Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of kingdom Fungi inferred from RNA polymerase II subunit genes

BMC Evol Biol. 2006 Sep 29:6:74. doi: 10.1186/1471-2148-6-74.

Abstract

Background: At present, there is not a widely accepted consensus view regarding the phylogenetic structure of kingdom Fungi although two major phyla, Ascomycota and Basidiomycota, are clearly delineated. Regarding the lower fungi, Zygomycota and Chytridiomycota, a variety of proposals have been advanced. Microsporidia may or may not be fungi; the Glomales (vesicular-arbuscular mycorrhizal fungi) may or may not constitute a fifth fungal phylum, and the loss of the flagellum may have occurred either once or multiple times during fungal evolution. All of these issues are capable of being resolved by a molecular phylogenetic analysis which achieves strong statistical support for major branches. To date, no fungal phylogeny based upon molecular characters has satisfied this criterion.

Results: Using the translated amino acid sequences of the RPB1 and RPB2 genes, we have inferred a fungal phylogeny that consists largely of well-supported monophyletic phyla. Our major results, each with significant statistical support, are: (1) Microsporidia are sister to kingdom Fungi and are not members of Zygomycota; that is, Microsporidia and fungi originated from a common ancestor. (2) Chytridiomycota, the only fungal phylum having a developmental stage with a flagellum, is paraphyletic and is the basal lineage. (3) Zygomycota is monophyletic based upon sampling of Trichomycetes, Zygomycetes, and Glomales. (4) Zygomycota, Basidiomycota, and Ascomycota form a monophyletic group separate from Chytridiomycota. (5) Basidiomycota and Ascomycota are monophyletic sister groups.

Conclusion: In general, this paper highlights the evolutionary position and significance of the lower fungi (Zygomycota and Chytridiomycota). Our results suggest that loss of the flagellum happened only once during early stages of fungal evolution; consequently, the majority of fungi, unlike plants and animals, are nonflagellated. The phylogeny we infer from gene sequences is the first one that is congruent with the widely accepted morphology-based classification of Fungi. We find that, contrary to what has been published elsewhere, the four morphologically defined phyla (Ascomycota, Basidiomycota, Zygomycota and Chytridiomycota) do not overlap with one another. Microsporidia are not included within kingdom Fungi; rather they are a sister-group to the Fungi. Our study demonstrates the applicability of protein sequences from large, slowly-evolving genes to the derivation of well-resolved and highly supported phylogenies across long evolutionary distances.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Ascomycota / classification
  • Ascomycota / genetics
  • Basidiomycota / classification
  • Basidiomycota / genetics
  • Bayes Theorem
  • Chytridiomycota / classification
  • Chytridiomycota / genetics
  • DNA, Fungal / genetics
  • DNA, Ribosomal / genetics
  • Evolution, Molecular*
  • Flagella / genetics*
  • Fungal Proteins / genetics*
  • Fungi / classification
  • Fungi / genetics*
  • Fungi / ultrastructure
  • Genes, Fungal*
  • Microsporidia / classification
  • Microsporidia / genetics
  • Molecular Sequence Data
  • Phylogeny
  • Protein Subunits / genetics
  • RNA Polymerase II / genetics*
  • RNA, Fungal / genetics
  • RNA, Ribosomal, 18S / genetics
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Species Specificity

Substances

  • DNA, Fungal
  • DNA, Ribosomal
  • Fungal Proteins
  • Protein Subunits
  • RNA, Fungal
  • RNA, Ribosomal, 18S
  • RNA Polymerase II