Mycosphaerella is polyphyletic.

Mycosphaerella, one of the largest genera of ascomycetes, encompasses several thousand species and has anamorphs residing in more than 30 form genera. Although previous phylogenetic studies based on the ITS rDNA locus supported the monophyly of the genus, DNA sequence data derived from the LSU gene distinguish several clades and families in what has hitherto been considered to represent the Mycosphaerellaceae. Several important leaf spotting and extremotolerant species need to be disposed to the genus Teratosphaeria, for which a new family, the Teratosphaeriaceae, is introduced. Other distinct clades represent the Schizothyriaceae, Davidiellaceae, Capnodiaceae, and the Mycosphaerellaceae. Within the two major clades, namely Teratosphaeriaceae and Mycosphaerellaceae, most anamorph genera are polyphyletic, and new anamorph concepts need to be derived to cope with dual nomenclature within the Mycosphaerella complex.

INTRODUCTION

The genus Mycosphaerella Johanson as presently circumscribed contains close to 3 000 species (Aptroot 2006), excluding its anamorphs, which represent thousands of additional species (Crous et al. 2000, 2001, 2004a, b, 2006a, b, 2007b, Crous & Braun 2003). Crous (1998) predicted that Mycosphaerella would eventually be split according to its anamorph genera, and Crous et al. (2000) recognised six sections, as originally defined by Barr (1972). This was followed by a set of papers (Crous , Goodwin ), where it was concluded, based on ITS DNA sequence data, that Mycosphaerella was monophyletic. A revision of the various coelomycete and hyphomycete anamorph concepts led Crous & Braun (2003) to propose a system whereby the asexual morphs could be allocated to various form genera affiliated with Mycosphaerella holomorphs.

In a recent study that formed part of the US “Assembling the Fungal Tree of Life” project, Schoch et al. (2006) were able to show that the Mycosphaerellaceae represents a family within Capnodiales. Furthermore, some variation was also depicted within the family, which supported similar findings in other recent papers employing LSU sequence data, such as Hunter et al. (2006), and Batzer et al. (2007). To further elucidate the phylogenetic variation observed within the Mycosphaerellaceae in these studies, a subset of isolates was selected for the present study, representing the various species recognised as morphologically distinct from Mycosphaerella s. str.

The genus Mycosphaerella has in recent years been linked to approximately 30 anamorph genera (Crous & Braun 2003, Crous ). Many of these anamorph genera resulted from a reassessment of cercosporoid forms. Chupp (1954) was of the opinion that they all represented species of the genus Cercospora Fresen., although he clearly recognised differences in their morphology. In a series of papers by Deighton, as well as others such as Sutton, Braun and Crous, the genus Cercospora was delimited based on its type species, Cercospora penicillata (Ces.) Fresen., while taxa formerly included in the genus by Chupp (1954) but differing in conidiophore arrangement, conidiogenesis, pigmentation, conidial catenulation, septation, and scar/hilum structure were allocated to other genera. Similar studies in which the type species were recollected and subjected to DNA sequence analysis were undertaken to characterise Mycosphaerella (Verkley ), and anamorph genera such as Pseudocercospora Speg., Stigmina Sacc., Phaeoisariopsis Ferraris (Crous ), Ramulispora Miura (Crous ), Batcheloromyces Marasas, P.S. van Wyk & Knox-Dav. (Taylor ), Phaeophleospora Rangel and Dothistroma Hulbary (Crous , 2001, Barnes ).

To assess the phylogeny of the species selected for the present study, DNA sequences were generated of the 28S rRNA (LSU) gene. In a further attempt to address monophyletic groups within this complex, these data were integrated with their morphological characteristics. To further resolve pleomorphism among the species studied, isolates were examined on a range of cultural media to induce possible synanamorphs.

MATERIALS AND METHODS

Isolates

Chosen isolates represent various species previously observed to be morphologically distinct from Mycosphaerella s. str. (Crous 1998, Crous et al. 2004a, b, 2006a, b, 2007b). In a few cases, specifically Teratosphaeria fibrillosa Syd. & P. Syd. and Coccodinium bartschii A. Massal., fresh material had to be collected from South Africa and Canada, respectively. Excised tissue pieces bearing ascomata were soaked in water for approximately 2 h, after which they were placed in the bottom of Petri dish lids, with the top half of the dish containing 2 % malt extract agar (MEA) (Gams ). Ascospore germination patterns were examined after 24 h, and single-ascospore and conidial cultures established as described by Crous (1998). Colonies were sub-cultured onto synthetic nutrient-poor agar (SNA), potato-dextrose agar (PDA), oatmeal agar (OA), MEA (Gams ), and incubated at 25 °C under continuous near-ultraviolet light to promote sporulation.

DNA phylogeny

Fungal colonies were established on agar plates, and genomic DNA was isolated following the CTAB-based protocol described in Gams et al. (2007). The primers V9G (de Hoog & Gerrits van den Ende 1998) and LR5 (Vilgalys & Hester 1990) were used to amplify part of the nuclear rDNA operon spanning the 3' end of the 18S rRNA gene (SSU), the first internal transcribed spacer (ITS1), the 5.8S rRNA gene, the second ITS region (ITS2) and the 5' end of the 28S rRNA gene (LSU). The primers ITS4 (White ), LR0R (Rehner & Samuels 1994), LR3R (www.biology.duke.edu/fungi/mycolab/primers.htm), and LR16 (Moncalvo ), were used as internal sequence primers to ensure good quality sequences over the entire length of the amplicon. The ITS1, ITS2 and 5.8S rRNA gene (ITS) were only sequenced for isolates of which these data were not available. The ITS data were not included in the analyses but deposited in GenBank where applicable. The PCR conditions, sequence alignment and subsequent phylogenetic analysis using parsimony, distance and Bayesian analyses followed the methods of Crous et al. (2006c). Gaps longer than 10 bases were coded as single events for the phylogenetic analyses; the remaining gaps were treated as new character states. Sequence data were deposited in GenBank (Table 1) and alignments in TreeBASE (www.treebase.org).

Table 1.

Isolates for which new sequences were generated.

Anamorph	Teleomorph	Accession number1	Host	Country	Collector	GenBank Accession number
Batcheloromyces eucalypti		CBS 313.76; CPC 3632	Eucalyptus tessellaris	Australia	J.L. Alcorn	EU019245
Batcheloromyces leucadendri		CBS 110892; CPC 1837	Leucadendron sp.	South Africa	L. Swart	EU019246
Batcheloromyces proteae		CBS 110696; CPC 1518	Protea cynaroides	South Africa	L. Viljoen	EU019247
Capnobotryella renispora		CBS 214.90*; CBS 176.88; IAM 13014; JCM 6932	Capnobotrys neessii	Japan	J. Sugiyama	EU019248
Catenulostroma abietis		CBS 290.90	Man, skin lesion	Netherlands	R.G.F. Wintermans	EU019249
Catenulostroma castellanii		CBS 105.75*; ATCC 24788	Man, tinea nigra	Venezuela	—	EU019250
Catenulostroma chromoblastomycosum		CBS 597.97	Man, chromoblastomycosis	Zaire	V. de Brouwere	EU019251
Catenulostroma elginense		CBS 111030; CPC 1958	Protea grandiceps	South Africa	J.E. Taylor	EU019252
Catenulostroma germanicum		CBS 539.88	Stone	Germany	—	EU019253
Catenulostroma macowanii		CBS 110756; CPC 1872	Protea nitida	South Africa	J.E. Taylor	EU019254
Catenulostroma microsporum	Teratosphaeria microspora	CBS 110890; CPC 1832	Protea cynaroides	South Africa	L. Swart	EU019255
Catenulostroma sp.	Teratosphaeria pseudosuberosa	CBS 118911; CPC 12085	Eucalyptus sp.	Uruguay	M.J. Wingfield	EU019256
Cercosporella centaureicola		CBS 120253	Centaurea solstitiales	Greece	D. Berner	EU019257
Cibiessia dimorphospora		CBS 120034; CPC 12636	Eucalyptus nitens	Australia	—	EU019258
Cibiessia minutispora		CPC 13071*	Eucalyptus henryii	Australia	A.J. Carnegie	EU019259
Cibiessia nontingens	Teratosphaeria sp.	CBS 120725*; CPC 13217	Eucalyptus tereticornis	Australia	B. Summerell	EU019260
Cladosporium bruhnei	Davidiella allicina	CBS 115683; ATCC 66670; CPC 5101	CCA-treated Douglas-fire pole	U.S.A., New York	C.J. Wang	EU019261
Cladosporium cladosporioides		CBS 109.21; ATCC 11277; ATCC 200940; IFO 6368; IMI 049625	Sooty mould on Hedera helix	U.K.	—	EU019262
Cladosporium sphaerospermum		CBS 188.54; ATCC 11290; IMI 049638	—	—	—	EU019263
Cladosporium uredinicola		ATCC 46649	Hyperparasite on Cronartium fusiforme f. sp. quercum	U.S.A., Alabama	—	EU019264
Coccodinium bartschii		CBS 121708; CPC 13861-13863	Sooty mould on unidentified tree	Canada	K.A. Seifert	EU019265
Dissoconium aciculare		CBS 342.82*; CPC 1534	Erysiphe, on Medicago lupulina	Germany	T. Hijwegen	EU019266
Dissoconium commune	“Mycosphaerella” communis	CBS 114238*; CPC 10440	Eucalyptus globulus	Spain	J.P.M. Vazquez	EU019267
Dissoconium dekkeri	“Mycosphaerella” lateralis	CBS 567.89*; CPC 1535	Juniperus chinensis	Netherlands	T. Hijwegen	EU019268
Fumagospora capnodioides	Capnodium salicinum	CBS 131.34	Sooty mould on Bursaria spinosa	Indonesia	—	EU019269
Hortaea werneckii		CBS 107.67*	Man, tinea nigra	Portugal	—	EU019270
Nothostrasseria dendritica	Teratosphaeria dendritica	CPC 12820	Eucalyptus nitens	Australia	A.J. Carnegie	EU019271
“Passalora” zambiae		CBS 112970*; CPC 1228	Eucalyptus globulus	Zambia	T. Coutinho	EU019272
		CBS 112971*; CMW 14782; CPC 1227	Eucalyptus globulus	Zambia	T. Coutinho	EU019273
Penidiella columbiana		CBS 486.80	Paepalanthus columbianus	Colombia	W. Gams	EU019274
Penidiella nectandrae		CBS 734.87*; ATCC 200932; INIFAT 87/45	Nectandra coriacea	Cuba	R.F. Castañeda & G. Arnold	EU019275
Penidiella rigidophora		CBS 314.95*	Leaf litter of Smilax sp.	Cuba	R.F. Castañeda	EU019276
Penidiella strumelloidea		CBS 114484*; VKM F-2534	Carex leaf, from stagnant water	Russia	S. Ozerskaya	EU019277
Penidiella venezuelensis		CBS 106.75*	Man, tinea nigra	Venezuela	D. Borelli	EU019278
Phaeotheca triangularis		CBS 471.90*	Wet surface of humidifier of airconditioning	Belgium	H. Beguin	EU019279
Phaeothecoidea eucalypti		CPC 13010	Corymbia henryii	Australia	B. Summerell	EU019280
		CPC 12918*	Eucalyptus botryoides	Australia	B. Summerell	EU019281
Pleurophoma sp.	Teratosphaeria fibrillosa	CPC 1876	Protea nitida	South Africa	J.E. Taylor	EU019282
Pseudotaeniolina globosa		CBS 109889*	Rock	Italy	C. Urzi	EU019283
Ramularia pratensis var. pratensis		CPC 11294	Rumex crispus	Korea	H.D. Shin	EU019284
Ramularia sp.		CBS 324.87	On Mycosphaerella sp., leaf spot on Brassica sp.	Netherlands	—	EU019285
Readeriella brunneotingens		CPC 13303	Eucalyptus tereticornis	Australia	P.W. Crous	EU019286
Readeriella destructans		CBS 111369*; CPC 1366	Eucalyptus grandis	Indonesia	M.J. Wingfield	EU019287
Readeriella epicoccoides	Teratosphaeria suttonii	CPC 12352	Eucalyptus sp.	U.S.A.,Hawaii	W. Gams	EU019288
Readeriella eucalypti		CPC 11186	Eucalyptus globulus	Spain	M.J. Wingfield	EU019289
Readeriella gauchensis		CBS 120303*; CMW 17331	Eucalyptus grandis	Uruguay	M.J. Wingfield	EU019290
Readeriella mirabilis		CBS 116293; CPC 10506	Eucalyptus fastigata	New Zealand	W. Gams	EU019291
Readeriella molleriana	Teratosphaeria molleriana	CBS 111164*; CMW 4940; CPC 1214	Eucalyptus globulus	Portugal	M.J. Wingfield	EU019292
Readeriella ovata complex		CPC 18	Eucalyptus cladocalyx	South Africa	P.W. Crous	EU019293
		CBS 111149; CPC 23	Eucalyptus cladocalyx	South Africa	P.W. Crous	EU019294
Readeriella stellenboschiana		CBS 116428; CPC 10886	Eucalyptus sp.	South Africa	P.W. Crous	EU019295
Readeriella zuluensis		CBS 120301*; CMW 17321	Eucalyptus grandis	South Africa	M.J. Wingfield	EU019296
Septoria tritici	Mycosphaerella graminicola	CBS 100335; IPO 69001.61	Triticum aestivum	—	G.H.J. Kema	EU019297
		CBS 110744; CPC 658	Triticum sp.	South Africa	P.W. Crous	EU019298
Trimmatostroma betulinum		CBS 282.74	Betula verrucosa	Netherlands	W.M. Loerakker	EU019299
Trimmatostroma salicis		CPC 13571	Salix alba	Germany	U. Braun	EU019300
	Teratosphaeria bellula	CBS 111700; CPC 1821	Protea eximia	South Africa	J.E. Taylor	EU019301
	Teratosphaeria mexicana	CPC 12349	Eucalyptus sp.	U.S.A.,Hawaii	W. Gams	EU019302
	Teratosphaeria nubilosa	CBS 114419; CPC 10497	Eucalyptus globulus	New Zealand	—	EU019303
		CBS 116005*; CMW 3282; CPC 937	Eucalyptus globulus	Australia	A. Carnegie	EU019304
	Teratosphaeria ohnowa	CBS 112896*; CMW 4937; CPC 1004	Eucalyptus grandis	South Africa	M.J. Wingfield	EU019305
	Teratosphaeria secundaria	CBS 115608; CPC 504	Eucalyptus grandis	Brazil	A.C. Alfenas	EU019306
	Teratosphaeria sp.	CBS 208.94; CPC 727	Eucalyptus grandis	Indonesia	A.C. Alfenas	EU019307

ATCC: American Type Culture Collection, Virginia, U.S.A.; CBS: Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands; CPC: Culture collection of Pedro Crous, housed at CBS; CMW: Culture collection of Mike Wingfield, housed at FABI, Pretoria, South Africa; IAM: Institute of Applied Microbiology, University of Tokyo, Institute of molecular and cellular bioscience, Tokyo, Japan; IFO: Institute For Fermentation, Osaka, Japan; IMI: International Mycological Institute, CABI-Bioscience, Egham, Bakeham Lane, U.K.; INIFAT: Alexander Humboldt Institute for Basic Research in Tropical Agriculture, Ciudad de La Habana, Cuba; JCM: Japan Collection Of Microorganisms, RIKEN BioResource Center, Japan; VKM: All-Russian Collection of Microorganisms, Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Russia.

