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Evolution of non-lichenized, saprotrophic species of Arthonia (Ascomycota, Arthoniales) and resurrection of Naevia, with notes on Mycoporum

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Abstract

Fungi that are barely lichenized or non-lichenized and closely related to lichenized taxa, the so-called borderline fungi, are an important element in reconstructing the evolutionary history of lichenized lineages. Arthoniaceae is a prime example including non-lichenized, saprotrophic lineages which potentially were precursors to lichenized taxa. In this study, we focused on saprotrophic species of Arthonia sensu lato, including new sequence data for Arthonia pinastri. We obtained fresh material of this taxon from a living branch of Fraxinus ornus in Italy to assess its taxonomic status and to elucidate its phylogenetic relationships within Arthonia. Thin sections of the thallus and ascomata of A. pinastri confirmed the absence of a photobiont. Maximum likelihood and Bayesian analyses of combined mtSSU, nuLSU and RPB2 sequence data placed the species close to A. dispersa (barely lichenized or non-lichenized) and A. punctiformis (non-lichenized) in a clade closely related to Arthonia sensu stricto, and the A. pinastri clade is here resurrected under the name Naevia. Ancestral character state analysis within a broader context of Arthoniales does not support the saprotrophic lifestyle to be a plesiomorphic feature, but suggests loss of lichenization in Naevia, as well as loss and possible regain in a second clade containing saprotrophic species and including taxa resembling Mycoporum, underlining the evolutionary plasticity of Arthoniales. These two clades constitute model taxa to further investigate the evolution of alternative biological lifestyles within the context of chiefly lichenized taxa.

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Acknowledgements

We thank the Thailand Research Fund (“The future of specialist fungi in a changing climate: baseline data for generalist and specialist fungi associated with ants, Rhododendron species and Dracaena species DBG6080013” and “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Sub-region RDG6130001”) and “The 2019 high-end foreign expert introduction plan to Kunming Institute of Botany (granted by the Ministry of Science and Technology of the People’s Republic of China (Grant Number G20190139006)) for funding this research. S.C. Karunarathna would like to thank the CAS President’s International Fellowship Initiative (PIFI) under the following grant: 2018PC0006 and the National Science Foundation of China (NSFC, project code 31851110759). We also thank Udeni Jayalal, Nalin Wijayawardene, Ming-Ying Zhang, Mohammed Warris, Lee B.G and Eleni Gentekaki for their support during this research. Dhanushka Wanasinghe would like to thank CAS President’s International Fellowship Initiative (PIFI) for funding his postdoctoral research (Number 2019PC0008), the National Science Foundation of China and the Chinese Academy of Sciences for financial support under the following Grants: 41761144055, 41771063 and Y4ZK111B01. We also extend our gratitude to Teuvo Ahti, David Hawksworth, Pier-Luigi Nimis and Rikard Sundin and Mats Wedin who helped to clarify the nomenclatural status of the genus Naevia.

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Authors and Affiliations

  1. CAS Key Laboratory for Plant Biodiversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming, 650201, Yunnan, People’s Republic of China

    Vinodhini Thiyagaraja, Dhanushka N. Wanasinghe, Samantha C. Karunarathna & Kevin D. Hyde

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

    Vinodhini Thiyagaraja & Kevin D. Hyde

  3. Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai, 50002, Thailand

    Vinodhini Thiyagaraja

  4. World Agro Forestry Centre East and Central Asia, Kunming, 650201, Yunnan, People’s Republic of China

    Vinodhini Thiyagaraja, Dhanushka N. Wanasinghe, Samantha C. Karunarathna & Kevin D. Hyde

  5. Botanischer Garten und Botanisches Museum, Freie Universität Berlin, Königin-Luise-Str. 6–8, 14195, Berlin, Germany

    Robert Lücking

  6. Research Department, Meise Botanic Garden, Nieuwelaan 38, 1860, Meise, Belgium

    Damien Ertz

  7. Service Général de l’Enseignement Supérieur et de la Recherche Scientifique, Fédération Wallonie-Bruxelles, Rue A. Lavallée 1, 1080, Brussels, Belgium

    Damien Ertz

  8. A.M.B.G. Gruppo Micologico Forlivese “Antonio Cicognani”, Via Roma 18, Forli, Italy

    Erio Camporesi

  9. A.M.B, Circolo Micologico “Giovanni carini”, C.P. 314, Brescia, Italy

    Erio Camporesi

  10. Societa per gli Studi Naturalistici della Romagna, C.P. 144, Bagnacavallo, RA, Italy

    Erio Camporesi

Authors
  1. Vinodhini Thiyagaraja
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  2. Robert Lücking
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  5. Samantha C. Karunarathna
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  6. Erio Camporesi
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  7. Kevin D. Hyde
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Correspondence to Kevin D. Hyde.

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Thiyagaraja, V., Lücking, R., Ertz, D. et al. Evolution of non-lichenized, saprotrophic species of Arthonia (Ascomycota, Arthoniales) and resurrection of Naevia, with notes on Mycoporum. Fungal Diversity 102, 205–224 (2020). https://doi.org/10.1007/s13225-020-00451-9

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