Evolutionary building lots on Ustilaginomycotina
Final Report Abstract
In recent years, a modern classification system for the Ustilaginomycotina has been developed, which is now widely accepted. Nevertheless, there are some phylogenetic relationships at different taxonomic levels that need to be re-examined in light of the combined morphological and molecular evidence available to us. When we started our project three evolutionary questions needed to be resolved: (i) Is the Entorrhizales clearly within the Ustilaginomycotina? (ii) Is Uleiella a genus of the Ustilaginomycotina? (iii) Is the Ceraceosorales the most basal evolutionary line within the Ustilaginomycotina? To address the first question, we assembled a dataset of rDNA (18S, 5.8S and 28S) and amino acid (RPB1 and RPB2) sequences to estimate the position of the genus Entorrhiza and a dataset of SSU and LSU sequences from 22 fungal species for inferring the phylogenetic placement of the genus Talbotiomyces. For the second question, we separately analysed a dataset of 86 species of Basidiomycota including 18S, 28S and rpb1 (exons B–C) sequences to roughly estimate the phylogenetic position and age of the Ustilaginomycotina, and generated a dataset of 23 Ustilaginomycota species including 18S, ITS, 28S, rpb2 and EF1α to accurately analyse the age and phylogenetic position of Uleiella within the Ustilaginomycotina. For the third question, datasets including 18S, 5.8S, 28S, RPB2, TEF1 and complete sequences were analysed. Entorrhiza appeared as a highly supported monophyletic lineage representing the sister group to the rest of the Dikarya, a phylogenetic placement that received both moderate maximum likelihood and maximum parsimony bootstrap support values. An alternative maximum likelihood tree with the constraint that Entorrhiza forms a monophyletic group with Basidiomycota could not be rejected. According to the first phylogenetic hypothesis, the teliospore tetrads of Entorrhiza represent the prototype of the dikaryan meiosporangium. The alternative hypothesis is supported by similarities in septal pore structure, cell wall and spindle pole bodies. The genus Talbotiomyces appeared to be a close relative of Entorrhiza forming a highly supported lineage: Entorrhiza species are characterised by septa with dolipores and occur on monocotyledons, while Talbotiomyces species are characterised by simple septal pores and are association with eudicots. These findings expand the host range of the recently described Entorrhizomycota from the Poales to other angiosperms. Divergence time estimates indicate that the majority of smut fungal orders diversified during the Triassic–Jurassic period, but the origin and relationships of several orders remain uncertain. The most recent common ancestor between Uleiella chilensis and Violaceomyces palustris has been dated to the Lower Cretaceous. Comparisons of divergence time estimates between smut fungi and host plants lead to the hypothesis that the early Ustilaginomycotina had a saprobic lifestyle. As there are only two extant species of Araucaria in South America, each hosting a unique Uleiella species, we suggest that either coevolution or a host shift followed by allopatric speciation are the most likely explanations for the current geographic restriction of Uleiella and its low diversity. Phylogenetic and age estimation analyses, ecology, the unusual life cycle and the peculiar combination of septal and haustorial characteristics support Uleiella chilensis as a distinct lineage among the Ustilaginomycotina. Our study indicated that Ceraceosorus belongs to the Ustilaginomycotina with some affinities to the Exobasidiomycetes. A new phylum Entorrhizomycota and a new order Talbotiomycetales ord. nov. (incl. Talbotiomycetaceae fam. nov.) are proposed to accommodate the genera Entorrhiza and Talbotiomyces, respectively. The origin of Entorrhizomycota was estimated around Upper Proterozoic and it diverged during the Eocene into the extant orders Talbotiomyces and Entorrhizales. The split of major lineages within Entorrhizales matches roughly Cyperaceae and Juncaceae divergence. Based on the phylogenetic and morphological separation of the species associated with Juncaceae, we proposed a new genus Juncorrhiza. A new genus, Juncorrhiza, was described to accommodate those classical species of the genus Entorrhiza containing warty ornamented spores and occurring associated with Juncaceae.
Publications
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(2015) Entorrhizomycota: a new fungal phylum reveals new perspectives on the evolution on Fungi. PLoS ONE 10: e0128183
Bauer R, Garnica S, Oberwinkler F, Riess K, Weiß M, Begerow D
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(2015) Identification of a new order of root-colonising fungi in the Entorrhizomycota: Talbotiomycetales ord. nov., on eudicotyledons. IMA Fungus 6: 129-133
Riess K, Bauer R, Kellner R, Kemler M, Piątek M, Vánky K, Begerow D
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(2016) On the evolutionary history of Uleiella chilensis, a smut fungus parasite of Araucaria araucana in South America: Uleiellales ord. nov. in Ustilaginomycetes. PLoS ONE 11: e0147107
Riess K, Schön M, Lutz M, Butin H, Oberwinkler F, Garnica S
