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Downloaded from by IP: 199.133.24.106 On: Mon, 18 Sep 2017 10:43:32 Spatafora Et Al UC Riverside UC Riverside Previously Published Works Title The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies. Permalink https://escholarship.org/uc/item/4485m01m Journal Microbiology spectrum, 5(5) ISSN 2165-0497 Authors Spatafora, Joseph W Aime, M Catherine Grigoriev, Igor V et al. Publication Date 2017-09-01 DOI 10.1128/microbiolspec.funk-0053-2016 License https://creativecommons.org/licenses/by-nc-nd/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies JOSEPH W. SPATAFORA,1 M. CATHERINE AIME,2 IGOR V. GRIGORIEV,3 FRANCIS MARTIN,4 JASON E. STAJICH,5 and MEREDITH BLACKWELL6 1Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331; 2Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907; 3U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598; 4Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1136 Interactions Arbres/Microorganismes, Laboratoire d’Excellence Recherches Avancés sur la Biologie de l’Arbre et les Ecosystèmes Forestiers (ARBRE), Centre INRA-Lorraine, 54280 Champenoux, France; 5Department of Plant Pathology and Microbiology and Institute for Integrative Genome Biology, University of California–Riverside, Riverside, CA 92521; 6Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803 and Department of Biological Sciences, University of South Carolina, Columbia, SC 29208 ABSTRACT The kingdom Fungi is one of the more diverse INTRODUCTION clades of eukaryotes in terrestrial ecosystems, where they In 1996 the genome of Saccharomyces cerevisiae was provide numerous ecological services ranging from published and marked the beginning of a new era in decomposition of organic matter and nutrient cycling to beneficial and antagonistic associations with plants and fungal biology (1). Since then, rapid advancements in animals. The evolutionary relationships of the kingdom both sequencing technologies and computational biol- have represented some of the more recalcitrant problems ogy have resulted in the sequencing of genomes for more in systematics and phylogenetics. The advent of molecular than 800 species (e.g., http://genome.jgi.doe.gov/fungi/). phylogenetics, and more recently phylogenomics, has greatly These genomes represent a windfall of data that are advanced our understanding of the patterns and processes informing evolutionary studies of fungi and the search associated with fungal evolution, however. In this article, for biological solutions to alternative fuels, bioremedi- we review the major phyla, subphyla, and classes of the kingdom Fungi and provide brief summaries of ecologies, ation, carbon sequestration, and sustainable agriculture morphologies, and exemplar taxa. We also provide examples and forestry (2). Indeed, the marriage between genomics of how molecular phylogenetics and evolutionary genomics have advanced our understanding of fungal evolution Received: 6 June 2017, Accepted: 11 June 2017, Published: 15 September 2017 within each of the phyla and some of the major classes. Editors: Joseph Heitman, Department of Molecular Genetics and In the current classification we recognize 8 phyla, 12 subphyla, Microbiology, Duke University Medical Center, Durham, NC 27710; and 46 classes within the kingdom. The ancestor of fungi Timothy Y. James, Department of Ecology and Evolutionary Biology, is inferred to be zoosporic, and zoosporic fungi comprise University of Michigan, Ann Arbor, MI 48109-1048 three lineages that are paraphyletic to the remainder of fungi. Citation: Spatafora JW, Aime MC, Grigoriev IV, Martin F, Stajich JE, Fungi historically classified as zygomycetes do not form a Blackwell M. 2017. The fungal tree of life: from molecular monophyletic group and are paraphyletic to Ascomycota systematics to genome-scale phylogenies. Microbiol Spectrum 5(5): FUNK-0053-2016. doi:10.1128/microbiolspec.FUNK-0053-2016. and Basidiomycota. Ascomycota and Basidiomycota are Correspondence: Joseph W. Spatafora, [email protected] each monophyletic and collectively form the subkingdom © 2017 American Society for Microbiology. All rights reserved. Dikarya. ASMscience.org/MicrobiolSpectrum 1 Downloaded from www.asmscience.org by IP: 199.133.24.106 On: Mon, 18 Sep 2017 10:43:32 Spatafora et al. and phylogenetics occurred early, both in the use of chytridiomycetes, zygomycetes, ascomycetes, and phylogenetic techniques to study genome evolution and basidiomycetes—defined by morphological traits asso- in the use of genome-scale data to infer evolutionary ciated with reproduction. (Note: The suffix “-mycetes” relationships. In this article we will review the impact is used to denote a class-level taxonomic group in fungal of