Ex-type cultures.

Taxonomy

Wherever possible, 30 measurements (× 1 000 magnification) were made of structures mounted in lactic acid, with the extremes of spore measurements given in parentheses. Ascospores were frequently also mounted in water to observe mucoid appendages and sheaths. Colony colours (surface and reverse) were assessed after 1-2 mo on MEA at 25 °C in the dark, using the colour charts of Rayner (1970). All cultures obtained in this study are maintained in the culture collection of the Centraalbureau voor Schimmelcultures (CBS) in Utrecht, the Netherlands (Table 1). Nomenclatural novelties and descriptions were deposited in MycoBank (www.MycoBank.org).

RESULTS

Amplification products of approximately 1 700 bases were obtained for the isolates listed in Table 1. The LSU region of the sequences was used to obtain additional sequences from GenBank which were added to the alignment. The manually adjusted alignment contained 97 sequences (including the two outgroup sequences) and 844 characters including alignment gaps. Of the 844 characters used in the phylogenetic analysis, 308 were parsimony-informative, 105 were variable and parsimony-uninformative, and 431 were constant.

The parsimony analysis of the LSU region yielded 1 135 equally most parsimonious trees (TL = 1 502 steps; CI = 0.446; RI = 0.787; RC = 0.351), one of which is shown in Fig. 1. Three orders are represented by the ingroup isolates, namely Chaetothyriales (100 % bootstrap support), Helotiales (100 % bootstrap support) and Capnodiales (100 % bootstrap support). These are discussed in detail in the Taxonomy and Discussion sections. A new collection of Coccodinium bartschii A. Massal clusters (100 % bootstrap support) with members of the Herpotrichiellaceae (Chaetothyriales), whereas the type species of the genus Trimmatostroma Corda, namely T. salicis Corda, as well as T. betulinum (Corda) S. Hughes, are allied (99 % bootstrap support) with the Dermateaceae (Helotiales). The Capnodiales encompasses members of the Capnodiaceae, Trichosphaeriaceae, Davidiellaceae, Schizothyriaceae and taxa traditionally placed in the Mycosphaerellaceae, which is divided here into the Teratosphaeriaceae, (65 % bootstrap support), and the Mycosphaerellaceae (76 % bootstrap support), which contains several subclades. Also included in the Capnodiales are Devriesia staurophora (W.B. Kendr.) Seifert & N.L. Nick., Staninwardia suttonii Crous & Summerell and Capnobotryella renispora Sugiy. as sister taxa to Teratosphaeriaceae s. str. Neighbour-joining analysis using three substitution models on the sequence data yielded trees supporting the same topologies, but differed from the parsimony tree presented with regard to the order of the families and orders at the deeper nodes, e.g., the Helotiales and Chaetothyriales are swapped around, as are the Capnodiaceae and the Trichosphaeriaceae/Davidiellaceae (data not shown). Using neighbour-joining analyses, the Mycosphaerellaceae s. str. clade obtained 71 %, 70 % and 70 % bootstrap support respectively with the uncorrected “p”, Kimura 2-parameter and HKY85 substitution models wherease the Teratosphaeriaceae clade obtained 74 %, 79 % and 78 % bootstrap support respectively with the same models. The Schizothyriaceae clade appeared basal in the Capnodiales, irrespective of which substitution model was used.

Fig. 1.

One of 1 135 equally most parsimonious trees obtained from a heuristic search with 100 random taxon additions of the LSU sequence alignment using PAUP v. 4.0b 10. The scale bar shows 10 changes, and bootstrap support values from 1000 replicates are shown at the nodes. Thickened lines indicate the strict consensus branches and ex-type sequences are printed in bold face. The tree was rooted to two sequences obtained from GenBank (Athelia epiphylla AY586633 and Paullicorticium ansatum AY586693).

Bayesian analysis was conducted on the same aligned LSU dataset using a general time-reversible (GTR) substitution model with inverse gamma rates and dirichlet base frequencies. The Markov Chain Monte Carlo (MCMC) analysis of 4 chains started from a random tree topology and lasted 23 881 500 generations. Trees were saved each 100 generations, resulting in 238 815 saved trees. Burn-in was set at 22 000 000 generations after which the likelihood values were stationary, leaving 18 815 trees from which the consensus tree (Fig. 2) and posterior probabilities (PP's) were calculated. The average standard deviation of split frequencies was 0.011508 at the end of the run. The same overall topology as that observed using parsimony was obtained, with the exception of the inclusion of Staninwardia suttonii in the Mycosphaerellaceae (PP value of 0.74) and not in the Teratosphaeriaceae. The Mycosphaerellaceae s. str. clade, as well as the Teratosphaeriaceae clade, obtained a PP value of 1.00.

Fig. 2.

Consensus phylogram (50 % majority rule) of 18 815 trees resulting from a Bayesian analysis of the LSU sequence alignment using MrBayes v. 3.1.2. Bayesian posterior probabilities are indicated at the nodes. Ex-type sequences are printed in bold face. The tree was rooted to two sequences obtained from GenBank (Athelia epiphylla AY586633 and Paullicorticium ansatum AY586693).

Based on the dataset generated in this study, several well-supported genera could be distinguished in the Mycosphaerella complex (Figs 1-2), for which we have identified morphological characters. These genera, and a selection of their species, are treated below.

Key to Mycosphaerella, and Mycosphaerella-like genera treated

1. Ascomata thyrothecial; anamorph Zygosporium................................................................................................................ .

1. Ascomata pseudothecial........................................................................................................................................................................... 2

2. Ascospores with irregular, angular lumens typical of Davidiella; anamorph Cladosporium s. str...............................................

2. Ascospores guttulate or not, lacking angular lumens; anamorph other than Cladosporium..................................................................... 3

3. Ascomata frequently linked by superficial stroma; hamathecial tissue, ascospore sheath, multi-layered endotunica, prominent periphysoids, and ascospores turning brown in asci frequently observed........................................................................

3. Ascomata not linked by superficial stroma; hamathecial tissue, ascospore sheath, multi-layered endotunica, prominent periphysoids, ascospores turning brown in asci not observed........................................................................................................................................ 4

4. Conidiophores solitary, pale brown, giving rise to primary and secondary, actively discharged conidia; anamorph Dissoconium................................................................................................................................................................... teleomorph Mycosphaerella-like

4. Conidiomata variable from solitary conidiophores to sporodochia, fascicles to pycnidia, but conidia not actively discharged..................................................................................................................................................................................................... s. str.

Treatment of phylogenetic clades

Davidiellaceae clade

Crous & U. Braun, Mycol. Progr. 2: 8. 2003.

Type species: Davidiella tassiana (De Not.) Crous & U. Braun, Mycol. Progr. 2: 8. 2003.

Basionym: Sphaerella tassiana De Not., Sferiacei Italici 1: 87. 1863.

Description: Schubert et al. (2007 - this volume).

Anamorph: Cladosporium Link, Ges. Naturf. Freunde Berlin Mag. Neuesten Entdeck. Gesammten Naturk. 7: 37. 1816.

Type species: Cladosporium herbarum (Pers.: Fr.) Link, Ges. Naturf. Freunde Berlin Mag. Neuesten Entdeck. Gesammten Naturk. 7: 37. 1816.

Basionym: Dematium herbarum Pers., Ann. Bot. (Usteri), 11 Stück: 32. 1794: Fr., Syst. Mycol. 3: 370. 1832.

Description: Schubert et al. (2007 - this volume).

Notes: The genus Davidiella (Davidiellaceae) was recently introduced for teleomorphs of Cladosporium s. str. (Braun ). The genus Cladosporium is well-established, and contains around 772 names (Dugan ), while Davidiella presently has 33 names (www.MycoBank.org), of which only around five have acknowledged Cladosporium states.

Teratosphaeriaceae clade

Syd. & P. Syd., Ann. Mycol. 10: 39. 1912.

Type species: Teratosphaeria fibrillosa Syd. & P. Syd., Ann. Mycol. 10: 40. 1912. Fig. 3.

Fig. 3.

Teratosphaeria fibrillosa (epitype material). A. Leaf spots. B. Subepidermal ascomata linked by means of stromatic tissue. C. Paraphyses among asci. D. Periphysoids. E. Ascospores becoming brown in asci. F-G. Multi-layered endotunica. H-K. Ascospores, becoming brown and verruculose. L-M. Germinating ascospores. Scale bars = 10 μm.

Description: Crous et al. (2004a; figs 182-185).

Notes: Although similar in morphology, the genus Teratosphaeria was separated from Mycosphaerella based on its ascomatal arrangement, and periphysate ostioles (Müller & Oehrens 1982). It was later synonymised under Mycosphaerella by Taylor et al. (2003), who showed that the type species clustered within Mycosphaerella based on ITS DNA sequence data. The LSU sequence data generated in the present study, has clearly shown that Mycosphaerella is polyphyletic, thus contradicting earlier reports of monophyly by Crous et al. (2000) and Goodwin et al. (2001), which were based on ITS data.

A re-examination of T. fibrillosa, the type species of Teratosphaeria, revealed several morphological features that characterise the majority of the taxa clustering in the clade, though several characters have been lost in some of the small-spored species. These characters are discussed below:

Teratosphaeria fibrillosa has a superficial stroma linking ascomata together, almost appearing like a spider's web on the leaf surface. Although this feature is not seen in other taxa in this clade, some species, such as M. suberosa Crous, F.A. Ferreira, Alfenas & M.J. Wingf. and M. pseudosuberosa Crous & M.J. Wingf. have a superficial stroma, into which the ascomata are inbedded (Crous 1998, Crous ).

Ascospores of Teratosphaeria become brown and verruculose while still in their asci. This feature is commonly observed in species such as M. jonkershoekensis P.S. van Wyk, Marasas & Knox-Dav., M. alistairii Crous, M. mexicana Crous, M. maxii Crous and M. excentricum Crous & Carnegie (Crous 1998, Crous & Groenewald 2006a, b, Crous ).

A few ascomata of T. fibrillosa were found to have some pseudoparaphysoidal remnants (cells to distinguish pseudoparaphyses), though they mostly disappear with age. This feature is rather uncommon, though pseudoparaphyses were observed in ascomata of M. eucalypti (Wakef.) Hansf.

Ascospores of Teratosphaeria were found to be covered in a mucous sheath, which is commonly observed in other taxa in this clade, such as M. bellula Crous & M.J. Wingf., M. pseudocryptica Crous, M. suberosa, M. pseudosuberosa, M. associata Crous & Carnegie, M. dendritica Crous & Summerell and M. fimbriata Crous & Summerell (Crous et al. 2004b, 2006b, 2007b). Re-examination of fresh collections also revealed ascospores of M. cryptica (Cooke) Hansf. and M. nubilosa (Cooke) Hansf. to have a weakly definable sheath. Germinating ascospores of species in this clade all exhibit a prominent mucoid sheath.

Asci of T. fibrillosa were observed to have a multi-layered endotunica, which, although not common, can be seen in species such as M. excentrica, M. maxii, M. alistairii, M. pseudosuberosa, M. fimbriata (Crous , 2007b, Crous & Groenewald 2006a, b), and also M. nubilosa.

Finally, ascomata of T. fibrillosa and T. proteae-arboreae P.S. van Wyk, Marasas & Knox-Dav. have well-developed ostiolar periphyses, which are also present in species such as M. suberosa, M. pseudosuberosa, M. maxii and T. microspora Joanne E. Taylor & Crous (Crous 1998, Crous et al. 2004a, b, 2006b). Morphologically thus, the Teratosphaeria clade is distinguishable from Mycosphaerella s. str., though these differences are less pronounced in some of the smaller-spored species. Based on these distinct morphological features, as well as its phylogenetic position within the Capnodiales, a new family is herewith proposed to accommodate species of Teratosphaeria:

Crous & U. Braun, fam. nov. MycoBank MB504464.

