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Stud Mycol 58(1): 1-32 2007
DOI: 10.3114/sim.2007.58.01
Copyright © 2007 CBS Fungal Biodiversity Centre
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Mycosphaerella is polyphyletic

P.W. Crous1,*, U. Braun2 and J.Z. Groenewald1

1 CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD, Utrecht, The Netherlands
2 Martin-Luther-Universität, Institut für Biologie, Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, D-06099 Halle, Germany

* Correspondence: Pedro W. Crous, p.crous{at}cbs.knaw.nl


   Abstract
TOP
 Abstract
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
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.

Taxonomic novelties: Batcheloromyces eucalypti (Alcorn) Crous & U. Braun, comb. nov., Catenulostroma Crous & U. Braun, gen. nov., Catenulostroma abietis (Butin & Pehl) Crous & U. Braun, comb. nov., Catenulostroma chromoblastomycosum Crous & U. Braun, sp. nov., Catenulostroma elginense (Joanne E. Taylor & Crous) Crous & U. Braun, comb. nov., Catenulostroma excentricum (B. Sutton & Ganap.) Crous & U. Braun, comb. nov., Catenulostroma germanicum Crous & U. Braun, sp. nov., Catenulostroma macowanii (Sacc.) Crous & U. Braun, comb. nov., Catenulostroma microsporum (Joanne E. Taylor & Crous) Crous & U. Braun, comb. nov., Catenulostroma protearum (Crous & M.E. Palm) Crous & U. Braun, comb. nov., Penidiella Crous & U. Braun, gen. nov., Penidiella columbiana Crous & U. Braun, sp. nov., Penidiella cubensis (R.F. Castañeda) U. Braun, Crous & R.F. Castañeda, comb. nov., Penidiella nectandrae Crous, U. Braun & R.F. Castañeda, nom. nov., Penidiella rigidophora Crous, R.F. Castañeda & U. Braun, sp. nov., Penidiella strumelloidea (Milko & Dunaev) Crous & U. Braun, comb. nov., Penidiella venezuelensis Crous & U. Braun, sp. nov., Readeriella blakelyi (Crous & Summerell) Crous & U. Braun, comb. nov., Readeriella brunneotingens Crous & Summerell, sp. nov., Readeriella considenianae (Crous & Summerell) Crous & U. Braun, comb. nov., Readeriella destructans (M.J. Wingf. & Crous) Crous & U. Braun, comb. nov., Readeriella dimorpha (Crous & Carnegie) Crous & U. Braun, comb. nov., Readeriella epicoccoides (Cooke & Massee) Crous & U. Braun, comb. nov., Readeriella gauchensis (M.-N. Cortinas, Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Readeriella molleriana (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Readeriella nubilosa (Ganap. & Corbin) Crous & U. Braun, comb. nov., Readeriella pulcherrima (Gadgil & M. Dick) Crous & U. Braun, comb. nov., Readeriella stellenboschiana (Crous) Crous & U. Braun, comb. nov., Readeriella toledana (Crous & Bills) Crous & U. Braun, comb. nov., Readeriella zuluensis (M.J. Wingf., Crous & T.A. Cout.) Crous & U. Braun, comb. nov., Teratosphaeria africana (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria alistairii (Crous) Crous & U. Braun, comb. nov., Teratosphaeria associata (Crous & Carnegie) Crous & U. Braun, comb. nov., Teratosphaeria bellula (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria cryptica (Cooke) Crous & U. Braun, comb. nov., Teratosphaeria dentritica (Crous & Summerell) Crous & U. Braun, comb. nov., Teratosphaeria excentrica (Crous & Carnegie) Crous & U. Braun, comb. nov., Teratosphaeria fimbriata (Crous & Summerell) Crous & U. Braun, comb. nov., Teratosphaeria flexuosa (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria gamsii (Crous) Crous & U. Braun, comb. nov., Teratosphaeria jonkershoekensis (P.S. van Wyk, Marasas & Knox-Dav.) Crous & U. Braun, comb. nov., Teratosphaeria maxii (Crous) Crous & U. Braun, comb. nov., Teratosphaeria mexicana (Crous) Crous & U. Braun, comb. nov., Teratosphaeria molleriana (Thüm.) Crous & U. Braun, comb. nov., Teratosphaeria nubilosa (Cooke) Crous & U. Braun, comb. nov., Teratosphaeria ohnowa (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria parkiiaffinis (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria parva (R.F. Park & Keane) Crous & U. Braun, comb. nov., Teratosphaeria perpendicularis (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria pluritubularis (Crous & Mansilla) Crous & U. Braun, comb. nov., Teratosphaeria pseudafricana (Crous & T.A. Cout.) Crous & U. Braun, comb. nov., Teratosphaeria pseudocryptica (Crous) Crous & U. Braun, comb. nov., Teratosphaeria pseudosuberosa (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria quasicercospora (Crous & T.A. Cout.) Crous & U. Braun, comb. nov., Teratosphaeria readeriellophora (Crous & Mansilla) Crous & U. Braun, comb. nov., Teratosphaeria secundaria (Crous & Alfenas) Crous & U. Braun, comb. nov., Teratosphaeria stramenticola (Crous & Alfenas) Crous & U. Braun, comb. nov., Teratosphaeria suberosa (Crous, F.A. Ferreira, Alfenas & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria suttonii (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov., Teratosphaeria toledana (Crous & Bills) Crous & U. Braun, comb. nov., Teratosphaeriaceae Crous & U. Braun, fam. nov.

