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Taxonomy, phylogeny, molecular dating and ancestral state reconstruction of Xylariomycetidae (Sordariomycetes)

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Abstract

Xylariomycetidae (Ascomycota) is a highly diversified group with variable stromatic characters. Our research focused on inconspicuous stromatic xylarialean taxa from China, Italy, Russia, Thailand and the United Kingdom. Detailed morphological descriptions, illustrations and combined ITS-LSU-rpb2-tub2-tef1 phylogenies revealed 39 taxa from our collections belonging to Amphisphaeriales and Xylariales. A new family (Appendicosporaceae), five new genera (Magnostiolata, Melanostictus, Neoamphisphaeria, Nigropunctata and Paravamsapriya), 27 new species (Acrocordiella photiniicola, Allocryptovalsa sichuanensis, Amphisphaeria parvispora, Anthostomella lamiacearum, Apiospora guiyangensis, A. sichuanensis, Biscogniauxia magna, Eutypa camelliae, Helicogermslita clypeata, Hypocopra zeae, Magnostiolata mucida, Melanostictus longiostiolatus, M. thailandicus, Nemania longipedicellata, N. delonicis, N. paraphysata, N. thailandensis, Neoamphisphaeria hyalinospora, Neoanthostomella bambusicola, Nigropunctata bambusicola, N. nigrocircularis, N. thailandica, Occultitheca rosae, Paravamsapriya ostiolata, Peroneutypa leucaenae, Seiridium italicum and Vamsapriya mucosa) and seven new host/geographical records are introduced and reported. Divergence time estimates indicate that Delonicicolales diverged from Amphisphaeriales + Xylariales at 161 (123–197) MYA. Amphisphaeriales and Xylariales diverged 154 (117–190) MYA with a crown age of 127 (92–165) MYA and 147 (111–184) MYA, respectively. Appendicosporaceae (Amphisphaeriales) has a stem age of 89 (65–117) MYA. Ancestral character state reconstruction indicates that astromatic, clypeate ascomata with aseptate, hyaline ascospores that lack germ slits may probably be ancestral Xylariomycetidae having plant-fungal endophytic associations. The Amphisphaeriales remained mostly astromatic with common septate, hyaline ascospores. Stromatic variations may have developed mostly during the Cretaceous period. Brown ascospores are common in Xylariales, but they first appeared in Amphisphaeriaceae, Melogrammataceae and Sporocadaceae during the early Cretaceous. The ascospore germ slits appeared only in Xylariales during the Cretaceous after the divergence of Lopadostomataceae. Hyaline, filiform and apiospores may have appeared as separate lineages, providing the basis for Xylariaceae, which may have diverged independently. The future classification of polyphyletic xylarialean taxa will not be based on stromatic variations, but the type of ring, the colour of the ascospores, and the presence or absence or the type of germ slit.

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Acknowledgements

This study was supported by the Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou province (Grant No. U1812401). Kevin D. Hyde thanks the Thailand Research grant entitled “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Subregion” (Grant No: RDG6130001), Thailand Science Research and Innovation (TSRI) grant entitled "Macrofungi diversity research from the Lancang-Mekong watershed and surrounding areas (Grant No: DBG6280009), and Chaing Mai University for the award of Visiting Professor. This research work was supported by the Mushroom Research Foundation (MRF) and the Chiang Mai University. Timur Bulgakov was supported by the State Research Task of the Subtropical Scientific Centre of the Russian Academy of Sciences (Theme No. 0492-2021-0007). Gareth Jones is supported under the Distinguished Scientist Fellowship Program (DSFP), King Saud University, Kingdom of Saudi Arabia. The authors extend their gratitude to Hiran Ariyawansa, Eleni Gentekaki, Samantha C. Karunarathna, Thilini Chethana, Shaun Pennycook, Saranyaphat Boonmee and Dinushani A. Daranagama for their valuable suggestions. We thank the technical staff of the Center of Excellence in Fungal Research, Sornram Sukpisit, Wilawan Punyaboon and Witchuda Taliam for their invaluable assistance. Feng Yao, Asha J. Dissanayake and Ning-Guo Liu are thanked for their valuable assistance.

Funding

Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou province, U1812401, Jian-Kui Jack Liu, Thailand Research, RDG6130001, Kevin D. Hyde, Thailand Science Research and Innovation (TSRI) grant, DBG6280009, Kevin D. Hyde.

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Authors and Affiliations

  1. School of Life Science and Technology, Center for Informational Biology, University of Electronic Science and Technology of China, Chengdu, 611731, People’s Republic of China

    Milan C. Samarakoon, Sajeewa S. N. Maharachchikumbura & Jian-Kui Liu

  2. Research Center in Bioresources for Agriculture, Industry and Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand

    Milan C. Samarakoon & Kevin D. Hyde

  3. Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand

    Milan C. Samarakoon, Itthayakorn Promputtha & Nakarin Suwannarach

  4. Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Milan C. Samarakoon & Kevin D. Hyde

  5. Mushroom Research Foundation, 128 M.3 Ban Pa Deng T. Pa Pae, A. Mae Taeng, Chiang Mai, 50150, Thailand

    Milan C. Samarakoon

  6. Institute of Microbiology, Technische Universität Braunschweig, Spielmannstraße 7, 38106, Brunswick, Germany

    Marc Stadler

  7. Department of Botany and Microbiology, College of Science, King Saud University, P.O Box 2455, Riyadh, 11451, Kingdom of Saudi Arabia

    E. B. Gareth Jones

  8. Research Center of Microbial Diversity and Sustainable Utilization, Chiang Mai University, Chiang Mai, 50200, Thailand

    Kevin D. Hyde & Nakarin Suwannarach

  9. A.M.B. Gruppo, Micologico Forlivese ‘‘Antonio Cicognani’’, Via Roma 18, Forlí, Italy

    Erio Camporesi

  10. Department of Plant Protection, Federal Research Centre the Subtropical Scientific Centre of the Russian Academy of Sciences, Yana Fabritsiusa Street 2/28, Sochi, Krasnodar Region, Russia, 354002

    Timur S. Bulgakov

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  1. Milan C. Samarakoon
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Samarakoon, M.C., Hyde, K.D., Maharachchikumbura, S.S.N. et al. Taxonomy, phylogeny, molecular dating and ancestral state reconstruction of Xylariomycetidae (Sordariomycetes). Fungal Diversity 112, 1–88 (2022). https://doi.org/10.1007/s13225-021-00495-5

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