A six-gene phylogenetic overview of Basidiomycota and allied phyla with estimated divergence times of higher taxa and a phyloproteomics perspective

In this paper, we provide a phylogenetic overview of Basidiomycota and related phyla in relation to ten years of DNA based phylogenetic studies since the AFTOL publications in 2007. We selected 529 species to address phylogenetic relationships of higher-level taxa using a maximum-likelihood framework and sequence data from six genes traditionally used in fungal molecular systematics (nrLSU, nrSSU, 5.8S, tef1-α, rpb1 and rpb2). These species represent 18 classes, 62 orders, 183 families, and 392 genera from the phyla Basidiomycota (including the newly recognized subphylum Wallemiomycotina) and Entorrhizomycota, and 13 species representing 13 classes of Ascomycota as outgroup taxa. We also conducted a molecular dating analysis based on these six genes for 116 species representing 17 classes and 54 orders of Basidiomycota and Entorrhizomycota. Finally we performed a phyloproteomics analysis from 109 Basidiomycota species and 6 outgroup taxa using amino-acid sequences retrieved from 396 orthologous genes. Recognition of higher taxa follows the criteria in Zhao et al (Fungal Divers 78:239–292, 2016): (i) taxa must be monophyletic and statistically well-supported in molecular dating analyses, (ii) their respective stem ages should be roughly equivalent, and (iii) stem ages of higher taxa must be older than those of lower level taxa. The time-tree indicates that the mean of stem ages of Basidiomycota and Entorrhizomycota are ca. 530 Ma; subphyla of Basidiomycota are 406–490 Ma; most classes are 358–393 Ma for those of Agaricomycotina and 245–356 Ma for those of Pucciniomycotina and Ustilaginomycotina; most orders of those subphyla split 120–290 Ma. Monophyly of most higher-level taxa of Basidiomycota are generally supported, especially those taxa introduced in the recent ten years: phylum Entorrhizomycota, classes Malasseziomycetes, Moniliellomycetes, Spiculogloeomycetes, Tritirachiomycetes and orders Amylocorticiales, Golubeviales, Holtermanniales, Jaapiales, Lepidostromatales, Robbauerales, Stereopsidales and Trichosporonales. However, the younger divergence times of Leucosporidiales (Microbotryomycetes) indicate that its order status is not supported, thus we propose combining it under Microbotryales. On the other hand, the families Buckleyzymaceae and Sakaguchiaceae (Cystobasidiomycetes) are raised to Buckleyzymales and Sakaguchiales due to their older divergence times. Cystofilobasidiales (Tremellomycetes) has an older divergence time and should be amended to a higher rank. We however, do not introduce it as new class here for Cystofilobasidiales, as DNA sequences from these taxa are not from their respective types and thus await further studies. Divergence times for Exobasidiomycetes, Cantharellales, Gomphales and Hysterangiales were obtained based on limited species sequences in molecular dating study. More comprehensive phylogenetic studies on those four taxa are needed in the future because our ML analysis based on wider sampling, shows they are not monophyletic groups. In general, the six-gene phylogenies are in agreement with the phyloproteomics tree except for the placements of Wallemiomycotina, orders Amylocorticiales, Auriculariales, Cantharellales, Geastrales, Sebacinales and Trechisporales from Agaricomycetes. These conflicting placements in the six-gene phylogeny vs the phyloproteomics tree are discussed. This leads to future perspectives for assessing gene orthology and problems in deciphering taxon ranks using divergence times.

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