Toward a Fully Resolved Fungal Tree of Life

Abstract

In this review, we discuss the current status and future challenges for fully elucidating the fungal tree of life. In the last 15 years, advances in genomic technologies have revolutionized fungal systematics, ushering the field into the phylogenomic era. This has made the unthinkable possible, namely access to the entire genetic record of all known extant taxa. We first review the current status of the fungal tree and highlight areas where additional effort will be required. We then review the analytical challenges imposed by the volume of data and discuss methods to recover the most accurate species tree given the sea of gene trees. Highly resolved and deeply sampled trees are being leveraged in novel ways to study fungal radiations, species delimitation, and metabolic evolution. Finally, we discuss the critical issue of incorporating the unnamed and uncultured dark matter taxa that represent the vast majority of fungal diversity. Expected final online publication date for the Annual Review of Microbiology, Volume 74 is September 8, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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

“…Many fungi are economically important as model organisms (e.g., the brewer's yeast Saccharomyces cerevisiae, the fission yeast Schizosaccharomyces pombe, and the bread mold Neurospora crassa); food sources (e.g., mushrooms and truffles); cell factories for the production of diverse organic acids, proteins, and natural products (e.g., the mold Aspergillus niger); or major pathogens of plants and animals (e.g., the rice blast fungus Magnaporthe grisea and the amphibian chytrid fungus Batrachochytrium dendrobatidis), including humans (e.g., Candida species causing candidiasis, Aspergillus species causing aspergillosis, and Cryptococcus species causing cryptococcosis) 3,5,6 . There are more than 200 orders of fungi that are classified into 12 phyla 6 (for an alternative scheme of classification, see Ref.…”

“…7 ). These 12 phyla are placed into six major groups: the subkingdoms Dikarya (which includes the phyla Ascomycota, Basidiomycota, and Entorrhizomycota) and Chytridiomyceta (which includes the phyla Chytridiomycota, Monoblepharidomycota, and Neocallimastigomycota), the phyla Mucoromycota, Zoopagomycota, and Blastocladiomycota, and the major group Opisthosporidia (which includes the phyla Aphelidiomycota, Cryptomycota/Rozellomycota, and Microsporidia, and is possibly paraphyletic) 6 . Evolutionary relationships among some of these groups, as well as among certain phyla and classes have been elusive, with morphological and molecular studies providing support for conflicting phylogenetic hypotheses or being equivocal in their support among alternatives 6,8 ( Supplementary Fig.…”

“…This is likely due to the parasitic lifestyles and highly reduced morphologies of many of the organisms involved that coincide with highly reduced and very rapidly evolving genomes (e.g., Microsporidia), that render their evolutionary placement challenging 9,10 . Ambiguity also exists with respect to the placement of Blastocladiomycota -either as a sister to the rest of fungi excluding Opisthosporidia or as a sister to the rest of fungi excluding Opisthosporidia and Chytridiomyceta 6,[11][12][13] .…”

“…Although aquatic, Blastocladiomycota have several traits found in terrestrial fungi, making their placement on the fungal phylogeny key for understanding the evolution of diverse fungal traits 6,14 . Mucoromycota and Zoopagomycota were previously classified into the 6 phylum Zygomycota based on the production of coenocytic hyphae and sexual reproduction by zygospores.…”

“…Other classifications have retained Glomeromycota and seven additional phyla for the former Zygomycota 7 . Finally, evolutionary relationships of major lineages within Chytridiomyceta (i.e., between Chytridiomycota, Neocallimastigomycota, Monoblepharidomycota), Basidiomycota (i.e., among Agaricomycotina, Pucciniomycotina, and Ustilaginomycotina), and phylum Ascomycota (e.g., between classes in Taphrinomycotina) are also elusive 6,8 ( Supplementary Fig. 1).…”