Fungal Diversity

, Volume 51, Issue 1, pp 249–277

A molecular, morphological and ecological re-appraisal of Venturiales―a new order of Dothideomycetes

Authors

  • Ying Zhang
    • Mushroom Research Foundation
    • Institute of Excellence in Fungal ResearchSchool of Science, Mae Fah Luang University
  • Pedro W. Crous
    • CBS-KNAW Fungal Biodiversity Centre
    • Microbiology, Department of BiologyUtrecht University
    • Wageningen University and Research Centre (WUR), Laboratory of Phytopathology
  • Conrad L. Schoch
    • National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health
  • Ali H. Bahkali
    • Botany and Microbiology DepartmentCollege of Science, King Saud University
  • Liang Dong Guo
    • State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences
    • Botany and Microbiology DepartmentCollege of Science, King Saud University
    • International Fungal Research & Development Centre, The Research Institute of Resource Insects, Chinese Academy of Forestry, Kunming
    • Institute of Excellence in Fungal ResearchSchool of Science, Mae Fah Luang University
Article

DOI: 10.1007/s13225-011-0141-x

Cite this article as:
Zhang, Y., Crous, P.W., Schoch, C.L. et al. Fungal Diversity (2011) 51: 249. doi:10.1007/s13225-011-0141-x

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 investigation. Zeuctomorpha is treated as a synonym of Acantharia.

Keywords

FusicladiumGeneric typeSympoventuriaceaeTaxonomyVenturiaceae

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 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) 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).
Table 1

Taxa used in the phylogenetic analysis and their corresponding GenBank accession numbers

 Species

voucher/culture

SSU

LSU

TEF1

RPB1

RPB2

Aliquandostipite khaoyaiensis

CBS 118232

AF201453

GU301796

GU349048

 

FJ238360

Alternaria alternata

CBS 916.96

DQ678031

DQ678082

DQ677927

 

DQ677980

Anteaglonium abbreviatum

ANM 925.1

 

GQ221877

GQ221924

  

Anteaglonium parvulum

SMH 5210

 

GQ221907

GQ221917

  

Apiosporina collinsii

CBS 118973

GU296135

GU301798

GU349057

GU357778

 

Apiosporina morbosa

dimosp

 

EF114694

   

Ascochyta pisi

CBS 126.54

DQ678018

DQ678070

DQ677913

 

DQ677967

Asterina fuchsiae

TH 590

GU586210

GU586216

   

Asterina phenacis

TH 589

GU586211

GU586217

   

Asterina weinmanniae

TH 592

GU586212

GU586218

   

Asterina zanthoxyli

TH 561

GU586213

GU586219

   

Aureobasidium pullulans

CBS 584.75

DQ471004

DQ470956

DQ471075

DQ471148

DQ470906

Botryosphaeria dothidea

CBS 115476

DQ677998

DQ678051

DQ767637

GU357802

DQ677944

Botryosphaeria stevensii

CBS 431.82

DQ678012

DQ678064

DQ677907

 

DQ677960

Capnodium coffeae

CBS 147.52

DQ247808

DQ247800

DQ471089

DQ471162

DQ247788

Capnodium salicinum

CBS 131.34

DQ677997

DQ678050

DQ677889

  

Caproventuria hanliniana

ATCC 96019

 

AF050290

   

Caproventuria hystrioides

CBS 117727

 

EU035459

   

Cladosporium cladosporioides

CBS 170.54

DQ678004

DQ678057

DQ677898

GU357790

DQ677952

Cochliobolus heterostrophus

CBS 134.39

AY544727

AY544645

DQ497603

 

DQ247790

Coleroa robertiani

CBS 458.64

 

xxx

   

Corynespora cassiicola

CBS 100822

GU296144

GU301808

GU349052

GU357772

GU371742

Davidiella tassiana

CBS 399.80

DQ678022

DQ678074

DQ677918

GU357793

DQ677971

Delitschia didyma

UME 31411

AF242264

DQ384090

   

Delitschia winteri

CBS 225.62

DQ678026

DQ678077

DQ677922

 

DQ677975

Didymella exigua

CBS 183.55

GU296147

  

GU357800

GU371764

Dissoconium aciculare

CBS 204.89

GU214523

GQ852587

   

