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Notes, Outline and Divergence Times of Basidiomycota

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Notes, Outline and Divergence Times of Basidiomycota Fungal Diversity (2019) 99:105–367 https://doi.org/10.1007/s13225-019-00435-4 (0123456789().,-volV)(0123456789().,- volV) Notes, outline and divergence times of Basidiomycota 1,2,3 1,4 3 5 5 Mao-Qiang He • Rui-Lin Zhao • Kevin D. Hyde • Dominik Begerow • Martin Kemler • 6 7 8,9 10 11 Andrey Yurkov • Eric H. C. McKenzie • Olivier Raspe´ • Makoto Kakishima • Santiago Sa´nchez-Ramı´rez • 12 13 14 15 16 Else C. Vellinga • Roy Halling • Viktor Papp • Ivan V. Zmitrovich • Bart Buyck • 8,9 3 17 18 1 Damien Ertz • Nalin N. Wijayawardene • Bao-Kai Cui • Nathan Schoutteten • Xin-Zhan Liu • 19 1 1,3 1 1 1 Tai-Hui Li • Yi-Jian Yao • Xin-Yu Zhu • An-Qi Liu • Guo-Jie Li • Ming-Zhe Zhang • 1 1 20 21,22 23 Zhi-Lin Ling • Bin Cao • Vladimı´r Antonı´n • Teun Boekhout • Bianca Denise Barbosa da Silva • 18 24 25 26 27 Eske De Crop • Cony Decock • Ba´lint Dima • Arun Kumar Dutta • Jack W. Fell • 28 29 30 31 Jo´ zsef Geml • Masoomeh Ghobad-Nejhad • Admir J. Giachini • Tatiana B. Gibertoni • 32 33,34 17 35 Sergio P. Gorjo´ n • Danny Haelewaters • Shuang-Hui He • Brendan P. Hodkinson • 36 37 38 39 40,41 Egon Horak • Tamotsu Hoshino • Alfredo Justo • Young Woon Lim • Nelson Menolli Jr. • 42 43,44 45 46 47 Armin Mesˇic´ • Jean-Marc Moncalvo • Gregory M. Mueller • La´szlo´ G. Nagy • R. Henrik Nilsson • 48 48 49 2 Machiel Noordeloos • Jorinde Nuytinck • Takamichi Orihara • Cheewangkoon Ratchadawan • 50,51 52 53 Mario Rajchenberg • Alexandre G. S. Silva-Filho • Marcelo Aloisio Sulzbacher • 42 54 18 55 Zdenko Tkalcˇec • Ricardo Valenzuela • Annemieke Verbeken • Alfredo Vizzini • 56 1 57,58 59 60 Felipe Wartchow • Tie-Zheng Wei • Michael Weiß • Chang-Lin Zhao • Paul M. Kirk Received: 15 July 2019 / Accepted: 31 August 2019 / Ó The Author(s) 2019 Abstract The Basidiomycota constitutes a major phylum of the kingdom Fungi and is second in species numbers to the Ascomycota. The present work provides an overview of all validly published, currently used basidiomycete genera to date in a single document. An outline of all genera of Basidiomycota is provided, which includes 1928 currently used genera names, with 1263 synonyms, which are distributed in 241 families, 68 orders, 18 classes and four subphyla. We provide brief notes for each accepted genus including information on classification, number of accepted species, type species, life mode, habitat, distribution, and sequence information. Furthermore, three phylogenetic analyses with combined LSU, SSU, 5.8s, rpb1, rpb2, and ef1 datasets for the subphyla Agaricomycotina, Pucciniomycotina and Ustilaginomycotina are conducted, respectively. Divergence time estimates are provided to the family level with 632 species from 62 orders, 168 families and 605 genera. Our study indicates that the divergence times of the subphyla in Basidiomycota are 406–430 Mya, classes are 211–383 Mya, and orders are 99–323 Mya, which are largely consistent with previous studies. In this study, all phylo- genetically supported families were dated, with the families of Agaricomycotina diverging from 27–178 Mya, Puccin- iomycotina from 85–222 Mya, and Ustilaginomycotina from 79–177 Mya. Divergence times as additional criterion in ranking provide additional evidence to resolve taxonomic problems in the Basidiomycota taxonomic system, and also provide a better understanding of their phylogeny and evolution. Keywords Classification Á Molecular clock Á Fungi Á Systematics Á Taxonomy Electronic supplementary material The online version of this Introduction article (https://doi.org/10.1007/s13225-019-00435-4) con- tains supplementary material, which is available to autho- rized users. The Outlines of the Fungi provide essential taxonomic information which are easy to use by workers in various & Rui-Lin Zhao disciplines incorporating mycological fields (Wijayawar- [email protected] dene et al. 2017, 2018a, b). In the Kingdom Fungi, the Extended author information available on the last page of the article phyla Ascomycota and Basidiomycota cover around 97% of all fungal species (Willis 2018). Wijayawardene et al. 123 106 Fungal Diversity (2019) 99:105–367 (2017) provided notes on 6450 genera of Ascomycota and simple pore as in the Ascomycota, being closed with a Wijayawardene et al. (2018a) provided an outline for this compact electron-dense formation, but for many repre- group. The outline of the Ascomycota was initiated by sentatives it has a thickening on both sides, appearing Eriksson and Hawksworth (1986). Follow-ups and rear- barrel-like (doliolum) in electronic microphotographs. The rangements were published in a series by Eriksson basidiomycetous cell wall is composed of chitin, whose (1991, 1998, 1999), Eriksson and Winka (1997) and fibrils are immersed in a matrix formed of (1 ? 3) - / Eriksson et al. (2003, 2004). These earlier outlines were b(1 ? 