The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies

Abstract

The kingdom Fungi is one of the more diverse clades of eukaryotes in terrestrial ecosystems, where they provide numerous ecological services ranging from decomposition of organic matter and nutrient cycling to beneficial and antagonistic associations with plants and animals. The evolutionary relationships of the kingdom have represented some of the more recalcitrant problems in systematics and phylogenetics. The advent of molecular phylogenetics, and more recently phylogenomics, has greatly advanced our understanding of the patterns and processes associated with fungal evolution, however. In this article, we review the major phyla, subphyla, and classes of the kingdom Fungi and provide brief summaries of ecologies, morphologies, and exemplar taxa. We also provide examples of how molecular phylogenetics and evolutionary genomics have advanced our understanding of fungal evolution within each of the phyla and some of the major classes. In the current classification we recognize 8 phyla, 12 subphyla, and 46 classes within the kingdom. The ancestor of fungi is inferred to be zoosporic, and zoosporic fungi comprise three lineages that are paraphyletic to the remainder of fungi. Fungi historically classified as zygomycetes do not form a monophyletic group and are paraphyletic to Ascomycota and Basidiomycota. Ascomycota and Basidiomycota are each monophyletic and collectively form the subkingdom Dikarya.

FIGURE 1

Fungal tree of life. Cladogram of the kingdom Fungi based on published multi-gene and genome-scale phylogenies (–14, 17, 18, 32, 33, 83, 98, 109, 112, 167, 168). Polytomies represent regions of the tree currently unresolved by molecular and genomic data.

FIGURE 2

Examples of zoosporic fungal diversity. (a) Rozella allomycis (Cryptomycota) parasitizing hyphae of Allomyces (Blastocladiomycota). Chytridiomycota: (b) C. hyalinus (Chytridiomycetes) monocentric, operculate zoosporangium with rhizoids; (c) Catenochytridium sp. (Chytridiomycetes) monocentric, operculate zoosporangium with rhizoids; (d) Monoblepharis polymorpha (Monoblepharidomycetes) mature zygote or oospore, empty and mature antheridia and antherozoids or male gametes emerging from antheridium (by Marilyn M. N. Mollicone); (e) Neocallimastix sp. (Neocallimastigomycetes) monocentric thallus with rhizoids (by Gary Easton); (f) Olpidium bornovanus (incertae sedis) zoospores (photo by D’Ann Rochon); (g) Neocallimastix sp. (Neocallimastigomycetes) multiflagellate zoospores (photo by Gary Easton).

FIGURE 3

Examples of zygomycete fungal diversity. Zoopagomycota: (a) adult fly infected by a species of Entomophthorales; (b) Basidiobolus conidium; (c) Conidiobolus conidia; (d) Zygopolaris thallus with trichospores (photo by R.W. Lichtwardt); (e) Linderina sporangium; (f) Kickxella sporangium; (g) Rhopalomyces sporangium; (h) Piptocephalis sporangium. Mucoromycota: (i) Glomus spore (photo from American Society for the Advancement of Science); (j) G. sinuosum sporocarp (photo by D. Redeker); (k) G. mosseae arbuscule (photo by K. Wex); (l) Mortierella sporangium; (m) Lobosporangium sporangium; (n) Rhizopus sporangium; (o) Thamnidium sporangium; (p) Pilobolus sporangium; (q) Phycomyces zygosporangium; (r) Cunninghamella zygosporangium; (s) Endogone sporocarp, zygospore (inset).

FIGURE 4

Examples of Ascomycota diversity. (A) Apothecia (yellow) of Orbilia, Orbiliomycetes (J. H. Petersen/MycoKey). (B) Apothecia of Aleuria, Pezizomycetes (J. H. Petertsen/MycoKey). (C) Thallus of Ophioparma with apothecia, Lecanoromycetes (B. McCune, Oregon State University). (D) Thallus of Lichinella, Lichinomycetes (B. McCune, Oregon State University). (E) Bitunicate asci of Thaxteriella, Dothideomycetes (S. Huhndorf, Field Museum). (F) Thallus of Arthonia with apothecia, Arthoniomycetes (B. McCune, Oregon State University). (G) Thallus of Prolixandromyces, Laboulbeniomycetes (A. Weir, SUNY-ESF). (H) Perithecia of Neurospora, Sordariomycetes (N. B. Raju, Stanford University). (I) Earth-tongue apothecia of Cudonia, Leotiomycetes (Z. Wang, Iowa State University). (J) Cleistothecia of Eupenicillium, Eurotiomycetes (D. Geiser, Penn State University). (K) Operculate ascus of Peziza (J. H. Petersen/MycoKey). (L) Ascostroma of Venturia, Dothideomycetes (T. Volk, University of Wisconsin at La Crosse). (M) Unitunicate asci Neurospora (N. B. Raju, Stanford University). (N) Prototunicate ascus of Eurotium (D. Geiser, Penn State University).

FIGURE 5

Examples of Basidiomycota diversity. Pucciniomycotina: (a) uredinia of Puccinia iridis; (b) fruiting body of Phleogena faginea; (c) aecia of Coleosporium; (d) yeast state of Symmetrospora oryzicola. Ustilaginomycotina: (e) smut galls of Ustilago maydis; (f) gall of Exobasidium; (g) culture of Moniliella sp. Agaricomycotina: (h) culture of Wallemia; (i) stinkhorn fruiting body of Phallus (photo by Nu Nguyen). (j) coral fruiting body of Clavaria; (k) crust fruiting body of Amylostereum; (l) club fruiting body of Clavariadelphis; (m) polypore, conk fruiting body of Pycnoporus; (n) gilled mushroom fruiting body of Russula; (o) pored mushroom fruiting body of Boletus; (p) puffball fruiting body of Lycoperdon.