Revision of Phaeosphaeriaceae

The limit of the Colletotrichum gloeosporioides species complex is defined genetically, based on a strongly supported clade within the Colletotrichum ITS gene tree. All taxa accepted within this clade are morphologically more or less typical of the broadly defined C. gloeosporioides, as it has been applied in the literature for the past 50 years. We accept 22 species plus one subspecies within the C. gloeosporioides complex. These include C. asianum, C. cordylinicola, C. fructicola, C. gloeosporioides, C. horii, C. kahawae subsp. kahawae, C. musae, C. nupharicola, C. psidii, C. siamense, C. theobromicola, C. tropicale, and C. xanthorrhoeae, along with the taxa described here as new, C. aenigma, C. aeschynomenes, C. alatae, C. alienum, C. aotearoa, C. clidemiae, C. kahawae subsp. ciggaro, C. salsolae, and C. ti, plus the nom. nov. C. queenslandicum (for C. gloeosporioides var. minus). All of the taxa are defined genetically on the basis of multi-gene phylogenies. Brief morphological descriptions are provided for species where no modern description is available. Many of the species are unable to be reliably distinguished using ITS, the official barcoding gene for fungi. Particularly problematic are a set of species genetically close to C. musae and another set of species genetically close to C. kahawae, referred to here as the Musae clade and the Kahawae clade, respectively. Each clade contains several species that are phylogenetically well supported in multi-gene analyses, but within the clades branch lengths are short because of the small number of phylogenetically informative characters, and in a few cases individual gene trees are incongruent. Some single genes or combinations of genes, such as glyceraldehyde-3-phosphate dehydrogenase and glutamine synthetase, can be used to reliably distinguish most taxa and will need to be developed as secondary barcodes for species level identification, which is important because many of these fungi are of biosecurity significance. In addition to the accepted species, notes are provided for names where a possible close relationship with C. gloeosporioides sensu lato has been suggested in the recent literature, along with all subspecific taxa and formae speciales within C. gloeosporioides and its putative teleomorph Glomerella cingulata. Taxonomic novelties: Name replacement - C. queenslandicum B. Weir & P.R. Johnst. New species - C. aenigma B. Weir & P.R. Johnst., C. aeschynomenes B. Weir & P.R. Johnst., C. alatae B. Weir & P.R. Johnst., C. alienum B. Weir & P.R. Johnst, C. aotearoa B. Weir & P.R. Johnst., C. clidemiae B. Weir & P.R. Johnst., C. salsolae B. Weir & P.R. Johnst., C. ti B. Weir & P.R. Johnst. New subspecies - C. kahawae subsp. ciggaro B. Weir & P.R. Johnst. Typification: Epitypification - C. queenslandicum B. Weir & P.R. Johnst.

Fungal taxonomists routinely encounter problems when dealing with asexual fungal species due to poly- and paraphyletic generic phylogenies, and unclear species boundaries. These problems are aptly illustrated in the genus Phoma. This phytopathologically significant fungal genus is currently subdivided into nine sections which are mainly based on a single or just a few morphological characters. However, this subdivision is ambiguous as several of the section-specific characters can occur within a single species. In addition, many teleomorph genera have been linked to Phoma, three of which are recognised here. In this study it is attempted to delineate generic boundaries, and to come to a generic circumscription which is more correct from an evolutionary point of view by means of multilocus sequence typing. Therefore, multiple analyses were conducted utilising sequences obtained from 28S nrDNA (Large Subunit - LSU), 18S nrDNA (Small Subunit - SSU), the Internal Transcribed Spacer regions 1 & 2 and 5.8S nrDNA (ITS), and part of the β-tubulin (TUB) gene region. A total of 324 strains were included in the analyses of which most belonged to Phoma taxa, whilst 54 to related pleosporalean fungi. In total, 206 taxa were investigated, of which 159 are known to have affinities to Phoma. The phylogenetic analysis revealed that the current Boeremaean subdivision is incorrect from an evolutionary point of view, revealing the genus to be highly polyphyletic. Phoma species are retrieved in six distinct clades within the Pleosporales, and appear to reside in different families. The majority of the species, however, including the generic type, clustered in a recently established family, Didymellaceae. In the second part of this study, the phylogenetic variation of the species and varieties in this clade was further assessed. Next to the genus Didymella, which is considered to be the sole teleomorph of Phoma s. str., we also retrieved taxa belonging to the teleomorph genera Leptosphaerulina and Macroventuria in this clade. Based on the sequence data obtained, the Didymellaceae segregate into at least 18 distinct clusters, of which many can be associated with several specific taxonomic characters. Four of these clusters were defined well enough by means of phylogeny and morphology, so that the associated taxa could be transferred to separate genera. Aditionally, this study addresses the taxonomic description of eight species and two varieties that are novel to science, and the recombination of 61 additional taxa.

