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Multiple origin of the lichenicolous life habit in Helotiales, based on nuclear ribosomal sequences

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Abstract

The Helotiales are an ecologically and morphologically highly diverse group of ascomycetes that also includes lichen-inhabiting (lichenicolous) species. We generated sequence data of three rDNA regions (nuSSU, nuLSU, 5.8S of ITS) from 28 lichenicolous specimens representing nine genera in order to determine their phylogenetic placement. Based on the most complete dataset of helotialean fungi to date, the analyses were performed using Maximum Likelihood (ML) and Bayesian approaches. Our results suggest that 1) the lichen-inhabiting life-style in Helotiales was subjected to gains or losses at least three times; 2) Thamnogalla, previously tentatively included in Ostropales, is shown to belong to Helotiales; 3) ascomata found intermixed with pycnidia of the asexual Diplolaeviopsis ranula and possessing the same pigments are tentatively considered as the sexual morph of this taxon, and are shown to belong to Helotiales; 4) the lichenicolous species of cf. Diplolaeviopsis, Llimoniella, Rhymbocarpus, Skyttea, Thamnogalla and Unguiculariopsis form a well-supported clade together with non-lichenicolous encoelioid fungi from the genera Ionomidotis, Cordierites and Encoelia; 5) Geltingia associata forms a highly supported clade with the fungicolous asexual fungus Eleutheromyces subulatus, whereas Pezizella epithallina clusters with an aquatic asexual fungus Tetracladium sp.; 6) Phaeopyxis punctum belongs to Ostropomycetidae (Lecanoromycetes), but its deep relationships to other groups remain unresolved based on rDNA sequences.

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Acknowledgments

We kindly thank Dr Zheng Wang who allowed us to use his original alignment. Rasmus Puusepp (University of Tartu) is thanked for performing lab work; the curators of NY and TU for the loan of specimens in their care; Drs Piret Lõhmus (Tartu), Sergio Pérez-Ortega (Madrid) and Jan Vondrák (Průhonice) for providing specimens of Phaeopyxis punctum, Geltingia associata and Llimoniella gregorellae respectively; Heidi Tamm for allowing us to use sequences of Encoelia furfuracea; Jaan Liira for taking photos of Llimoniella specimens. Kadri Põldmaa, Kadri Pärtel (both from University of Tartu) and Prof. Donald Pfister (Harvard University, USA) are thanked for discussions on the taxonomy of helotialean fungi, and the two first for early comments on the manuscript. Finally we would like to thank two anonymous reviewers for their valuable comments and suggestions to improve the manuscript. The study of AS was financed by the centre of Excellence (FIBIR), by the target financing project no. SF0180012s09 and by the Institutional research funding project IUT20-30.

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Authors and Affiliations

  1. Institute of Ecology and Earth Sciences, University of Tartu, 40 Lai st., EE-51005, Tartu, Estonia

    Ave Suija

  2. Département Bryophytes et Thallophytes, Jardin botanique national de Belgique, Domaine de Bouchout, B-1860, Meise, Belgium

    Damien Ertz

  3. Department of Environmental Science and Policy, George Mason University, MSN 5G8, 10900 University Boulevard, Manassas, VA, 20110-2203, USA

    James D. Lawrey

  4. Musée national d’historie naturelle, 25 rue Munster, L-2160, Luxembourg, Luxembourg

    Paul Diederich

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  1. Ave Suija
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Correspondence to Ave Suija.

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Appendix

Table 2 GenBank accession numbers of downloaded sequences used for inferring phylogenetic relationship of lichenicolous taxa
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Suija, A., Ertz, D., Lawrey, J.D. et al. Multiple origin of the lichenicolous life habit in Helotiales, based on nuclear ribosomal sequences. Fungal Diversity 70, 55–72 (2015). https://doi.org/10.1007/s13225-014-0287-4

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