Ascomata pseudotheciales, superficiales vel immersa, saepe in stromate ex cellulis brunneis pseudoparenchymatibus disposita, globulares, uniloculares, papillata, apice ostiolato, periphysata, saepe cum periphysoidibus; tunica multistratosa, ex cellulis brunneis angularibus composita, strato interiore ex cellulis applanatis hyalinis; saepe cum pseudoparaphysibus subcylindricis, ramosis, septatis, anastomosibus. Asci fasciculati, octospori, bitunicati, saepe cum endotunica multistratosa. Ascosporae ellipsoideae-fusiformes vel obovoideae, 1-septatae, hyalinae, deinde pallide brunneae et verruculosae, saepe mucosae.

Ascomata pseudothecial, superficial to immersed, frequently situated in a stroma of brown pseudoparenchymatal cells, globose, unilocular, papillate, ostiolate, canal periphysate, with periphysoids frequently present; wall consisting of several layers of brown textura angularis; inner layer of flattened, hyaline cells. Pseudoparaphyses frequently present, subcylindrical, branched, septate, anastomosing. Asci fasciculate, 8-spored, bitunicate, frequently with multi-layered endotunica. Ascospores ellipsoid-fusoid to obovoid, 1-septate, hyaline, but becoming pale brown and verruculose, frequently covered in mucoid sheath.

Typus: Teratosphaeria Syd. & P. Syd., Ann. Mycol. 10: 39. 1912.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504466.

Basionym: Mycosphaerella africana Crous & M.J. Wingf., Mycologia 88: 450. 1996.

(Crous & Carnegie) Crous & U. Braun, comb. nov. MycoBank MB504467.

Basionym: Mycosphaerella associata Crous & Carnegie, Fungal Diversity 26: 159. 2007.

(Crous) Crous & U. Braun, comb. nov. MycoBank MB504468.

Basionym: Mycosphaerella alistairii Crous, in Crous & Groenewald, Fungal Planet, No. 4. 2006.

Anamorph: Batcheloromyces sp.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504469.

Basionym: Mycosphaerella bellula Crous & M.J. Wingf., Mycotaxon 46: 20. 1993.

(Cooke) Crous & U. Braun, comb. nov. MycoBank MB504470.

Basionym: Sphaerella cryptica Cooke, Grevillea 20: 5. 1891.

≡ Mycosphaerella cryptica (Cooke) Hansf., Proc. Linn. Soc. New South Wales 81: 35. 1956.

Anamorph: (Ganap. & Corbin) Crous & U. Braun, comb. nov. MycoBank MB504471.

Basionym: Colletogloeum nubilosum Ganap. & Corbin, Trans. Brit. Mycol. Soc. 72: 237. 1979.

≡ Colletogloeopsis nubilosum (Ganap. & Corbin) Crous & M.J. Wingf., Canad. J. Bot. 75: 668. 1997.

(Crous & Summerell) Crous & U. Braun, comb. nov. MycoBank MB504472.

Basionym: Mycosphaerella dendritica Crous & Summerell, Fungal Diversity 26: 161. 2007.

Anamorph: (Hansf.) Nag Raj, Canad. J. Bot. 61: 25. 1983.

Basionym: Spilomyces dendriticus Hansf., Proc. Linn. Soc. New South Wales 81: 32. 1956.

(Crous & Carnegie) Crous & U. Braun, comb. nov. MycoBank MB504473.

Basionym: Mycosphaerella excentrica Crous & Carnegie, Fungal Diversity 26: 164. 2007.

Anamorph: (B. Sutton & Ganap.) Crous & U. Braun, comb. nov. MycoBank MB504475.

Basionym: Trimmatostroma excentricum B. Sutton & Ganap., New Zealand J. Bot. 16: 529. 1978.

Syd. & P. Syd., Ann. Mycol. 10: 40. 1912.

≡ Mycosphaerella fibrillosa (Syd. & P. Syd.) Joanne E. Taylor & Crous, Mycol. Res. 107: 657. 2003.

Specimens examined: South Africa, Western Cape Province, Bains Kloof near Wellington, on living leaves of Protea grandiflora, 26 Feb. 1911, E.M. Doidge, holotype PREM; Stellenbosch, Jonkershoek valley, S33° 59' 44.7”, E18° 58' 50.6”, 1 Apr. 2007, on leaves of Protea sp., P.W. Crous & L. Mostert, epitype designated here CBS H-19913, culture ex-epitype CBS 121707 = CPC 13960.

(Crous & Summerell) Crous & U. Braun, comb. nov. MycoBank MB504476.

Basionym: Mycosphaerella fimbriata Crous & Summerell, Fungal Diversity 26: 166. 2007.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504477.

Basionym: Mycosphaerella flexuosa Crous & M.J. Wingf., Mycol. Mem. 21: 58. 1998.

(Crous) Crous & U. Braun, comb. nov. MycoBank MB504478.

Basionym: Mycosphaerella gamsii Crous, Stud. Mycol. 55: 113. 2006.

(P.S. van Wyk, Marasas & Knox-Dav.) Crous & U. Braun, comb. nov. MycoBank MB504479.

Basionym: Mycosphaerella jonkershoekensis P.S. van Wyk, Marasas & Knox-Dav., J. S. African Bot. 41: 234. 1975.

(Crous) Crous & U. Braun, comb. nov. MycoBank MB504480.

Basionym: Mycosphaerella maxii Crous, in Crous & Groenewald, Fungal Planet No. 6. 2006.

(Crous) Crous & U. Braun, comb. nov. MycoBank MB504481.

Basionym: Mycosphaerella mexicana Crous, Mycol. Mem. 21: 81. 1998.

Joanne E. Taylor & Crous, Mycol. Res. 104: 631. 2000.

≡ Mycosphaerella microspora (Joanne E. Taylor & Crous) Joanne E. Taylor & Crous, Mycol. Res. 107: 657. 2003.

Anamorph: (Joanne E. Taylor & Crous) Crous & U. Braun, comb. nov. MycoBank MB504482.

Basionym: Trimmatostroma microsporum Joanne E. Taylor & Crous, Mycol. Res. 104: 631. 2000.

(Thüm.) Crous & U. Braun, comb. nov. MycoBank MB504483.

Basionym: Sphaerella molleriana Thüm., Revista Inst. Sci. Lit. Coimbra 28: 31. 1881.

≡ Mycosphaerella molleriana (Thüm) Lindau, Nat. Pfanzenfam. 1: 424. 1897.

= Mycosphaerella vespa Carnegie & Keane, Mycol. Res. 102: 1275. 1998.

= Mycosphaerella ambiphylla A. Maxwell, Mycol. Res. 107: 354. 2003.

Anamorph: (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504484.

Basionym: Colletogloeopsis molleriana Crous & M.J. Wingf., Canad. J. Bot. 75: 670. 1997.

(Cooke) Crous & U. Braun, comb. nov. MycoBank MB504485.

Basionym: Sphaerella nubilosa Cooke, Grevillea 19: 61. 1892.

≡ Mycosphaerella nubilosa (Cooke) Hansf., Proc. Linn. Soc. New South Wales 81: 36. 1965.

= Mycosphaerella juvenis Crous & M.J. Wingf., Mycologia 88: 453. 1996.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504486.

Basionym: Mycosphaerella ohnowa Crous & M.J. Wingf., Stud. Mycol. 50: 206. 2004.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504487.

Basionym: Mycosphaerella parkiiaffinis Crous & M.J. Wingf., Fungal Diversity 26:168. 2007.

(R.F. Park & Keane) Crous & U. Braun, comb. nov. MycoBank MB504488.

Basionym: Mycosphaerella parva R.F. Park & Keane, Trans. Brit. Mycol. Soc. 79: 99. 1982.

= Mycosphaerella grandis Carnegie & Keane, Mycol. Res. 98: 414. 1994.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504489.

Basionym: Mycosphaerella perpendicularis Crous & M.J. Wingf., Stud. Mycol. 55: 113. 2006.

(Crous & Mansilla) Crous & U. Braun, comb. nov. MycoBank MB504490.

Basionym: Mycosphaerella pluritubularis Crous & Mansilla, Stud. Mycol. 55: 114. 2006.

(Crous & T.A. Cout.) Crous & U. Braun, comb. nov. MycoBank MB504491.

Basionym: Mycosphaerella pseudafricana Crous & T.A. Cout., Stud. Mycol. 55: 115. 2006.

(Crous) Crous & U. Braun, comb. nov. MycoBank MB504492.

Basionym: Mycosphaerella pseudocryptica Crous, Stud. Mycol. 55: 116. 2006.

Anamorph: sp.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504493.

Basionym: Mycosphaerella pseudosuberosa Crous & M.J. Wingf., Stud. Mycol. 55: 118. 2006.

Anamorph: sp.

(Crous & T.A. Cout.) Crous & U. Braun, comb. nov. MycoBank MB504494.

Basionym: Mycosphaerella quasicercospora Crous & T.A. Cout., Stud. Mycol. 55: 119. 2006.

(Crous & Mansilla) Crous & U. Braun, comb. nov. MycoBank MB504495.

Basionym: Mycosphaerella readeriellophora Crous & Mansilla, Stud. Mycol. 50: 207. 2004.

Anamorph: Crous & Mansilla, Stud. Mycol. 50: 207. 2004. Fig. 18.

Fig. 18.

A-E. Readeriella mirabilis. A. Conidium with conidial cirrus. B. Conidiogenous cells with percurrent proliferation. C. Macroconidia. D. Slightly pigmented, verruculose conidiogenous cell. E. Macro- and microconidia. F-I. Readeriella readeriellophora (type material). F. Colony on OA. G. Central stromatal tissue giving rise to conidiophores. H. Conidiogenous cells. I. Conidia. Scale bars = 10 μm.

(Crous & Alfenas) Crous & U. Braun, comb. nov. MycoBank MB504496.

Basionym: Mycosphaerella secundaria Crous & Alfenas, Stud. Mycol. 55: 122. 2006.

(Crous & Alfenas) Crous & U. Braun, comb. nov. MycoBank MB504497.

Basionym: Mycosphaerella stramenticola Crous & Alfenas, Stud. Mycol. 55: 123. 2006.

(Crous, F.A. Ferreira, Alfenas & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504498.

Basionym: Mycosphaerella suberosa Crous, F.A. Ferreira, Alfenas & M.J. Wingf., Mycologia 85: 707. 1993.

(Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504499.

Basionym: Mycosphaerella suttonii Crous & M.J. Wingf. (suttoniae), Canad. J. Bot. 75: 783. 1997.

Anamorph: (Cooke & Massee) Crous & U. Braun, comb. nov. MycoBank MB504500.

Basionym: Cercospora epicoccoides Cooke & Massee apud Cooke, Grevillea 19: 91. 1891.

≡ Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A. Ferreira & B. Sutton, S. African J. Bot. 63: 113. 1997.

≡ Kirramyces epicoccoides (Cooke & Massee) J. Walker, B. Sutton & Pascoe, Mycol. Res. 96: 919. 1992.

= Hendersonia grandispora McAlp., Proc. Linn. Soc. New South Wales 28: 99. 1903.

= Phaeoseptoria eucalypti Hansf., Proc. Linn. Soc. New South Wales 82: 225. 1957.

= Phaeoseptoria luzonensis T. Kobayashi, Trans. Mycol. Soc. Japan 19: 377. 1978.

Synanamorph: sp.

(Crous & Bills) Crous & U. Braun, comb. nov. MycoBank MB504501.

Basionym: Mycosphaerella toledana Crous & Bills, Stud. Mycol. 50: 208. 2004.

Anamorph: (Crous & Bills) Crous & U. Braun, comb. nov. MycoBank MB504502.

Basionym: Phaeophleospora toledana Crous & Bills, Stud. Mycol. 50: 208. 2004.

Key to treated anamorph genera of Teratosphaeria (Teratosphaeriaceae)

1. Hyphae submerged to superficial, disarticulating into arthroconidia......................................................................................................... 2

1. Hyphae not disarticulating into arthroconidia............................................................................................................................................ 3

2. Mature, brown hyphae disarticulating into thick-walled, spherical, smooth to verruculose 0(-2) transversely septate, brown conidia........................................................................................................................... (= Friedmanniomyces)

2. Hyphae superficial, brown to green-brown, smooth, disarticulating to form pale brown, cylindrical, 0-3-septate conidia with subtruncate ends, frequently with a Readeriella synanamorph......................................................................................................................

3. Hyphal ends forming endoconidia; hyphae pale to medium brown, verruculose, end cells dividing into several brown, verruculose, thick-walled, ellipsoid to obovoid endoconidia.................................................................................................................

3. Endoconidia absent.................................................................................................................................................................................... 4

4. Conidiogenous cells integrated in hyphae; well-developed conidiomata or long, solitary, macronematous, terminally penicillate conidiophores absent................................................................................................................................................................................ 5

4. Conidiomata well-developed or with long, solitary, terminally penicillate conidiophores........................................................................... 7

5. Conidia in chains, holoblastic, pseudocladosporium-like in morphology, but scars and hila not excessively thickened, nor refractive, producing chlamydospores in culture; species are mostly heat resistant...................................................................................

