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Highlights of the Didymellaceae: a Polyphasic Approach to Characterise Phoma and Related Pleosporalean Genera

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Highlights of the Didymellaceae: a Polyphasic Approach to Characterise Phoma and Related Pleosporalean Genera available online at www.studiesinmycology.org StudieS in Mycology 65: 1–60. 2010. doi:10.3114/sim.2010.65.01 Highlights of the Didymellaceae: A polyphasic approach to characterise Phoma and related pleosporalean genera M.M. Aveskamp1, 3*#, J. de Gruyter1, 2, J.H.C. Woudenberg1, G.J.M. Verkley1 and P.W. Crous1, 3 1CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; 2Dutch Plant Protection Service (PD), Geertjesweg 15, 6706 EA Wageningen, The Netherlands; 3Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands *Correspondence: Maikel M. Aveskamp, [email protected] #Current address: Mycolim BV, Veld Oostenrijk 13, 5961 NV Horst, The Netherlands Abstract: 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 toPhoma . 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. Key words: Boeremia, coelomycetes, Didymella, Didymellaceae, DNA phylogeny, Epicoccum, Leptosphaerulina, Macroventuria, Peyronellaea, Phoma, Pleosporales, taxonomy, Stagonosporopsis. Taxonomic novelties: New genus: Boeremia Aveskamp, Gruyter & Verkley. New species: Phoma brasiliensis Aveskamp, Gruyter & Verkley, Ph. bulgarica Aveskamp, Gruyter & Verkley, Ph. dactylidis Aveskamp, Gruyter & Verkley, Ph. dimorpha Aveskamp, Gruyter & Verkley, Ph. longicolla Aveskamp, Gruyter & Verkley, Ph. minor Aveskamp, Gruyter & Verkley, Ph. pedeiae Aveskamp, Gruyter & Verkley, Ph. saxea Aveskamp, Gruyter & Verkley. New varieties: Boeremia exigua var. gilvescens Aveskamp, Gruyter & Verkley, B. exigua var. pseudolilacis Aveskamp, Gruyter & Verkley. New combinations: Boeremia crinicola (Siemasko) Aveskamp, Gruyter & Verkley, B. diversispora (Bubák) Aveskamp, Gruyter & Verkley, B. exigua var. exigua (Desm.) Aveskamp, Gruyter & Verkley, B. exigua var. heteromorpha (Schulzer & Sacc.) Aveskamp, Gruyter & Verkley, B. exigua var. lilacis (Sacc.) Aveskamp, Gruyter & Verkley, B. exigua var. linicola (Naumov & Vassiljevsky) Aveskamp, Gruyter & Verkley, B. exigua var. populi (Gruyter & Scheer) Aveskamp, Gruyter & Verkley, B. exigua var. coffeae (Henn.) Aveskamp, Gruyter & Verkley, B. exigua var. viburni (Roum. ex. Sacc.) Aveskamp, Gruyter & Verkley, B. foveata (Foister) Aveskamp, Gruyter & Verkley, B. lycopersici (Cooke) Aveskamp, Gruyter & Verkley, B. noackiana (Allesch.) Aveskamp, Gruyter & Verkley, B. sambuci-nigrae (Sacc.) Aveskamp, Gruyter & Verkley, B. strasseri (Moesz) Aveskamp, Gruyter & Verkley, B. telephii (Vestergr.) Aveskamp, Gruyter & Verkley, Epicoccum pimprinum (P.N. Mathur, S.K. Menon & Thirum.) Aveskamp, Gruyter & Verkley, E. sorghi (Sacc.) Aveskamp, Gruyter & Verkley, Peyronellaea americana (Morgan-Jones & J.F. White) Aveskamp, Gruyter & Verkley, Pey. alectorolophi (Rehm.) Aveskamp, Gruyter & Verkley, Pey. anserina (Marchal) Aveskamp, Gruyter & Verkley, Pey. arachidicola (Khokhr.) Aveskamp, Gruyter & Verkley, Pey. aurea (Gruyter, Noordel. & Boerema) Aveskamp, Gruyter & Verkley, Pey. calorpreferens (Boerema, Gruyter & Noordel.) Aveskamp, Gruyter & Verkley, Pey. coffeae-arabicae (Aveskamp, Verkley & Gruyter) Aveskamp, Gruyter & Verkley, Pey. curtisii (Berk.) Aveskamp, Gruyter & Verkley, Pey. eucalyptica (Sacc.) Aveskamp, Gruyter & Verkley, Pey. gardeniae (S. Chandra & Tandon) Aveskamp, Gruyter & Verkley, Pey. lethalis (Ellis & Bartholomew) Aveskamp, Gruyter & Verkley, Pey. pomorum var. pomorum (Thüm.) Aveskamp, Gruyter & Verkley, Pey. pomorum var. circinata (Kusnezowa) Aveskamp, Gruyter & Verkley, Pey. pomorum var. cyanea (Jooste & Papendorf) Aveskamp, Gruyter & Verkley, Pey. obtusa (Fuckel) Aveskamp, Gruyter & Verkley, Pey. pinodella (L.K. Jones) Aveskamp, Gruyter & Verkley, Pey. pinodes (Berk. & A. Bloxam) Aveskamp, Gruyter & Verkley, Pey. protuberans (Lév.) Aveskamp, Gruyter & Verkley, Pey. sancta (Aveskamp, Gruyter & Verkley) Aveskamp, Gruyter & Verkley, Pey. subglomerata (Boerema, Gruyter & Noordel.) Aveskamp, Gruyter & Verkley, Pey. zeae-maydis (Arny & R.R. Nelson)Aveskamp, Gruyter & Verkley, Phoma clematidis-rectae (Petr.) Aveskamp, Woudenberg & Gruyter, Ph. noackiana (Allesch.) Aveskamp, Gruyter & Verkley, Stagonosporopsis ajacis (Thüm.) Aveskamp, Gruyter & Verkley, S. andigena (Turkenst.) Aveskamp, Gruyter & Verkley, S. artemisiicola (Hollós) Aveskamp, Gruyter & Verkley, S. astragali (Cooke & Harkn.) Aveskamp, Gruyter & Verkley, S. caricae (Sydow & P. Sydow) Aveskamp, Gruyter & Verkley, S. crystalliniformis (Loer., R. Navarro, M. Lôbo & Turkenst.) Aveskamp, Gruyter & Verkley, S. cucurbitacearum (Fr.) Aveskamp, Gruyter & Verkley, S. dorenboschii (Noordel. & Gruyter) Aveskamp, Gruyter & Verkley, S. heliopsidis (H.C. Greene) Aveskamp, Gruyter & Verkley, S. ligulicola var. ligulicola (K.F. Baker, Dimock & L.H. Davis) Aveskamp, Gruyter & Verkley, S. ligulicola var. inoxydabilis (Boerema) Aveskamp, Gruyter & Verkley, S. loticola (Died.) Aveskamp, Gruyter & Verkley, S. oculo-hominis (Punith.) Aveskamp, Gruyter & Verkley, S. rudbeckiae (Fairm.) Aveskamp, Gruyter & Verkley, S. trachelii (Allesch.) Aveskamp, Gruyter & Verkley, S. valerianellaea (Gindrat, Semecnik & Bolay) Aveskamp, Gruyter & Verkley. New names: Peyronellaea australis Aveskamp, Gruyter & Verkley, Phoma fungicola Aveskamp, Gruyter & Verkley, Ph. novae- verbascicola Aveskamp, Gruyter & Verkley. Copyright 2010 CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. Open access under CC BY-NC-ND license. You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 1 AveSkAMp et al. INTRODUCTION habitat of Phoma spp. is the marine environment (Kohlmeyer & Volkmann-Kohlmeyer 1991), in which Phoma species are regularly Coelomycetous fungi (Grove 1935) are geographically widespread found that are completely new to science (e.g. Osterhage et al. and are found in numerous ecological niches. Sutton (1980) 2000, Yarden et al. 2007). mentions exponents of this anamorph group inhabiting soil, The genus Phoma has always been considered to be one of organic debris, and water, as well as species that parasitise other the largest fungal genera, with more than 3 000 infrageneric taxa fungi, lichens, insects and vertebrates. A substantial percentage described (Monte et al. 1991). The number of species described of the coelomycetes is associated with plant material, either as in Phoma rose to this level due to the common practice of host opportunists or as primary pathogens (Sutton 1980). associated nomenclature, in combination
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