Elsevier

Fungal Biology

Volume 121, Issue 9, September 2017, Pages 798-824
Fungal Biology

A revised family-level classification of the Polyporales (Basidiomycota)

https://doi.org/10.1016/j.funbio.2017.05.010Get rights and content

Highlights

  • We generated rpb1, nrLSU, and nrITS sequences across the Polyporales.

  • We performed Maximum Likelihood and Bayesian analyses for three dataset combinations.

  • We recognize 18 families in the Polyporales, including three described as new.

  • Three small clades and four species cannot be placed in any recognized family.

  • We recommend the use of rbp1 data for future family-level studies in the Polyporales.

Abstract

Polyporales is strongly supported as a clade of Agaricomycetes, but the lack of a consensus higher-level classification within the group is a barrier to further taxonomic revision. We amplified nrLSU, nrITS, and rpb1 genes across the Polyporales, with a special focus on the latter. We combined the new sequences with molecular data generated during the PolyPEET project and performed Maximum Likelihood and Bayesian phylogenetic analyses. Analyses of our final 3-gene dataset (292 Polyporales taxa) provide a phylogenetic overview of the order that we translate here into a formal family-level classification. Eighteen clades are assigned a family name, including three families described as new (Cerrenaceae fam. nov., Gelatoporiaceae fam. nov., Panaceae fam. nov.) and fifteen others (Dacryobolaceae, Fomitopsidaceae, Grifolaceae, Hyphodermataceae, Incrustoporiaceae, Irpicaceae, Ischnodermataceae, Laetiporaceae, Meripilaceae, Meruliaceae, Phanerochaetaceae, Podoscyphaceae, Polyporaceae, Sparassidaceae, Steccherinaceae). Three clades are given informal names (/hypochnicium,/climacocystis and/fibroporia + amyloporia). Four taxa (Candelabrochete africana, Mycoleptodonoides vassiljevae, Auriporia aurea, and Tyromyces merulinus) cannot be assigned to a family within the Polyporales. The classification proposed here provides a framework for further taxonomic revision and will facilitate communication among applied and basic scientists. A survey of morphological, anatomical, physiological, and genetic traits confirms the plasticity of characters previously emphasized in taxonomy of Polyporales.

Introduction

Polyporales is one of the most intensively studied clades of Fungi. According to MycoBank, there have been 577 taxonomic proposals in Polyporales from 2010 to 2017, including 42 new genera and one new family, Fragiliporiaceae (Zhao et al. 2015). Over the same period, 2183 publications with the keyword ‘Polyporales’ are recorded in PubMed. As major wood-decay fungi, species of Polyporales are of interest to both fungal ecologists and applied scientists. The first species of Agaricomycotina to have its genome sequenced, the model white-rot fungus Phanerochaete chrysosporium, is a member of Polyporales (Martinez et al. 2004). The first brown-rot genome, Rhodonia (Postia) placenta, was also a polypore (Martinez et al. 2009). At present, there are 46 genomes of Polyporales hosted by the Joint Genome Institute MycoCosm portal (Grigoriev et al. 2013), which is about 22 % of all 212 Agaricomycotina genomes, or about 6 % of all 772 fungal genomes. However, with roughly 1800 described species, Polyporales account for only about 1.5 % of all known species of Fungi (Kirk et al. 2008).

Polyporales were sampled extensively in phylogenetic studies using ribosomal RNA (rRNA) genes (Hibbett and Vilgalys, 1993, Hibbett and Donoghue, 1995, Boidin et al., 1998, Larsson et al., 2004, Binder et al., 2005). From such analyses, four informally named clades of Polyporales were recognized:/antrodia,/core polyporoid,/phlebioid and/residual (the/notation is used here to denote clade names; /antrodia is read as ‘(the) antrodia clade’), but support for these groups, and their interrelationships, was often lacking. Addition of protein-coding genes, including RNA polymerase II subunit 2 (rpb2), and translation elongation factor 1-α (tef1) was necessary to achieve strong support for monophyly of Polyporales as a whole, and many internal nodes (Matheny et al. 2007).