Dissoconium commune

CBS 110747

GU214525

GQ852589

   

Dothidea insculpta

CBS 189.58

DQ247810

DQ247802

DQ471081

DQ471154

AF107800

Dothidea sambuci

DAOM 231303

AY544722

AY544681

DQ497606

 

DQ522854

Dothidotthia aspera

CPC 12933

EU673228

EU673276

   

Dothidotthia symphoricarpi

CBS119687

EU673224

EU673273

   

Dothiora cannabinae

CBS 737.71

DQ479933

DQ470984

DQ471107

DQ471182

DQ470936

Dothistroma septosporum

CBS 112498

GU214533

GQ852597

   

Elsinoë centrolobi

CBS 222.50

DQ678041

DQ678094

DQ677934

GU357798

 

Elsinoë phaseoli

CBS 165.31

DQ678042

DQ678095

DQ677935

GU357799

 

Fusicladium africanum

CPC 12829

 

EU035424

   

Fusicladium africanum

CPC 12828

 

EU035423

   

Fusicladium intermedium

CBS 110746

 

EU035432

   

Fusicladium pini

CBS 463.82

 

EU035436

   

Gibbera conferta

CBS 191.53

GU296150

GU301814

GU349041

GU357758

 

Gibbera rosea

CBS 213.58

 

xxx

   

Guignardia bidwellii

CBS 237.48

DQ678034

DQ678085

 

GU357794

DQ677983

Hysterium angustatum

CBS 123334

FJ161167

FJ161207

FJ161111

 

FJ161129

Hysterium barrianum

ANM 1495

GU323182

GQ221885

   

Jahnula aquatica

R68-1

EF175633

EF175655

   

Leptosphaeria biglobosa

CBS 303.51

 

GU301826

GU349010

  

Leptosphearia maculans

DAOM 229267

DQ470993

DQ470946

DQ471062

DQ471136

DQ470894

Lophium mytilinum

CBS 114111

EF596819

EF596819

   

Macrophomina phaseolina

CBS 227.33

DQ678037

DQ678088

DQ677929

 

DQ677986

Macroventuria anomochaeta

CBS 525.71

 

GU456315

GU456262

 

GU456346

Metacoleroa dickiei

medipc

EF114719

EF114695

   

Metacoleroa dickiei

Kruys 503

DQ384100

DQ384100

   

Microthyrium microscopicum

CBS 115976

GU296175

GU301846

GU349042

 

GU371734

Mycosphaerella graminicola

CBS 292.38

DQ678033

DQ678084

  

DQ677982

Mycosphaerella punctiformis

CBS 113265

DQ471017

DQ470968

DQ471092

DQ471165

DQ470920

Myriangium duriaei

CBS 260.36

AY016347

DQ678059

DQ677900

 

DQ677954

Mytilinidion acicola

EB 0349

GU323185

GU323209

  

GU371757

Opegrapha dolomitica

DUKE 0047528

DQ883706

 

DQ883732

DQ883717

DQ883714

Phaeocryptopus gaeumannii

CBS 267.37

EF114722

EF114698

 

GU357770

 

Phaeocryptopus nudus

CBS 268.37

GU296182

GU301856

GU349034

GU357745

 

Phaeotrichum benjaminii

CBS 541.72

AY016348

AY004340

DQ677892

GU357788

DQ677946

Phoma herbarum

CBS 276.37

DQ678014

DQ678066

DQ677909

GU357792

DQ677962

Platychora ulmi

CBS 361.52

EF114726

EF114702

   

Protoventuria alpina

CBS 140.83

EU035444

    

Protoventuria barriae

ATCC 90285

 

EF114728

   

Protoventuriabarriae

CBS 300.93

 

xxx

   

Protoventuria major

CBS 114594

 

xxx

   

Pyrenophora tritici

OSC 100066

 

AY544672

DQ677882

  

Rhytidhysteron rufulum

CBS 306.38

GU296191

FJ469672

GU349031

FJ238444

 

Schismatomma decolorans

DUKE 0047570

AY548809

AY548815

DQ883725

 

DQ883715

Scorias spongiosa

CBS 325.33

DQ678024

DQ678075

DQ677920

 