6)b–glucans and also mannans in yeast cells. chiefly based morphological characteristics. With the use Unlike the ascomycetes, the guanine-cytosine content of of molecular data, a more natural classification was the total DNA typically exceeds 50% in basidiomycetous developed and published as the Outlines of the Ascomycota species. In addition, basidiomycetes differ from ascomy- (Lumbsch and Huhndorf 2007, 2010). The most recent cetes in a number of biochemical traits, such as the for- update is that of Wijayawardene et al. (2018a). The outli- mation of urease, siderochromes, and the type of nes of the 1980s and 2018, however, are very different with ubiquinone system, which enables, for example, a clear each other, but both of them provided a working model that distinction between basidiomycete and ascomycete yeasts. other mycologists could strive to confirm or modify. The Like in all dikarya, mitosis in basidiomycetes proceeds outlines in 2007 and 2010 only included sexual morphs, with preservation of the nuclear membrane (intranuclear whereas the 2018 outline was the first to include asexual pleuromitosis) and only in some Urediniomycetes, the morphs with links provided by Hyde et al. (2011) and nuclear membrane partially degrades during mitosis (semi- Wijayawardene et al. (2012, 2017), and is becoming a open pleuromitosis). The nuclear spindle polar bodies in stable system with continual updates (Wijayawardene et al. some early divering basidiomycetes, as well as in asco- 2018a, b). Notes and outlines of the early diverging fungi mycetes are discoid, but many representatives have hemi- were provided by Wijayawardene et al. (2018b). Studies on spherical and bi-globular spindle polar bodies (Zmitrovich Basidiomycota on the other hand, have not followed such and Wasser 2011). Agaricomycotina produce macroscopic an approach, in spite of there being a real need for this to structures for sexual reproduction (basidioma) which are happen. Notes on all genera of Basidiomycota and an typical mushrooms, boletes, puffballs, earthstars or other Outline of the Basidiomycota are urgently needed. Once structures and may be above ground or sequestrate. Some such outline is in place, it can be modified and improved, taxa do not seem to form basidioma but are nevertheless much like the outline of Ascomycota, until it also becomes members of the Basidiomycota. These taxa include rusts stable. We therefore provide an account of all genera of and smuts, which comprise Pucciniomycotina and Usti- Basidiomycota with short notes on basic taxonomic infor- laginomycotina. Yeasts-forming taxa, which are usually mation and references to recent studies. We expect this to found in their asexual life mode, are also members of be followed by an outline of the Fungi (Wijayawardene Basidiomycota, and can be found in all these three sub- et al. 2019) and this to be continually updated, perhaps on a phyla. According to the latest version of Ainsworth & 2–3 year basis, until we reach a consensus for the classi- Bisby’s Dictionary of the Fungi (Kirk et al. 2008), there are fication of all of the Fungi. 1589 genera and more than 30,000 species of Basidiomy- Basidiomycota constitute a major phylum of the king- cota, which comprise nearly 32% of all described fungal dom Fungi and is second in species numbers to the taxa (Dai et al. 2015). Ascomycota (Wijayawardene et al. 2017, 2018a). Other Since the last edition of Ainsworth & Bisby’s Dictionary phyla are Aphelidiomycota, Blastocladiomycota, Cal- of the Fungi (Kirk et al. 2008), numerous sequenced-based carisporiellomycota, Chytridiomycota, Entomophthoromy- studies have enabled the introduction of a vast array of new cota, Entorrhizomycota, Glomeromycota, taxa, which has greatly enriched the known diversity of Kickxellomycota, Microsporidiomycota, Mortierellomy- Basidiomycota. At the same time, related new taxonomic cota, Mucoromycota, Olpidiomycota, Rozellomycota and categories have been proposed. For example, in phyloge- Zoopagomycota (Tedersoo et al. 2018), although the netic studies of basidiomycetous yeasts, three new classes acceptance of some phyla is disputed (Spatafora et al. Malasseziomycetes, Monilielliomycetes, and Spicu- 2016). logloeomycetes, were introduced as well as three new Species of Basidiomycota are characterized by basidia orders, 16 new families, and 47 new genera (Nasr et al. as meiosporocysts in the sexual life stage. Karyogamy and 2014a; Wang et al. 2014a, 2015d, e; Liu et al. 2015b; Riess meosis proceed in the basidia and basidiospores are pro- et al. 2016). On the other hand, many new changes have duced. The basidiomycetous hyphae, which have an elec- also occurred in the Agaricomycotina. Approximately 60 tron-dense (multi-layered or visually single-layered) wall, new genera have been recognized for agarics, 40 for are divided by septa into mononucleate, binucleate, or boletes, and 50 for bracket fungi (Desjardin et al. 2009; multinucleate segments. The septal pore may resemble a Hjortstam and Ryvarden 2010a; Petersen and Hughes 123 Fungal Diversity (2019) 99:105–367 107 2010; Cui et al. 2011b; Vellinga et al. 2011; Vizzini et al. Mya and orders 120–290 Mya were inferred by Zhao et al. 2011a; Hao et al. 2014; Hofstetter et al. 2014; Smith et al.
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