Xenomeris. Species of Venturiaceae sensu
Barr (1968) have a parasitic or saprobic habit, and they
usually grow in living or dead leaves, stalks, or twigs of
various higher plants, rarely on Sphagnum or dung. Many
species of Venturiaceae parasitize perennial plants, and
some of them are notable cosmopolitan plant pathogens,
causing diseases such as apple scab (Venturia inaequalis),
pear scab (V. pyrina), poplar shoot blight (V. populina),
soybean black leaf blight (Arkoola nigra), and the
widespread black knot disease of cherry (Dibotryon
morbosum) (von Arx and Müller 1975; Talbot 1971).
Currently, 27 genera are included in Venturiaceae
(Lumbsch and Huhndorf 2010).
Venturiaceae was assigned to Pleosporales based on its
“Pleospora type of centrum and bitunicate asci” (Barr
1968, 1979). However, this placement is not supported by
recent phylogenic studies (Kodsueb et al. 2006; Kruys et al.
2006; Winton et al. 2007). Results obtained by Kruys et al.
(2006) based on combined nuSSU, nuLSU and mtSSU
DNA sequences indicated that Venturiaceae forms a clade
outside Pleosporales, a well-supported monophyletic group
with members of Phaeotrichaceae. Kodsueb et al. (2006)
noted a close relationship with Tubeufiaceae based on 28S
nurDNA sequences, but their affinity with Pleosporales
lacked clear statistical support. The polyphyletic nature of
Venturiaceae was indicated by Winton et al. (2007) based
on the analysis of combined nuSSU and nuLSU rDNA
Fungal Diversity (2011) 51:249–277
sequences. Although core members of Venturiaceae form a
monophyletic group, their ordinal placement remains
unsettled in all these papers.
It is now possible to gain a better understanding of
Venturiaceae by combining recently obtained DNA sequences from a brader sampling of taxa. The aim of present
investigation is therefore to re-examine the taxonomic
status of Venturiaceae based on morphological, ecological,
molecular phylogenetic data and anamorphic states and to
evaluate its ordinal placement and relationships within
Dothideomycetes.
Materials and methods
Morphological studies
The type specimens of 15 representative genera as well as
collections of an additional four genera of Venturiaceae (sensu
Lumbsch and Huhndorf 2010) were loaned from NY, K, L,
PH and S. Some type specimens or collections are in poor
condition, while others could not be located during the
course of this study and therefore, only 12 generic type
species are described here. Measurements and descriptions of
sections of the ascomata, hamathecium, asci and ascospores
were carried out by immersing ascomata in water or in 10%
lactic acid. Microphotography was taken with material
mounted in water or 10–100% lactic acid. Slides were
rendered semi-permanent by the addition of 90% lactic acid.
Photographs were taken on an Olympus BX50 microscope
using an Olympus CA 35 AD-4 camera. The generic
descriptions are based on the type species of each genus. In
this study, the terms “ascoma” (pl. ascomata) refers to a
unilocular fruiting body, and “ascostroma” (pl. ascostromata)
to a multilocular fruiting body. Other morphological criteria
follow to Zhang et al. (2009, 2012).
DNA amplification and sequencing
Cultures used in this study were obtained from the
Centraalbureau voor Schimmelcultures in the Netherlands
(CBS). Fungal isolates and DNA extraction isolates were
on PDA and MEA, and total genomic DNA extracted from
mycelia following the protocols as outlined by Shenoy et al.
(2007, 2010). DNA amplification and sequencing were
performed following the protocol of Zhang et al. (2009).
Sequence alignment and phylogenetic analyses
The phylogeny was performed with four markers: partial
sequence from the small and large subunits of the nuclear
ribosomal RNA genes (nuSSU, nuLSU) and three protein
coding genes, translation elongation factor-1 alpha (TEF1)
Fungal Diversity (2011) 51:249–277
and the largest and second largest subunits of RNA
polymerase (RPB1, RPB2) and. Sequences were downloaded from GenBank according to Table 1. Each of the
individual ribosomal genes was aligned in SATé under
default settings with at least 20 iterations (Liu et al. 2009).
The protein coding genes were aligned in BioEdit (Hall
2004) and completed with manual adjustment. Introns and
variable columns were removed and all genes were concatenated in a single nucleotide alignment with 54.77% missing
and gap characters out of a total set of 5,496. The final data
matrix had 94 taxa including outgroups (Table 1). Previous
results indicated no clear conflict amongst the majority of the
data used (Schoch et al. 2009) and a phylogenetic analysis of
the concatenated alignment was performed at the CIPRES
webportal (Miller et al. 2010) using RAxML v. 7.2.8 as part
of the “RAxML-HPC2 on TG” tool (Stamatakis 2006;
Stamatakis et al. 2008) applying unique model parameters
for each gene and codon (11 partitions). A general time
reversible model (GTR) was applied with a discrete gamma
distribution and four rate classes. One hundred thorough
maximum likelihood (ML) tree searches were done in
RAxML v. 7.2.7 under the same model, each one starting
from a separate randomised tree and the best scoring tree
selected with a final ln value of −62920.113547. Two
isolates of Arthoniomycetes (Schismatomma decolorans and
Opegrapha dolomitica), the sister class to Dothideomycetes,
were used as outgroup. One thousand non parametric
bootstrap iterations were run with the GTR model and a
discrete gamma distribution. The resulting replicates were
plotted on to the best scoring tree obtained previously. The
phylogram with bootstrap values above the branches is
presented in Fig. 1 by using graphical options available in
TreeDyn v. 198.3 (Chevenet et al. 2006).
We also analyzed the same data set mentioned previously
using the Bayesian method of Huelsenbeck et al. (2001) by
implementing Markov Chain Monte Carlo (MCMC) sampling using the software MrBayes v.3.1.2 (Huelsenbeck and
Ronquist 2001) at the CIPRES webportal. Data was partitioned as in the RAxML run and the same likelihood models
were applied with four discrete gamma categories. The
Bayesian prior distributions treated all trees as equally likely.
Two parallel runs were performed with four chains each and
this was continued for 2000 000 generations. Every 100th tree
was saved and the two runs were examined for convergence.
The first 50% of each run was discarded as burn in and the
remaining two sets of 10 000 trees combined. The best scoring
RAxML tree was used as a template and the percentage
presence of all nodes within the combined set of 20 000 trees
plotted on its nodes as Bayesian posterior probabilities. These
are indicated as values below nodes in Fig. 1.
In order to see if missing data had any influence on our
previous phylogeny we trimmed all taxa which did not have
LSU present and removed all other genes, resulting in a matrix
251
with 1,200 characters and 90 taxa. This data set had only 20.42%
missing characters. Schismatomma decolorans was used as a
outgroup. Using the CIPRES webportal as before, we ran a
combined ML tree search with bootstrap resampling and a
bootstopping criterion in effect (Pattengale et al. 2010).
Likelihood of the final tree was estimated using the same
model parameters as for the previous RAxML run but the rapid
bootstrap option was used in this case. The run was stopped
after 450 bootstraps and combined with an optimized tree with
a final likelihood value of −10697.749925. The tree was
plotted as described but all ordinal level clades were collapsed
in MEGA 5 (Tamura et al. 2011). This is shown in Fig. 2.
Taxonomy
Venturiales Yin. Zhang, C.L. Schoch & K.D. Hyde, ord.
nov. MycoBank: MB 513386
Ascomata immersa, erumpentia vel superficialia, vel in
stroma vel infra adusta clypei, aliquando coalitus subiculum,
globosi vel subglobosi vel conicus, integer vel apices setosi,
ostiolati. Pseudoparaphyses vulgo dissolvis, asci bitunicati,
fissitunicati; ascosporae hyalinae viridae olivaceae vel
brunneae, obovoidae, oblongae, uniseptatae, symmetricae
vel asymmetricae.
Familia typica: Venturiaceae.
Habitat saprobic or parasitic on leave or stems of
dicotyledons, rarely on monocotyledons. Ascomata immersed, erumpent to superficial, scattered or gregarious, or
as locules in a stroma or below a blackened clypeus, globose,
subglobose, or dome-shaped or flat-conical, with or without
seta around papilla or covering whole ascomata, ostiolate,
sometimes ascomata sitting on a well-developed subiculum.
Hamathecium of narrowly cellular pseudoparaphyses, mostly
evanescent and rarely persistent. Asci 8-spored, bitunicate,
fissitunicate, broadly or usually obclavate, usually lacking a
pedicel. Ascospores hyaline, light greenish olivaceous to
brown, 1-septate, symmetrical, asymmetrical or apiosporous.
Anamorphs: Fusicladium sensu stricto, Pollaccia, Spilocaea, Sympodiella-like, Pseudocladosporium, ?Didymochora, Veronaeopsis and Zeloasperisporium.
Type family: Venturiaceae.