DQ677973

Spilocaea oleaginea

So-91

AF338393

AF338397

 

  

Spilocaea pomi

CBS 176.42

 

GU348998

GU349089

  

Sympoventuria capensis

CPC 12839

 

DQ885905

   

Sympoventuria capensis

CPC 12840

 

DQ885904

   

Teratosphaeria fibrillosa

CBS 121707

GU296199

GU323213

 

GU357767

 

Teratosphaeria stellenboschiana

CBS 116428

GU214583

EU019295

   

Trichodelitschia bisporula

CBS 262.69

GU349000

GU348996

GU349020

GU371812

GU371802

Trichodelitschia munkii

Kruys201

DQ384070

DQ384096

   

Trypethelium nitidiusculum

Nelsen 4002a

 

GU327728

   

Trypethelium nitidiusculum

AFTOL 2099

 

FJ267701

GU327732

  

Trypethelium tropicum

25

 

GU327730

   

Tubeufia cerea

CBS 254.75

DQ471034

DQ470982

DQ471105

DQ471180

DQ470934

Tubeufia paludosa

CBS 120503

GU296203

GU301877

GU349024

GU357754

GU371731

Tubeufia paludosa

CBS 245.49

DQ767649

DQ767654

DQ767638

 

DQ767643

Tyrannosoru spinicola

CBS 124.88

DQ471025

DQ470974

DQ471098

DQ471171

DQ470928

Venturia inaequalis

ATCC 60070

EF114737

EF114712

   

Venturia inaequalis

CBS 815.69

GU296204

GU301878

GU349023

GU357756

 

Venturia inaequalis

CBS 594.70

GU296205

GU301879

GU349022

GU357757

 

Venturia populina

CBS 256.38

GU296206

GU323212

 

GU357769

 

Veronaeopsis simplex

CBS 588.66

 

EU041877

   

Xenomeris juniperi

xejucf

EF114734

EF114709

   

Xenomeris raetica

CBS 485.61

EF114741

EF114716

   
https://static-content.springer.com/image/art%3A10.1007%2Fs13225-011-0141-x/MediaObjects/13225_2011_141_Fig1_HTML.gif
Fig. 1

A RAxML maximum likelihood tree from 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

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 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.
https://static-content.springer.com/image/art%3A10.1007%2Fs13225-011-0141-x/MediaObjects/13225_2011_141_Fig2_HTML.gif
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

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, aliquandocoalitus 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 and several Fusicladium-like or Sympodiella-like anamorph species. Herein a new family, Sympoventuriaceae, is introduced to accommodate the second lineage.

Sympoventuriaceae Yin. Zhang, C.L. Schoch & K.D. Hyde, fam. nov. MycoBank: MB 563117

Ascomata immersi, subglobosi, papillati, ostiolati. Pseudoparaphyseshyalinis, 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. 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 inSympoventuriaceae

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.

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 well-developed 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 apedicellate. 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 inVenturiaceae

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 ofVenturiaceae
  1. 1a.

    Ascospores apiosporous Apiosporina (incl. Dibotryon)

     
  2. 1b.

    Ascospore septum median or submedian, but not apiosporous. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

     
  3. 2a.

    Hyphae grow inside of the substrate . . . . . . . . . . . .3

     
  4. 2b.

    Hyphae superficial, ascomata superficial . . . . . . . . .4

     
  5. 3a.

    Ascomata superficial, produced on thin subcuticular stroma . . . . . . . . . . . . . . . . . . . . . . . . . . . .Coleroa

     
  6. 3b.

    Ascomata immersed to erumpent, without subcuticular stroma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .5

     
  7. 4a.

    Ascomata without subiculum, not cupulate when dry, ascospores pale brown when mature . . . Pseudoparodiella

     
  8. 4b.

    Ascomata without subiculum, cupulate when dry, ascospores dark brown when mature . . . . . Acantharia

     
  9. 4c.

    Ascomata produced on well defined subiculum, not cupulate when dry, ascospores olivaceous brown when mature . . . . . . . . . . . . . . . . . . . . . . . . Metacoleroa

     
  10. 5a.

    Parasitic, having Pollaccia or Spilocaea anamorphs, ascospores smooth without germ slits . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .Venturia sensu stricto

     
  11. 5b.

