A coupled process of same- and opposite-sex mating generates polyploidy and genetic diversity in Candida tropicalis

PLoS Genet. 2018 May 7;14(5):e1007377. doi: 10.1371/journal.pgen.1007377. eCollection 2018 May.

Abstract

Sexual reproduction is a universal mechanism for generating genetic diversity in eukaryotes. Fungi exhibit diverse strategies for sexual reproduction both in nature and in the laboratory. In this study, we report the discovery of same-sex (homothallic) mating in the human fungal pathogen Candida tropicalis. We show that same-sex mating occurs between two cells carrying the same mating type (MTLa/a or α/α) and requires the presence of pheromone from the opposite mating type as well as the receptor for this pheromone. In ménage à trois mating mixes (i.e., "a x a + α helper" or "α x α + a helper" mixes), pheromone secreted by helper strains promotes diploid C. tropicalis cells to undergo same-sex mating and form tetraploid products. Surprisingly, however, the tetraploid mating products can then efficiently mate with cells of the opposite mating type to generate hexaploid products. The unstable hexaploid progeny generated from this coupled process of same- and opposite-sex mating undergo rapid chromosome loss and generate extensive genetic variation. Phenotypic analysis demonstrated that the mating progeny-derived strains exhibit diverse morphologies and phenotypes, including differences in secreted aspartic proteinase (Sap) activity and susceptibility to the antifungal drugs. Thus, the coupling of same- and opposite-sex mating represents a novel mode to generate polyploidy and genetic diversity, which may facilitate the evolution of new traits in C. tropicalis and adaptation to changing environments.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Candida tropicalis / genetics*
  • Candida tropicalis / metabolism
  • Candida tropicalis / physiology
  • Candidiasis / microbiology
  • Crosses, Genetic
  • Diploidy
  • Genes, Mating Type, Fungal / genetics*
  • Genetic Variation*
  • Genotype
  • Humans
  • Phenotype
  • Pheromones / metabolism
  • Polyploidy*
  • Tetraploidy

Substances

  • Pheromones

Grants and funding

This work was supported by the National Natural Science Foundation of China (31625002 and 31370175 to GH), National Science and Technology Major Project (2018ZX10101004-003-002), and start-up grants to HD and GH from Fudan University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.