Note: The phylogenetic comparison of selected species
from Dothideomycetes is shown in Figs. 1 and 2. This
includes representatives of all major orders in the class, and
unambiguously supports Venturiales as a separate entity. In
spite of our complete sampling the placement of a sister
lineage to Venturiales remains uncertain. We also find weak
to moderate support for a relationship to Microthyriales
(based on relationship to a single isolate) and Phaeotrichaceae. Within Venturiales two lineages can be defined, i.e. the
main group containing Venturia and allies (Venturiaceae) and
a separate lineage containing Veronaeopsis, Sympoventuria
252
Fungal Diversity (2011) 51:249–277
Table 1 Taxa used in the phylogenetic analysis and their corresponding GenBank accession numbers
Species
voucher/culture
SSU
LSU
TEF1
Aliquandostipite khaoyaiensis
Alternaria alternata
Anteaglonium abbreviatum
Anteaglonium parvulum
Apiosporina collinsii
Apiosporina morbosa
Ascochyta pisi
Asterina fuchsiae
CBS 118232
CBS 916.96
ANM 925.1
SMH 5210
CBS 118973
dimosp
CBS 126.54
TH 590
AF201453
DQ678031
GU301796
DQ678082
GQ221877
GQ221907
GU301798
EF114694
DQ678070
GU586216
GU349048
DQ677927
GQ221924
GQ221917
GU349057
Asterina phenacis
Asterina weinmanniae
Asterina zanthoxyli
Aureobasidium pullulans
Botryosphaeria dothidea
Botryosphaeria stevensii
Capnodium coffeae
Capnodium salicinum
Caproventuria hanliniana
Caproventuria hystrioides
Cladosporium cladosporioides
Cochliobolus heterostrophus
Coleroa robertiani
Corynespora cassiicola
Davidiella tassiana
Delitschia didyma
Delitschia winteri
Didymella exigua
Dissoconium aciculare
TH 589
TH 592
TH 561
CBS 584.75
CBS 115476
CBS 431.82
CBS 147.52
CBS 131.34
ATCC 96019
CBS 117727
CBS 170.54
CBS 134.39
CBS 458.64
CBS 100822
CBS 399.80
UME 31411
CBS 225.62
CBS 183.55
CBS 204.89
Dissoconium commune
Dothidea insculpta
Dothidea sambuci
Dothidotthia aspera
Dothidotthia symphoricarpi
Dothiora cannabinae
Dothistroma septosporum
Elsinoë centrolobi
Elsinoë phaseoli
Fusicladium africanum
Fusicladium africanum
Fusicladium intermedium
Fusicladium pini
Gibbera conferta
Gibbera rosea
Guignardia bidwellii
Hysterium angustatum
Hysterium barrianum
CBS 110747
CBS 189.58
DAOM 231303
CPC 12933
CBS119687
CBS 737.71
CBS 112498
CBS 222.50
CBS 165.31
CPC 12829
CPC 12828
CBS 110746
CBS 463.82
CBS 191.53
CBS 213.58
CBS 237.48
CBS 123334
ANM 1495
Jahnula aquatica
Leptosphaeria biglobosa
Leptosphearia maculans
Lophium mytilinum
R68-1
CBS 303.51
DAOM 229267
EF175633
DQ470993
EF175655
GU301826
DQ470946
CBS 114111
EF596819
EF596819
GU296135
DQ678018
GU586210
GU586211
GU586212
GU586213
DQ471004
DQ677998
DQ678012
DQ247808
DQ677997
DQ678004
AY544727
GU296144
DQ678022
AF242264
DQ678026
GU296147
GU214523
GU214525
DQ247810
AY544722
EU673228
EU673224
DQ479933
GU214533
DQ678041
DQ678042
GU296150
DQ678034
FJ161167
GU323182
GU586217
GU586218
GU586219
DQ470956
DQ678051
DQ678064
DQ247800
DQ678050
AF050290
EU035459
DQ678057
AY544645
xxx
GU301808
DQ678074
DQ384090
DQ678077
RPB1
RPB2
FJ238360
DQ677980
GU357778
DQ677913
DQ677967
DQ471075
DQ767637
DQ677907
DQ471089
DQ677889
DQ471148
GU357802
DQ677898
DQ497603
GU357790
DQ677952
DQ247790
GU349052
DQ677918
GU357772
GU357793
GU371742
DQ677971
GU357800
DQ677975
GU371764
DQ471162
DQ677922
DQ470906
DQ677944
DQ677960
DQ247788
GQ852587
GQ852589
DQ247802
AY544681
EU673276
EU673273
DQ470984
GQ852597
DQ678094
DQ678095
EU035424
EU035423
EU035432
EU035436
GU301814
xxx
DQ678085
FJ161207
GQ221885
DQ471081
DQ497606
DQ471154
AF107800
DQ522854
DQ471107
DQ471182
DQ470936
DQ677934
DQ677935
GU357798
GU357799
GU349041
GU357758
GU357794
DQ677983
FJ161129
DQ471136
DQ470894
FJ161111
GU349010
DQ471062
Fungal Diversity (2011) 51:249–277
253
Table 1 (continued)
Species
voucher/culture
SSU
LSU
TEF1
Macrophomina phaseolina
Macroventuria anomochaeta
Metacoleroa dickiei
Metacoleroa dickiei
Microthyrium microscopicum
Mycosphaerella graminicola
Mycosphaerella punctiformis
Myriangium duriaei
Mytilinidion acicola
Opegrapha dolomitica
Phaeocryptopus gaeumannii
Phaeocryptopus nudus
CBS 227.33
CBS 525.71
medipc
Kruys 503
CBS 115976
CBS 292.38
CBS 113265
CBS 260.36
EB 0349
DUKE 0047528
CBS 267.37
CBS 268.37
DQ678037
DQ678088
GU456315
EF114695
DQ384100
GU301846
DQ678084
DQ470968
DQ678059
GU323209
DQ677929
GU456262
DQ677986
GU456346
GU349042
GU371734
DQ677982
DQ470920
DQ677954
GU371757
DQ883714
Phaeotrichum benjaminii
Phoma herbarum
Platychora ulmi
Protoventuria alpina
Protoventuria barriae
Protoventuriabarriae
Protoventuria major
Pyrenophora tritici
Rhytidhysteron rufulum
Schismatomma decolorans
Scorias spongiosa
Spilocaea oleaginea
Spilocaea pomi
Sympoventuria capensis
Sympoventuria capensis
Teratosphaeria fibrillosa
Teratosphaeria stellenboschiana
Trichodelitschia bisporula
CBS 541.72
CBS 276.37
CBS 361.52
CBS 140.83
ATCC 90285
CBS 300.93
CBS 114594
OSC 100066
CBS 306.38
DUKE 0047570
CBS 325.33
So-91
CBS 176.42
CPC 12839
CPC 12840
CBS 121707
CBS 116428
CBS 262.69
Trichodelitschia munkii
Trypethelium nitidiusculum
Trypethelium nitidiusculum
Trypethelium tropicum
Tubeufia cerea
Tubeufia paludosa
Tubeufia paludosa
Tyrannosoru spinicola
Venturia inaequalis
Venturia inaequalis
Venturia inaequalis
Venturia populina
Veronaeopsis simplex
Xenomeris juniperi
Xenomeris raetica
Kruys201
Nelsen 4002a
AFTOL 2099
25
CBS 254.75
CBS 120503
CBS 245.49
CBS 124.88
ATCC 60070
CBS 815.69
CBS 594.70
CBS 256.38
CBS 588.66
xejucf
CBS 485.61
EF114719
DQ384100
GU296175
DQ678033
DQ471017
AY016347
GU323185
DQ883706
EF114722
GU296182
AY016348
DQ678014
EF114726
EU035444
GU296191
AY548809
DQ678024
AF338393
GU296199
GU214583
GU349000
DQ384070
DQ471034
GU296203
DQ767649
DQ471025
EF114737
GU296204
GU296205
GU296206
EF114734
EF114741
EF114698
GU301856
AY004340
DQ678066
EF114702
EF114728
xxx
xxx
AY544672
FJ469672
AY548815
DQ678075
AF338397
GU348998
DQ885905
DQ885904
GU323213
EU019295
GU348996
DQ384096
GU327728
FJ267701
GU327730
DQ470982
GU301877
DQ767654
DQ470974
EF114712
GU301878
GU301879
GU323212
EU041877
EF114709
EF114716
RPB1
DQ471092
DQ677900
DQ471165
DQ883732
GU349034
DQ883717
GU357770
GU357745
DQ677892
DQ677909
GU357788
GU357792
DQ677882
GU349031
DQ883725
DQ677920
RPB2
DQ677946
DQ677962
FJ238444
DQ883715
DQ677973
GU349089
GU357767
GU349020
GU371812
GU371802
DQ471105
GU349024
DQ767638
DQ471098
DQ471180
GU357754
DQ470934
GU371731
DQ767643
DQ470928
GU349023
GU349022
GU357756
GU357757
GU357769
GU327732
DQ471171
254
Fungal Diversity (2011) 51:249–277
Fungal Diversity (2011) 51:249–277
A RAxML maximum likelihood tree obtained from a data set of 94
taxa and five genes (SSU, LSU, TEF1, RPB1, RPB2) with Arthoniomycetes
species as outgroup. Numbers above the nodes are bootstrap from 1000
repetitions. Only values above 50% are shown and branches recovered in
more than 90% of bootstrap trees are thickened. Culture and voucher
numbers are indicated after species names and relevant taxa are bolded
Fig. 1
and several Fusicladium-like or Sympodiella-like anamorph
species. Herein a new family, Sympoventuriaceae, is introduced to accommodate the second lineage.
Fig. 2 A simplified RAXML
maximum likelihood tree from
obtained from 90 taxa and LSU
data only. All ordinal level
clades were collapsed ad bootstrap numbers from 450 repetitions are shown above the nodes
255
Sympoventuriaceae Yin. Zhang, C.L. Schoch & K.D.
Hyde, fam. nov. MycoBank: MB 563117
Ascomata immersi, subglobosi, papillati, ostiolati.
Pseudoparaphyses hyalinis, septatis. Asci bitunicati,
fissitunicati. Ascosporae hyalinae, obovoidae, oblongae,
uniseptatae.
Habitat saprobic. Ascomata subglobose, immersed,
black, papillate, ostiolate. Pseudoparaphyses hyaline, septate,
constricted at septa, anastomosing, extending above the asci.
256
Asci 8-spored, bitunicate, fissitunicate, subcylindrical, pedicellate. Ascospores hyaline, fusoid-ellipsoidal, constricted at
median septum.
Anamorphs: Sympodiella-like, Fusicladium-like,
Veronaeopsis.
Type genus: Sympoventuria Crous & Seifert.
Genus included in Sympoventuriaceae
Multigene phylogenetic analysis in this study indicated that
species of Venturiales are subdivided into two groups
which represent two familial clades, i.e. Sympoventuriaceae
and Venturiaceae. Sympoventuriaceae is represented by
Sympoventuria, and can be distinguished from species of
Venturiales by its saprobic life style, presence of pseudoparaphyses, and hyaline, symmetrical ascospores.
Fungal Diversity (2011) 51:249–277
late. Ascospores hyaline, yellowish, light greenish olivaceous
to brown, 1-septate, symmetrical, asymmetrical or apiosporous.
Anamorphs: Fusicladium, Pollaccia, Spilocaea and ?
Pseudocladosporium-like.
Type genus: Venturia Sacc.
Genera included in Venturiaceae
Based on both morphological, ecological comparisons and
limited molecular phylogenetic analysis, eight genera are
included within Venturiaceae, viz. Acantharia, Apiosporina,
Dibotryon, Caproventuria, Coleroa, Pseudoparodiella, Venturia and Metacoleroa. However further molecular analysis
is necessary to confirm the inclusion of some genera, such as
Acantharia, Coleroa and Pseudoparodiella.
Key to the genera of Venturiaceae
Sympoventuria Crous & Seifert, Fungal Divers 25: 31 (2007).
Generic description:
Habitat saprobic on leaf litter. Ascomata subglobose,
immersed, black, inconspicuous, papillate, ostiolate. Pseudoparaphyses hyaline, septate, constricted at septa, anastomosing, extending above the asci. Asci hyaline, subcylindrical,
stipitate, 8-spored. Ascospores hyaline, fusoid-ellipsoidal,
constricted at median septum (from Crous et al. 2007b).
Anamorph reported for genus: Sympodiella-like.
Type species:
Sympoventuria capensis Crous & Seifert, Fungal Divers
25: 32 (2007).
Anamorph: Sympodiella-like.
Note: The small-sized immersed ascomata agree with
Venturia sensu stricto, but the persistent pseudoparaphyses,
saprobic life style, hyaline, 1-septate, symmetric ascospores
and subcylindrical asci of Sympoventuria capensis differ
from those of Venturia sensu stricto (Crous et al. 2007b;
Sivanesan 1977). DNA based phylogenies support the
placement of Sympoventuria within Venturiales, but not
Venturiaceae (Crous et al. 2007b, Fig. 1). Currently, only
one monotypic ascomycetous genus, Sympoventuria, is
included in Sympoventuriaceae, while the anamorphic
genus Veronaeopsis and a clade containing “Fusicladium
pini” and “F. intermedium” may represent distinct genera.
Venturiaceae E. Müll. & Arx ex M.E. Barr, Mycologia 71:
947 (1979). emend.
