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Elucidation of the life cycle of the endophytic genus Muscodor and its transfer to Induratia in Induratiaceae fam. nov., based on a polyphasic taxonomic approach

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Abstract

Molecular phylogenetic studies of cultures derived from some specimens of plant-inhabiting Sordariomycetes using ITS, LSU, rpb2 and tub2 DNA sequence data revealed close affinities to strains of Muscodor. The taxonomy of this biotechnologically important genus, which exclusively consists of endophytes with sterile mycelia that produce antibiotic volatile secondary metabolites, was based on a rather tentative taxonomic concept. Even though it was accommodated in Xylariaceae, its phylogenetic position had so far remained obscure. Our phylogeny shows that Muscodor species have affinities to the xylarialean genera Emarcea and Induratia, which is corroborated by the fact that their sexual states produce characteristic apiospores. These data allow for the integration of Muscodor in Induratia, i.e. the genus that was historically described first. The multi-locus phylogenetic tree clearly revealed that a clade comprising Emarcea and Induratia forms a monophylum separate from representatives of Xylariaceae, for which we propose the new family Induratiaceae. Divergence time estimations revealed that Induratiaceae has been diverged from the Xylariaceae + Clypeosphaeriaceae clade at 93 (69–119) million years ago (Mya) with the crown age of 61 (39–85) Mya during the Cretaceous period. The ascospore-derived cultures were studied for the production of volatile metabolites, using both, dual cultures for assessment of antimicrobial effects and extensive analyses using gas chromatography coupled with mass spectrometry (GC–MS). The antimicrobial effects observed were significant, but not as strong as in the case of the previous reports on Muscodor species. The GC–MS results give rise to some doubt on the validity of the previous identification of certain volatiles. Many peaks in the GC–MS chromatograms could not be safely identified by database searches and may represent new natural products. The isolation of these compounds by preparative chromatography and their subsequent characterisation by nuclear magnetic resonance (NMR) spectroscopy or total synthesis will allow for a more concise identification of these volatiles, and they should also be checked for their individual contribution to the observed antibiotic effects. This will be an important prerequisite for the development of biocontrol strains.

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Acknowledgements

We wish to thank Anke Skiba for expert technical assistance, Yasmina Marin Felix for help with the microscopic studies of the Induratia SMH specimen and Konstanze Bensch (Mycobank) and Roland Kirschner (Taiwan) for valuable advice on how to handle the difficult nomenclatural problems that were created by the mycologists who had previously erected invalid species in Muscodor. Sabine Huhndorf is thanked for the use of her specimen (SMH 1255). Kevin D. Hyde would like to thank the Thailand Research Fund for a grant entitled “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Sub region (grant no: RDG6130001) for supporting this study. Jian-Kui (Jack) Liu thanks the Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou province (Grant No. U1812401). This research work was supported by Chiang Mai University. Milan C. Samarakoon is grateful to the Mushroom Research Foundation (MRF), Chiang Rai, Thailand for providing a Postgraduate Scholarship. Mark Brönstrup thanks for support from EMBRIC, the EU-funded European Marine Biological Research Infrastructure Cluster [654008]. The authors extend their gratitude to Sajeewa S.N. Maharachchikumbura, Eric H.C. McKenzie, Saranyaphat Boonmee, Shaun Pennycook, Dinushani A. Daranagama, Nimali I. de Silva, Binu Samarakoon, Wilawan Punyaboon and Sornram Sukpisit for their valuable suggestions and support.

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Author notes

  1. Milan C. Samarakoon and Benjarong Thongbai contributed equally to this study.

Authors and Affiliations

  1. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, 132, Lanhei Road, Kunming, 650201, People’s Republic of China

    Milan C. Samarakoon, Benjarong Thongbai & Kevin D. Hyde

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

    Milan C. Samarakoon & Kevin D. Hyde

  3. School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu, 611731, People’s Republic of China

    Milan C. Samarakoon & Jian-Kui (Jack) Liu

  4. Guizhou Key Laboratory of Agricultural Biotechnology, Guizhou Academy of Agricultural Sciences, Guiyang, 550006, People’s Republic of China

    Milan C. Samarakoon & Jian-Kui (Jack) Liu

  5. Department of Microbial Drugs, Helmholtz-Zentrum für Infektionsforschung GmbH, Inhoffenstrasse 7, 38124, Brunswick, Germany

    Benjarong Thongbai, Christopher Lambert & Marc Stadler

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

    Milan C. Samarakoon & Itthayakorn Promputtha

  7. Department of Chemical Biology, Helmholtz-Zentrum für Infektionsforschung GmbH, Inhoffenstrasse 7, 38124, Brunswick, Germany

    Mark Brönstrup & Ulrike Beutling

  8. Illinois Natural History Survey, University of Illinois, 1816 South Oak Street, Champaign, IL, 61820-6970, USA

    Andrew N. Miller

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

    Itthayakorn Promputtha

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  1. Milan C. Samarakoon
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Correspondence to Kevin D. Hyde.

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Samarakoon, M.C., Thongbai, B., Hyde, K.D. et al. Elucidation of the life cycle of the endophytic genus Muscodor and its transfer to Induratia in Induratiaceae fam. nov., based on a polyphasic taxonomic approach. Fungal Diversity 101, 177–210 (2020). https://doi.org/10.1007/s13225-020-00443-9

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