Convergent evolution of a fused sexual cycle promotes the haploid lifestyle

Nature. 2014 Feb 20;506(7488):387-390. doi: 10.1038/nature12891. Epub 2014 Jan 5.

Abstract

Sexual reproduction is restricted to eukaryotic species and involves the fusion of haploid gametes to form a diploid cell that subsequently undergoes meiosis to generate recombinant haploid forms. This process has been extensively studied in the unicellular yeast Saccharomyces cerevisiae, which exhibits separate regulatory control over mating and meiosis. Here we address the mechanism of sexual reproduction in the related hemiascomycete species Candida lusitaniae. We demonstrate that, in contrast to S. cerevisiae, C. lusitaniae exhibits a highly integrated sexual program in which the programs regulating mating and meiosis have fused. Profiling of the C. lusitaniae sexual cycle revealed that gene expression patterns during mating and meiosis were overlapping, indicative of co-regulation. This was particularly evident for genes involved in pheromone MAPK signalling, which were highly induced throughout the sexual cycle of C. lusitaniae. Furthermore, genetic analysis showed that the orthologue of IME2, a 'diploid-specific' factor in S. cerevisiae, and STE12, the master regulator of S. cerevisiae mating, were each required for progression through both mating and meiosis in C. lusitaniae. Together, our results establish that sexual reproduction has undergone significant rewiring between S. cerevisiae and C. lusitaniae, and that a concerted sexual cycle operates in C. lusitaniae that is more reminiscent of the distantly related ascomycete, Schizosaccharomyces pombe. We discuss these results in light of the evolution of sexual reproduction in yeast, and propose that regulatory coupling of mating and meiosis has evolved multiple times as an adaptation to promote the haploid lifestyle.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Biological Evolution*
  • Candida / cytology
  • Candida / genetics*
  • Candida / physiology*
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation / genetics
  • Genes, Essential / genetics
  • Haploidy*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • MAP Kinase Signaling System
  • Meiosis / genetics*
  • Meiosis / physiology*
  • Pheromones / metabolism
  • Protein-Serine-Threonine Kinases / metabolism
  • Reproduction / genetics
  • Reproduction / physiology
  • Saccharomyces cerevisiae / cytology
  • Saccharomyces cerevisiae / physiology
  • Saccharomyces cerevisiae Proteins / metabolism
  • Schizosaccharomyces / cytology
  • Schizosaccharomyces / physiology
  • Sex
  • Transcription Factors / metabolism

Substances

  • Fungal Proteins
  • Intracellular Signaling Peptides and Proteins
  • Pheromones
  • STE12 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Transcription Factors
  • IME2 protein, S cerevisiae
  • Protein-Serine-Threonine Kinases

Associated data

  • GEO/GSE51794