Habitat saprobic or parasitic on leaves or stems of
dicotyledons, rarely on monocotyledons. With or without
ascostroma. Ascomata immersed, erumpent to superficial,
scattered or gregarious, sometimes composed of a welldeveloped subiculum, globose, subglobose, with or without
setae around papilla, ostiolate. Hamathecium of narrowly
cellular pseudoparaphyses, mostly evanescent and rarely
persistent. Asci 8-spored, bitunicate, fissitunicate, usually
obclavate to obpyriform, rarely cylindrical, usually apedicel-
1a. Ascospores apiosporous Apiosporina (incl. Dibotryon)
1b. Ascospore septum median or submedian, but not
apiosporous. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2a. Hyphae grow inside of the substrate . . . . . . . . . . . .3
2b. Hyphae superficial, ascomata superficial . . . . . . . . .4
3a. Ascomata superficial, produced on thin subcuticular
stroma . . . . . . . . . . . . . . . . . . . . . . . . . . . .Coleroa
3b. Ascomata immersed to erumpent, without subcuticular stroma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .5
4a. Ascomata without subiculum, not cupulate when dry,
ascospores pale brown when mature . . . Pseudoparodiella
4b. Ascomata without subiculum, cupulate when dry,
ascospores dark brown when mature . . . . . Acantharia
4c. Ascomata produced on well defined subiculum, not
cupulate when dry, ascospores olivaceous brown when
mature . . . . . . . . . . . . . . . . . . . . . . . . Metacoleroa
5a. Parasitic, having Pollaccia or Spilocaea anamorphs,
ascospores smooth without germ slits . . . . . . . . . . . . ..
. . . . . . . . . . . . . . . . . . . . . . .Venturia sensu stricto
5b. Saprobic, having Pseudocladosporium anamorphs,
ascospores smooth without germ slits Caproventuria
5c. Saprobic, having Helicodendron anamorphs, ascospores smooth or longitudinally ridged ascospores
with or without germ slits . . . . . . . . . . . Tyrannosorus
Acantharia Theiss. & Syd., Annls mycol. 16: 15 (1918).
= Zeuctomorpha Sivan., P.M. Kirk & Govindu, Bitunicate
Ascomycetes and their Anamorphs (Vaduz): 572 (1984).
Generic description:
Habitat parasitic or saprobic. Ascomata small-sized,
gregarious, superficial, globose, subglobose to ovate, usually
cupulate when dry, thickly clothed with opaque, black setae.
Peridium comprising two-strata of cell types. Hamathecium
of cellular pseudoparaphyses, evanescent in mature
ascomata. Asci 8-spored, bitunicate, fissitunicate, obclavate, apedicellate. Ascospores obliquely uniseriate and
partially overlapping at the apex and biseriate at the base,
Fungal Diversity (2011) 51:249–277
subcylindrical to ellipsoidal, with broadly to narrowly
rounded or tapered ends, brown to dark brown with a
greenish tint, 1-septate, constricted at the septum, the
upper cell often shorter and broader than the lower one,
smooth-walled.
Anamorph reported for genus: Fusicladium-like, Stigmina (Sivanesan 1984b).
Type species:
Acantharia echinata (Ellis & Everh.) Theiss. & Syd.,
Annls mycol. 16: 15 (1918).
(Fig. 3)
Fig. 3 Acantharia echinata
(from NY, holotype). a, b. Superficial ascoma gregarious on
the substrate surface. c. Section
of an ascoma. Note large heavily
pigmented thick-walled cells. df. Obclavate asci. g-i. Released
ascospores. Scale bars: a=5 mm,
b=0.5 mm, c=50 μm,
d-i=10 μm
257
≡ Dimerosporium echinatum Ellis & Everh., Erythea 1:
145 (1893).
Ascomata 70–157 μm high×115–186 μm diam., gregarious, forming densely crowded, orbicular patches of 3–
5 mm diam., superficial, globose, subglobose to ovate,
cupulate when dry, thickly clothed with opaque, black
setae, 70–110 μm long, 5–7 μm thick at the base (Fig. 3a,
b). Peridium 20–27.5 μm wide, up to 40 μm thick near the
base, comprising two-strata of cell types, outer layer
composed of 1–3 layers of large heavily pigmented thickwalled cells of textura angularis, cells 8–13 μm diam., cell
258
wall 1–4 μm thick, basal cells smaller and walls thicker;
inner layer composed of lightly pigmented cells of textura
angularis, up to 3×12 μm diam. (Fig. 3c). Hamathecium of
cellular pseudoparaphyses, 2–4 μm broad, embedded in
mucilage, evanescent in mature ascomata. Asci 65–100×
14–25 μm (x=80.8×19.6 μm, n=10), 8-spored, bitunicate,
fissitunicate, obclavate, without pedicel (Fig. 3d-f). Ascospores 17.5–22.5×9–12.5 μm (x=20.3×9.8 μm, n=10),
obliquely uniseriate and partially overlapping at the apex and
biseriate at centre or sometimes at the base, broadly cylindrical
to ellipsoidal with broadly to narrowly rounded or tapered
ends, brown to dark brown with greenish tint, 1-septate,
constricted at the septum, the upper cell often shorter and
broader than the lower one, smooth-walled (Fig. 3g-i).
Material examined: USA: California, Amador County,
Jackson, on living leaves of Quercus chrysolepis, leg. Geo.
Hansen, com. Marshall A. Howe (NY, holotype).
Anamorph: Fusicladium-like sp. (Sivanesan 1984b).
Note: The folicolous habitat, superficial, setose ascomata,
evanescent pseudoparaphyses, obclavate asci, and 1-septate,
brown and constricted ascospores are typical of Venturiaceae.
Acantharia arecae (Sivan., P.M. Kirk & Govindu) Yin.
Zhang & K.D. Hyde, comb. nov.
≡ Zeuctomorpha arecae Sivan., P.M. Kirk & Govindu, in
Sivanesan, Bitunicate Ascomycetes and their Anamorphs
(Vaduz): 572 (1984).
Material examined: INDIA: Shimogee, on Areca catechu
L. leaf, 1 Nov. 1979, H.C. Govindu (IMI 246067, holotype
of Zeuctomorpha arecae).
Anamorph: Acroconidiellina arecae (Sivanesan 1984a).
Note: The small-sized setose ascomata, obclavate to
obpyriform asci, asymmetrical pigmented ascospores of
Zeuctomorpha point to Acantharia (Sivanesan 1984b). The
anamorphic state of Zeuctomorpha (Acroconidiellina arecae)
is also comparable with that of Acantharia (Fusicladiumlike). Thus we treat Zeuctomorpha arecae here as a synonym
of Acantharia arecae. Similarly, Zeuctomorpha is treated as
a synonym of Acantharia. Zeuctomorpha arecae however,
differs in having a thickened ascal apex with a distinct ocular
chamber while its occurrence on palms is also contradictory
to the understanding of the Venturiaceae (Zhang et al. 2012).
Fresh collections and molecular study are needed to confirm
whether these genera are synonymous and whether Acantharia should be included in Venturiaceae.
Apiosporina Höhn., Sber. Akad. Wiss. Wien, Math.-naturw.
Kl., Abt. I 119: 439 (1910).
= Dibotryon Theiss. & Syd., Annls mycol.13: 663
(1915).
Generic description:
Habitat parasitic (or saprobic?) on leaves or stems of
dicotyledons. Ascomata small-sized, gregarious, superficial,
Fungal Diversity (2011) 51:249–277
globose to subglobose, developing on a hyphal mass, easily
removable from the substrate, small papillate and ostiolate.
Peridium thin, composed of several layers of heavily
pigmented thick-walled cells of textura angularis. Hamathecium of rare, septate, pseudoparaphyses. Asci 8-spored, bitunicate to narrowly obclavate, cylindrical, with a short, thick,
furcate or knob-like pedicel or pedicel lacking. Ascospores
biseriate and partially overlapping, ovoid to narrowly ovoid,
hyaline to pale brown, apiosporous, 1-septate near the lower
end, barely constricted at the septum, smooth-walled.
Anamorph reported for genus: Cladosporium sp. or
Fusicladium sp. (Sivanesan 1984a).
Type species:
Apiosporina collinsii (Schwein.) Höhn., Sber. Akad. Wiss.
Wien, Math.-naturw. Kl., Abt. I 119: 439 [47 repr.] (1910).
(Fig. 4)
≡ Sphaeria collinsii Schwein., Trans. Am. phil. Soc. 4:
211 (1832).
Ascomata 140–172 μm diam., gregarious, superficial,
globose to subglobose, developing on a hyphal mass, easily
removable from the substrate, black with rough and shiny
surface, papillate small and ostiolate (Fig. 4a). Peridium
20–33 μm wide, composed of 3–4 layers of heavily
pigmented thick-walled cells of textura angularis, cells 5–
10 μm diam., cell wall up to 2.5 μm thick, the innermost
layer cell-wall thinner. Hamathecium of rare, septate, 4–
6 μm broad pseudoparaphyses. Asci 63–77×8–10 μm (x=
70.9×9.3 μm, n=10), 8-spored, bitunicate, fissitunicate
dehiscence not observed, cylindrical to narrowly obclavate,
with a short, thick, knob-like pedicel or pedicel lacking
(Fig. 4b, c). Ascospores 12.5–15×5–6 μm (x=13.4×
5.3 μm, n=10), biseriate and partially overlapping, ovoid
to narrowly ovoid, hyaline, 1-septate, apiosporous, slightly
constricted at the septum, the upper cell often 4–5 times
longer and much broader than the lower one, smoothwalled (Fig. 4d).
Material examined: CANADA: Saskatchwan, on leaves
of Cotoneaster sp. (K(M):158702, ex herb. Broome).
Anamorph: Cladosporium sp. (Sivanesan 1984a).
Apiosporina morbosa (Schwein.) Arx, Acta bot. neerl. 3:
86 (1954).
(Fig. 5)
≡Dibotryon morbosum (Schwein.) Theiss. & Syd.,
Annls mycol. 13(5/6): 663 (1915).
≡ Sphaeria morbosa Schwein., Schr. naturf. Ges.
Leipzig 1: 40 (1822).
Ascomata densely developing in branches, erumpent and
form a swelling up to 1 cm thick, black, hard. Ascomata
160–230 μm high×170–250 μm diam., densely gregarious
on the surface of ascostromata, subglobose, triangular or
oblong, often flattened on the top, wall black (Fig. 5a, b).
Peridium 30–45 μm wide, 1-layered, composed of small
heavily pigmented thick-walled cells of textura angularis,
Fungal Diversity (2011) 51:249–277
259
Fig. 4 Apiosporina collinsii
((K(M):158702, ex herb.
Broome). a. Ascomata gregarious on the substrate surface. b.
Squash mounts with a large
number of asci. c. Cylindrical 8spored asci. d. Released ascospores. Scale bars: a=0.5 mm, b,
c=10 μm, d=5 μm
cells 3–7 μm diam., cell wall 2–4 μm thick, cells at the
base of the ascomata larger, up to 10 μm diam. (Fig. 5b).
Hamathecium of dense, 1.5–2(−3) μm broad, septate,
branched pseudoparaphyses (Fig. 5d). Asci 68–90×12.5–
15 μm (x= 73 × 13 μm, n = 10), 8-spored, bitunicate,
fissitunicate dehiscence not seen, subcylindrical or broadly
clavate, with a short, furcate pedicel which is 8–15 μm long,
with an inconspicuous ocular chamber (Fig. 5c). Ascospores
15–18(−19)×(5-)6–7.5 μm (x=17.4×6.8 μm, n=10), biseriate, clavate, apiosporous, tapered towards the base, apex
obtusely rounded, one septate near the lower end, barely
constricted at the septum, hyaline to pale brown, smoothwalled (Fig. 5e).