Keywords Ascomycetes / Batcheloromyces / Colletogloeopsis / Readeriella / Teratosphaeria / Trimmatostroma / DNA sequence comparisons / systematics


   INTRODUCTION
TOP
 Abstract
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
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 et al. 2001, Goodwin et al. 2001), 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 et al. 2007b). 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 et al. 2004), and anamorph genera such as Pseudocercospora Speg., Stigmina Sacc., Phaeoisariopsis Ferraris (Crous et al. 2006a), Ramulispora Miura (Crous et al. 2003), Batcheloromyces Marasas, P.S. van Wyk & Knox-Dav. (Taylor et al. 2003), Phaeophleospora Rangel and Dothistroma Hulbary (Crous et al. 2000, 2001, Barnes et al. 2004).

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
TOP
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
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 et al. 2007). 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 et al. 2007), 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 et al. 1990), LR0R (Rehner & Samuels 1994), LR3R (www.biology.duke.edu/fungi/mycolab/primers.htm), and LR16 (Moncalvo et al. 1993), 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).


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  		Table 1. Isolates for which new sequences were generated.

 

Taxonomy
Wherever possible, 30 measurements (x 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
TOP
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
DNA phylogeny
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.


Figure 1
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  		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.


Figure 2
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  		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).

 
Taxonomy
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

Treatment of phylogenetic clades
Davidiellaceae clade
Davidiella 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 et al. 2003). The genus Cladosporium is well-established, and contains around 772 names (Dugan et al. 2004), while Davidiella presently has 33 names (www.MycoBank.org), of which only around five have acknowledged Cladosporium states.

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

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


Figure 3
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  		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:

  1. 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 et al. 2006b).
  2. 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 et al. 2007b).
  3. 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.
  4. 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.
  5. 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 et al. 2006b, 2007b, Crous & Groenewald 2006a, b), and also M. nubilosa.
  6. 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:

Teratosphaeriaceae 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.

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

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

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

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

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

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

Anamorph: Batcheloromyces sp.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

{equiv} 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.

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

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

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

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

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

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

Teratosphaeria jonkershoekensis (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.

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

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

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

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

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

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

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

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

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

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

{equiv} 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: Readeriella molleriana (Crous & M.J. Wingf.) Crous & U. Braun, comb. nov. MycoBank MB504484.

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

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

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

{equiv} Mycosphaerella nubilosa (Cooke) Hansf., Proc. Linn. Soc. New South Wales 81: 36. 1965.
= Mycosphaerella juvenis Crous & M.J. Wingf., Mycologia 88: 453. 1996.

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

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

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

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

Teratosphaeria parva (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.

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

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

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

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

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

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

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

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

Anamorph: Readeriella sp.

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

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

Anamorph: Catenulostroma sp.

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

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

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

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

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


Figure 18
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  		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.

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

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

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

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

Teratosphaeria suberosa (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.

Teratosphaeria suttonii (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: Readeriella epicoccoides (Cooke & Massee) Crous & U. Braun, comb. nov. MycoBank MB504500.

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

{equiv} Phaeophleospora epicoccoides (Cooke & Massee) Crous, F.A. Ferreira & B. Sutton, S. African J. Bot. 63: 113. 1997.
{equiv} 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: Pseudocercospora sp.

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

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

Anamorph: Readeriella toledana (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)

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

Acidomyces 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.

Batcheloromyces 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).


Figure 4
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  		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 et al. 2006a), 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).


Figure 5
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  		Fig. 5. Trimmatostroma salicis. A. Sporodochia on twig. B-E. Chains of disarticulating conidia. Scale bars = 10 µm.

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

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

Capnobotryella 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.

Catenulostroma 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 et al. 1996) 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 et al. 1996: 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 et al. 1995, Butin et al. 1996, Gorbushina et al. 1996, Kogej et al. 2006, Krumbein et al. 1996). Furthermore, isolates from humans (ex skin lesions and ex chronic osteomycelitis of human patients) and Ilex leaves are known (Butin et al. 1996). 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 et al. 1996, Kogej et al. 2006). 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

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


Figure 6
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  		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.

 
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.

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

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) x 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) x 4-5(-7) µm, 1-10-septate, medium brown, smooth to finely verruculose.


Figure 7
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  		Fig. 7. Catenulostroma germanicum (type material). A-D. Chains of disarticulating conidia in vitro. Scale bars = 10 µm.

 
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.

Catenulostroma elginense (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 Teratosphaeria excentrica.

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

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) x 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.

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

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

{equiv} Coniothecium punctiforme G. Winter, Hedwigia 24: 33. 1885, non C. punctiforme Corda, Icones Fungorum (Prague) 1: 2. 1837.
{equiv} Trimmatostroma macowanii (Sacc.) M.B. Ellis, More Dematiacous Hyphomycetes: 29. 1976.

Catenulostroma microsporum, see Teratosphaeria microspora.

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

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

Cibiessia 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.

Devriesia 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.

Hortaea 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 et al. 2000). The generic distinction with Capnobotryella is less clear, except that the latter tends to have darker, thick-walled conidia, and reduced, less prominent phialides.

Penidiella 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 et al. 2006d). 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 et al. 1997) 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