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Reconstructing the early evolution of Fungi using a six-gene phylogeny

Abstract

The ancestors of fungi are believed to be simple aquatic forms with flagellated spores, similar to members of the extant phylum Chytridiomycota (chytrids). Current classifications assume that chytrids form an early-diverging clade within the kingdom Fungi and imply a single loss of the spore flagellum, leading to the diversification of terrestrial fungi. Here we develop phylogenetic hypotheses for Fungi using data from six gene regions and nearly 200 species. Our results indicate that there may have been at least four independent losses of the flagellum in the kingdom Fungi. These losses of swimming spores coincided with the evolution of new mechanisms of spore dispersal, such as aerial dispersal in mycelial groups and polar tube eversion in the microsporidia (unicellular forms that lack mitochondria). The enigmatic microsporidia seem to be derived from an endoparasitic chytrid ancestor similar to Rozella allomycis, on the earliest diverging branch of the fungal phylogenetic tree.

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Figure 1: Phylogeny of the kingdom Fungi using bayesian analysis of the combined, six-gene data set.

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Acknowledgements

Funding for the project was provided by the National Science Foundation’s ‘Assembling the Tree of Life’ and ‘Research Coordination Network’ programs. For technical assistance we thank L. Bukovnik, C. Roberts and H. Matthews. We also thank the following individuals for sharing research materials: M. C. Aime, W. R. Buck, M. S. Cole, P. Crane, Y. Dalpe, D. M. Hillis, S. L. Joneson, R. Petersen, C. Printzen, E. Vellinga, H. Whisler and A. Zavarzin. We are very thankful to B. Mueller, J. Harer, B. Rankin, J. Pormann and S. Dilda for providing access to the Duke CSEM computer cluster. P. Keeling provided unpublished information used to analyse EFL in Fungi.

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Correspondence to Timothy Y. James or Rytas Vilgalys.

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Data for this project have been deposited in GenBank (see Supplementary Notes 1 for accession numbers), and the alignments can be accessed on the Assembling the Fungal Tree of Life website at http://www.aftol.org/.Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes 1

A table of the strains and species used and the sources and GenBank numbers for the gene sequences used in this study. (PDF 618 kb)

Supplementary Notes 2

These file shows the results of a Bayesian phylogenetic analysis of the six gene super-matrix using only nucleotide data. Note: Figure 1 of the manuscript shows a phylogeny based on a heterogeneous nucleotide-amino acid model, whereas this phylogeny uses nucleotides divided into genes and codons. (PDF 120 kb)

Supplementary Notes 3

This file contains the results of analysis of individual gene partitions (and relevant combinations) and the Bayesian posterior probabilities and maximum likelihood bootstrap support for nodes of interest. (PDF 66 kb)

Supplementary Notes 4

This file contains a phylogeny of a paralogous copy of elongation factor 1-α (EFL). It shows the species of basal fungi from which this gene copy has been sequenced, and demonstrates a relationship between Basidiobolus and the Entomophthorales. (PDF 115 kb)

Supplementary Notes 5

This file contains the methods and results from tests of long branch attraction between Rozella allomycis and microsporidia. (PDF 67 kb)

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James, T., Kauff, F., Schoch, C. et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818–822 (2006). https://doi.org/10.1038/nature05110

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