Material examined: USA: Pennsylvania, Bethlehem, in
Prunis cultis, Syn. #1416. leg. L.D. von Schweinitz s.n. Det.
L.D. von Schweinitz (PH-01048831, 01048832, 01048838,
01048839, 01048840, as Sphaeria morbosa Schw., syntype;
PH-01048834).
Anamorph: ?Fusicladium sp. (Sivanesan 1984a).
Note: The anamorphic state of A. collinsii was reported
as Cladosporium sp. (Sivanesan 1984a), which was
assigned to Fusicladium sensu lato by Braun et al. (2003).
A narrow concept of Fusicladium, however, is accepted
in this study. Dibotryon had been treated as a synonym of
Apiosporina (von Arx and Müller 1975; Barr 1968; Crous
et al. 2007a). Although the black knots on branches of
Prunis cultis formed by Dibotryon morbosum can be
readily distinguished from the black spots on leaves
formed by Apiosporina, their congeneric relationship
was confirmed by molecular data (Winton et al. 2007,
Figs. 1 and 2).
Caproventuria U. Braun, Monogr. Cercosporella, Ramularia Allied Genera (Phytopath. Hyphom.) 2: 396 (1998).
Generic description:
Habitat saprobic. Ascomata non-stromatic, subglobose,
ampulliform, obpyriform, urceolate, papillate, ostiolate,
pseudoparaphysate, membranaceous, dark, setose throughout. Setae dark brown, aseptate, simple or occasionally
forked, apex acute, smooth, wall thickened below, but thinwalled towards the apex. Peridium pseudoparenchymatous,
composed of angular to rounded, dark brown cells. Asci 8spored, bitunicate, numerous, subclavate to cylindrical.
Ascospores monostichous or distichous, ellipsoid-ovoid,
260
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Fig. 5 Dibotryon morbosa
(PH-01048831, syntype). a.
Ascomata densely gregarious on
the substrate surface. b. Section
of ascomata. c. Asci in pseudoparaphyses. d. Septate pseudoparaphyses. e. Released
apiosporous ascospores. Scale
bars: a=0.5 mm, b=100 μm, c,
d=10 μm
with a single submedian septum, mostly somewhat constricted at the septum, smooth, yellowish olivaceous (from
Braun 1998).
Anamorph reported for genus: Pseudocladosporium
(Braun et al. 2003).
Type species:
Caproventuria hanliniana (U. Braun & Feiler) U. Braun,
Monogr. Cercosporella, Ramularia Allied Genera (Phytopath. Hyphom.) 2: 396 (1998).
≡ Capronia hanliniana U. Braun & Feiler, Microbiol.
Res. 150: 90 (1995).
Anamorph: Pseudocladosporium brevicatenatum (U.
Braun & Feiler) U. Braun 1998.
Note: Braun (1998) treated Caproventuria as separate
genus from Venturia based on its saprobic life style and
Pseudocladosporium anamorphic state, compared to the
parasitic life style and Pollaccia or Spilocaea anamorphic
state possessed by Venturia sensu stricto. Crous et al.
(2007b), however, treated Pseudocladosporium as a synonym of Fusicladium sensu lato based on the combined LSU
and ITS nurDNA sequences comparison, and considered the
arrangement of the conidiophores (solitary, fasciculate,
sporodochial), the proliferation of conidiogenous cells
(sympodial, percurrent) and shape, size as well as formation
of conidia (solitary, catenate) to be of little taxonomic value
at generic level. This proposal, however, is not supported in
this study, as narrow generic concepts of Venturia and
Fusicladium are accepted here. In addition, according to our
multigene phylogenetic analysis, species of Caproventuria
and Tyrannosorus form a unambiguously supported clade
Fungal Diversity (2011) 51:249–277
separating from the clade Venturia sensu stricto. Based on
both the anamorph and molecular phylogeny, Caproventuria
is a well defined genus of Venturiaceae.
Coleroa Rabenh., Herb. myc., ed. 1no. 1456 (1850).
Generic description:
Habitat parasitic and saprobic on dicotyledons. Ascomata small-sized, scattered, or in small groups, superficial,
globose, subglobose, setae few to numerous, papillate, ostiolate. Peridium thin, composed of lightly pigmented thinFig. 6 Coleroa chaetomium
(L11558.38). a. Ascomata scattered on the substrate surface. b.
Section of an ascoma. c, d.
Somewhat obclavate, 8-spored
asci without pedicel. e. Released
ascospores. Scale bars: a=
0.5 mm, b=50 μm, c, d=10 μm,
e=5 μm
261
walled cells of textura angularis. Hamathecium ca. 2 μm
broad, evanescing. Asci 8-spored, bitunicate, fissitunicate,
fusiform to obclavate, with or without pedicel. Ascospores
ellipsoidal with broadly to narrowly rounded ends, pale brown
with greenish tint, 1-septate, constricted at the septum.
Anamorph reported for genus: none.
Type species:
Coleroa chaetomium (Kunze ex Fr.) Rabenh., Rabenh.
Krypt.-Fl., Edn 2 (Leipzig) 1:198 (1850). (Fig. 6)
262
≡ Dothidea chaetomium Kunze ex Fr., Syst. mycol.
(Lundae) 2: 563 (1823).
Ascomata 130–170 μm high×80–130(−160) μm diam.,
scattered, or in small groups of 2–4 with confluent peridium,
superficial, produced on thin subcuticular stroma, globose,
subglobose, wall black, setae few to numerous, septate or
non-septate, variable in length, up to 130 μm, 5–7 μm thick
near the base, reddish-brown, paler at the apex, ostiole short
(Fig. 6a). Peridium 15–25 μm wide, composed of lightly
pigmented thin-walled cells of textura angularis, cells 5–
12 μm diam., cell wall <1 μm thick (Fig. 6b). Hamathecium
ca. 2 μm broad, cellular, septate, usually evanescing in
mature ascomata. Asci 45–58 × 12–16 μm (x= 53.3 ×
13.5 μm, n=10), 8-spored, bitunicate, fissitunicate, fusiform
to obclavate, with or without pedicel, with an inconspicuous
ocular chamber (Fig. 6c, d). Ascospores 11–14(−17)×5.5–
6 μm (x=13.2×5.9 μm, n=10), obliquely uniseriate and
partially overlapping to biseriate in centre, ellipsoidal
with broadly to narrowly rounded ends, pale brown with
greenish tint, 1-septate, constricted at the septum, the
upper cell often longer and broader than the lower one,
verrucose (Fig. 6e).
Material examined: ITALY: Treviso, Bosco Montello, on
the leaf surface of Rubus caesius, Sept. 1876. P.A. Saccardo
(L11558.30 as Venturia kunzei Sacc.); ROMANIA: Plopeni,
on Rubus caesius L., Aug. 1971, leg. & det. G. Negrean
(L11558.4); on Rubus idaeus, leg. J. Smarods, 18 Oct. 1942
(L11558.16); L11558.39, as Dothidea chaetomium; on
leaves of Rubus sp., leg. Kretzschmar (L11558.38, as
Phacidium rubi Fries); 9 Oct. 1903, leg. G. Oertel.
(L11558.3).
Anamorph: none reported.
Note: The scattered, setose ascomata, deliquescing
pseudoparaphyses, fusoid to obclavate asci and the 1septate, constricted ascospores of Coleroa chaetomium
suggest an affinity to Venturiaceae.
Pseudoparodiella F. Stevens, Illinois Biol. Monogr.
(Urbana) 11: 166 (1927).
Generic description:
Habitat parasitic on leaf surface of dicotyledonous
plants. Ascomata small-sized, scattered or gregarious,
superficial, globose. Peridium thin, composed of a few
layers of lightly pigmented thin-walled cells of textura
angularis. Hamathecium of rare, 2–3 μm broad pseudoparaphyses. Asci 8-spored, bitunicate, fissitunicate dehiscence
not observed, obclavate, with a short, thick, knob-like
pedicel, with an ocular chamber. Ascospores biseriate and
partially overlapping, broadly fusoid to ellipsoidal with
broadly to narrowly rounded ends, olivaceous to pale
brown, 1-septate, constricted at the septum, the upper cell
slightly longer and broader than the lower one.
Anamorph reported for genus: none.
Fungal Diversity (2011) 51:249–277
Type species:
Pseudoparodiella vernoniae F. Stevens, Illinois Biol.
Monogr. (Urbana) 11: 166 (1927).
(Fig. 7)
Ascomata 80–130 μm diam., scattered or gregarious,
superficial, globose, easily removed from the substrate, wall
black, apex opening not observed (too small to see clearly)
(Fig. 7a). Peridium 10–15 μm wide, composed of 2–3
layers of lightly pigmented thin-walled cells of textura
angularis, cells 4–6 μm diam., cell wall 0.5–1 μm thick, up
to 2 μm thick at the outer layer (Fig. 7b). Hamathecium of
rare, 2–3 μm broad pseudoparaphyses. Asci 55–72×17–
22 μm (x=62.5×20.3 μm, n=10), 8-spored, bitunicate,
fissitunicate dehiscence not observed, obclavate, with a short,
thick, knob-like pedicel which is usually less than 10 μm
long, with an ocular chamber (Fig. 7c). Ascospores 16–19×
6–8 μm (x=17×7 μm, n=10), biseriate and partially overlapping, broadly fusoid to ellipsoidal with broadly to
narrowly rounded ends, olive pale brown, 1-septate, constricted at the septum, the upper cell slightly longer and
broader than the lower one, smooth-walled (Fig. 7d).
Material examined: SPAIN: Peralta, on leaves of
Vernonia canescens, 7 Dec. 1923, leg. & det. F.L. Stevens
(K(M):154549, holotype).
Anamorph: none reported.
Note: The small-sized ascomata produced on leaves of
dicotyledons, rare pseudoparaphyses, obclavate asci, 1-septate
olivaceous brown ascospores agree with Venturiaceae.
Metacoleroa Petr., Annls mycol. 25: 332 (1927).
Anamorph reported for genus: none.
Type species:
Metacoleroa dickiei (Berk. & Broome) Petr. [as ‘dieckiei’], Annls mycol. 25: 332 (1927).
≡ Sphaeria dickiei Berk. & Broome, Ann. Mag. nat.
Hist., Ser. 2 9: 317 (1852).
Material examined: UK: Carlton House, on leaves of
Linnaea borealis, 1827, Richardson (K(M): 143928;
syntype).
Anamorph: none reported.
Note: No mature ascoma were found on the specimen
examined. Based on DNA sequence analysis, Metacoleroa
clustered with Venturia sensu lato, thus was treated as
synonym (Crous et al. 2007a). However the phylogeny
presented in Crous et al. (2007a) was not well resolved and
our analysis did not resolve this either (Fig. 1). This
proposal needs further study.
Tyrannosorus Unter. & Malloch, Mycol. Res. 99(8): 910 (1995).
Generic description:
Habitat saprobic. Ascomata solitary, dark brown to
black, ovate to pyriform, ostiolate, covered with brown
setae. Peridium pseudoparenchymatous. Hamathecium trabeculate pseudoparaphyses. Asci bitunicate, saccate to
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263
Fig. 7 Pseudoparodiella vernoniae (K(M):154549, holotype).
a. Setose ascomata scattered on
the substrate surface. b. Section of
an ascoma c. Squash mounts with
two asci. d. Released, 1-septate
ascospores. Scale bars:
a=200 μm, b=20 μm, c,
d=10 μm
clavate with a thickened endotunica. Ascospores brown,
fusoid, 1-septate, indistinctly striate, each cell with 3–5
elongate germ slits (from Untereiner et al. 1995).