The PolyPEET project (http://wordpress.clarku.edu/polypeet/), which was active from 2010 to 2016, focused on systematics of Polyporales. PolyPEET supported research on taxonomy of Trametes (Justo and Hibbett, 2011, Carlson et al., 2014), Phanerochaete (Floudas & Hibbett 2015), Lentinus (Seelan et al. 2015), and the brown-rot polypores (Ortiz-Santana et al., 2013, Spirin et al., 2013a, Spirin et al., 2013b), as well as comparative genomics (Binder et al., 2013, Hibbett et al., 2013, Ruiz-Dueñas et al., 2013, Riley et al., 2014), sapwood and foliar endophytes (which contain a surprising diversity of Polyporales; Martin et al. 2015), and bioremediation (Young et al. 2015).

Binder et al. (2013) presented the most comprehensive phylogenetic analyses for Polyporales so far, including analyses of a 373-species, six-gene supermatrix, containing sequences from genes encoding rRNA (nrLSU, 5.8S, and nrSSU), RNA polymerase II subunits 1 and 2 (rpb1, rpb2), and tef1. Binder et al. also analysed ten Polyporales genomes, and performed phylogenetic informativeness profiling to assess the resolution afforded by individual genes. The analyses of Binder et al. upheld/antrodia,/core polyporoid,/phlebioid and/residual, with varying levels of support. Several lineages outside these major clades were also recovered. Phylogenetic informativeness profiling suggested that the RNA polymerase II large subunit (rpb1) is the most informative gene among those traditionally used in Polyporales systematics. Unfortunately, it also turned out to be the least represented in public databases.

Polyporales is now well accepted as a strongly supported clade of Agaricomycetes (Hibbett et al. 2014). However, further taxonomic revision and general communication about Polyporales is hampered by the lack of a consensus classification within the group. As reviewed by Binder et al. (2013), there are forty nomenclaturally valid family names in Polyporales, plus the new Fragiliporiaceae, although many names are rarely used. The present study continues where that of Binder et al. (2013) left off and evaluates the status of 37 of the legitimate family names available in the Polyporales. New molecular data were obtained from across the Polyporales, emphasizing rpb1 and focussing on taxa of phylogenetic and nomenclatural relevance. The new data were combined with sequences generated during the PolyPEET project and from other resources, including genomes, yielding a dataset with 292 species. A classification with eighteen families and four informal unranked clades is proposed, and the distribution of morphological, anatomical, physiological, and genetic characters that have been emphasized in prior taxonomy of Polyporales is reviewed.

Section snippets

Fungal isolates and DNA extraction

Culture collections and specimens were retrieved from the Center for Forest Mycology Research (USDA Forest Service, Madison, Wisconsin, U.S.A.), the Finnish Museum of Natural History at the University of Helsinki (Herbarium H), supplemented with c. 60 new collections and cultures made during the PolyPEET project. Protocols for culture growth and DNA extraction were the same ones outlined in Justo & Hibbett (2011).

PCR amplification and sequencing

The target loci for this study were nrITS, nrLSU, and rpb1, with a special focus

New sequences and alignments

A total of 144 rpb1, 127 nrITS, and 67 nrLSU were generated in this study. The final rpb1-only alignment contains 292 ingroup taxa and 1612 total characters, with 1415 variable positions (87 %). The nrDNA alignment contains 310 ingroup, combined nrLSU + nrITS sequences (some taxa appear more than once), and 2276 characters, with 1482 variable positions (65 %). The 3-gene dataset contains 292 ingroup taxa (no duplicated taxa), and 3888 characters, with 2897 variable positions (74 %).

All newly

Taxonomy

When deciding on the application of existing family names a pragmatic approach has been chosen, attaching the available names to well-defined and well-supported clades in the phylogenies. For areas of the phylogeny still in need of additional research we have chosen to use family names that are already published (e.g. Podoscyphaceae), acknowledging that defining their limits and composition will need further studies. In cases where no family name is available, or if they cannot be applied with

Discussion

The classification of Polyporales presented here integrates results from prior analyses by members of the PolyPEET consortium (Justo and Hibbett, 2011, Miettinen et al., 2012, Miettinen et al., 2016, Ortiz-Santana et al., 2013, Floudas and Hibbett, 2015) with those of many other research groups (Krüger and Gargas, 2004, Spirin and Zmitrovich, 2004, Sotome et al., 2008, Zhao et al., 2015, Han et al., 2016, Li et al., 2016). The combination of rpb1 and ribosomal RNA genes provides robust

Acknowledgements

This is the final paper of the PolyPEET project, which was supported by the U. S. National Science Foundation Partnerships for Enhancing Expertise in Taxonomy Program (DEB-0933081). Research under PolyPEET was complemented by projects on genomics of wood-decay fungi conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. The authors are

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