Gene order evolution and paleopolyploidy in hemiascomycete yeasts

Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9272-7. doi: 10.1073/pnas.142101099. Epub 2002 Jul 1.

Abstract

The wealth of comparative genomics data from yeast species allows the molecular evolution of these eukaryotes to be studied in great detail. We used "proximity plots" to visually compare chromosomal gene order information from 14 hemiascomycetes, including the recent Génolevures survey, to Saccharomyces cerevisiae. Contrary to the original reports, we find that the Génolevures data strongly support the hypothesis that S. cerevisiae is a degenerate polyploid. Using gene order information alone, 70% of the S. cerevisiae genome can be mapped into "sister" regions that tile together with almost no overlap. This map confirms and extends the map of sister regions that we constructed previously by using duplicated genes, an independent source of information. Combining gene order and gene duplication data assigns essentially the whole genome into sister regions, the largest gap being only 36 genes long. The 16 centromere regions of S. cerevisiae form eight pairs, indicating that an ancestor with eight chromosomes underwent complete doubling; alternatives such as segmental duplications can be ruled out. Gene arrangements in Kluyveromyces lactis and four other species agree quantitatively with what would be expected if they diverged from S. cerevisiae before its polyploidization. In contrast, Saccharomyces exiguus, Saccharomyces servazzii, and Candida glabrata show higher levels of gene adjacency conservation, and more cases of imperfect conservation, suggesting that they split from the S. cerevisiae lineage after polyploidization. This finding is confirmed by sequences around the C. glabrata TRP1 and IPP1 loci, which show that it contains sister regions derived from the same duplication event as that of S. cerevisiae.

Publication types

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

MeSH terms

  • Ascomycota / classification*
  • Ascomycota / genetics*
  • Candida / classification
  • Candida / genetics
  • Centromere / genetics
  • Chromosome Mapping
  • Evolution, Molecular
  • Gene Duplication
  • Gene Order*
  • Genes, Fungal*
  • Genome, Fungal
  • Kluyveromyces / classification
  • Kluyveromyces / genetics
  • Models, Genetic
  • Molecular Sequence Data
  • Polyploidy*
  • Saccharomyces / classification
  • Saccharomyces / genetics
  • Saccharomyces cerevisiae / classification
  • Saccharomyces cerevisiae / genetics
  • Species Specificity

Associated data

  • GENBANK/AF520060
  • GENBANK/AF520061