Anamorph reported for genus: Helicodendron (Untereiner
et al. 1995).
Type species:
Tyrannosorus pinicola (Petrini & P.J. Fisher) Unter. &
Malloch, Mycol. Res. 99(8): 910 (1995).
≡ Capronia pinicola Petrini & P.J. Fisher, Trans. Br.
mycol. Soc. 88(1): 68 (1987).
Anamorph: Helicodendron pinicola E. Müll., Petrini, P.
J. Fisher, Samuels & Rossman ex Voglmayr & P.J. Fisher,
Mycol. Res. 101(9): 1124 (1997).
Note: Tyrannosorus was separated from Capronia and was
introduced as a monotypic genus represented by T. pinicola
based on its helicosporous anamorph and longitudinally ridged
ascospores with multiple germ slits (Untereiner et al. 1995).
According to our molecular phylogenetic analysis based on
five genes, i.e. nuLSU, nuSSU, RPB1, 2 and TEF1,
Caproventuria hanliniana and C. hystrioides together with
Tyrannosorus pinicola form a unambiguously supported clade
separating from Venturia sensu stricto. Both Tyrannosorus and
Caproventuria share setose ascomata, 1-septate, brown or
yellowish olivaceous ascospores, which are typical of Venturiaceae. The helicosporous anamorph of Tyrannosorus pinicola
(Helicodendron pinicola) is quite different from the Pseudocladosporum anamorph of Caproventuria species. In addition,
the indistinctly striate ascospores with germ slits of Tyrannosorus pinicola are also quite different from species of
Caproventuria (Braun 1998; Untereiner et al. 1995). Thus
here we treat Caproventuria and Tyrannosorus as separate
genera of Venturiaceae.
Venturia Sacc., Syll. fung. (Abellini) 1: 586 (1882).
Generic description:
Habitat parasitic on dicotyledonous leaves. Ascomata
small-sized, solitary, scattered, or gregarious, initially immersed, becoming erumpent, globose, subglobose, wall black,
264
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papillate, ostiolate. Peridium thin, composed of a few layers of
pigmented cells of textura angularis. Hamathecium rare,
evanescent in mature ascomata. Asci 8-spored (rarely 4spored), bitunicate, fissitunicate dehiscence unknown, oblong
to obclavate, with a short, thick pedicel or pedicel lacking, with
an inconspicuous ocular chamber. Ascospores obliquely uniseriate and partially overlapping to biseriate, especially at the
base, ellipsoidal, with broadly rounded ends, pale brown, 1septate, slightly constricted at the septum, the upper cell shorter
than the lower one, smooth-walled.
Anamorph reported for genus: Spilocaea, Pollaccia (Barr
1968; Crous et al. 2007a; Sivanesan 1984a).
Type species:
Venturia inaequalis (Cooke) G. Winter, Hedwigia 36: 81
(1897) (Fig. 8)
≡ Sphaerella inaequalis Cooke, J. Bot. 4: 248 (1866).
Ascomata 90–180 μm high×90–200(−240) μm diam.,
solitary, scattered, or gregarious, initially immersed, becoming erumpent, globose, subglobose, wall black, ostiolate with a distinct papilla (Fig. 8a). Peridium 20–28 μm
wide, 1-layered, composed of (2-)3–4 layers of pigmented
cells of textura angularis, cells 5–10 μm diam., cell wall
0.8–1.5 μm thick (Fig. 8d). Hamathecium rare, ca. 2 μm
broad, evanescent in mature ascomata (Fig. 8e). Asci (53-)
Fig. 8 Venturia inaequalis (L 0054534, isotype of Didymosphaeria
inaequalis (Cooke) Nissl.). a. Ascostroma on the surface of substrate.
b, c. Ascus. d. Section of the peridium comprising a few layers of
texture of angularis cells. e. Decomposing pseudoparaphyses. f, g.
Ascospores with one septum. Scale bars: a=0.5 mm, b, c, e - g=
10 μm, d=20 μm
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70–90×9.5–14 μm (x=73.5×10.8 μm, n=10), 8-spored
(rarely 4-spored), bitunicate, fissitunicate dehiscence not
observed, oblong to obclavate, with a short, thick pedicel or
pedicel lacking, with an inconspicuous ocular chamber
(Fig. 8b, c). Ascospores 13–17×6–8 μm (x=14.8×7.2 μm,
n=10), obliquely uniseriate and partially overlapping to
biseriate, especially at the base, ellipsoidal, with broadly
rounded ends, pale brown, 1-septate, slightly constricted at
the septum, the upper cell shorter than the lower one (4:5-)
2:3(−1:2), smooth-walled (Fig. 8f, g).
Material examined: CZECH REPUBLIC: Brno
(‘Brünn’), on leaves of Sorbus torminalis (Rosaceae).
Niessl s.n., Mar. 1913, distributed in Rabenhorst, Fungi
Europaei 2663, leg. de Niessl (L 0054534, isotype of
Didymosphaeria inaequalis (Cooke) Nissl.).
Anamorph: Spilocaea pomi (Schubert et al. 2003).
Note: A relatively broad concept for Venturia was adopted
by Sivanesan (1977), who considered the genus to comprise
species having separate or aggregated ascomata with or
without stroma, or forming below a blackened clypeus,
symmetrical or asymmetrical, olive green, pale brown or dark
brown ascospores and being parasitic on leaves or stems of
dicotyledons. DNA sequence analysis had indicated that
species of Venturia clustered together with Apiosporina
collinsii, Caproventuria hanliniana and Metacoleroa dickiei,
and thus Caproventuria and Metacoleroa were treated as
synonyms of Venturia (Crous et al. 2007a), although their
ecological, morphological or anamorphic states are distinct
from each other (see the key of genera). This proposal,
however, needs further consideration and study. Herein we
apply a narrower generic concept for Venturia, which
comprises parasitic species closely related to the generic type
of Venturia (V. inaequalis).
Other genera included in Venturiales
Based on morphology, the genera Arkoola, Atopospora,
Botryostroma, Lasiobotrys, Rhizogene, Trichodothella and
Trichodothis may be related to Venturiaceae. Thus we provisionally include them in Venturiaceae, but their ordinal and/or
familial status needs confirmation based on DNA sequence data.
Arkoola J. Walker & Stovold, Trans. Br. mycol. Soc. 87: 28
(1986).
Anamorph reported for genus: none.
Type species:
Arkoola nigra J. Walker & Stovold, Trans. Br. mycol. Soc.
87: 29 (1986).
Anamorph: none reported.
Note: The superficial, setose ascomata produced on mycelium
and greenish-brown, asymmetrical, thin-walled ascospores fit
Venturiaceae well. The large-sized ascomata, cylindrical asci
and short pedicels of Arkoola however, differ from other
genera of Venturiaceae (Walker and Stovold 1986).
265
Atopospora Petr., Annls mycol. 23: 100 (1925).
Anamorph reported for genus: ?Didymochora
(Sivanesan 1984a).
Type species:
Atopospora betulina (Fr.) Petr., Annls mycol. 23: 101 (1925).
≡ Xyloma betulinum Fr., Observ. mycol. (Havniae) 1:
198 (1815).
Anamorph: ?Didymochora betulina (Sivanesan 1984a).
Note: The multiloculate ascostromata, fusoid asci and
lightly pigmented, biseriate, apiosporous ascospores suggest an affinity to Venturiales (Müller and von Arx 1962).
Botryostroma Höhn., Sber. Akad. Wiss. Wien, Math.naturw. Kl., Abt. 1 120: 424 [46 repr.] (1911).
Anamorph reported for genus: none.
Type species:
Botryostroma inaequale (G. Winter) Höhn. [as ‘inaequalis’], Sber. Akad. Wiss. Wien, Math.-naturw. Kl., Abt. 1
120: 425 [47 repr.] (1911).
≡ Lizonia inaequalis G. Winter, Hedwigia 22: 261
(1883).
Anamorph: none reported.
Note: The ascomata of Botryostroma inaequale are
produced under a clypeus, with numerous persistent
pseudoparaphyses among asci. All these characters do not
fit Venturiales. However, the obclavate or fusiform asci,
lightly pigmented, apiosporous ascospores suggest an
affinity to Venturiales (Müller and von Arx 1962).
Lasiobotrys Kunze, in Kunze & Schmidt, Mykologische
Hefte (Leipzig) 2: 88 (1823).
Anamorph reported for genus: none.
Type species:
Lasiobotrys lonicerae Kunze, in Fries, Syst. mycol.
(Lundae) 2: 88 (1823).
Anamorph: none reported.
Note: The most striking morphological character of
Lasiobotrys is its ascomata produced among hyphae under
a stromatal disc (forming a “roof-like” structure) (see
Müller and von Arx 1962). The apiosporous, lightly
pigmented ascospores, subclavate to obclavate asci are
comparable with taxa of Venturiales.
Rhizogene Syd. & P. Syd., Annls mycol. 18: 181 (1921) [1920].
Anamorph reported for genus: none.
Type species
Rhizogene symphoricarpi (Syd. & P. Syd.) Syd. & P. Syd.,
Annls mycol. 18: 181 (1921) [1920].
≡ Lasiobotrys symphoricarpi Syd. & P. Syd., Annls
mycol. 16: 244 (1918).
Anamorph: none reported.
Note: Ascomata of Rhizogene symphoricarpi are produced radially around the circumference of the stromatal
266
disc, which is covered with short setae. The subclavate to
somewhat obclavate asci and lightly pigmented, submedianly 1-septate ascospores are comparable with Venturiales (Müller and von Arx 1962).
Trichodothella Petr., in Blumer, Ergebn. wiss. Unters.
schweiz. NatnParks, N.S. 14: 37 (1946).
Anamorph reported for genus: none.
Type species:
Trichodothella blumeri Petr. ex S. Blumer, Ergebn. Wiss.
Unters. Schweiz. Natn Parks, N.S. 14: 37 (1946).
Anamorph: none reported.
Note: Considering the position of ascomata on the
ascostromata, Trichodothella is a “transition” genus—the
ascomata of which are produced radially around the
circumference of the stromatal disc, but under the hyphae
around the ascostromata (Müller and von Arx 1962).
Trichodothis Theiss. & Syd., Annls mycol. 12: 176 (1914).
Generic description:
Habitat saprobic or parasitic? on leaf surface of dicotyledonous. Ascostromata medium-sized, solitary, scattered, or in
small groups, superficial, multilocular, discoid, with straight
or flexuous aggregations of hairs sticking together and
forming stellate projections around the ascostroma. Locules
small-sized, globose to subglobose, forming one layer within
the ascostroma. Peridium one layered, lower peridium
composed of light pigmented cells of textura angularis,
upper peridium composed of more heavily pigmented thickwalled cells of textura angularis. Hamathecium of dense,
cellular pseudoparaphyses, septate, hyaline. Asci 8-spored,
bitunicate, fissitunicate dehiscence not observed, saccate,
without pedicel. Ascospores 3-4-seriate, broadly ellipsoidal
with broadly rounded ends, hyaline and becoming pale
brown when old, 1-septate, slightly constricted at the septum.
