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Towards a Natural Classification of Dothidotthia and Thyrostroma in Dothidotthiaceae (Pleosporineae, Pleosporales) Article

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Towards a Natural Classification of Dothidotthia and Thyrostroma in Dothidotthiaceae (Pleosporineae, Pleosporales) Article Mycosphere 10(1): 701–738 (2019) www.mycosphere.org ISSN 2077 7019 Article Doi 10.5943/mycosphere/10/1/15 Towards a natural classification of Dothidotthia and Thyrostroma in Dothidotthiaceae (Pleosporineae, Pleosporales) Senwanna C1,2,3, Wanasinghe DN1,3,4, Bulgakov TS5, Wang Y6, Bhat DJ7, Tang AMC8, Mortimer PE1, Xu J1,4, Hyde KD1,3,4 and Phookamsak R 1,3,4* 1 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, People’s Republic of China 2 Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand 3 Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand 4 World Agroforestry Centre, East and Central Asia, Heilongtan, Kunming 650201, Yunnan, People’s Republic of China 5 Russian Research Institute of Floriculture and Subtropical Crops, Yana Fabritsiusa Street, 2/28, Sochi 354002, Krasnodar Region, Russia 6 Department of Plant Pathology, College of Agriculture, Guizhou University, Guiyang, Guizhou 550025, China 7 No. 128/1-J, Azad Housing Society, Curca, P.O. Goa Velha-403108, India 8 Division of Applied Science, College of International Education, The Hong Kong Baptist University, Hong Kong, People’s Republic of China Senwanna C, Wanasinghe DN, Bulgakov TS, Wang Y, Bhat DJ, Tang AMC, Mortimer PE, Xu J, Hyde KD, Phookamsak R 2019 – Towards a natural classification of Dothidotthia and Thyrostroma in Dothidotthiaceae (Pleosporineae, Pleosporales). Mycosphere 10(1), 701–738, Doi 10.5943/mycosphere/10/1/15 Abstract Dothidotthia and Thyrostroma (Dothidotthiaceae, Pleosporineae, Pleosporales) species are plant pathogens causing canker, dieback and leaf spots on a wide range of hosts. However, the naming species is difficult, due to insufficient protologues, poor phylogenetic understanding due to the lack of sequence data from type species and low-quality illustrations. Moreover, the connections between asexual and sexual morphs of these genera are unclear. In this study, fresh samples of Dothidotthia and Thyrostroma were collected from symptomatic twigs and branches in southern European Russia. Multi-gene phylogenetic analyses based on a concatenated LSU, SSU, ITS and TEF1-α sequence dataset were used to investigate the phylogenetic position and confirm relationships of the asexual and sexual morphs in these genera of Dothidotthiaceae. In this study, Dothidotthia can easily be distinguished from Thyrostroma based on multi-gene phylogenetic analyses coupled with morphological characters. The new species, Dothidotthia robiniae, Thyrostroma celtidis, T. lycii, T. moricola, T. robiniae, T. styphnolobii, T. tiliae, T. ulmicola and T. ulmigenum are introduced. In addition, Neodothidotthia negundinicola clusters with species of Dothidotthia and hence Neodothidotthia is synonymized under Dothidotthia. Two new combinations, D. negundinicola and D. negundinis, are introduced. Key words – 9 new species – Ascomycota – Dothideomycetes – Holomorph – Phylogeny – Taxonomy Submitted 5 July 2019, Accepted 29 October 2019, Published 31 October 2019 Corresponding Author: Rungtiwa Phookamsak – e-mail [email protected] 701 Introduction Pleosporineae M.E. Barr is a suborder of Pleosporales Luttr. ex M.E. Barr which includes 22 families, viz. Acrocalymmaceae Crous & Trakun., Ascocylindricaceae Abdel-Wahab, Bahkali, E.B.G. Jones, Ariyaw. & K.D. Hyde, Camarosporiaceae Wanas., Wijayaw., K.D. Hyde & Crous, Camarosporidiellaceae Wanas., Wijayaw., Crous & K.D. Hyde, Coniothyriaceae W.B. Cooke, Cucurbitariaceae G. Winter, Didymellaceae Gruyter, Aveskamp & Verkley, Dothidotthiaceae Crous & A.J.L. Phillips, Halojulellaceae Suetrong, K.D. Hyde & E.B.G. Jones, Leptosphaeriaceae M.E. Barr, Libertasomycetaceae Crous, Microsphaeropsidaceae Qian Chen, L. Cai & Crous, Neocamarosporiaceae Wanas., Wijayaw., Crous & K.D. Hyde, Neophaeosphaeriaceae Ariyaw. & K.D. Hyde, Neopyrenochaetaceae Valenz.-Lopez, Crous, Cano, Guarro & Stchigel, Parapyrenochaetaceae Valenz.-Lopez, Crous, Stchigel, Guarro & Cano, Phaeosphaeriaceae M.E. Barr, Pleosporaceae Nitschke, Pseudopyrenochaetaceae Valenz.-Lopez, Crous, Stchigel, Guarro & Cano, Pyrenochaetopsidaceae Valenz.