A revised family-level classification of the Polyporales (Basidiomycota)
Graphical abstract
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
References (80)
- et al.
Revisiting the taxonomy of Phanerochaete (Polyporales, Basidiomycota) using a four gene dataset and extensive ITS sampling
Fungal Biology
(2015) - et al.
Lower level relationships in the mushroom genus Cortinarius (Basidiomycota, Agaricales): a comparison of RPB1, RPB2 and ITS phylogenies
Molecular Phylogenetics and Evolution
(2005) Molecular phylogeny of Hyphoderma and the reinstatement of Peniophorella
Mycological Research
(2007)- et al.
High phylogenetic diversity among corticioid homobasidiomycetes
Mycological Research
(2004) - et al.
Taxonomic and phylogenetic studies reveal a new species from Funalia gallica complex (Polyporales, Basidiomycota)
Mycological Progress
(2016) - et al.
Extensive characterization of the new genus Rickiopora (Polyporales)
Fungal Biology
(2016) - et al.
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics
Polyporaceae s.l
(2005)- et al.
Corticiaceae s.l
(2010) - et al.
The phylogenetic distribution of resupinate forms in the homobasidiomycetes
Systematics and Biodiversity
(2005)
Phylogenetic and phylogenomic overview of the Polyporales
Mycologia
Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae dominated by corticioid forms
Mycologia
Taxonomie moleculaire des Aphyllophorales
Mycotaxon
Species delimitation in Trametes: a comparison of ITS, RPB1, RPB2 and TEF1 gene phylogenies
Mycologia
Bayesian phylogenetics with BEAUti and the BEAST 1.7
Molecular Biology and Evolution
Canker formation and decay in sugar maple and paper birch infected by Cerrena unicolor
Canadian Journal of Forest Research
Aleurodiscus-Confertobasidium
Coronicium-Hyphoderma
Hyphodermella-Mycoacia
Mycoaciella-Phanerochaete
Phlebia-Sarcodontia
Schizopora-Suillosporium
The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes
Science
ITS primers with enhanced specificity for basidiomycetes e application to the identification of mycorrhizae and rusts
Molecular Ecology
MycoCosm portal: gearing up for 1000 fungal genomes
Nucleic Acids Research
Pseudolagarobasidium (Basidiomycota): on the reinstatement of a genus of parasitic, saprophytic, and endophytic resupinate fungi
Botany
Taxonomy and phylogeny of the brown-rot fungi: Fomitopsis and its related genera
Fungal Diversity
Phylogenetic relationships of Lentinus (Basidiomycotina) inferred from molecular and morphological characters
Systematic Botany
Progress toward a phylogenetic classification of the Polyporaceae through parsimony analyses of ribosomal DNA sequences
Canadian Journal of Botany
Toward genome-enabled mycology
Mycologia
Agaricomycetes
Introduction and keys
Phlebiella-Thanatephorus-Ypsilonidium
Polyporales genomes reveal the genetic architecture underlying tetrapolar and bipolar mating systems
Mycologia
Higher Taxa of Basidiomycetes
Phylogenetic classification of Trametes (Basidiomycota, Polyporales) based on a five-marker dataset
Taxon
MAFFT multiple sequence alignment software version 7: improvements in performance and usability
Molecular Biology and Evolution
Dictionary of the Fungi
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