The anamorphic genus Phoma was subdivided into nine sections based on morphological characters, and included teleomorphs in Didymella, Leptosphaeria, Pleospora and Mycosphaerella, suggesting the polyphyly of the genus. Recent molecular, phylogenetic studies led to the conclusion that Phoma should be restricted to Didymellaceae. The present study focuses on the taxonomy of excluded Phoma species, currently classified in Phoma sections Plenodomus, Heterospora and Pilosa. Species of Leptosphaeria and Phoma section Plenodomus are reclassified in Plenodomus, Subplenodomus gen. nov., Leptosphaeria and Paraleptosphaeria gen. nov., based on the phylogeny determined by analysis of sequence data of the large subunit 28S nrDNA (LSU) and Internal Transcribed Spacer regions 1 & 2 and 5.8S nrDNA (ITS). Phoma heteromorphospora, type species of Phoma section Heterospora, and its allied species Phoma dimorphospora, are transferred to the genus Heterospora stat. nov. The Phoma acuta complex (teleomorph Leptosphaeria doliolum), is revised based on a multilocus sequence analysis of the LSU, ITS, small subunit 18S nrDNA (SSU), β-tubulin (TUB), and chitin synthase 1 (CHS-1) regions. Species of Phoma section Pilosa and allied Ascochyta species were determined to belong to Pleosporaceae based on analysis of actin (ACT) sequence data. Anamorphs that are similar morphologically to Phoma and described in Ascochyta, Asteromella, Coniothyrium, Plectophomella, Pleurophoma and Pyrenochaeta are included in this study. Phoma-like species, which grouped outside the Pleosporineae based on a LSU sequence analysis, are transferred to the genera Aposphaeria, Paraconiothyrium and Westerdykella. The genera Medicopsis gen. nov. and Nigrograna gen. nov. are introduced to accommodate the medically important species formerly known as Pyrenochaeta romeroi and Pyrenochaeta mackinnonii, respectively. Taxonomic novelties: New genera: Medicopsis Gruyter, Verkley & Crous, Nigrograna Gruyter, Verkley & Crous, Paraleptosphaeria Gruyter, Verkley & Crous, Subplenodomus Gruyter, Verkley & Crous. New species: Aposphaeria corallinolutea Gruyter, Aveskamp & Verkley, Paraconiothyrium maculicutis Verkley & Gruyter. New combinations: Coniothyrium carteri (Gruyter & Boerema) Verkley & Gruyter, C. dolichi (Mohanty) Verkley & Gruyter, C. glycines (R.B. Stewart) Verkley & Gruyter, C. multiporum (V.H. Pawar, P.N. Mathur & Thirum.) Verkley & Gruyter, C. telephii (Allesch.) Verkley & Gruyter, Heterospora (Boerema, Gruyter & Noordel.) Gruyter, Verkley & Crous, H. chenopodii (Westend.) Gruyter, Aveskamp & Verkley, H. dimorphospora (Speg.) Gruyter, Aveskamp & Verkley, Leptosphaeria errabunda (Desm.) Gruyter, Aveskamp & Verkley, L. etheridgei (L.J. Hutchison & Y. Hirats.) Gruyter, Aveskamp & Verkley, L. macrocapsa (Trail) Gruyter, Aveskamp & Verkley, L. pedicularis (Fuckel) Gruyter, Aveskamp & Verkley, L. rubefaciens (Togliani) Gruyter, Aveskamp & Verkley, L. sclerotioides (Sacc.) Gruyter, Aveskamp & Verkley, L. sydowii (Boerema, Kesteren & Loer.) Gruyter, Aveskamp & Verkley, L. veronicae (Hollós) Gruyter, Aveskamp & Verkley, Medicopsis romeroi (Borelli) Gruyter, Verkley & Crous, Nigrograna mackinnonii (Borelli) Gruyter, Verkley & Crous, Paraconiothyrium flavescens (Gruyter, Noordel. & Boerema) Verkley & Gruyter, Paracon. fuckelii (Sacc.) Verkley & Gruyter, Paracon. fusco-maculans (Sacc.) Verkley & Gruyter, Paracon. lini (Pass.) Verkley & Gruyter, Paracon. tiliae (F. Rudolphi) Verkley & Gruyter, Paraleptosphaeria dryadis (Johanson) Gruyter, Aveskamp & Verkley, Paralept. macrospora (Thüm.) Gruyter, Aveskamp & Verkley, Paralept. nitschkei (Rehm ex G. Winter) Gruyter, Aveskamp & Verkley, Paralept. orobanches (Schweinitz: Fr.) Gruyter, Aveskamp & Verkley, Paralept. praetermissa (P. Karst.) Gruyter, Aveskamp & Verkley, Plenodomus agnitus (Desm.) Gruyter, Aveskamp & Verkley, Plen. biglobosus (Shoemaker & H. Brun) Gruyter, Aveskamp & Verkley, Plen. chrysanthemi (Zachos, Constantinou & Panag.) Gruyter, Aveskamp & Verkley, Plen. collinsoniae (Dearn. & House) Gruyter, Aveskamp & Verkley, Plen. confertus (Niessl ex Sacc.) Gruyter, Aveskamp & Verkley, Plen. congestus (M.T. Lucas) Gruyter, Aveskamp & Verkley, Plen. enteroleucus (Sacc.) Gruyter, Aveskamp & Verkley, Plen. fallaciosus (Berl.) Gruyter, Aveskamp & Verkley, Plen. hendersoniae (Fuckel) Gruyter, Aveskamp & Verkley, Plen. influorescens (Boerema & Loer.) Gruyter, Aveskamp & Verkley, Plen. libanotidis (Fuckel) Gruyter, Aveskamp & Verkley, Plen. lindquistii (Frezzi) Gruyter, Aveskamp & Verkley, Plen. lupini (Ellis & Everh.) Gruyter, Aveskamp & Verkley, Plen. pimpinellae (Lowen & Sivan.) Gruyter, Aveskamp & Verkley, Plen. tracheiphilus (Petri) Gruyter, Aveskamp & Verkley, Plen. visci (Moesz) Gruyter, Aveskamp & Verkley, Pleospora fallens (Sacc.) Gruyter & Verkley, Pleo. flavigena (Constantinou & Aa) Gruyter & Verkley, Pleo. incompta (Sacc. & Martelli) Gruyter & Verkley, Pyrenochaetopsis pratorum (P.R. Johnst. & Boerema) Gruyter, Aveskamp & Verkley, Subplenodomus apiicola (Kleb.) Gruyter, Aveskamp & Verkley, Subplen. drobnjacensis (Bubák) Gruyter, Aveskamp & Verkley, Subplen. valerianae (Henn.) Gruyter, Aveskamp & Verkley, Subplen. violicola (P. Syd.) Gruyter, Aveskamp & Verkley, Westerdykella capitulum (V.H. Pawar, P.N. Mathur & Thirum.) de Gruyter, Aveskamp & Verkley, W. minutispora (P.N. Mathur ex Gruyter & Noordel.) Gruyter, Aveskamp & Verkley. New names: Pleospora angustis Gruyter & Verkley, Pleospora halimiones Gruyter & Verkley.