5. Conidia solitary on indistict to well defined phialides on hyphae............................................................................................................... 6

6. Conidiogenous cells integrated in the distal ends of hyphae; conidia thick-walled, brown, smooth, 1-septate.........................................................................................................................................................................

6. Conidiophores short and frequently reduced to conidiogenous cells that proliferate percurrently via wide necks, giving rise to hyaline, 0(-2)-septate, broadly ellipsoidal conidia................................................................................................................................................

7. Conidia brown, with hyaline basal appendages; conidiomata pycnidial, conidiogenous cells phialidic, but also percurrent, subhyaline.......................................................................................................................................................................

7. Conidia brown, but basal appendages lacking, amero- to scolecospores................................................................................................ 8

8. Conidiomata pycnidial to acervular........................................................................................................................................................... 9

8. Conidiomata not enclosed by host tissue, fasciculate to sporodochial or solitary, hyphomycetous........................................................ 10

9. Conidia solitary, dry, without mucilaginous sheath...................................................................................................................

9. Conidia catenulate, with persistant mucilaginous sheath.....................................................................................................

10. Conidiophores usually solitary, rarely densely fasciculate to synnematous (in vivo), penicillate, with a branched, apical conidiogenous apparatus giving rise to ramoconidia and branched chains of secondary conidia; scars not to slightly thickened and darkened-refractive....................................................................................................................................................................................................

10. Conidiophores not penicillate, without a branched conidiogenous apparatus, in vivo fasciculate to sporodochial................................. 11

11. Biotrophic; fruiting composed of sporodochia and radiating layers of hyphae arising from the stromata, conidiophores arising from superficial sporodochia and radiating hyphae, conidiogenous cells unilocal, with conspicuous annellations, conidia solitary or in fragile disarticulating chains, aseptate or transversely 1-3-septate, usually with distinct frills, secession rhexolytic..............

11. Biotrophic, leaf-inhabiting, with distinct, subepidermal to erumpent, well-developed sporodochia, or saxicolous, saprobic, sometimes causing opportunistic human infections; radiating layers of hyphae arising from sporodochia; conidiogenous cells without annellations; conidia in true simple or branched basipetal chains, transversely 1- to pluriseptate or with longitudinal and oblique septa (dictyosporous), occasionally distoseptate......................................................................................................................

To explain the arguments behind the selection and synonymies of some of these anamorphic genera, they are briefly discussed below:

Baker et al., Appl. Environ. Microbiol. 70: 6270. 2004. (nom. inval.)

Type species: Acidomyces richmondensis Baker et al., Appl. Environ. Microbiol. 70: 6270. 2004. (nom. inval.)

Notes: The genus presently clusters among isolates in the Teratosphaeria clade based on sequences deposited in GenBank. Acidomyces lacks a Latin description and holotype specimen, and is thus invalidly described. The genus, which was distinguished from other taxa based on its DNA phylogeny (Dothideomycetes), forms filamentous hyphae with disarticulating cells. It is unclear how it differs from Friedmanniomyces Onofri and Pseudotaeniolina J.L. Crane & Schokn.

Marasas, P.S. van Wyk & Knox-Dav., J. S. African Bot. 41: 41. 1975.

Type species: Batcheloromyces proteae Marasas, P.S. van Wyk & Knox-Dav., J. S. African Bot. 41: 43. 1975.

Description: Crous et al. (2004a; figs 4-26).

Fig. 4.

Batcheloromyces leucadendri in vitro. A-B. Batcheloromyces state with synanamorph (arrows). C-D. Conidia occurring solitary or in short chains. Scale bar = 10 μm.

Notes: Batcheloromyces is presently circumscribed as a genus that forms emergent hyphae, giving rise to superficial sporodochial plates, forming brown, verrucose, erect conidiophores that proliferate holoblastically, with ragged percurrent proliferations that become visible with age. Conidia are produced singly or in fragile, disarticulating chains, are brown, thick-walled, 0-3 transversely euseptate (though at times they appear as distoseptate). The genus Batcheloromyces has in recent years been confused with Stigmina (Sutton & Pascoe 1989) on the basis that some collections showed conidiophores to give rise to solitary conidia only, though conidial catenulation was clearly illustrated by Taylor et al. (1999). In culture colonies tend to sporulate in a slimy mass (on OA), though a synanamorph can be seen (in B. leucadendri, Fig. 4) to sporulate via holoblastic conidiogenesis on hyphal tips of the aerial mycelium, forming elongate-globose to ellipsoid, muriformly septate, thick-walled conidia, that occur in clusters.

The finding that Stigmina s. str. [based on S. platani (Fuckel) Sacc., the type species] is a generic synonym of Pseudocercospora Speg. (Crous ), and that the type species of Trimmatostroma (T. salicis, Fig. 5) belongs to the Helotiales (Fig. 1), raises the question of where to place stigmina- and trimmatostroma-like anamorphs that reside in the Teratosphaeria clade. Although the stigmina-like species can be accommodated in Batcheloromyces (see Sutton & Pascoe 1989), a new genus is required for Teratosphaeria anamorphs that have a trimmatostroma-like morphology. The recognition of Batcheloromyces and the introduction of a new anamorph genus for trimmatostroma-like anamorphs of Teratosphaeria are also morphologically justified. Batcheloromyces is easily distinguishable from Stigmina s. str. by its special structure of the fruiting body, composed of sporodochia and radiating layers of hyphae arising from the sporodochia and the conidia often formed in delicate disarticulating chains. Trimmatostroma-like anamorphs of Teratosphaeria are morphologically also sufficently distinct from Trimmatostroma s. str. (see notes under Catenulostroma Crous & U. Braun) as well as Batcheloromyces (see key above).

Fig. 5.

Trimmatostroma salicis. A. Sporodochia on twig. B-E. Chains of disarticulating conidia. Scale bars = 10 μm.

(Alcorn) Crous & U. Braun, comb. nov. MycoBank MB504503.

Basionym: Stigmina eucalypti Alcorn, Trans. Brit. Mycol. Soc. 60: 151. 1973.

Sugiy., in Sugiyama, Pleomorphic Fungi: The Diversity and its Taxonomic Implications (Tokyo): 148. 1987.

Type species: Capnobotryella renispora Sugiy., in Sugiyama, Pleomorphic Fungi: The Diversity and its Taxonomic Implications (Tokyo): 148. 1987.

Description: Sugiyama & Amano (1987, figs 7.5-7.8).

Notes: The genus forms brown, septate, thick-walled hyphae, with ellipsoidal, 0-1-septate conidia forming directly on the hyphae, via minute phialides. Hambleton et al. (2003) also noted the occurrence of endoconidiation.

Crous & U. Braun, gen. nov. MycoBank MB504474.

Etymology: Named after its catenulate conidia, and stromata giving rise to sporodochia.

Hyphomycetes. Differt a Trimmatostromate habitu phytoparasitico, maculis formantibus, conidiophoris saepe fasciculatis, per stoma emergentibus vel habitu saxiphilo-saprophytico, interdum sejunctis ex mycosibus humanis.

Habit plant pathogenic, leaf-spotting or saxicolous-saprobic, occasionally isolated from opportunistic human mycoses. Mycelium internal and external; hyphae dark brown, septate, branched. Conidiomata in vivo vary from acervuli to sporodochia or fascicles of conidiophores arising from well-developed or reduced, pseudoparenchymatal stromata. Setae and hyphopodia absent. Conidiophores arising from hyphae or stromata, solitary, fasciculate to sporodochial, in biotrophic, plant pathogenic species emerging through stomata, little differentiated, semimacronematous, branched or not, continuous to septate, brown, smooth to verruculose. Conidiogenous cells integrated, terminal or conidiophores reduced to conidiogenous cells, holoblastic-thalloblastic, meristematic, unilocal, delimitation of conidium by a single septum with retrogressive delimitation of next conidium giving an unconnected chain of conidia, brown, smooth to verruculose, conidiogenous scars (conidiogenous loci) inconspicuous, truncate, neither thickened nor darkened. Conidia solitary or usually forming simple to branched basipetal chains of transversely to muriformly eu- or distoseptate, 1- to multiseptate, brown, smooth, verruculose to verrucose conidia, conidial secession schizolytic.

Type species: Catenulostroma protearum (Crous & M.E. Palm) Crous & U. Braun, comb. nov.

Description: Crous & Palm (1999), Crous et al. (2004a; figs 364-365).

Notes: Catenulostroma contains several plant pathogenic species previously placed in Trimmatostroma, a morphologically similar but, based on its type species, phylogenetically distinct genus belonging to Helotiales (Fig. 1). Trimmatostroma s. str. is well-distinguished from most Catenulostroma species by being saprobic, living on twigs and branches of woody plants, or occasionally isolated from leaf litter, i.e., they are not associated with leaf spots. The conidiomata of Trimmatostroma species are subepidermal, acervular-sporodochial with a well defined wall of textura angularis, little differentiated, micronematous conidiophores giving rise to long chains of conidia that disarticulate at the surface to form a grey-black to brown powdery mass. The generic affinity of other species assigned to Trimmatostroma, e.g. those having a lichenicolous habit, is unresolved.

Trimmatostroma abietis Butin & Pehl (Butin ) clusters together with the plant pathogenic Catenulostroma species, but differs from these species in having a more complex ecology. Trimmatostroma abietis is usually foliicolous on living or necrotic conifer needles on which characteristic acervuli to sporodochia with densely arranged, fasciculate fertile hyphae are formed, comparable to the fasciculate conidiomata of the plant pathogenic species of Catenulostroma (Butin : 205, fig. 1). Although not discussed by Butin et al. (1996), T. abietis needs to be compared to T. abietina Doherty, which was orginally described from Abies balsamea needles collected in Guelph, Canada (Doherty 1900). Morphologically the two species appear to be synonymous, except for reference to muriformly septate conidia, which is a feature not seen in vivo in the type of T. abietis. Furthermore, as this is clearly a species complex, this matter can only be resolved once fresh Canadian material has been collected to serve as epitype for T. abietina.

Isolates from stone, agreeing with T. abietis in cultural, morphological and physiological characteristics, have frequently been found (Wollenzien , Butin , Gorbushina , Kogej , Krumbein ). Furthermore, isolates from humans (ex skin lesions and ex chronic osteomycelitis of human patients) and Ilex leaves are known (Butin ). De Hoog et al. (1999) included strains of T. abietis from stone, man and Ilex leaves in molecular sequence analyses and demonstrated their genetical identity based on 5.8S rDNA and ITS2 data, but strains from conifer needles were not included. Furthermore, we consider T. abietis, as presently defined, to represent a species complex, with Dutch isolates from Pinus again appearing distinct from German Abies isolates, suggesting that different conifer genera could harbour different Catenulostroma species. Isolates from stone form stromatic, durable microcolonies, which are able to grow under extreme xerophilic environmental conditions. Cultural growth resembles that of other meristematic black yeasts (Butin , Kogej ). Another fungus isolated from stone in Germany is in vitro morphologically close to C. abietis, but differs in forming conidia with oblique septa. Furthermore, a human pathogenic isolate from Africa clusters together with other Catenulostroma species. The habit and origin of this human pathogenic fungus in nature and its potential morphology on “natural” substrates, which typically deviates strongly from the growth in vitro, are still unknown. However, C. abietis, usually growing as a foliicolous and saxicolous fungus, has already shown the potential ability of Catenulostroma species to cause opportunistic human infections.

Key to Catenulostroma species

1. Conidia formed in basipetal chains, smooth, 4-celled, consisting of two basal cells with truncate lateral sides, each giving rise to a secondary globose apical cell, that can extend and develop additional septa, appearing as two lateral arms.................

1. Conidia variable in shape, but without two basal cells giving rise to two lateral arms............................................................................... 2

2. Conidia smooth or almost so, at most very faintly rough-walled; usually foliicolous on conifer needles or saxicolous, forming stromatic, xerophilic durable microcolonies on stone, occasionally causing opportunistic human infections............................................................ 3

2. Conidia distinctly verruculose to verrucose; plant pathogenic, forming leaf spots.................................................................................... 5

3. Conidia (8-)20-35(-60) × 4-5(-7) μm, 1-10-septate...................................................................................

3. Conidia much shorter, 8-20 μm long, 0-5-septate................................................................................................................................... 4

4. Conidia 0-5 times transversely septate, mostly two-celled; usually foliicolous on conifer needles or saxicolous......................

4. Conidia 2-4 times transversely septate and often with 1-2 oblique septa; isolated from stone.......................................

5. Conidia rather broad, usually wider than 10 μm....................................................................................................................................... 6

5. Conidia narrower, width below 10 μm....................................................................................................................................................... 7

6. Conidia distoseptate, rather long, (12-)25-35(-45) × (7-)10-15(-25) μm; conidiomata large, up to 250 μm diam, on Protea anceps..............................................................................................................................................................................................

6. Conidia euseptate, shorter, (9-)16-20(-36) × (10-)14-18(-27) μm; sporodochia 90-100 × 40-80 μm; on Protea grandiceps................................................................................................................................................................................................

7. Conidia 1- to multiseptate, (10-)15-17(-23) × (5-)6.5-7(-9) μm; on various Proteaceae.................................................

7. Conidia in vivo predominantly 1-septate, (8-)13-15(-21) × (3.5-)5.5-6(-8) μm; on Protea cynaroides........................................................................................................................................

(Butin & Pehl) Crous & U. Braun, comb. nov. MycoBank MB504504.

Basionym: Trimmatostroma abietis Butin & Pehl, Antonie van Leeuwenhoek 69: 204. 1996.