genomic-scale phylogenies, along with standard mo- nomenclature, e.g., Agaricomycetes. Its use as a lower- lecular phylogenies, on our understanding of the evo- case noun, however, signifies an informal name and lution of the fungal tree of life and the classification that not an explicit taxonomic rank.) The chytridiomycetes, communicates it. or zoosporic fungi, were recognized based on their pro- Genomic data provide the maximum amount of duction of zoospores, characterized by a single posterior, discrete genetic information available for phylogenetic smooth flagellum. The zygomycetes were characterized analyses, and hundreds to thousands of genes have been by gametangial conjugation and the production of identified as useful phylogenetic markers (3). Markov zygospores, coenocytic hyphae, and typically asexual clustering algorithms have been proven powerful tools reproduction by sporangia. The ascomycetes and ba- to identify orthologous clusters of proteins that can be sidiomycetes were identified by the production of asci filtered for single-copy clusters that are useful in phylo- and basidia, respectively, possession of regularly sep- genetic analyses (4). This approach has transformed tate hyphae, and a dikaryotic nuclear phase in their phylogenetics by no longer requiring selection of an life cycle. The classification of the kingdom Fungi used a priori set of markers (e.g., rDNA, RPB2, etc.), but here recognizes eight phyla (Fig. 1, Table 1), with the rather promotes the mining of a data set of genomes zoosporic fungi comprising the first three lineages of for the largest set of appropriate markers. Furthermore, the kingdom—Cryptomycota/Microsporidia, Chytridio- hidden Markov models have proven to be valuable tools mycota, and Blastocladiomycota—since the divergence for identifying and retrieving these markers in newly from the last universal common ancestor (LUCA) of sequenced genomes and rapidly growing genome-scale Fungi. phylogenetic data sets (5). The resolution of zoosporic fungi as paraphyletic The estimation of species trees from genome-scale rejects the flagellum as a diagnostic trait (synapomor- data sets is not without challenges, however. Phylo- phy) for a monophyletic group of flagellated fungi. genetic analyses of genomic data have revealed that Rather, it is an ancestral (symplesiomorphic) trait in- different genes within a genome can have different evo- herited from the LUCA of the kingdom Fungi. Most lutionary histories, i.e., phylogenetic conflict (6). Sources extant species of fungi are nonflagellated and are the of conflict include incomplete lineage sorting (or deep result of multiple losses of the flagellum during fungal coalescence), hybridization, and horizontal gene trans- evolution. Two losses of the flagellum have occurred, fer, and the detection and characterization of this con- giving rise to the Microsporidia and the most recent flict in the context of phylogenetic inference are still in common ancestor (MRCA) of the remaining phyla of their infancy (7). The application of standard measures zygomycetes, ascomycetes, and basidiomycetes. Infer- of topological support, such as the bootstrap partition, ences of additional losses of the flagellum are required can also be difficult to interpret, due to the observation for the placement of nonflagellated species among the that nodes that resolve differently in different gene data Chytridiomycota (11) and possibly for the placement sets can have high or maximum bootstrap partition of the enigmatic zoosporic genus Olpidium among values in a subset of analyses (e.g., 8, 9). At the time of zygomycetes (12), but the absolute number of losses the writing of this manuscript the majority of genome- is unclear. The zygomycetes are also paraphyletic and scale phylogenetic analyses focus on the analysis of are classified in two phyla: Zoopagomycota and Mu- concatenated superalignments, but development and use coromycota (13). This classification rejects the zygo- of supertree methods, gene tree-species tree reconcilia- spore as a synapomorphy for the zygomycetes; rather, tions, and alternative measures of nodal support are it was inherited from the MRCA of terrestrial fungi increasing (e.g., 8, 10) and will be developed further over and lost in the MRCA of ascomycetes and basidio- the coming years. mycetes. The monophyly of ascomycetes and basidio- Despite the challenges mentioned above, phylo- mycetes has been confirmed, and they are classified as genetic analyses of genome-scale data sets, and more the phyla Ascomycota and Basidiomycota, respectively, traditional multigene data sets, have greatly advanced of the subkingdom Dikarya (14). More information our understanding
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