-Lopez, Crous, Cano, Guarro & Stchigel, Shiraiaceae Y.X. Liu, Zi Y. Liu & K.D. Hyde and Tzeananiaceae Ariyaw., A.J.L. Phillips & Chuang (Zhang et al. 2012, Hyde et al. 2013, Wanasinghe et al. 2017a, Ariyawansa et al. 2018). Many genera and families of Pleosporineae are well-resolved based upon their morphological characteristics coupled with phylogenetic affinities i.e. Camarosporidiellaceae, Cucurbitariaceae, Didymellaceae, Leptosphaeriaceae, Phaeosphaeriaceae and Pleosporaceae (Phookamsak et al. 2014, 2017, Ariyawansa et al. 2015a, b, Chen et al. 2017, Wanasinghe et al. 2017a, b, Jaklitsch et al. 2018). In contrast, some genera and families are not well-resolved. This is because of limited taxon sampling and brief protologues (Liu et al. 2016, 2017). Barr (1989) accepted Dothidotthia as a member of Botryosphaeriaceae based on its morphological characters, such as immersed ascomata becoming erumpent to nearly superficial on woody twigs, broad and bitunicate asci. Nevertheless, multi-gene phylogenetic analyses showed that Dothidotthia resides in Pleosporales following which Phillips et al. (2008) introduced Dothidotthiaceae. Subsequent studies by Zhang et al. (2012), Hyde et al. (2013), Wijayawardene et al. (2014, 2018) and Liu et al. (2017) accepted this taxonomic arrangement. Species of Dothidotthiaceae have been commonly reported as parasitic on living plants, as well as saprobes on wood or branches of dead or decaying plants in terrestrial habitats (Hyde et al. 2013, Marin-Felix et al. 2017). Currently, Dothidotthia Höhn, Neodothidotthia Crous, Mycocentrospora Deighton, Phaeomycocentrospora Crous, H.D. Shin & U. Braun, Pleiochaeta (Sacc.) S. Hughes, Thyrostroma Höhn. and Wilsonomyces Adask., J.M. Ogawa & E.E. Butler are recognized in this family (Marin- Felix et al. 2017, Wijayawardene et al. 2018, Crous et al. 2019). However, Mycocentrospora, Phaeomycocentrospora and Pleiochaeta exhibit different morphological characters from the type genus (especially in conidia shape and appendages) but were accommodated in Dothidotthiaceae. The genus Thyrostroma was introduced by Höhnel (1911), with T. compactum (Sacc.) Höhn. as the type species. The generic synonym of Thyrostroma has been reported as Coryneum Sacc., Stegonsporium Corda, Stigmina Sacc., and Thyrococcum Höhn, Thyrostromella Höhnel and Wilsonomyces (Höhnel 1911, Morgan-Jones 1971, Sutton & Pascoe 1989, Sutton 1997, Index Fungorum 2019). However, Thyrostromella is still treated in Ascomycota genera incertae sedis (Wijayawardene et al. 2018) and Coryneum, Stigmina, Stegonsporium and Wilsonomyces were accepted as distinct genera (Ramaley 2005, Marin-Felix et al. 2017, Wijayawardene et al. 2018). Thyrostroma species have been reported as plant pathogens causing stem canker and dieback on various hosts, with a cosmopolitan distribution (Yuan & Old 1990, Kolemasova 1999, Kuz’michev et al. 2001, Sokolova 2003, Sokolova et al. 2006, Phillips et al. 2008, Kolganikhina & Sokolova 2012, Stravinskienė et al. 2015, Crous et al. 2016, Marin-Felix et al. 2017, Farr & Rossman 2019). However, based on morphology, Slippers et al. (2013) placed Thyrostroma in Botryosphaeriaceae. Dothidotthia has been reported as a sexual morph of Thyrostroma based on the production of hyphomycetes in culture from asci (Ramaley 2005). There is, however, no phylogenetic evidence for this link between these two genera. Wijayawardene et al. (2014) suggested that the usage of both names is desirable until the above-mentioned links are proven. Phylogenetic analyses based on LSU sequence data performed by Marin-Felix et al. (2017) showed that Thyrostroma clustered in 702 the Dothidotthiaceae as originally proposed by Phillips et al. (2008). Furthermore, the type species of Thyrostroma, T. compactum formed a distinct clade from Dothidotthia in Dothidotthiaceae. It was therefore assumed that Thyrostroma and Dothidotthia are not congeneric (Marin-Felix et al. 2017). Although Thyrostroma is an old genus of Dothideomycetes (Wijayawardene et al. 2014), the taxonomic concepts and phylogenetic analyses of this genus remain unclear. The objective of the present study was to clarify the taxonomic placement of Dothidotthia and Thyrostroma in Dothidotthiaceae and identify taxa based on morphology coupled with multi- gene phylogeny. Thirty-one thyrostroma-like taxa collected from Russia were examined and their DNA sequence data were obtained for use in multi-gene phylogenetic analyses. Materials & Methods Collections, isolation and identification Symptomatic specimens (Fig. 1) were collected from many hosts in different Provinces of Russia during 2015–2016. Collected specimens were brought to the laboratory in small paper bags. Specimens were examined with a Motic SMZ 168 series and the appearance of fruiting structures on the host surface was captured using a ZEISS STEREO Discovery.V8 stereomicroscope fitted with AxioCamERc5s camera. Squash mounts of fungal microscopic structures and free-hand sections of ascomata and sporodochia on glass slides in double-distilled water (ddH2O) were prepared for photography. Micro characteristics were examined and captured using a Nikon ECLIPSE 80i compound microscope, connected with a Cannon 600D digital camera and illustrated with DIC microscopy. Fungal structures were measured using Tarosoft®
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