Anamorphs reported for genus: none.
Type species:
Trichodothis comata (Berk. & Ravenel) Theiss. & Syd.,
Annls mycol. 12: 176 (1914).
(Fig. 9)
≡ Asterina comata Berk. & Ravenel, Grevillea 4 (no.
29): 10 (1875).
Ascostromata 72–157 μm high×243–529 μm diam.
(excluding the stellate aggregations), solitary, scattered, or
in small groups, superficial, multilocular, discoid, with
straight or flexuous, septate, dark brown aggregations of
hairs sticking together and forming stellate projections
around the ascostromata, projections black, cylindrical, 6–
8 μm broad. Locules 60–95 μm high×75–115 μm diam.,
globose to subglobose, forming a single layer within
ascostromata, and extending as far as 100–214 μm out of
the edge of ascostromata (Fig. 9a, c). Peridium 28–42 μm
wide, one layered, lower peridium composed of light
pigmented cells of textura angularis, cells 5–9 μm diam.,
cell wall 1.5–2.5 μm thick, apex cells smaller and walls
Fungal Diversity (2011) 51:249–277
thicker, upper peridium composed of more heavily pigmented thick-walled cells of textura angularis (Fig. 9b, d,
e). Hamathecium of dense, cellular pseudoparaphyses, ca.
2.5–4 μm diam., septate, hyaline (Fig. 9e, f). Asci 55–70×
15–22 μm, 8-spored, bitunicate, fissitunicate dehiscence
not observed, saccate, without pedicel, ocular chamber not
observed (Fig. 9g). Ascospores 14–23×6.5–10.5 μm, 3–4
seriate, broadly ellipsoidal with obtusely rounded ends,
hyaline and becoming pale brown when old, 1-septate,
slightly constricted at the septum, smooth-walled (Fig. 9h).
Material examined: USA: South Carolina, Santee
Canal, on Magnolia grandiflora leaf, 1819; leg. H.W.
Ravenel (K(M): 143933, ex herb. Berkeley, syntype).
Anamorph: none reported.
Note: Trichodothis comata is characterized by its
ascostromata covered by dark brown hairs, broad pseudoparaphyses, saccate asci and hyaline, 1-septate ascospores
(Müller and von Arx 1962, Fig. 9). Trichodothis is most
comparable with Lasiobotrys, Rhizogene and Trichodothella, which have ascomata beneath or radially around the
circumference of the stromatal disc (Müller and von Arx
1962). All these characters make it difficult to be assigned
Trichodothis in a family or even order. Because the
morphology of asci and ascospores are most comparable
with Venturiales, we questionably accept it in Venturiales,
until further molecular phylogenetic result is available.
Genera excluded from Venturiales
Crotone, Polyrhizon, Lineostroma, Phragmogibbera,
Platychora, Phaeocryptopus, Rosenscheldiella, Uleodothis
and Xenomeris do not share common ancestry with
Venturiales based either on recent DNA sequence analyses
or on morphological characters. Thus they are excluded
from this order.
Crotone Theiss. & Syd., Annls mycol. 13: 629 (1915).
Generic description:
Habitat saprobic on lower surface of leaves of dicotyledons. Ascostromata large-sized, solitary, scattered, or in
small groups, erumpent to nearly superficial, with basal
wall remaining immersed in host tissue, flat globose to
subglobose. Locules small-sized, globose to subglobose,
forming one layer near the surface of ascostromata, area
between locules of ascostromata filled with heavily pigmented, thick-walled cells of textura angularis. Peridium
composed of heavily pigmented, thick-walled cells of
textura angularis, cells of ascostromata larger, hyaline and
walls thinner. Hamathecium appears to lack pseudoparaphyses. Asci 8-spored, bitunicate, broadly subclavate to
obclavate, without pedicel. Ascospores uniseriate, biseriate
to 4-seriate, broadly clavate, narrowly fusoid to fusoid with
broadly to narrowly rounded ends, brown, 1-septate,
constricted at the septum, the upper cell often longer and
broader than the lower one, rough-walled.
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267
Fig. 9 Trichodothis comata (K
(M): 143933, syntype). a. An
flattented ascostroma on the
substrate surface. b, c. Section
of a partial ascostroma. d, e.
Section of a partial peridium
comprising a few layers of
texture of angularis cells. f.
Pseudoparaphyses with
immature asci. g. Ascus.
h. Released 1-septate ascospore.
Scale bars: a=0.5 mm, b,
c=100 μm, d-f=50 μm, g,
h=20 μm
Anamorph reported for genus: none.
Type species:
Crotone drimydis (Lév.) Theiss. & Syd., Annls mycol. 13:
629 (1915).
(Fig. 10)
≡ Dothidea drimydis Lév. [as ‘drymidis’], Annls Sci.
Nat., Bot., sér. 3 3: 55 (1845).
Ascostromata 230–570 μm high×615–915 μm diam.,
solitary, scattered, or in small groups of 2–4, erumpent to
nearly superficial, with basal wall remaining immersed in
host tissue, flat globose to subglobose, wall black,
roughened, usually ornamented with some white collared
ornaments (Fig. 10a). Locules 75–90 μm diam., globose to
268
Fungal Diversity (2011) 51:249–277
Fig. 10 Crotone drymidis (K(M): 143929, syntype). a. Ascostroma on the host surface. b. Section of a partial ascostroma. c. Dehiscent ascus. d.
Squash mounts with several asci. e, h. Released ascospores. f, g. Ascus. Scale bars: a=0.5 mm, b, d=100 μm, c, f, g=20 μm, e, h=10 μm
subglobose, forming one layer near the surface of
ascostromata, area between locules of ascostromata
filled with heavily pigmented thick-walled cells of
textura angularis, up to 10 μm diam., cell wall 3–5 μm
thick (Fig. 10b). Peridium 35–80 μm wide on the surface
part of ascostromata, composed of heavily pigmented
thick-walled cells of textura angularis, cells up to 10×
3.8 μm diam., cell wall 2–5 μm thick, cells of ascostromata larger, hyaline and walls thinner (Fig. 10b).
Hamathecium appears to lack pseudoparaphyses. Asci
55–105 × 10–17.5 μm (x= 79.2 × 13.5 μm, n = 10), 8spored, bitunicate, broadly subclavate to obclavate,
without pedicel, ocular chamber not seen (Fig. 10c, d,
f, g). Ascospores 17.5–25 μm×4.5–7.5 μm (x=20.4×
5.5 μm, n=10), uniseriate, biseriate to 4-seriate, narrowly
clavate, narrowly fusoid to fusoid with broadly to
narrowly rounded ends, brown, 1-septate, constricted at
the septum, the upper cell often longer (ca. 2-times) and
broader than the lower one, rough-walled (Fig. 10e, h).
Material examined: CHILE: on the lower side of the
leaves of Drymidis chilensis, 1841 (K(M): 143929, ex herb.
Berkeley, syntype).
Anamorph: none reported.
Note: Locules of Crotone drimydis are arranged in a
layer in the hemispherical ascostromata, which forms on the
lower surface of Drymidis chilensis leaves. The genus may
belong in Dothideaceae, Elsinoaceae or Myrangiaceae,
families in which taxa form in ascostromata with ascomata
as a single layer. The saccate asci in the Elsinoaceae or
Myrangiaceae are somewhat comparable with those of
Crotone drimydis.
Gibbera Fr., Syst. orb. veg. (Lundae) 1: 110 (1825).
Anamorphs reported for genus: Dictyodochium, Stigmina-like and Virgariella (Sivanesan 1984a, b).
Type species:
Gibbera vaccinii (Sowerby) Fr., Summa veg. Scand.,
Section Post. (Stockholm): 412 (1849).
Fungal Diversity (2011) 51:249–277
≡ Sphaeria vaccinii Sowerby, Col. fig. Engl. Fung.
Mushr. 3: 156, tab. 373:1 (1803).
Anamorph: none reported.
Note: The narrowly fusoid ascospores, asci with furcate
pedicel as well as its Dictyodochium, Stigmina-like and
Virgariella anamorphic states (Sivanesan 1984a, b) all
refute its placement within Venturiales. Barr (1968) has
considered Gibbera comparable with Phaeocryptopus and
Xenomeris, as they all have “erumpent basal stroma bearing
the ascostromata which do not form superficial mycelium”.
Both Phaeocryptopus and Xenomeris have been assigned to
Capnodiales (Schoch et al. 2009; Winton et al. 2007), thus
Gibbera may also be closely related to Capnodiales. Based
on the mulitigene phylogenetic analysis, G. conferta nested
within the clade of Venturiales, while G. rosea clustered
within Helotiales (class Leotiomycetes) (Crous et al.
2007a). No firm conclusion can be reached, however, until
it is possible to analyse DNA sequences of the type species,
G. vaccinii.
Platychora Petr., Annls mycol. 23(1/2): 102 (1925)
Anamorph reported for genus: ? Piggotia (Hyde et al.
2011).
Type species:
Platychora ulmi Duval, Bot. Taschenbuch 6: 105 (1795).
Anamorph: unknown.
Note: The fusoid hyaline apiosporous ascospores of
Platychora ulmi are comparable with Dibotryon and
Apiosporina, but its gregarious ascomata, which are
immersed at first, then becomes erumpent to superficial,
are quite different from other genera in Venturiaceae. Based
on molecular phylogenetic data, Platychora ulmi should
reside within the family of Didymellaceae, Pleosporales
(Zhang et al. 2009, Fig. 1).
Polyrhizon Theiss. & Syd., Annls mycol. 12: 281 (1914).
Generic description:
Habitat saprobic on leaves of dicotyledons. Ascostromata
producing round, black spots in leaves. Ascomata
gregarious in the ascostromata, immersed to erumpent,
globose, subglobose, or broadly conical. Peridium 1layered, composed of small, lightly pigmented, thickwalled cells of textura prismatica. Hamathecium of dense,
long cellular pseudoparaphyses, anastomosing and
branching between and above the asci. Asci 8-spored,
bitunicate, fissitunicate, cylindrical to fusoid, with a short
furcate pedicel, which is less than 10 μm long, with a
small ocular chamber. Ascospores biseriate, broadly fusoid
to subclavate with broadly to narrowly rounded ends,
reddish brown, 1-septate, constricted at the septum, the
upper cell often broader and shorter than the lower one,
baculate.
Anamorph reported for genus: none.
269
Type species:
Polyrhizon terminaliae (Syd.) Syd., Annls mycol. 12: 281
(1914). (Fig. 11)
≡ Dothidea terminaliae Syd., in Sydow & Butler, Annls
mycol. 9: 401 (1911).
Ascostromata producing round, black spots in leaves,
spots up to 2.5–3 mm. Ascomata 150–260 μm high×(90-)
150–280 μm diam., gregarious in ascostromata, immersed
to erumpent, globose, subglobose, or broadly conical
(Fig. 11a). Peridium 10–20 μm wide laterally, up to
45 μm thick at the apex, thinner at the base, single layered,
composed of small lightly pigmented thick-walled cells
of textura prismatica, ca. 2×5 μm diam., cells more
heavily pigmented near apex and hyaline in the base.
