A genome-scale phylogeny of Fungi; insights into early evolution, radiations, and the relationship between taxonomy and phylogeny

Abstract

Phylogenomic studies based on genome-scale amounts of data have greatly improved understanding of the tree of life. Despite their diversity, ecological significance, and biomedical and industrial importance, large-scale phylogenomic studies of Fungi are lacking. Furthermore, several evolutionary relationships among major fungal lineages remain controversial, especially those at the base of the fungal phylogeny. To begin filling these gaps and assess progress toward a genome-scale phylogeny of the entire fungal kingdom, we compiled a phylogenomic data matrix of 290 genes from the genomes of 1,644 fungal species that includes representatives from most major fungal lineages; we also compiled 11 additional data matrices by subsampling genes or taxa based on filtering criteria previously shown to improve phylogenomic inference. Analyses of these 12 data matrices using concatenation- and coalescent-based approaches yielded a robust phylogeny of the kingdom in which ∼85% of internal branches were congruent across data matrices and approaches used. We found support for several relationships that have been historically contentious (e.g., for the placement of Wallemiomycotina (Basidiomycota), as sister to Agaricomycotina), as well as evidence for polytomies likely stemming from episodes of ancient diversification (e.g., at the base of Basidiomycota). By examining the relative evolutionary divergence of taxonomic groups of equivalent rank, we found that fungal taxonomy is broadly aligned with genome sequence divergence, but also identified lineages, such as the subphylum Saccharomycotina, where current taxonomic circumscription does not fully account for their high levels of evolutionary divergence. Our results provide a robust phylogenomic framework to explore the tempo and mode of fungal evolution and directions for future fungal phylogenetic and taxonomic studies.

Phylogenomics of a new fungal phylum reveals multiple waves of reductive evolution across Holomycota

“…We obtained an almost fully-resolved phylogeny showing sanchytrids as a new fast-evolving lineage sister to Blastocladiomycota, and Olpidium as an independent lineage sister to the non-flagellated fungi. Contrasting with previous weakly-supported analyses 13,22,37-39 , we robustly placed the root of the fungal tree between chytrids and all other fungi. Our new phylogenomic framework of Fungi supports a conservative model of four flagellum losses in Holomycota and highlights the importance of early-diverging unicellular Holomycota in the evolution of hyphal-based multicellularity.…”

“…Likewise, if radiation characterized early fungal evolution 22 , the accumulation of enough sequence substitutions during diversification would have been limited. This would explain the difficulty to resolve the deepest branches of the fungal tree, the fact that Chytridiomycota and Blastocladiomycota have alternatively been recovered as sisters of all other fungi 21,26,27,39,65 and the low support and discrepancies observed for the split between Glomeromycota and Mucoromycota (with additional constraints related to their symbiotic adaptation to land plants 24,67,68 ). The solid position of the root of the fungal tree on the chytrid branch revealed by our phylogenomic analyses with a richer dataset is additionally consistent with the distribution of so-considered derived characters in Blastocladiomycota, including sporic meiosis, relatively small numbers of carbohydrate metabolism genes and, in some species, hyphal-like apical growing structures (Allomyces) and narrow sporangia exit tubes (e.g.…”

“…Likewise, if radiation characterized early fungal evolution 22 , the accumulation of enough sequence substitutions during diversification would have been limited. This would explain the difficulty to resolve the deepest branches of the fungal tree, the fact that Chytridiomycota and Blastocladiomycota have alternatively been recovered as sisters of all other fungi 21,26,27,39,65 and the low support and discrepancies observed for the split between Glomeromycota and (which was not certified by peer review) is the author/funder. All rights reserved.…”

Step-by-Step Evolution of Telomeres: Lessons from Yeasts

“…The phylogenies of eukaryotes, opisthokonts, and holozoans were inferred from Burki et al. (2020) , Li et al. (2020) , and Torruella et al.…”

New Method for Identifying Fungal Kingdom Enzyme Hotspots from Genome Sequences

“…Table S2 includes only the number of unique “Function;Family” observations, reflecting the enzyme function specificity diversity of the fungal species analyzed. Taxonomy and phylogeny follow the recently reported advances in fungal systematics [ 18 , 19 , 20 ].…”