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


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.


  1. Karol, K. G., McCourt, R. M., Cimino, M. T. & Delwiche, C. F. The closest living relatives of land plants. Science 294, 2351–2353 (2001)

    ADS  CAS  Article  Google Scholar 

  2. Groth-Malonek, M., Pruchner, D., Grewe, F. & Knoop, V. Ancestors of trans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosses with vascular plants. Mol. Biol. Evol. 22, 117–125 (2005)

    CAS  Article  Google Scholar 

  3. Lang, B. F., O’Kelly, C., Nerad, T., Gray, M. W. & Burger, G. The closest unicellular relatives of animals. Curr. Biol. 12, 1773–1778 (2002)

    CAS  Article  Google Scholar 

  4. James, T. Y., Porter, D., Leander, C. A., Vilgalys, R. & Longcore, J. E. Molecular phylogenetics of the Chytridiomycota supports the utility of ultrastructural data in chytrid systematics. Can. J. Bot. 78, 336–350 (2000)

    CAS  Google Scholar 

  5. Tanabe, Y., Saikawa, M., Watanabe, M. M. & Sugiyama, J. Molecular phylogeny of Zygomycota based on EF-1α and RPB1 sequences: limitations and utility of alternative markers to rDNA. Mol. Phylogenet. Evol. 30, 438–449 (2004)

    CAS  Article  Google Scholar 

  6. Schüßler, A., Schwarzott, D. & Walker, C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105, 1413–1421 (2001)

    Article  Google Scholar 

  7. Tehler, A., Little, D. P. & Farris, J. S. The full-length phylogenetic tree from 1551 ribosomal sequences of chitinous fungi, Fungi. Mycol. Res. 107, 901–916 (2003)

    CAS  Article  Google Scholar 

  8. Cavalier-Smith, T. & Chao, E. E. The opalozoan Apusomonas is related to the common ancestor of animals, fungi, and choanoflagellates. Proc. R. Soc. Lond. B 261, 1–9 (1995)

    ADS  Article  Google Scholar 

  9. Steenkamp, E. T., Wright, J. & Baldauf, S. L. The protistan origins of animals and fungi. Mol. Biol. Evol. 23, 93–106 (2005)

    Article  Google Scholar 

  10. Barr, D. J. S. Evolution and kingdoms of organisms from the perspective of a mycologist. Mycologia 84, 1–11 (1992)

    Article  Google Scholar 

  11. Ustinova, I., Krienitz, L. & Huss, V. A. R. Hyaloraphidium curvatum is not a green alga, but a lower fungus; Amoebidium parasiticum is not a fungus, but a member of the DRIPs. Protist 151, 253–262 (2000)

    CAS  Article  Google Scholar 

  12. Nagahama, T., Sato, H., Shimazu, M. & Sugiyama, J. Phylogenetic divergence of the entomophthoralean fungi: evidence from nuclear 18S ribosomal RNA gene sequences. Mycologia 87, 203–209 (1995)

    CAS  Article  Google Scholar 

  13. McKerracher, L. J. & Heath, I. B. The structure and cycle of the nucleus-associated organelle in two species of Basidiobolus.. Mycologia 77, 412–417 (1985)

    Article  Google Scholar 

  14. Blackwell, M. & Malloch, D. Similarity of Amphoromorpha and secondary capilliconidia of Basidiobolus.. Mycologia 81, 735–741 (1989)

    Article  Google Scholar 

  15. Keeling, P. J. & Fast, N. M. in Insect–Fungal Associations: Ecology and Evolution (eds Vega, F. E. & Blackwell, M.) 97–118 (Oxford Univ. Press, Oxford, 2005)

  16. Hirt, R. P. et al. Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl Acad. Sci. USA 96, 580–585 (1999)

    ADS  CAS  Article  Google Scholar 

  17. Katinka, M. D. et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi.. Nature 414, 450–453 (2001)

    ADS  CAS  Article  Google Scholar 

  18. Keeling, P. J. Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet. Biol. 38, 298–309 (2003)

    CAS  Article  Google Scholar 

  19. Cavalier-Smith, T. in The Mycota (eds McLaughlin, D. J., McLaughlin, E. G. & Lemke, P. A.) 3–37 (Springer, New York, 2001)