Hamathecium of dense, long cellular pseudoparaphyses,
2–3 μm broad, anastomosing and branching between and
above the asci. Asci (39-)50–67×10–16 μm (x=52.1×
11.7 μm, n=10 μm), 8-spored, bitunicate, fissitunicate
cylindrical to fusoid, with a short furcate pedicel which is
less than 10 μm long, with a small ocular chamber (to
3 μm wide×2 μm high) (Fig. 11c, d). Ascospores 24–28×
7.5–10 μm (x= 25.1 × 8.5 μm, n = 10 μm), biseriate,
broadly fusoid to subclavate with broadly to narrowly
rounded ends, reddish brown, 1-septate, constricted at the
septum, the upper cell often broader and shorter than the
lower one, baculate (Fig. 11b).
Material examined: INDIA: Wynaad, Cataffa, on the
upper surface of leaves of Terminalia catapha, 14 Nov.
1909, leg. W. Mc Rae (S reg. nr F8238, as Dothidea
terminaliae, holotype).
Anamorph: none reported.
Note: The persistent cellular pseudoparaphyses, broadly
clavate asci with short furcate pedicels, and the almost
median septate, baculate ascospores of Polyrhizon terminaliae refute those of Venturiales, but fit Pleosporineae
(Pleosporales). Further study is needed for confirmation of
its ordinal or familial status.
Lineostroma H.J. Swart, Trans. Br. mycol. Soc. 91: 464 (1988).
Generic description:
Habitat necrotrophic parasitic on Banksia. Ascostromata
linear, solitary, scattered, initially immersed, becoming
erumpent. Ascomata linearly arranged in ascostromata,
wall black, roughened, globose, subglobose to triangular.
Peridium thickness uneven, usually thinner at the base, 1layered, composed of brown-walled cells of textura
angularis. Hamathecium of long trabeculate pseudoparaphyses. Asci 8-spored, bitunicate, fissitunicate, subcylindrical to obclavate, with a short pedicel. Ascospores
broadly fusoid to oblong, with broadly to narrowly
rounded ends, dark brown, 1-septate, constricted at the
septum.
Anamorph reported for genus: none.
270
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Fig. 11 Polyrhizon terminaliae
(S reg. nr F8238, holotype). a.
A cluster of ascomata on the
substrate surface. b. Released
ascospores. c, d. Asci with short
furcate pedicels. Scale bars:
a=0.5 mm, b-d=10 μm
Type species:
Lineostroma banksiae (Cooke) H.J. Swart, Trans. Br.
mycol. Soc. 91: 464 (1988). (Fig. 12)
≡ Didymosphaeria banksiae Cooke, Grevillea 19: 90
(1890).
Ascostromata linear, 600–860 μm long, 140–240 μm
broad, 55–115 μm high, solitary, scattered, initially immersed,
becoming erumpent, with up to 15 locules (Fig. 12a).
Ascomata 110–165 μm high×90–215 μm diam., linearly
arranged in ascostromata, wall black, roughened, globose,
subglobose to triangular (Fig. 12a, b, c). Peridium 13–40 μm
wide, thickness uneven, usually thinner at the base, 1-layered,
composed of brown-walled cells of textura angularis, sides
and apex cells 2.5–5×2.5–9 μm diam., cell wall 1–2 μm
thick, base cells smaller and walls thicker (Fig. 12b). Hamathecium of <1 μm broad, dense, long trabeculate pseudoparaphyses. Asci 50–65×7–8.5 μm, 8-spored, bitunicate, fissitunicate,
subcylindrical to obclavate, with a short pedicel, 6.5–9 μm
long. Ascospores (10-)14-17.5×5–7.5 μm, uniseriate and
partially overlapping to biseriate near the base, broad fusoid
to oblong, with broadly to narrowly rounded ends, dark brown,
1-septate, constricted at the septum (Fig. 12d-g).
Material examined: AUSTRALIA: Victoria, on leaves
Banksia sp. leg. Martin (K(M): 143926, syntype).
Anamorph: none reported.
Note: The linearly arranged ascomata, persistent pseudoparaphyses as well as the nearly symmetrical, 1-septate
ascospores indicated that is should be a species of
Pleosporineae (Pleosporales). Lineostroma banksiae is
one of the most common ascomycetes found on leaves of
Banksia in Australia (Swart 1988).
Phragmogibbera Samuels & Rogerson, Mem. N. Y. bot.
Gdn 64: 178 (1990).
Generic description:
Habitat fungicolous on Xylariaceae. Ascostromata
erumpent from ostioles of host Xylaria, turbinate. Ascomata
globose, wall black, carbonaceous, non papillate, ostiolate
not sure. Peridium tissue continuous with the stroma, 2layered. Hamathecium of rare, septate pseudoparaphyses.
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271
Fig. 12 Lineostroma banksiae (K(M): 143926, syntype). a. Linear ascostroma on the host surface. b, c. Section of ascomata. d-g. Released
ascospores. Scale bars: a=0.5 mm, b, c=100 μm, d-g=10 μm
Asci 8-spored, bitunicate, fissitunicate dehiscence not
observed, broadly cylindrical to narrowly clavate, with a
conspicuous ocular chamber. Ascospores partially to completely biseriate, narrowly curved, fusoid, end cells colourless and central cells brown, multi-septate, constricted at
each septum.
Anamorph reported for genus: Stigmina-like (Samuels
and Rogerson 1990).
Type species:
Phragmogibbera xylariicola Samuels & Rogerson, Mem.
N. Y. bot. Gdn 64: 178 (1990).
(Fig. 13)
Ascostromata erumpent from ostioles of host Xylaria,
turbinate, ca. 300 μm high×400 μm wide, comprising at
first a hemisphaerical, brown head of conidia on a short,
black stipe; ascomata ultimately forming in groups of 5–7
around the periphery of the stipe below the conidial
hymenium after the cessation of conidial production. Medulla
of stroma consisting of a central, obpyramidal core of
colourless hyphal elements surrounded by colourless to pale
yellow, pseudoparenchymatous cells measuring ca. 7.5 μm
across, and an outer layer ca. 25 μm thick of dark brown to
black, KOH blue-green pseudoparenchyma (Fig. 13a). Ascomata globose, wall black, roughened to nearly smooth,
carbonaceous, non papillate, becoming slightly umbilicate or
not collapsed when dry, method of opening of mature
ascomata not observed, arising as outgrowths of the
stromatal tissue, ascomatal wall ca. 75 wide, tissues
continuous with the stroma. Peridium tissue continuous with
the stroma, ca. 75 μm wide, 2-layered (Fig. 13b). Hamathecium of rare, 1–1.5 μm broad, septate pseudoparaphyses.
Asci 125–175×12–22 μm, 8-spored, bitunicate, fissitunicate
dehiscence not observed, broadly cylindrical to narrowly
clavate, with a conspicuous ocular chamber (Fig. 13c).
Ascospores 32–39×5–7.5(−10) μm (x=35×6 μm, n=10),
partially to completely biseriate, narrowly curved fusoid, end
cells colourless and central cells brown, 3-septate, constricted
at each septum, smooth-walled (Fig. 13d).
Anamorph: Stigmina-like (Samuels and Rogerson
1990).
Cells at upper surface of stroma producing conidiophores. Conidiophores pale brown, septate, sparingly
branched, each branch terminating in a single conidium
272
Fungal Diversity (2011) 51:249–277
Fig. 13 Phragmogibbera
xylariicola (NY Gary J.
Samuels 1238, isotype). a.
Ascostromata erumpent from
ostiole of Xylaria. b. Section of
a partial ascostroma. c. Clavate
immature asci. d. Narrowly
fusoid ascospores. Note the
hyaline end cells. Scale bars:
a=0.5 mm, b=100 μm, c,
d=10 μm
and proliferating percurrently, eventually ca. 100 μm long,
3–5 μm wide. Conidia cylindrical to narrowly clavate, 25–
42 × 7.5–11.2 μm, (1-)2–3 distoseptate, dark brown,
smooth, with a torn, circular basal abscission scar.
Material examined: VENEZUELA: Cerro de la Nelina,
summit camp #5, valley at north base of Pico Phelps, 1000–
1,250 m, 00º49′N, 66º00′W, cloud forest, on Xylaria
schweinitzii ?, 12–13 Apr. 1984 (NY Gary J. Samuels
1238, isotype).
Note: The narrowly fusoid, 3-septate ascospores, clavate asci with a furcate pedicel all refute its placement
within Venturiales. We assign it to Dothideomycetes
incertae sedis.
Phaeocryptopus Naumov, Bull. Soc. mycol. Fr. 30: 424 (1915).
Anamorph reported for genus: none.
Type species:
Phaeocryptopus abietis Naumov, Bull. Soc. mycol. Fr. 30:
424 (1914).
Anamorph: none reported.
Note: Phylogenetic analysis indicates that Phaeocryptopus nudus nested within Dothideales and P. gaeumannii
within Mycosphaerellaceae (Winton et al. 2007). Both of
taxa however, are not the generic types. Thus the ordinal or
familial status of Phaeocryptopus awaits molecular phylogenetic studies on P. abietis.
Rosenscheldiella Theiss. & Syd., Annls mycol. 13: 645 (1915).
Generic description:
Habitat parasitic? on leaves of dicotyledons. Ascomata
tightly clustered on the surface of substrate, small-sized,
superficial, globose, subglobose, wall black, roughened,
ostiolate. Peridium 1-layered, composed of heavily pigmented thick-walled cells of textura angularis. Hamathecium composed of evanescing pseudoparaphyses. Asci 8spored, bitunicate, fissitunicate obclavate, with a short,
thick pedicel. Ascospores tri-seriate near the base, ellipsoidal to fusoid with broadly rounded ends, hyaline, 1septate, septum median to submedian, constricted at the
septum.
Fungal Diversity (2011) 51:249–277
273
Fig. 14 Rosenscheldiella styracis (S reg. nr F7328, lectotype).
a. Ascomata clustered on the
host surface. b, e. Squash
mounts with a large number of
asci. c. Section of partial peridium. d. Obclavate ascus. f.
Released ascospores. g. Broken
ascus with spores releasing.
Scale bars: a=1 mm,
b-e=20 μm, f, g=10 μm
Anamorph reported for genus: none.
Type species:
Rosenscheldiella styracis (Henn.) Theiss. & Syd., Annls
mycol. 13: 645 (1915).
≡ Naemacyclus styracis Henn., Hedwigia 48: 8 (1908).
(Fig. 14)
Ascomata tightly clustered on the surface of substrate,
cluster 0.8–1.6 mm diam., single ascoma 155–200 μm
high×120–150 μm diam., superficial, globose, subglobose,
wall black, roughened, ostiolate (Fig. 14a). Peridium 25–
30 μm wide laterally, single layered, composed of heavily
pigmented thick-walled cells of textura angularis, cells 5–
274
6×5–9 μm diam., cell wall 1.5–3.5 μm thick (Fig. 14c).
Hamathecium of evanescing pseudoparaphyses. Asci 75–90
(−105)×17.5–22.5 μm, 8-spored, bitunicate, fissitunicate,
obclavate, with a short, thick pedicel which is ca. 5 μm
long, with a small ocular chamber and an small apical
apparatus (to 0.5 μm wide×2 μm high) (Fig. 14b, d, e).
Ascospores 25–33×7.5–10 μm, tri-seriate near the base,
ellipsoidal to fusoid with broadly rounded ends, hyaline, 1septate, constricted at the septum, the upper cell often
broader and shorter than the lower one, verrucose
(Fig. 14f).