Notes: Catenulostroma abietis needs to be compared to Trimmatostroma abietina Doherty (Abies balsamea needles Canada), which is either an older name for this species, or a closely related taxon. Presently T. abietina is not known from culture, and needs to be recollected.

Crous & U. Braun, sp. nov. MycoBank MB504505. Fig. 6.

Fig. 6.

Catenulostroma chromoblastomycosum (type material). A. Sporodochium on pine needle in vitro. B-H. Chains of disarticulating conidia. Scale bars: A = 350, B, E, G, H = 10 μm.

Etymology: Named after the disease symptoms observed due to opportunistic human infection.

Differt a C. abieti et C. germanico conidiis longioribus, (8-)20-35(-60) × 4-5(-7) μm, 1-10-septatis.

Description based on cultures sporulating on WA supplemented with sterile pine needles. Mycelium consisting of branched, septate, smooth to finely verruculose, medium to dark brown, thick-walled, 3-4 μm wide hyphae. Conidiomata brown, superficial, sporodochial, up to 350 μm diam. Conidiophores reduced to inconspicuous conidiogenous loci on hyphae, 2-4 μm wide, neither darkened nor thickened or refractive. Conidia occurring in branched chains, that tend to remain attached to each other, subcylindrical with subtruncate ends, straight to slightly curved, (8-)20-35(-60) × 4-5(-7) μm, 1-10-septate, medium brown, smooth to finely verruculose.

Cultural characteristics: Colonies on PDA erumpent, spreading, slow growing, with sparse to moderate aerial mycelium and smooth, irregular, submerged margins; greenish black (surface).

Specimen examined: Zaire, Pawa, isolated from man with chromoblastomycosis, Mar. 1997, V. de Brouwere, holotype CBS H-19935, culture ex-type CBS 597.97.

Notes: Catenulostroma chromoblastomycosum was originally identified as an isolate of Stenella araguata Syd. The latter fungus is morphologically distinct, however, having much shorter and narrower conidia, formed in acropetal chains, as well as quite different conidiogenous loci and conidial hila which are small, thickened and darkened.

(Joanne E. Taylor & Crous) Crous & U. Braun, comb. nov. MycoBank MB504506.

Basionym: Trimmatostroma elginense Joanne E. Taylor & Crous, Mycol. Res.104: 633. 2000.

Catenulostroma excentricum, see .

Crous & U. Braun, sp. nov. MycoBank MB504507. Fig. 7.

Fig. 7.

Catenulostroma germanicum (type material). A-D. Chains of disarticulating conidia in vitro. Scale bars = 10 μm.

Etymology: Named after the geographic location of its type strain in Germany.

Differt a C. abieti conidiis 1-2 oblique septatis.

Mycelium consisting of branched, septate, smooth, pale to medium brown, 2-4 μm wide hyphae, giving rise to conidial chains. Conidiophores integrated, subcylindrical, branched or not, septate, little differentiated, micronematous, 3-5 μm wide, 3- to multiseptate, medium brown, thick-walled; conidiogenous cells integrated, terminal, inconspicuous, unilocal, conidiogenous loci inconspicuous. Conidia in simple or branched basipetal chains, subcylindrical, straight to flexuous, (8-)10-15(-20) × 4-5(-6) μm, 2-4 transversely septate or with 1-2 oblique septa, medium to dark brown, thick-walled, smooth.

Cultural characteristics: Colonies on OA erumpent, spreading, with even, smooth margins and sparse to moderate aerial mycelium; olivaceous-grey, with iron-grey margins (surface). Colonies reaching 12 mm diam after 1 mo at 25 °C in the dark; colonies fertile.

Specimen examined: Germany (former West-Germany), isolated from stone, Oct. 1988, J. Kuroczkin, holotype CBS H-19936, culture ex-type CBS 539.88.

Notes: Catenulostroma germanicum was originally deposited as Taeniolina scripta (P. Karst.) P.M. Kirk. It is clearly distinct, however, as the latter fungus forms intricate, branched, brown conidia (Kirk 1981), unlike those of C. germanicum. Phylogenetically C. germanicum forms part of the C. abietis species complex.

(Sacc.) Crous & U. Braun, comb. nov. MycoBank MB504508.

Basionym: Coniothecium macowanii Sacc., Syll. Fung. 4: 512. 1886.

≡ Coniothecium punctiforme G. Winter, Hedwigia 24: 33. 1885, non C. punctiforme Corda, Icones Fungorum (Prague) 1: 2. 1837.

≡ Trimmatostroma macowanii (Sacc.) M.B. Ellis, More Dematiacous Hyphomycetes: 29. 1976.

Catenulostroma microsporum, see .

(Crous & M.E. Palm) Crous & U. Braun, comb. nov. MycoBank MB504509.

Basionym: Trimmatostroma protearum Crous & M.E. Palm, Mycol. Res. 103: 1303. 1999.

Crous, Fungal Diversity 26: 151. 2007.

Type species: Cibiessia dimorphospora Crous & C. Mohammed, Fungal Diversity 26: 151. 2007.

Description: Crous et al. (2007b; figs 3-5).

Notes: The genus Cibiessia was introduced to accommodate species with chains of disarticulating conidia (arthroconidia). Some species have been shown to have a Readeriella synanamorph.

Seifert & N.L. Nick., Can. J. Bot. 82: 919. 2004.

Type species: Devriesia staurophora (W.B. Kendr.) Seifert & N.L. Nick., Canad. J. Bot. 82: 919. 2004.

Description: Seifert et al. (2004; figs 2-42).

Notes: The genus is characterised by producing chains of pale brown, subcylindrical to fusiform, 0-1-septate conidia with somewhat thickened, darkened hila, forming chlamydospores in culture, and being heat resistant. Morphologically they resemble taxa placed in Pseudocladosporium U. Braun (= Fusicladium Bonord.; Venturiaceae), though phylogenetically Devriesia is not allied to this family.

Nishim. & Miyaji, Jap. J. Med. Mycol. 26: 145. 1984.

Type species: Hortaea werneckii (Horta) Nishim. & Miyaji, Jap. J. Med. Mycol. 26: 145. 1984.

Description: de Hoog et al. (2000, illust. p. 721).

Notes: The genus forms brown, septate, thick-walled hyphae, with ellipsoidal, 0-1-septate (becoming muriformly septate), hyaline to pale brown conidia forming directly on the hyphae, via phialides with percurrent proliferation. Isolates of H. werneckii are restricted to tropical or subtropical areas, where they occur as halophilic saprobes, frequently being associated with tinea nigra of humans (de Hoog ). The generic distinction with Capnobotryella is less clear, except that the latter tends to have darker, thick-walled conidia, and reduced, less prominent phialides.

Crous & U. Braun, gen. nov. MycoBank MB504463.

Etymology: Named after its penicillate conidiophores.

Differt a Periconiellae conidiophoris apice penicillato ex cellulis conidiogenis et ramoconidiis compositis, cellulis conidiogenis saepe 1-3(-4) locis conidiogenis, terminalibus vel subterminalibus, subdenticulatis, non vel subincrassatis, non vel leviter fuscatis-refractivis, ramoconidiis praesentibus, saepe numerosis, conidiis ramicatenatis.

Mycelium consisting of branched, septate, smooth to verruculose, subhyaline to pale brown hyphae. Conidiophores macronematous, occasionally also with some micronematous conidiophores; macronematous conidiophores arising from superficial mycelium or stromata, solitary, fasciculate or in synnemata, erect, brown, thin- to thick-walled, smooth to finely verruculose; terminally penicillate, branched terminal part consisting of a conidiogenous apparatus composed of a series of conidiogenous cells and/or ramoconidia. Conidiogenous cells integrated, terminal, intercalary or pleurogenous, unbranched, pale to medium brown, smooth to finely verruculose, tapering to a flattened or rounded apical region or tips slightly inflated, polyblastic, sympodial, giving rise to a single or several sets of ramoconidia on different levels; with relatively few conidiogenous loci, 1-3(-4), terminal or subterminal, subdenticulate, denticle-like loci usually conical, terminally truncate, usually unthickened or at most very slightly thickened, not to slightly darkened or somewhat refractive. Conidia in branched acropetal chains. Ramoconidia 0-1-septate, pale to medium brown, smooth to verruculose, thin-walled, ellipsoidal, obovoid, fusiform, subcylindrical to obclavate; conidia subcylindrical, fusiform to ellipsoid-ovoid, 0-1-septate, pale olivaceous to brown, smooth to verruculose, thin-walled, catenate; hila truncate, unthickened or almost so, barely to somewhat darkened-refractive.

Type species: Penidiella columbiana Crous & U. Braun, sp. nov.

Notes: Three ramichloridium-like genera cluster within Capnodiales, namely Periconiella Sacc. [type: P. velutina (G. Winter) Sacc.], Ramichloridium Stahel ex de Hoog [type: R. apiculatum (J.H. Mill., Giddens & A.A. Foster) de Hoog] and Penidiella [type: P. columbiana Crous & U. Braun]. All three genera have brown, macronematous conidiophores with similar conidial scars. Within this complex, Ramichloridium is distinct in having a prominent rachis giving rise to solitary conidia. Periconiella and Penidiella are branched in the apical part of their conidiophores, and lack a rachis. In Periconiella conidia are solitary or formed in short, mostly simple chains, ramoconidia are lacking. The apical conidiogenous apparatus is composed of conidiogenous cells or branches with integrated, usually terminal conidiogenous cells, which are persistent. The conidiogenous cells are subcylindrical to somewhat clavate, usually not distinctly attenuated towards the tip, and have several, often numerous loci, aggregated or spread over the whole cell, terminal to usually lateral, flat, non-protuberant, not denticle-like, usually distinctly thickened and darkened, at least at the rim. In contrast, Penidiella has a quite distinct branching system, consisting of a single terminal conidiogenous cell giving rise to several ramoconidia that form secondary ramoconidia, etc., or the branched apparatus is composed of several terminal and sometimes lateral conidiogenous cells giving rise to sequences of ramoconidia (conidiogenous cells and ramoconidia are often barely distinguishable, with conidiogenous cells disarticulating, becoming ramoconidia). The branched apparatus may be loose to dense, metula-like. The conidiogenous cells have only few, usually 1-3 (-4), terminal or subterminal subdenticulate loci, and ramoconidia are prominent and numerous, giving rise to branched chains of secondary conidia with flat-tipped hila. Some species of Penidiella with compact, metula-like branched apices are morphologically close to Metulocladosporiella Crous, Schroers, J.Z. Groenew., U. Braun & K. Schub. (Crous ). This genus encompasses two species of banana diseases belonging to Herpotrichiellaceae (Chaetothyriales), characterised by having conidiophore bases with rhizoid hyphal appendages and abundant micronematous conidiophores. Penidiella species with less pronounced penicillate apices, e.g. P. strumelloidea (Milko & Dunaev) Crous & U. Braun, are comparable with species of the genus Pleurotheciopsis B. Sutton (see Ellis 1976). The latter genus is distinct in having unbranched, often percurrently proliferating conidiophores, lacking ramoconidia and colourless conidia formed in simple chains.

Cladosporium helicosporum R.F. Castañeda & W.B. Kendr. (Castañeda ) is another penidiella-like fungus with terminally branched conidiophores, subdenticulate conidiogenous loci and conidia in long acropetal chains, but its affinity to Penidiella has still to be proven.

Key to Penidiella species

1. Conidiophores in vivo in well-developed, dense fascicles and distinct synnemata arising from a basal stroma; on fallen leaves of Ficus sp., Cuba...............................................................................................................................................................................

1. Conidiophores solitary, at most loosely aggregated.................................................................................................................................. 2

2. Conidiophores with a terminal conidiogenous cell, often somewhat swollen, giving rise to several ramoconidia (on one level) that form chains of straight to distinctly curved conidia; isolated from leaf of Carex sp., Russia....................................................

2. Penicillate apex of the conidiophores composed of a system of true branchlets, conidiogenous cells and ramoconidia or at least a sequence of ramoconidia on several levels; conidia usually straight......................................................................................................................... 3

3. Mycelium verruculose; long filiform conidiophores ending with a subdenticulate cell giving rise to sets of penicillate conidiogenous cells or ramoconidia which are barely distinguishable and turn into each other; ramoconidia and conidia consistently narrow, (1.5-)2(-2.5) μm wide, and aseptate, ramoconidia sometimes heterochromous; on living leaves of Nectandra coriacea, Cuba...................

3. Mycelium more or less smooth; penicillate apex at least partly with true branchlets; conidia wider, 2-5 μm, at least partly septate, uniformly pigmented................................................................................................................................................................................................. 4

4. Hyphae, conidiophores and conidia frequently distinctly constricted at the septa; penicillate apex of the conidiophores sparingly developed, branchlets more or less divergent; isolated from leaf litter of Smilax sp., Cuba..................................................................

4. Hyphae and conidia without distinct constrictions at the septa; penicillate apex of the conidiophores usually well-developed, with abundant branchings................................................................................................................................................................................................. 5

5. Conidiophores short, up to 120 × 3-4 μm, frequently with intercalary conidiogenous cell, swollen at the conidiogenous portion just below the upper septum which render the conidiophores subnodulose to distinctly nodulose, apex ± loosely penicillate; conidia (4-)5-7(-8) μm long; occasionally with micronematous conidiophores; isolated from man with tinea nigra, Venezuela.........................

5. Conidiophores much longer, up to 800 μm, 7-9 μm wide at the base, not distinctly nodulose, penicillate apex loose to often more compact, tight, metula-like; conidia longer, 7-25 × 2-5 μm; micronematous conidiophores lacking; isolated from dead leaf of Paepalanthus columbianus, Colombia.......................................................................................................................................................