  20. Corradi, N., Hijri, M., Fumagalli, L. & Sanders, I. R. Arbuscular mycorrhizal fungi (Glomeromycota) harbour ancient fungal tubulin genes that resemble those of the chytrids (Chytridiomycota). Fungal Genet. Biol. 41, 1037–1045 (2004)

    CAS  Article  Google Scholar 

  21. Held, A. A. Rozella and Rozellopsis: Naked endoparasitic fungi which dress up as their hosts. Bot. Rev. 47, 451–515 (1981)

    Article  Google Scholar 

  22. Shimodaira, H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492–508 (2002)

    Article  Google Scholar 

  23. Gill, E. E. & Fast, N. M. Assessing the microsporidia–fungi relationship: combined phylogenetic analysis of eight genes. Gene 375, 103–109 (2006)

    CAS  Article  Google Scholar 

  24. KirkP. M.CannonP. F.DavidJ. C.StalpersJ. A. (eds) Ainsworth & Bisby’s; Dictionary of the Fungi 60 (CAB International, Wallingford, UK, 2001)

  25. Lutzoni, F. et al. Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am. J. Bot. 91, 1446–1480 (2004)

    Article  Google Scholar 

  26. Binder, M. et al. The phylogenetic distribution of resupinate forms across the major clades of mushroom-forming fungi (Homobasidiomycetes). Systematics and Biodiversity 3, 113–157 (2005)

    Article  Google Scholar 

  27. Moncalvo, J-M. et al. One hundred and seventeen clades of euagarics. Mol. Phylogenet. Evol. 23, 357–400 (2002)

    CAS  Article  Google Scholar 

  28. Hibbett, D. S., Gilbert, L-B. & Donoghue, M. J. Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407, 506–508 (2000)

    ADS  CAS  Article  Google Scholar 

  29. Medina, M. et al. Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa. Int. J. Astrobiol. 2, 203–211 (2003)

    Article  Google Scholar 

  30. Powell, M. J. Fine structure of the unwalled thallus of Rozella polyphagi in its host Polyphagus euglenae.. Mycologia 76, 1039–1048 (1984)

    Article  Google Scholar 

  31. Berbee, M. L. & Taylor, J. W. in The Mycota (eds McLaughlin, D. J., McLaughlin, E. G. & Lemke, P. A.) 229–245 (Springer, New York, 2001)

  32. Heckman, D. S. et al. Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129–1133 (2001)

    CAS  Article  Google Scholar 

  33. Pirozynski, K. A. & Malloch, D. W. The origin of land plants: a matter of mycotrophism. Biosystems 5, 153–164 (1975)

    Article  Google Scholar 

  34. Schüßler, A. Molecular phylogeny, taxonomy, and evolution of arbuscular mycorrhiza fungi and Geosiphon pyriformis.. Plant Soil 244, 75–83 (2002)

    ADS  Article  Google Scholar 

  35. Keeling, P. J. & Inagaki, Y. A class of eukaryotic GTPase with a punctuate distribution suggesting multiple functional replacements of translation elongation factor 1α. Proc. Natl Acad. Sci. USA 101, 15380–15384 (2004)

    ADS  CAS  Article  Google Scholar 

  36. Maddison, D. & Maddison, W. MacClade Version 4.05: Analysis of Phylogeny and Character Evolution (Sinauer Associates, Sunderland, Massachusetts, USA, 2002)

  37. Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)

    Article  Google Scholar 

  38. Huelsenbeck, J. P. & Ronquist, F. MrBayes: bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    CAS  Article  Google Scholar 

  39. Wilgenbusch, J. C., Warren, D. L. & Swofford, D. L. AWTY: A system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. (2004)

  40. Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504 (2002)

    CAS  Article  Google Scholar 

  41. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. Version 1.0. (2003)

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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 and permissions information is available at 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).

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