Material examined: BRAZIL: S. Paulo, Morro Pellado,
on leaves of Styrax sp., July 1904, Puttemans (S reg. nr
F7328, lectotype).
Anamorph: none reported.
Note: Based on the DNA sequence analysis R. brachyglottidis and R. korthalsellae are members of the Mycosphaerellaceae sensu Crous et al. (2007a) (Sultan et al. 2011).
Uleodothis Theiss. & Syd., Annls mycol. 13: 305 (1915).
Anamorph reported for genus: none.
Type species:
Uleodothis balansiana (Sacc., Roum. & Berl.) Theiss. &
Syd., Annls mycol. 13: 305 (1915).
≡ Plowrightia balansiana Sacc., Roum. & Berl., Revue
mycol., Toulouse 7: 157 (1885).
Anamorph: none reported.
Note: Uleodothis had been assigned to Mycosphaerellaceae
(Pseudosphaeriales) by Müller and von Arx (1962). Luttrell
(1973) assigned it to Venturiaceae. Its ascomata immersed in
ascostromata, persistent pseudoparaphyses, cylindrical asci and
hyaline ascospores are atypical of genera in Venturiales.
Xenomeris Syd., in Sydow & Werdermann, Annls mycol.
22: 185 (1924).
Anamorphs reported for genus: ?Sclerophoma and
Hormonema (Sivanesan 1984a).
Type species:
Xenomeris pruni Syd., Annls mycol. 22: 185 (1924).
Anamorphs: ?Sclerophoma sp. and Hormonema sp.
(Sivanesan 1984a).
Note: Molecular phylogenetic analysis indicated that
Xenomeris raetica and X. juniperi (Sthughesia juniperi?)
belong to Capnodiales (Winton et al. 2007). However,
neither of these species are the generic type.
Discussion
Phylogeny
The phylogenetic analysis of the present study affirmed the
polyphyletic nature of Venturiaceae sensu Barr (1979).
Fungal Diversity (2011) 51:249–277
Phaeocryptopus gaeumannii, P. nudus, Xenomeris juniperi
and X. raetica resided in Capnodiales (Schoch et al. 2009;
Winton et al. 2007). According to the present molecular
phylogeny (Fig. 1), core taxa of Venturiaceae, i.e. Apiosporina, Caproventuria, Dibotryon, Metacoleroa and Venturia, form a well-supported monophyletic group, and
placed as a distinct lineage, separate from Botryosphaeriales, Jahnulales, Dothideomycetidae and Pleosporomycetidae. Our second, more limited phylogenetic analysis using
only LSU data corroborates the combined 5-gene data set
(Fig. 2). Similar results were obtained by some recent
phylogenetic studies (Crous et al. 2007a; Kodsueb et al.
2006; Kruys et al. 2006; Winton et al. 2007). Thus a new
order of Dothideomycetes—Venturiales is introduced in this
study to accommodate Venturia s. str. and its aggregates.
Venturia sensu Sivanesan (1977) accommodates a large
number of species (250, http://www.mycobank.org/Myco
Taxo.aspx, June/2011). The generic types of Caproventuria
(C. hanliniana) and Metacoleroa (M. dickiei) clustered in
the Venturia clade, which was subsequently treated as
synonyms of Venturia by Crous et al. (2007a). Caproventuria was primarily distinguished from Venturia based on
its distinct Pseudocladosporium anamorphs as well as its
saprobic life style (Braun et al. 2003). The well-developed
subiculum of Metacoleroa and the apiosporous ascospores
of Apiosporina (incl. Dibotryon) readily distinguish them
from Venturia. We thus choose to retain them as separate
genera from Venturia, and to apply a narrower generic
concept for Venturia than used in the past.
Phaeocryptopus nudus clustered in the Dothideales, and
P. gaeumannii and Xenomeris raetica in the Capnodiales as
reported previously (Crous et al. 2007a; Schoch et al. 2009;
Winton et al. 2007). However, these assignments are not
based on the study of generic types. Some of the previous
phylogenetic studies based on nuSSU rDNA sequence
showed inconsistent placement of Venturia liriodendri,
such as grouping with Curreya pityophila (Silva-Hanlin
and Hanlin 1999; Olivier et al. 2000) or with Phaeodothis
winteri (Eriksson and Hawksworth 2003). When mature,
Venturia liriodendri has abundant pseudoparaphyses and
pale-brown ascospores, instead of the deliquescing pseudoparaphyses and greenish ascospores of typical Venturia
spp. (Hanlin 1987). It appears, therefore, that Venturia
liriodendri would be better placed in Pleosporineae
(Pleosporales).
Wu et al. (2011a) epitypified the generic type of Tothia
Bat. (T. fuscella (Sacc.) Bat.), and found it nesting within
the clade of Venturiales based on analysis of LSU and ITS
or LSU and SSU nurDNA sequences Wu et al. (2011a, b).
The dilute brown ascospores of T. fuscella differ from the
representatives of Microthyriaceae (Wu et al. 2011a, b),
and agree with those of Venturiales. But the flat-conical and
thyriothecial ascomata of T. fuscella are unusual within
Fungal Diversity (2011) 51:249–277
Venturiales. The dendrogram obtained by Wu et al. (2011b)
indicated that T. fuscella is basal to the clade of Venturiaceae, but the support is inconsistent. Thus the familial
status of Tothia cannot be determined yet.
Previous phylogenetic analysis indicated that Venturiales
may be closely related to species of Microthyriales and
Phaeotrichaceae (Schoch et al. 2009). This is corroborated
here, although a relationship between Microthyriales and
Venturiales is not well resolved. The 1-septate usually
pigmented ascospores and deliquescing pseudoparaphyses
of Venturiales are mostly comparable with species of
Botryosphaeriales and Capnodiales as has been noticed
by Crous et al. (2007a). In particular, venturialean genera
such as Phaeocryptopus, Xenomeris and Rosenscheldiella
have been assigned to Capnodiales (Sultan et al. 2011;
Winton et al. 2007). Ecological habitats, ascospore shape
and colour may help to distinguish these three orders, but
DNA sequences are determinative. The poor resolution for
interspecific relationships within Venturiaceae seen in this
study and others (e.g. Crous et al. 2007a) suggests that the
currently applied DNA markers will need to be expanded
drastically in order to determine radiation events more
precisely. This also means that generic and/or familial
classification will likely remain unstable for the foreseeable
future.
Morphology and ecology
Most of the venturialean genera have deliquescing or
rare pseudoparaphyses. Pseudoparaphyses usually persist
and are numerous in saprobic fungi, viz. freshwater
(Amniculicolaceae) or marine taxa (Aigialaceae), while
they are usually evanescent in parasitic fungi, i.e. in taxa
of Botryosphaeriales (Schoch et al. 2006) and Didymellaceae (de Gruyter et al. 2009). Studies of the hamathecium
have mainly focused on the presence, morphology or
ontogeny, while the function of it is unclear (Eriksson
1981; Singer and Gamundi 1963). Venturiaceae had been
placed in Pleosporales according to its “Pleospora-type
centrum and bitunicate asci” (Barr 1968, 1979; Cannon
and Kirk 2007). Although the “Pleospora-type” centrum
developmental type was recorded for several species of
Venturia (Kerr 1961; Walker and Stovold 1986), hamathecial types (Pleospora-type or Sporormia-type) has been
shown to have little phylogenetic significance, at least at
family level classification (Liew et al. 2000; Reynolds
1991). In particular, comparing with the centrum developmental type, the presence (or absence) of hamathecium
seems be more significant in classification of Dothideomycetes (Schoch et al. 2006).
The shape of ascus and length of ascus pedicels
might have taxonomic significance in Dothideomycetes.
These characters have shown significance in distinguish-
275
ing Lophiostoma and Lophiotrema, two morphologically
comparable genera within Pleosporales (Hirayama and
Tanaka 2011). The generic types of venturialean genera
mostly have obclavate or obpyriform asci, i.e. Pseudoparodiella vernoniae and Venturia inaequalis (see Figs. 7 and
8). Compared with the cylindrical to cylindro-clavate asci
with short or long furcate pedicels possessed by saprobic
fungi, some dothideomycetous plant pathogens have
obclavate or obpyriform asci with or without small knoblike pedicels, for instance in Mycosphaerella (Mycosphaerellaceae), Macroventuria (Pleosporaceae) and Bricookea
(Phaeosphaeriaceae).
Thin-walled, mostly asymmetrical and olivaceous ascospores is another striking character of Venturiales. Anamorphic states are reported from some genera of
Venturiales, especially on those plant pathogens, such as
Venturia and Apiospora. The anamorphic states mostly
infect and reproduce during the growing season, and the
teleomorphic state helps to overwinter, which matures by
the following spring when the host intiates growth. The
parasitic species of Venturiales lacking anamorphs infect
their hosts by means of ascospores, and produce ascomata
on the substrates during the growing season (Kerr 1961). In
this case, the ascospores as well as other reproductive
structures of Venturiaceae play important roles to overwinter on fallen host leaves. Thus the relatively small, thinwalled and asymmetrical ascospores have an important role
in this life cycle.
Summary
Based on the ITS nurDNA sequences analysis results, Beck
et al. (2005) accepted Fusicladium sensu lato, which
included Pollaccia and Spilocaea. Based on 28S nurDNA
sequences analysis, a broader generic concept of Fusicladium was accepted, which included Pseudocladosporium as
another synonym of Fusicladium sensu lato (incl. Pollaccia
and Spilocaea) (Crous et al. 2007a). In this study, five
genes are used for phylogenetic analysis, i.e. 18S, 28S
nurDNA sequences as well as the protein genes RPB1, 2
and TEF1, and a narrow concept of Venturia is accepted,
which includes only some parasitic species closely related
to the generic type of Venturia (V. inaequalis). Concurrently, a narrower concept of Fusicladium is accepted, and
Pollaccia, Pseudocladosporium and Spilocaea are treated
as separate genera herein.
The majority of economic interest in Venturiales is
closely tied to members of the type genus Venturia,
containing several species with host specific associations.
The type species of Venturia, V. inaequalis, is the causal
agent of apple scab, the most important disease on apples
worldwide (Carisse and Bernier 2002). This species has
276
been studied intensively for over 100 years with extensive
genetic and epidemiological data available (MacHardy
1996). More recently it has been the focus of studies on
molecular agents of host infection with whole genome
sequences underway (Bowen et al. 2011). In spite of this
pending increase in genetic data and long historical
record, much of the phylogenetic relationships with
Venturia as well as it relationships to other members of
the newly described order remain poorly understood. A
polyphasic approach by integrating morphological, ecological, biological methods and DNA and protein based
sequence comparisons is critical to access a modern
taxonomy that reflects evolutionary theories of Venturiales
as well as other orders of Dothideomycetes (Zhang et al.
2012).
Acknowledgements Ying Zhang would like to thank the Mushroom
Research Foundation, Chiang Mai, Thailand for providing her with a
post doctoral fellowship for this study. We are grateful to the Directors
and Curators of NY, K, L, PH, S for the loan of specimens in their
keeping. E.H.C. McKenzie is thanked for his comments on an earlier
version of the script. This work was supported by Thailand Research
Fund BRG528002. The Global Research Network for Fungal Biology
and King Saud University are also thanked for support. Conrad L.
Schoch acknowledges support by the Intramural Research Program of
the NIH, National Library of Medicine.
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