Crous & U. Braun, sp. nov. MycoBank MB504510. Figs 8-9.

Fig. 8.

Penidiella columbiana (type material). A. Conidiophores on pine needle in vitro. B-H. Conidiophores with chains of disarticulating conidia. Scale bars: A = 450, B-C = 10 μm.

Fig. 9.

Penidiella columbiana (type material). A. Conidiophores. B. Ramoconidia. C. Secondary conidia. Scale bar = 10 μm. U. Braun del.

Etymology: Named after its country of origin, Colombia.

Mycelium ex hyphis ramosis, septatis, levibus, pallide brunneis, 2-3 μm latis compositum. Conidiophora ex hyphis superficialibus oriunda, penicillata, erecta, brunnea, crassitunicata, minute verruculosa, ad 800 μm longa, ad basim 7-9 μm lata, ad apicem pluriramosa, ex ramibus diversibus et cellulis conidiogenis composita, ramibus primariis (-2) subcylindraceis, 1-7-septatis, 50-120 × 4-6 μm; ramibus secundariis (-2) subcylindraceis, 1-5-septatis, 40-60 × 4-6 μm; ramibus tertiariis et subsequentibus 1-4-septatis, 10-30 × 3-5 μm. Cellulae conidiogenae terminales vel laterales, non ramosae, 5-15 × 3-5 μm, modice brunneae, minute verruculosae, apicem versus attenuatae, truncatae vel rotundatae, polyblasticae, sympodiales, cicatrices conidiales incrassatae, sed leviter fuscatae et non refractivae. Ramoconidia 0-1-septata, modice brunnea, levia, ellipsoidea, obclavata vel obovoidea, cum 1-3 hilis terminalibus, 10-20 × 3-5 μm; conidia subcylindrica vel ellipsoidea, 0-1-septata, pallide brunnea, catenata (-10), hila truncata, non incrassata, vix vel leviter fuscata.

Mycelium consisting of branched, septate, smooth, pale brown, 2-3 μm wide hyphae. Conidiophores arising from superficial mycelium, terminally penicillate, erect, brown, wall up to 1 μm wide, almost smooth to finely verruculose, up to 800 μm tall, 7-9 μm wide at the base; conidiogenous region consisting of a series of branches composed of true branchlets, conidiogenous cells and ramoconidia, branched portion usually rather compact, even metula-like, but also looser, with divergent branches; primary branches (-2), subcylindrical, 1-7-septate, 50-120 × 4-6 μm; secondary branches (-2), subcylindrical, 1-5-septate, 40-60 × 4-6 μm; tertiary and additional branches 1-4-septate, 10-30 × 3-5 μm. Conidiogenous cells terminal, intercalary or lateral, unbranched, 5-15 × 3-5 μm, medium brown, finely verruculose, tapering to a flattened or rounded (frequently swollen) apical region, scars thickened, but only somewhat darkened, not refractive. Ramoconidia 0-1-septate, medium brown, smooth, wall ≤ 1 μm wide, ellipsoidal to obclavate or obovoid, with 1-3 apical hila, 10-25 × 3-5 μm, ramoconidia with broadly truncate base, not or barely attenuated, up to 4 μm wide, or at least somewhat attenuated at the base, hila 1.5-3 μm wide. Conidia subcylindrical to ellipsoid, 0(-1)-septate, pale brown, in chains of up to 10, 7-15 × 2-3 μm, hila truncate, unthickened, barely to somewhat darkened, 1-2 μm wide.

Cultural characteristics: Colonies on PDA erumpent, spreading, with moderate aerial mycelium and smooth, even, submerged margins; olivaceous-grey in central part, iron-grey in outer region (surface); colonies fertile.

Specimen examined: Colombia, Páramo de Guasca, 3400 m alt., isolated from dead leaf of Paepalanthus columbianus (Eriocaulaceae), Aug. 1980, W. Gams, holotype CBS H-19937, culture ex-type CBS 486.80.

Notes: This isolate was originally identified as belonging to the Stenella araguata species complex. The latter name has been somewhat confused in the literature, and has been incorrectly applied to isolates associated with opportunistic human infections (de Hoog ). The “araguata” species complex is treated elsewhere in the volume (see Crous - this volume).

(R.F. Castañeda) U. Braun, Crous & R.F. Castañeda, comb. nov. MycoBank MB504511. Fig. 10.

Fig. 10.

Penidiella cubensis (type material). A. Swollen stromatic base of synnema. B. Conidiophores. C. Ramoconidia. D. Secondary conidia. Scale bar = 10 μm. U. Braun del.

Basionym: Cladosporium cubense R.F. Castañeda, Fungi Cubenses II (La Habana): 4. 1987.

In vivo: Colonies on fallen leaves, amphigenous, effuse, pilose, brown. Mycelium usually external, superficial, but also internal, composed of branched, septate, brown, thin-walled, smooth to rough-walled hyphae, 2-3 μm wide. Stromata present, 40-80 μm diam, brown, immersed. Conidiophores densely fasciculate or in distinct synnemata, arising from stromata, erect, synnemata up to about 1000 μm long and (10-)20-40(-50) μm wide, individual threads filiform, pluriseptate throughout, brown, thin-walled (≤ 0.5 μm), smooth or almost so to distinctly verruculose, apically penicillate. Conidiogenous cells integrated, terminal and intercalary, 10-30 μm long, subcylindrical, terminal conidiogenous cells often slightly enlarged at the tip, with (1-)2-3(-4) terminal or subterminal subdenticulate conidiogenous loci, short conically truncate, 1-2 μm diam, unthickened or almost so, but often slightly refractive or darkened-refractive, intercalary conidiogenous cells usually with a single lateral locus just below the upper septum, conidiogenous cells giving rise to a single set of primary ramoconidia, or a sequence of ramoconidia at different levels. Ramoconidia cylindrical to ellipsoid-fusoid, 8-18(-25) × 2-3 μm, aseptate, pale olivaceous, olivaceous-brown to brown, thin-walled, smooth or almost so to faintly verruculose, ramoconidia with broadly truncate base, barely narrowed, or ramoconidia more or less attenuated at the base, hila 1-2 μm wide, unthickened or almost so, but often slightly refractive or darkened-refractive. Conidia in long acropetal chains, narrowly ellipsoid-ovoid, fusiform, 5-12(-15) × (1-)1.5-3 μm, aseptate, pale olivaceous to brownish, thin-walled, smooth to faintly rough-walled, ends attenuated, hila 1-1.5 μm wide, unthickened, not darkened, at most somewhat refractive.

Specimen examined: Cuba, Guantánamo, Maisí, on fallen leaves of Ficus sp., 24 Apr. 1986, M. Camino, holotype INIFAT C86/134 (HAL 2019 F, ex holotype).

Notes: Cladosporium cubense was not available in culture and molecular sequence data are not available, but type material could be re-examined and revealed that this species is quite distinct from Cladosporium s. str., but agreeing with the concept of the genus Penidiella. Penidiella cubensis differs from all other species of this genus in having densely fasciculate conidiophores to synnematous conidiomata, arising from stromata.

Crous, U. Braun & R.F. Castañeda, nom. nov. MycoBank MB504512. Fig. 11.

Fig. 11.

Penidiella nectandrae (type material). A. Conidiophores. B. Ramoconidia. C. Secondary conidia. Scale bar = 10 μm. U. Braun del.

Basionym: Cladosporium ferrugineum R.F. Castañeda, Fungi Cubenses II (La Habana): 4. 1987, homonym, non C. ferrugineum Allesch., 1895.

In vivo: Colonies amphigenous, brown. Mycelium internal and external, superficial, composed of sparingly branched hyphae, septate, 1-3 μm wide, pale olivaceous-brown or brown, thin-walled (≤ 0.5 μm), smooth or almost so to distinctly verruculose, fertile cells giving rise to conidiophores somewhat swollen at the branching point, up to 5 μm diam, and somewhat darker. Stromata lacking. Conidiophores erect, straight, filiform, up to 350 μm long, 2.5-4 μm wide, pluriseptate throughout, brown, darker below and paler above, thin-walled, smooth, apex penicillate, terminal cell of the conidiophore with 2-4 short denticle-like loci giving rise to sets of conidiogenous cells or ramoconidia that then form a sequence of new sets of ramoconidia on different levels, i.e., the loose to dense, metula-like branching system is composed of conidiogenous cells and ramoconidia which are often barely distinguishable and turn into each other; conidiogenous loci terminal or subterminal, usually 1-3(-4), subdenticulate, 1-2 μm diam, conical, apically truncate, unthickened or almost so, not to somewhat darkened-refractive. Ramoconidia with truncate base, barely attenuated, or ramoconidia distinctly attenuated at the truncate base, up to 20 × 2 μm, aseptate, at the apex with 2-3(-4) subdenticulate hila, subcylindrical, very pale olivaceous, olivaceous-brown to brown, sometimes with different shades of brown (heterochromatous), thin-walled (≤ 0.5 μm), smooth to faintly verruculose. Conidia in long acropetal chains, narrowly ellipsoid-ovoid, fusiform to cylindrical, 5-16 × (1.5-)2(-2.5) μm, aseptate, very pale olivaceous, olivaceous-brown to brown, thin-walled, smooth to very faintly rough-walled, primary conidia with rounded apex and trunacte base, somewhat attenuated, secondary conidia truncate at both ends, hila 1-1.5 μm diam, unthickened or almost so, at most slightly darkened-refractive.

Cultural characteristics: Colonies on PDA slimy, smooth, spreading; aerial mycelium absent, margins smooth, irregular; surface black with patches of cream. Colonies reaching 20 mm diam after 1 mo at 25 °C in the dark; colonies sterile on PDA, SNA and OA.

Specimen examined: Cuba, Matanzas, San Miguel de los Baños, isolated from living leaves of Nectandra coriacea (Lauraceae), 24 Jan. 1987, R.F. Castañeda and G. Arnold, holotype INIFAT C87/45, culture ex-type CBS 734.87, and HAL 2018 F (ex-holotype).

Notes: Although the ex-type strain of Cladosporium ferrugineum is sterile, its LSU DNA phylogeny reveals it to be unrelated to Cladosporium s. str. (see Fig. 1 in Crous - this volume). Based on a re-examination of the type material it could clearly be shown that the morphology of this species fully agrees with the concept of the new genus Penidiella, which is supported by its phylogenetic position within Capnodiales.

Crous, R.F. Castañeda & U. Braun, sp. nov. MycoBank MB504513. Figs 12-13.

Fig. 12.

Penidiella rigidophora (type material). A-F. Micronematous conidiophores giving rise to chains of conidia. G-H. Macronematous conidiophores (note base in G, and apex in H). I. Conidia. Scale bars = 10 μm.

Fig. 13.

Penidiella rigidophora (type material). A. Hyphae. B. Conidiophores. C. Ramoconidia. D. Secondary conidia. Scale bar = 10 μm. U. Braun del.

≡ Cladosporium rigidophorum R.F. Castañeda, nom. nud. (herbarium name).

Differt a specibus Penidiellae conidiophoris dimorphosis, hyphis et conidiis ad septa saepe distincte constrictis.

Mycelium consisting of strongly branched, septate, smooth or almost so, pale olivaceous to medium brown, guttulate, commonly constricted at septa, 2-6 μm wide hyphae, swollen cells up to 8 μm wide, wall up to 1(-1.5) μm wide. Conidiophores dimorphic. Macronematous conidiophores separate, erect, subcylindrical, predominantly straight to slightly curved, terminally loosely penicillate, up to 120 μm long, and 4-5 μm wide at the base, which is neither lobed nor swollen, and lacks rhizoids, up to 10-septate, medium to dark brown, wall up to 1(-1.5) μm wide. Micronematous conidiophores erect, subcylindrical, up to 40 μm tall, 3-4 μm wide, 1-3-septate, pale to medium brown (concolorous with hyphae). Conidiogenous cells predominantly terminal, rarely intercalary, medium brown, smooth, subcylindrical, but frequently swollen at apex, 10-20 × 5-6 μm, loci (predominantly single in micronematous conidiophores, but up to 4 in macronematous conidiophores) flat-tipped, sub-denticulate or not, 1-1.5 μm wide, barely to slightly darkened and thickened-refractive. Conidia in branched chains, medium brown, verruculose, (appearing like small spines under light microscope), ellipsoid to cylindrical-oblong, up to 1(-1.5) μm wide, frequently constricted at septa, which turn dark with age; ramoconidia (10-)13-17(-25) × 3-4(-5) μm, 1(-3)-septate; secondary conidia (7-)8-10(-12) × 3-4(-5); hila unthickened to very slightly thickened and darkened, not refractive, (0.5-)1(-1.5) μm.

Cultural characteristics: Colonies on PDA erumpent, spreading, with lobate margins and moderate aerial mycelium; iron-grey (surface), with a greenish black margin; reverse greenish black. Colonies reaching 20 mm diam after 1 mo at 25 °C in the dark; colonies fertile.

Specimen examined: Cuba, isolated from leaf litter of Smilax sp. (Smilacaceae), 6. Nov. 1994, R.F. Castañeda, holotype CBS H-19938, culture ex-type CBS 314.95.

Notes: Cladosporium rigidophorum is a herbarium name, which was never validly published. The ex-type strain, however, represents a new species of Penidiella, for which a valid name with Latin diagnosis is herewith provided. This species is easily distinguishable from all other taxa of Penidiella by forming distinct constrictions at hyphal and conidial septa as well as micronematous conidiophores (except for P. venezuelensis in which a few micronematous conidiophores have been observed). It is also phylogenetically distinct from the other taxa of Penidiella (see Fig. 1 in Crous - this volume).