    Saprobic, having Pseudocladosporium anamorphs, ascospores smooth without germ slits Caproventuria

     
  12. 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, 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)
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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. d-f. Obclavate asci. g-i. Released ascospores. Scale bars: a = 5 mm, b = 0.5 mm, c = 50 μm, d-i = 10 μm

≡ 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 thick-walled cells of textura angularis, cells 8–13 μm diam., cell 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 65100 × 14–25 μm (\( \bar{x} \) = 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 (\( \bar{x} \) = 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 (Fusicladium-like). 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, 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)
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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 8-spored asci. d. Released ascospores. Scale bars: a = 0.5 mm, b, c = 10 μm, d = 5 μm

≡ 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 6377 × 8–10 μm (\( \bar{x} \) = 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 (\( \bar{x} \) = 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, smooth-walled (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)
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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

≡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, 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 6890 × 12.5–15 μm (\( \bar{x} \) = 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 (\( \bar{x} \) = 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, smooth-walled (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 thin-walled towards the apex. Peridium pseudoparenchymatous, composed of angular to rounded, dark brown cells. Asci 8-spored, bitunicate, numerous, subclavate to cylindrical. Ascospores monostichous or distichous, ellipsoid-ovoid, 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 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 thin-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)
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Fig. 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

≡ 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 4558 × 12–16 μm (\( \bar{x} \) = 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 (\( \bar{x} \) = 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 1-septate, 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.

Type species:

Pseudoparodiella vernoniae F. Stevens, Illinois Biol. Monogr. (Urbana) 11: 166 (1927). (Fig. 7)
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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

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 5572 × 17–22 μm (\( \bar{x} \) = 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 1619 × 6–8 μm (\( \bar{x} \) = 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 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, 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 4-spored), 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, 1-septate, 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)
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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

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-)70–90 × 9.5–14 μm (\( \bar{x} \) = 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 1317 × 6–8 μm (\( \bar{x} \) = 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 inVenturiales

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).

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 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 thick-walled 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)
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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

Asterina comata Berk. & Ravenel, Grevillea 4 (no. 29): 10 (1875).

Ascostromata 72157 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 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 1423 × 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 fromVenturiales

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.

Anamorph reported for genus: none.

Type species:

Crotone drimydis (Lév.) Theiss. & Syd., Annls mycol. 13: 629 (1915). (Fig. 10)
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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

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 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 55105 × 10–17.5 μm (\( \bar{x} \) = 79.2 × 13.5 μm, n = 10), 8-spored, 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 (\( \bar{x} \) = 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).

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 1-layered, composed of small, lightly pigmented, thick-walled 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.

Type species:

Polyrhizon terminaliae (Syd.) Syd., Annls mycol. 12: 281 (1914). (Fig. 11)
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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

≡ 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 (\( \bar{x} \) = 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 2428 × 7.5–10 μm (\( \bar{x} \) = 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, 1-layered, 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.

Type species:

Lineostroma banksiae (Cooke) H.J. Swart, Trans. Br. mycol. Soc. 91: 464 (1988). (Fig. 12)
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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

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 5065 × 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, 2-layered. Hamathecium of rare, septate pseudoparaphyses. 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)
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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

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 125175 × 12–22 μm, 8-spored, bitunicate, fissitunicate dehiscence not observed, broadly cylindrical to narrowly clavate, with a conspicuous ocular chamber (Fig. 13c). Ascospores 3239 × 5–7.5(−10) μm (\( \bar{x} \) = 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 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 8-spored, bitunicate, fissitunicate obclavate, with a short, thick pedicel. Ascospores tri-seriate near the base, ellipsoidal to fusoid with broadly rounded ends, hyaline, 1-septate, septum median to submedian, constricted at the septum.

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)
https://static-content.springer.com/image/art%3A10.1007%2Fs13225-011-0141-x/MediaObjects/13225_2011_141_Fig14_HTML.gif
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

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 5–6 × 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, 1-septate, 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). 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 DothideomycetesVenturiales 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/MycoTaxo.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 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 distinguishing 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 knob-like 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, thin-walled 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 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.

Copyright information

© Kevin D. Hyde (outside the USA) 2011