What Defines the “Kingdom” Fungi?
- Authors: Thomas A. Richards1,2, Guy Leonard3, Jeremy G. Wideman4
- Editors: Joseph Heitman5, Timothy Y. James6
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VIEW AFFILIATIONS HIDE AFFILIATIONSAffiliations: 1: Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom; 2: Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research (CIFAR), Toronto, Canada; 3: Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom; 4: Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom; 5: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 6: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109-1048
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Received 15 February 2017 Accepted 25 February 2017 Published 23 June 2017
- Correspondence: Thomas A. Richards, [email protected]
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Abstract:
The application of environmental DNA techniques and increased genome sequencing of microbial diversity, combined with detailed study of cellular characters, has consistently led to the reexamination of our understanding of the tree of life. This has challenged many of the definitions of taxonomic groups, especially higher taxonomic ranks such as eukaryotic kingdoms. The Fungi is an example of a kingdom which, together with the features that define it and the taxa that are grouped within it, has been in a continual state of flux. In this article we aim to summarize multiple lines of data pertinent to understanding the early evolution and definition of the Fungi. These include ongoing cellular and genomic comparisons that, we will argue, have generally undermined all attempts to identify a synapomorphic trait that defines the Fungi. This article will also summarize ongoing work focusing on taxon discovery, combined with phylogenomic analysis, which has identified novel groups that lie proximate/adjacent to the fungal clade—wherever the boundary that defines the Fungi may be. Our hope is that, by summarizing these data in the form of a discussion, we can illustrate the ongoing efforts to understand what drove the evolutionary diversification of fungi.
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Citation: Richards T, Leonard G, Wideman J. 2017. What Defines the “Kingdom” Fungi?. Microbiol Spectrum 5(3):FUNK-0044-2017. doi:10.1128/microbiolspec.FUNK-0044-2017.




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Abstract:
The application of environmental DNA techniques and increased genome sequencing of microbial diversity, combined with detailed study of cellular characters, has consistently led to the reexamination of our understanding of the tree of life. This has challenged many of the definitions of taxonomic groups, especially higher taxonomic ranks such as eukaryotic kingdoms. The Fungi is an example of a kingdom which, together with the features that define it and the taxa that are grouped within it, has been in a continual state of flux. In this article we aim to summarize multiple lines of data pertinent to understanding the early evolution and definition of the Fungi. These include ongoing cellular and genomic comparisons that, we will argue, have generally undermined all attempts to identify a synapomorphic trait that defines the Fungi. This article will also summarize ongoing work focusing on taxon discovery, combined with phylogenomic analysis, which has identified novel groups that lie proximate/adjacent to the fungal clade—wherever the boundary that defines the Fungi may be. Our hope is that, by summarizing these data in the form of a discussion, we can illustrate the ongoing efforts to understand what drove the evolutionary diversification of fungi.

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Figures

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FIGURE 1
Diversity and distribution of gene families known to function in chitin cell wall synthesis or remodeling. (A) The diversity of domain architectures (as identified using PFAM [ 184 ]) for chitin cell wall synthesis or remodeling gene families. Note the gene fusion between a myosin head domain motor protein and a chitin synthase which was previously suggested to be fungus-specific ( 92 ). (B) The taxonomic distribution of putative homologues across a subset of eukaryotic taxa identified using a custom-built set of domain-specific hidden Markov models kindly provided by Jason Stajich and Divya Sain ( 185 ). The fungal component of the phylogenetic tree is based on Spatafora et al. ( 186 ).

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FIGURE 2
Diversity and distribution of gene families known to function in hyphal growth. (A) A cartoon illustrating how proteins interact relating to subprocesses which govern vesicle trafficking associated with hyphal growth. Functions are briefly discussed in the main body of this manuscript and are marked i to viii. (B) The taxonomic distribution of putative orthologues identified using reciprocal BLAST searches and phylogenetic methods across a subset of eukaryotic taxa (data not shown). The fungal component of the phylogenetic tree is based on Spatafora et al. ( 186 ).

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FIGURE 3
Cartoon illustration summarizing how features previously discussed as defining the protist-fungal transition have been shown to have a mosaic distribution within the Fungi and/or outside the Fungi among other eukaryotes. White connecting nodes illustrate linked characters/traits.

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FIGURE 4
Schematic phylogenetic tree illustrating additional groups branching proximate to the origin of the fungal clade and the phylogenetic uncertainty among the deep branches of the Fungi and associated groups. Basal clone group 1 is composed of environmental sequences, which in some analyses is placed close to fungi ( 149 ).
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