(Milko & Dunaev) Crous & U. Braun, comb. nov. MycoBank MB504514. Figs 14-15.

Fig. 14.

Penidiella strumelloidea (type material). A-B. Micronematous conidiophores. C-D. Macronematous conidiophores. E-G. Conidia. Scale bars = 10 μm.

Fig. 15.

Penidiella strumelloidea (type material). A. Hyphae. B. Conidiophores. C. Ramoconidia. D. Secondary conidia. Scale bars = 10 μm. U. Braun del.

Basionym: Cladosporium strumelloideum Milko & Dunaev, Novosti Sist. Nizsh. Rast. 23: 134. 1986.

Mycelium consisting of branched, septate, smooth, hyaline to pale olivaceous, 1-4 μm wide hyphae, sometimes constricted at somewhat darker septa. Conidiophores solitary, erect, arising from superficial mycelium, micronematous, i.e., reduced to conidiogenous cells, or macronematous, subcylindrical, straight to slightly curved, subcylindrical throughout or often somewhat attenuated towards the apex, 12-80 × (2-)2.5-4 μm, 0-6-septate, medium brown, smooth, wall ≤ 0.75 μm, penicillate apex formed by a terminal conidiogenous cell giving rise to a single set of ramoconidia. Conidiogenous cells terminal, integrated, subcylindrical, straight, 8-12 × 1.5-2(-2.5) μm, pale brown, thin-walled, smooth, apex obtusely rounded to somewhat clavate; loci terminal, occasionally subterminal or lateral, unthickened or almost so to slightly thickened and darkened, not refractive, 1-1.5 μm wide. Conidia in branched chains; ramoconidia subcylindrical, with 1-3 terminal loci, olivaceous-brown, smooth; secondary conidia ellipsoidal, with one side frequently straight and the other convex, straight to slightly curved, (8-)10-12(-20) × 2(-3) μm, subhyaline to olivaceous-brown, smooth, thin-walled; hila unthickened or almost so to somewhat thickened and darkened, not refractive, 1 μm wide.

Cultural characteristics: Colonies on PDA erumpent, spreading, with abundant, dense to woolly aerial mycelium, and uneven, feathery margins; surface pale olivaceous grey, reverse iron-grey. Colonies reaching 25 mm diam after 1 mo at 25 °C in the dark; colonies fertile.

Specimen examined: Russia, Yaroslavl Region, Rybinsk Reservoir, mouth of Sutka River, isolated from leaf of Carex sp. (Cyperaceae), from stagnant water, S. Ozerskaya, holotype BKMF-2534, culture ex-type CBS 114484.

Notes: Penidiella strumelloidea resembles other species of Penidiella by having penicillate conidiophores with a conidiogenous apparatus giving rise to branched conidial chains. It differs, however, from all other species of this genus in having a rather simple penicillate apex composed of a single terminal conidiogenous cell giving rise to one set of ramoconidia which form frequently somewhat curved conidia. It is also phylogenetically distinct from the other taxa of Penidiella (see Fig. 1 in Crous - this volume).

Crous & U. Braun, sp. nov. MycoBank MB504515. Figs 16-17.

Fig. 16.

Penidiella venezuelensis (type material). A. Microconidiophore. B. Apical part of macroconidiophore. C-F. Chains of conidia. Scale bars = 10 μm.

Fig. 17.

Penidiella venezuelensis (type material). A. Hypha. B. Micronematous conidiophores. C. Macronematous conidiophores. D-E. Ramoconidia. F. Secondary conidia. Scale bar = 10 μm. U. Braun del.

Etymology: Named after the geographic location of its type strain, Venezuela.

Differt a P. columbiana conidiophoris bevioribus et angustioribus, ad 20 × 3-4 μm, subnodulosis, apice plus minusve laxe penicillatis et conidiis brevioribus, (4-)5-7(-8) μm longis.

Mycelium consisting of branched, septate, smooth to faintly rough-walled, thin-walled, subhyaline, pale olivaceous to medium brown, (1.5-)2-3 μm wide hyphae. Conidiophores solitary, erect, macronematous, subcylindrical, straight to flexuous to once geniculate, up to 120 μm long, 3-4 μm wide, 1-12-septate, pale to medium olivaceous-brown or brown, thin-walled (up to about 1 μm), terminally penicillate, branched portion composed of true branchlets and/or a single set or several sets of ramoconidia, branchlets up to 50 μm long; occasionally with a few additional micronematous conidiophores, about 10-15 × 2-3 μm. Conidiogenous cells terminal and intercalary, unbranched, subcylindrical, 5-12 × 3-4 μm, medium brown, smooth or almost so to finely verruculose, apex of conidiogenous cells frequently swollen, up to 6 μm diam, with 1-3(-4) flat-tipped, non to slightly thickened, non to slightly darkened-refractive loci, 1-1.5 μm wide, frequently appearing subdenticulate, up to 1.5 μm long, intercalary conidiogenous cells also slightly swollen at the conidiogenous portion just below the upper septum, which render the conidiophores subnodulose to nodulose, swellings round about the conidiophore axis or unilateral. Conidia ellipsoid-ovoid, subcylindrical, pale to medium olivaceous-brown or brown, finely verruculose, wall ≤ 0.5 μm wide, guttulate or not, occurring in branched chains. Ramoconidia 0-1(-3)-septate, 5-15(-22) × 3-4(-5) μm, with 1-3 subdenticulate apical hila; secondary conidia 0(-1)-septate, ellipsoid, obovoid to irregular, (4-)5-7(-8) × (2-)2.5-3(-4) μm; hila non to slightly thickened, non to slightly darkened-refractive, (0.5-)1(-1.5) μm wide.

Cultural characteristics: Colonies on OA erumpent, spreading, with dense, compact aerial mycelium, and even, smooth margins; olivaceous-grey (surface), margins iron-grey. Colonies reaching 22 mm diam after 1 mo at 25 °C in the dark.

Specimen examined: Venezuela, isolated from man with tinea nigra, Jan. 1975, D. Borelli, holotype CBS H-19934, culture ex-type CBS 106.75.

Notes: The type culture of Penidiella venezuelensis was originally determined as Stenella araguata from which it is, however, quite distinct by having smooth mycelium, long penicillate conidiophores with subdenticulate conidiogenous loci, smaller conidia, and agreeing with the concept of the genus Penidiella. It is phylogenetically distinct from the other taxa of Penidiella (see Fig. 1 in Crous - this volume).

J.L. Crane & Schokn., Mycologia 78: 88. 1986.

? = Friedmanniomyces Onofri, Nova Hedwigia 68: 176. 1999.

Type species: Pseudotaeniolina convolvuli (Esfand.) J.L. Crane & Schokn., Mycologia 78: 88. 1986.

Description: Crane & Schoknecht (1986, figs 3-19).

Fig. 19.

Readeriella brunneotingens (type material). A. Leaf spot. B. Colony on MEA. C-D. Conidia. Scale bar = 10 μm.

Notes: No cultures or sequence data are available of the type species, and Pseudotaeniolina globosa De Leo, Urzì & de Hoog was placed in Pseudotaeniolina based on its morphology and ecology. The genus Friedmanniomyces is presently known from two species (Selbmann ). Morphologically Friedmanniomyces is similar to Pseudotaeniolina, but fresh material of Pseudotaeniolina convolvuli needs to be recollected before this can be clarified.

Syd. & P. Syd., Ann. Mycol. 6: 484. 1908.

= Kirramyces J. Walker, B. Sutton & Pascoe, Mycol. Res. 96: 919. 1992.

= Colletogloeopsis Crous & M.J. Wingf., Canad. J. Bot. 75: 668. 1997.

Synanamorphs: Crous, Fungal Diversity 26: 151. 2007; also pseudocercospora-like, see Crous (1998).

Type species: Readeriella mirabilis Syd. & P. Syd., Ann. Mycol. 6: 484. 1908.

Description: Crous et al. (2004b; figs 36-38).

Notes: Several coelomycete genera are presently available to accommodate anamorphs of Capnodiales that reside in Teratosphaeriaceae, for which Readeriella is the oldest name. Other genera such as Phaeophleospora Rangel, Sonderhenia H.J. Swart & J. Walker and Lecanosticta Syd. belong to Mycosphaerellaceae.

Readeriella is polyphyletic within Teratosphaeriaceae. The recognition and circumscription (synonymy) of this genus follows the principles for anamorph genera within Capnodiales as outlined in the introduction to this volume. The only unifying character is conidial pigmentation, and the mode of conidiogenesis. Conidiogenous cells range from mono- to polyphialides with periclinal thickening, to phialides with percurrent proliferation, as observed in the type species, R. mirabilis (Fig. 18). Within the form genus conidia vary from aseptate to multiseptate, smooth to rough, and have a range of synanamorphs. Readeriella mirabilis has a synanamorph with cylindrical, aseptate conidia, while other species of Readeriella again have Cibiessia synanamorphs (scytalidium-like, with chains of dry, disarticulating conidia), suggesting the conidial morphology to be quite plastic. A re-examination of R. readeriellophora Crous & Mansilla revealed pycnidia to form a central cushion on which the conidiogenous cells are arranged (Fig. 18). This unique feature is commonly known in genera such as Coniella Höhn. and Pilidiella Petr. & Syd. (Diaporthales) (Van Niekerk ), and has never been observed among anamorphs of the Capnodiales. Another species of Readeriella, namely “Phaeophleospora” toledana Crous & Bills, again forms paraphyses interspersed among conidiogenous cells, a rare feature in this group of fungi, while several species have conidiomata ranging from acervuli to pycnidia (Cortinas ). Phylogenetically this coelomycete morphology, with its characteristic conidiogenesis, has evolved several times in Teratosphaeriaceae.

(Crous & Summerell) Crous & U. Braun, comb. nov. MycoBank MB504516.

Basionym: Colletogloeopsis blakelyi Crous & Summerell, Fungal Diversity 23: 342. 2006.

Crous & Summerell, sp. nov. MycoBank MB504517. Fig. 19.

Etymology: Named after the diffuse brown pigment visible in agar when cultivated on MEA.

Readeriellae gauchensi similis, sed coloniis viridi-atris et pigmento brunneo in agaro diffundente distinguenda.

Leaf spots amphigenous, irregular specks up to 3 mm diam, medium brown with a thin, raised, concolorous border. Conidiomata amphigenous, substomatal, exuding conidia in black masses; conidiomata pycnidial in vivo and in vitro, globose, brown to black, up to 120 μm diam; wall consisting of 3-4 cell layers of brown cells of textura angularis. Conidiogenous cells brown, verruculose, aseptate, doliiform to ampulliform, or reduced to inconspicuous loci on hyphae (in vitro), proliferating percurrently near the apex, 5-7 × 3-5 μm; sympodial proliferation also observed in culture. Conidia brown, smooth to finely verruculose, ellipsoidal to subcylindrical, apex obtuse to subobtuse, tapering to a subtruncate or truncate base (1-1.5 μm wide) with inconspicuous, minute marginal frill, (5-)6-7(-8) × 2-3(-3.5) μm in vitro, becoming 1-septate; in older cultures becoming swollen, and up to 2-septate, 15 μm long and 5 μm wide.

Cultural characteristics: Colonies on MEA reaching 20 mm diam after 2 mo at 25 °C; colonies erumpent, aerial mycelium sparse to absent, margins smooth but irregularly lobate; surface irregularly folded, greenish black, with profuse sporulation, visible as oozing black conidial masses; a diffuse dark-brown pigment is also produced, resulting in inoculated MEA plates appearing dark-brown.

Specimen examined: Australia, Queensland, Cairns, Eureka Creek, 48 km from Mareeba, S 17° 11' 13.2”, E 145° 02' 27.4”, 468 m, on leaves of Eucalyptus tereticornis, 26 Aug. 2006, P.W. Crous, CBS-H 19838 holotype, culture ex-type CPC 13303 = CBS 120747.

Notes: Conidial dimensions of R. brunneotingens closely match those of Readeriella gauchensis (M.-N. Cortinas, Crous & M.J. Wingf.) Crous (Cortinas ). The two species can be distinguished in culture, however, in that colonies of R. brunneotingens are greenish black in colour, sporulate profusely, and exude a diffuse, brown pigment into the agar, whereas colonies of R. gauchensis are more greenish olivaceous, and exude a yellow pigment into the agar (Cortinas ).

(Crous & Summerell) Crous & U. Braun, comb. nov. MycoBank MB504518.

Basionym: Colletogloeopsis considenianae Crous & Summerell, Fungal Diversity 23: 343. 2006.

(M.J. Wingf. & Crous) Crous & U. Braun, comb. nov. MycoBank MB504519.

Basionym: Kirramyces destructans M.J. Wingf. & Crous, S. African J. Bot. 62: 325. 1996.

≡ Phaeophleospora destructans (M.J. Wingf. & Crous) Crous, F.A. Ferreira & B. Sutton, S. African J. Bot. 63: 113. 1997.

(Crous & Carnegie) Crous & U. Braun, comb. nov. MycoBank MB504520.

Basionym: Colletogloeopsis dimorpha Crous & Carnegie, Fungal Diversity 23: 345. 2006.

(M.-N. Cortinas, Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504521.

Basionym: Colletogloeopsis gauchensis M.-N. Cortinas, Crous & M.J. Wingf., Stud. Mycol. 55: 143. 2006.

(Gadgil & M. Dick) Crous & U. Braun, comb. nov. MycoBank MB504522.

