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ARS Home » Midwest Area » Peoria, Illinois » National Center for Agricultural Utilization Research » Mycotoxin Prevention and Applied Microbiology Research » Research » Publications at this Location » Publication #326546
Title: A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data

Author
item SPATAFORA, JOSEPH - Oregon State University
item CHANG, YING - Oregon State University
item BENNY, GERALD - University Of Florida
item LAZARUS, KATY - University Of Florida
item SMITH, MATTHEW - University Of Florida
item BERBEE, MARY - University Of British Columbia
item BONITO, GREGORY - Michigan State University
item CORRADI, NICOLAS - University Of Ottawa
item GRIGORIEV, IGOR - Joint Genome Institute
item O Donnell, Kerry

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/6/2016
Publication Date: 10/13/2016
Publication URL: http://handle.nal.usda.gov/10113/5695406
Citation: Spatafora, J.W., Chang, Y., Benny, G.L., Lazarus, K., Smith, M.E., Berbee, M.L., Bonito, G., Corradi, N., Grigoriev, I., O'Donnell, K., et al. 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 108(5):1028-1046.

Interpretive Summary: This study was initiated to assess whether current classification of the early diverging zygomycete fungi accurately reflects their evolutionary relationships. These fungi are ecologically important as symbionts of plants, as economically destructive pathogens of plants and animals, and they are widely used in the production of food, pharmaceuticals, and in other industrial processes. Despite significant advances in our understanding of evolutionary relationships within Kingdom Fungi, the earliest diverging events are still poorly understood. Resolving the evolution of the early diverging lineages is essential to identify characteristics of the ancestral fungi, to determine what traits emerged with the dawn of terrestrial ecosystems, and to obtain an accurate assessment of the morphological and genetic homologies that are associated with fungal lifestyles. To better document the diversity and evolution of zygomycetes, we have used genome-scale data to evaluate the phylogenetic position of these fungi. Based on phylogenetic analyses of 192 proteins from 25 zygomycete genomes, we discovered substantial support for two natural groups: one comprising Entomophthoromycota, Kickxellomycotina, and Zoopagomycotina (EKZ clade) and the other consisting of Mortierellomycotina, Mucoromycotina, and Glomeromycota (MMG clade). Importantly, these results reject the recognition of the zygomycetes because they do not represent a genealogically exclusive group. Therefore, a revised classification of the MMG and EKZ clades was proposed. This research will be of interest to a wide range of scientists in agriculture, medicine, and industry because it provides the first natural and predictive classification of these agronomically, medically, and industrially important fungi.

Technical Abstract: Zygomycete fungi were classified as a single phylum, Zygomycota, based on sexual reproduction by zygospores, frequent asexual reproduction by sporangia, absence of multicellular sporocarps, and production of coenocytic hyphae, all with some exceptions. Molecular phylogenies based on one or a few genes did not support themonophyly of the phylum, however, and the phylum was subsequently abandoned. Here we present phylogenetic analyses of a genome-scale data set for 46 taxa, including 25 zygomycetes and 192 proteins, and we demonstrate that zygomycetes comprise two major clades that form a paraphyletic grade. A formal phylogenetic classification is proposed herein and includes two phyla, six subphyla, four classes and 16 orders. On the basis of these results, the phyla Mucoromycota and Zoopagomycota are circumscribed. Zoopagomycota comprises Entomophtoromycotina, Kickxellomycotina and Zoopagomycotina; it constitutes the earliest diverging lineage of zygomycetes and contains species that are primarily parasites and pathogens of small animals (e.g. amoeba, insects, etc.) and other fungi, i.e. mycoparasites. Mucoromycota comprises Glomeromycotina, Mortierellomycotina, and Mucoromycotina and is sister to Dikarya. It is the more derived clade of zygomycetes and mainly consists of mycorrhizal fungi, root endophytes, and decomposers of plant material. Evolution of trophic modes, morphology, and analysis of genome-scale data are discussed.