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Chapter 4 : Phylogenetics and Phylogenomics of the Fungal Tree of Life

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Abstract:

Phylogenetic trees, once restricted to studies on systematics, are now used throughout all disciplines of fungal biology and provide the evolutionary context for a broad suite of studies that include understanding the evolution of major life forms, description of complex biotic communities, and predictive experimental biology. This is especially true in the genomic era, where a rapid convergence of phylogenetics and genomics is occurring and is resulting in the emerging field of phylogenomics. This chapter provides a review of (i) the current status of fungal phylogenetics based on multigene phylogenies, (ii) current evolutionary hypotheses on the evolutionary relationships of organisms that are classified in the Kingdom Fungi, and (iii) the use of genome-scale sampling to infer evolutionary relationships of the fungi. The goal of the Deep Hypha Research Coordination Network was to accelerate the collection of multigene sequence data across the Fungal Tree of Life. By the Fungal Tree of Life, we explicitly refer to the monophyletic Kingdom Fungi (Fungi) and all of its subgroups. One of the more elusive areas of research in fungal phylogenetics has been the calibration of the Fungal Tree of Life to geologic time. Here we focus on the use of genome-scale data sets in phylogenetic analyses. Multigene analyses have had a major impact on phylogenetic studies of the Fungi, resulting in our most thorough understanding of evolutionary relationships of the Kingdom to date.

Citation: Spatafora J, Robbertse B. 2010. Phylogenetics and Phylogenomics of the Fungal Tree of Life, p 36-49. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch4

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FIGURE 1

Fungal Tree of Life. Phylogenetic tree depicting the major phyla and subphyla of the Kingdom Fungi. Hypotheses for major morphological transitions are depicted along the backbone of the tree. Lineages of zoosporic and zygosporangium-producing fungi are shown along the right of the tree with the symbols of stylized zoospores and zygosporangia, respectively. Dashed lines represent early-diverging lineages of uncertain placement (e.g., and Microsporidia) or internal nodes that are resolved in cited studies but with <70% bootstrap values (e.g., Blastocladiomycota and Glomeromycota). Phylogenetic relationships are based on , and .

Citation: Spatafora J, Robbertse B. 2010. Phylogenetics and Phylogenomics of the Fungal Tree of Life, p 36-49. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch4
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Image of FIGURE 2
FIGURE 2

Phylogeny and classification of Fungi: Basidiomycota. Dashed lines indicate taxa that are of uncertain placement. Reproduced with permission from .

Citation: Spatafora J, Robbertse B. 2010. Phylogenetics and Phylogenomics of the Fungal Tree of Life, p 36-49. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch4
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Image of FIGURE 3
FIGURE 3

Phylogeny and classification of Fungi: Ascomycota. Dashed lines indicate taxa that are of uncertain placement. Reproduced with permission from .

Citation: Spatafora J, Robbertse B. 2010. Phylogenetics and Phylogenomics of the Fungal Tree of Life, p 36-49. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch4
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Image of FIGURE 4
FIGURE 4

Different calibration points change estimated divergence dates. Ascomycota split from Basidiomycota after the origin of two phyla not shown, the Chytridiomycota and Glomeromycota. In the top diagram we assumed that the 400 million-year-old fossil represents Sordariomycetes as indicated by the letter “S.” This pushes the minimum age for the origin of the stem lineages of all five fungal phyla, including the Glomeromycota, to 1,489 million years ago, more than three times the age of the first fossil evidence of land plants. In the middle diagram we assumed that represents Pezizomycotina but not necessarily Sordariomycetes. Applying calibrations from plant and animal fossils in addition to assuming that represents Pezizomycotina gave an estimate of 792 million years ago for the origin of the fungal phyla, still almost twice the age of the first fossil evidence for vascular plants. In the bottom diagram, assuming that provided a minimum age for the Ascomycota, indicated by the letter “A,” at 400 million years resulted in the estimate that fungal phyla had been established by 452 million years ago, roughly the age of the first land plants. In this scenario, however, the ages for the divergences among vertebrates are far too recent given fossil data. This discrepancy might result from using fossils from one kingdom (Fungi) to calibrate events in the same kingdom and another kingdom (Animalia), as discussed in the text. Reproduced with permission from .

Citation: Spatafora J, Robbertse B. 2010. Phylogenetics and Phylogenomics of the Fungal Tree of Life, p 36-49. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch4
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Image of FIGURE 5
FIGURE 5

Maximum likelihood phylogeny reconstructed using a concatenated alignment of 153 universally distributed fungal genes. The concatenated alignment contains 42 taxa and exactly 38,000 amino acid positions. The optimum model according to ModelGenerator ( ) was found to be WAG+I+G. The number of rate categories was 4 (alpha 5 0.83), and the proportion of invariable sites was approximated at 0.20. Bootstrap scores for all nodes are displayed. is found at the base of the WGD node. Reproduced with permission from .

Citation: Spatafora J, Robbertse B. 2010. Phylogenetics and Phylogenomics of the Fungal Tree of Life, p 36-49. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch4
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