Basionym: Septoria pulcherrima Gadgil & M. Dick, New Zealand J. Bot. 21: 49. 1983.

≡ Stagonospora pulcherrima (Gadgil & M. Dick) H.J. Swart, Trans. Brit. Mycol. Soc. 90: 285. 1988.

= Cercospora eucalypti Cooke & Massee, Grevillea 18: 7. 1889.

≡ Kirramyces eucalypti (Cooke & Massee) J. Walker, B. Sutton & Pascoe, Mycol. Res. 96: 920. 1992.

≡ Phaeophleospora eucalypti (Cooke & Massee) Crous, F.A. Ferreira & B. Sutton, S. African J. Bot. 63: 113. 1997.

Notes: The epithet “eucalypti” is preoccupied by Readeriella eucalypti (Gonz. Frag.) Crous (Summerell ), and thus the synonym “pulcherrima” becomes the next available name for this species.

Readeriella readeriellophora, see . Fig. 18.

(Crous) Crous & U. Braun, comb. nov. MycoBank MB504523.

Basionym: Colletogloeopsis stellenboschiana Crous, Stud. Mycol. 55: 110. 2006.

(M.J. Wingf., Crous & T.A. Cout.) Crous & U. Braun, comb. nov. MycoBank MB504524.

Basionym: Coniothyrium zuluense M.J. Wingf., Crous & T.A. Cout., Mycopathologia 136: 142. 1997.

≡ Colletogloeopsis zuluensis (M.J. Wingf., Crous & T.A. Cout.) M.-N. Cortinas, M.J. Wingf. & Crous (zuluense), Mycol. Res. 110: 235. 2006.

B. Sutton, Trans. Br. Mycol. Soc. 57: 540. 1971.

Type species: Staninwardia breviuscula B. Sutton, Trans. Br. Mycol. Soc. 57: 540. 1971.

Description: Sutton (1971; fig. 1).

Notes: The genus Staninwardia presently contains two species, namely S. breviuscula and Staninwardia suttonii Crous & Summerell (Summerell ), though its placement in Capnodiales was less well resolved. The genus forms acervuli on brown leaf spots, with brown, catenulate conidia covered in a mucilaginous sheath.

Schizothyriaceae clade

Desm., Ann. Sci. Nat., Bot., sér. 3:11. 1849.

Type species: Schizothyrium acerinum Desm., Ann. Sci. Nat., Bot., sér. 3:11. 1849.

Description: Batzer et al. (2007; figs 3-7).

Notes: Species of Schizothyrium (Schizothyriaceae) have Zygophiala E.W. Mason anamorphs, and were recently shown to be allied to Mycosphaerellaceae (Batzer ). Although species of Schizothyrium have thyrothecia, they cluster among genera with pseudothecial ascomata, questioning the value of this character at the family level. Based on its bitunicate asci and 1-septate ascospores, the teleomorph is comparable to others in the Capnodiales.

Mycosphaerellaceae clade

Mycosphaerella subclade

Johanson, Öfvers. Förh. Kongl. Svenska Vetensk.-Akad. 41(9): 163. 1884.

Type species: Mycosphaerella punctiformis (Pers.: Fr.) Starbäck, Bih. Kongl. Svenska Vetensk.-Akad. Handl. 15(3, 2): 9. 1889.

Anamorph: Ramularia endophylla Verkley & U. Braun, Mycol. Res. 108: 1276. 2004.

Description: Verkley et al. (2004; figs 3-16).

Notes: The genus Mycosphaerella has in the past been linked to 23 anamorph genera (Crous ), while additional genera have been linked via DNA-based studies, bringing the total to at least 30 genera (Crous & Braun 2003, Crous ). However, based on ITS and SSU DNA phylogenetic studies and a reassessment of morphological characters and conidiogenesis, several anamorph genera have recently been reduced to synonymy (Crous & Braun 2003, Crous ). Furthermore, the DNA sequence data generated to date clearly illustrate that the anamorph genera in Mycosphaerella are polyphyletic, residing in several clades within Mycosphaerella. If future collections not known from culture or DNA sequences are to be described in form genera, we recommend that the concepts as explained in Crous & Braun (2003) be used until such stage as they can be placed in Mycosphaerella, pending a modification of Art. 59 of the International Code of Botanical Nomenclature. The genus Mycosphaerella and its anamorphs represent a future topical issue of the Studies in Mycology, and will thus be treated separately.

Dissoconium subclade

de Hoog, Oorschot & Hijwegen, Proc. K. Ned. Akad. Wet., Ser. C, Biol. Med. Sci. 86(2): 198. 1983.

Type species: Dissoconium aciculare de Hoog, Oorschot & Hijwegen, Proc. K. Ned. Akad. Wet., Ser. C, Biol. Med. Sci. 86(2): 198. 1983.

? = Uwebraunia Crous & M.J. Wingf., Mycologia 88: 446. 1996.

Teleomorph: Mycosphaerella-like.

Description: de Hoog et al. (1983), Crous (1998), Crous et al. (2004b; figs 3-10).

Notes: The genus Dissoconium presently encompasses six species (Crous ), of which two, M. lateralis Crous & M.J. Wingf. (D. dekkeri de Hoog & Hijwegen), and M. communis Crous & Mansilla (D. commune Crous & Mansilla) are also known from their Mycosphaerella-like teleomorphs. No teleomorph genus will be introduced for this clade, however, until more sexual species have been collected to help clarify the morphological features of this genus. A further complication lies in the fact that yet other species, morphologically distinct from Dissoconium, also cluster in this clade (Crous, unpubl. data).

“Passalora” zambiae subclade

Crous & T.A. Cout., Stud. Mycol. 50: 209. 2004.

Description: Crous et al. (2004b; figs 32-33).

Notes: This fungus was placed in the form genus “Passalora” based on its smooth mycelium, giving rise to conidiophores forming branched chains of brown conidia with thickened, darkened, refractive hila. Although derived from single ascospores, the teleomorph material was lost, and thus it needs to be recollected before the relavance of its phylogenetic position can be fully understood.

Additional teleomorph genera considered

A. Massal., Atti Inst. Veneto Sci. Lett. Arti, Série 2, 5: 336. 1860. (Fig. 20).

Fig. 20.

Coccodinium bartschii. A. Ascomata on host. B. Ostiolar area. C. Periphysoids. D-E. Ascospores shot onto agar. F-I. Asci with thick ectotunica. J-K. Young ascospores. L-M. Mature ascospores. N. Colony on MEA. O-Q. Conidiogenous cells giving rise to conidia. R-S. Conidia. Scale bars: A, N = 250, B, D, F-G, I, L-M, O = 10 μm.

Type species: Coccodinium bartschii A. Massal., Atti Inst. Veneto Sci. Lett. Arti, Série 2, 5: 337. 1860.

Description: Eriksson (1981, figs 34-35).

Notes: The genus Coccodinium (Coccodiniaceae) is characterised by having ascomata that are sessile on a subiculum, or somewhat immersed, semiglobose, collapsed when dry, brownish, uniloculate, with a centrum that stains blue in IKI (iodine potassium iodide). Asci are bitunicate, stalked, 8-spored, saccate, and have a thick, undifferentiated endotunica. Periphyses and periphysoids are well-developed and numerous. Ascospores are elongate, fusiform, ellipsoidal or clavate, transversely septate or muriform, hyaline or brownish (Eriksson 1981), and lack a mucous sheath. Based on a SSU sequence (GenBank accession U77668) derived from a strain identified as C. bartschii (Winka ), Coccodinium appears to be allied to the taxa treated here in Teratosphaeria. Freshly collected cultures are relatively slow growing, and on MEA they form erumpent round, black colonies with sparse hyphal growth. On the surface of these colonies hyphal strands, consisting of brown, globose cells, give rise to conidia. Older cells (up to 15 μm diam) become fertile, giving rise to 1-3 conidia via inconspicuous phialidic loci. Conidia are fusoid-ellipsoidal to clavate, 3-5-septate, becoming constricted at the transverse septa, apex obtuse, base subtruncate, guttulate, smooth, widest in the upper third of the conidium, 15-40 × 4-7 μm. Phylogenetically Coccodinium is thus allied to the Chaetothyriales (Fig. 1), and not the Teratosphaeriaceae.

Trevis., Consp. Verruc.: 17. 1860. (Fig. 21).

Fig. 21.

Stigmidium schaereri. A. Lichenicolous habit on Dacampia hookeri. B. Vertical section through an ascoma. C-D. Asci. E-G. Ascospores. H. Older, brown ascospores. Scale bars = 10 μm.

Type species: Stigmidium schaereri (A. Massal.) Trevis., Consp. Verruc.: 17. 1860.

Description: Roux & Triebel (1994, figs 47-50).

Notes: The type species of the genus is lichenicolous, characterised by semi-immersed, black, globose ascomata with ostiolar periphyses and periphysoids. Asci are 8-spored, fasciculate, bitunicate, (endotunica not giving a special reaction in Congo red or toluidine blue). Ascospores are fusoid-ellipsoidal, medianly 1-septate, guttulate, thin-walled, lacking a sheath. Presently no culture is available, and thus the placement of Stigmidium remains unresolved.

DISCUSSION

From the LSU sequence data presented here, it is clear that Mycosphaerella is not monophyletic as previously suggested (Crous , Goodwin ). The first step to circumscribe natural genera within this complex was taken by Braun et al. (2003), who separated Cladosporium anamorphs from this complex, and erected Davidiella (Davidiellaceae; Schoch ) to accommodate their teleomorphs. The present study reinstates the genus Teratosphaeria for a clade of largely extremotolerant fungi (Selbmann ) and foliar pathogens of Myrtaceae and Proteaceae (Crous , b, 2006b, 2007b), and further separates generic subclades within the Mycosphaerellaceae, while Batzer et al. (2007) again revealed Schizothyrium Desm. (Schizothyriaceae) to cluster within the Mycosphaerellaceae. Our results, however, provide support for recognition of Schizothyrium as a distinct genus, although Schizothyriaceae was less well supported as being separate from Mycosphaerellaceae (Capnodiales).

Although pleomorphism represents a rather unstudied phenomenon in this group of fungi, it has been observed in several species. Within the Teratosphaeria clade, Crous et al. (2007b) recently demonstrated teleomorphs to have Readeriella and Cibiessia synanamorphs, while the black yeast genera that belong to this clade, commonly have more than one anamorph state in culture. The present study also revealed Readeriella mirabilis to have two conidial types in culture, and to be highly plastic regarding its mode of conidiogenesis, and Readeriella to be the oldest generic name available for a large group of leaf-spotting coelomycetes in the Teratosphaeriaceae (Capnodiales).

Although not commonly documented, there are ample examples of synanamorphs in Capnodiales. Within Mycosphaerella, Beilharz et al. (2004) described Passalora perplexa Beilharz, Pascoe, M.J. Wingf. & Crous as a species with a coelomycete and yeast synanamorph, while Crous & Corlett (1998) described Mycosphaerella stigmina-platani F.A. Wolf to have a Cercostigmina U. Braun and Xenostigmina Crous synanamorph, and recent collections also revealed the presence of a similar species that has typical “Stigmina” (distoseptate conidia) and Pseudocercospora (euseptate conidia) synanamorphs (Crous, unpubl. data), and Crous (1998) reported Readeriella epicoccoides (coelomycete) to have a Cercostigmina (hyphomycete) synanamorph in culture.

Although the Mycosphaerella complex encompasses thousands of names, it may appear strange that it is only now that more clarity is obtained regarding the phylogenetic relationships among taxa in this group. This is partly due to the fact that these organisms are cultivated with difficulty, and also that the first paper to address the taxonomy of this complex based on DNA sequence data was only relatively recently published (Stewart ). In the latter study, the genus Paracercospora Deighton (scars minutely thickened along the rim), was shown to be synonymous with the older genus Pseudocercospora. Similarily, Crous et al. (2001) showed that Cercostigmina (rough, irregular percurrent proliferations) was also synonymous with Pseudocercospora. This led Crous & Braun (2003) to conclude that conidiomatal type, conidial catenulation, septation and proliferation of conidiogenous cells were of less importance in separating species at the generic level. Mycovellosiella Rangel and Phaeoramularia Munt.-Cvetk. were subsequently reduced to synonymy with the older name, Passalora Fr., and characters identified as significant at the generic level were pigmentation (Cercospora vs. Passalora), scar structure (Passalora vs. Pseudocercospora), and verruculose superficial hyphae (Stenella vs. Passalora). Due to the unavailability of cultures, no decision was made regarding Stenella (verrucose conidia and mycelium), Stigmina (distoseptate conidia), and several other, less well-known genera such as Asperisporium Maubl., Denticularia Deighton, Distocercospora N. Pons & B. Sutton, Prathigada Subram., Ramulispora, Pseudocercosporidium Deighton, Stenellopsis B. Huguenin and Verrucisporota D.E. Shaw & Alcorn. In a recent study, however, Crous et al. (2006a) were able to show that Phaeoisariopsis (synnemata, conidia with slightly thickened hila) and Stigmina (distoseptate conidia) were also synonyms of Pseudocercospora.

The present study shows that most anamorph genera are polyphyletic within Teratosphaeria, and paraphyletic within Capnodiales. In some cases, generic concepts of anamorphs based on morphology and conidium ontogeny conform well with phylogenetic relationships, though this is not true in all cases due to convergence. Nevertheless, anamorphs still convey valuable morphological information that is contained in the anamorph name, and naming anamorphs continue to provide a practical system to identify the various asexual taxa encountered.