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.

Highlights

  • Sexual reproduction drives the evolution of new traits and adaptation to new environments in eukaryotic organisms

  • The fungal pathogen Candida tropicalis lives as a commensal in humans but is widely distributed in diverse environments

  • We report the discovery of same-sex mating and reveal an unusual process in which same- and opposite-sex mating are coupled in this fungus

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Summary

Introduction

Sexual reproduction drives the evolution of new traits and adaptation to new environments in eukaryotic organisms. Many fungal species exhibit opposite- and same-sex mating (or heterothallic and homothallic reproduction, respectively), both in nature and under experimental conditions [3,4,5]. The human fungal pathogens Candida albicans and Cryptococcus neoformans undergo both opposite- and same-sex mating in the laboratory [3, 4]. The vast majority of natural isolates of C. neoformans are of the α mating type and same-sex mating can occur between both isogenic and non-isogenic α strains in a pheromone-dependent manner [3]. In C. neoformans and C. albicans, sexual mating and subsequent meiosis or chromosome loss often results in aneuploid forms and the generation of genetic and phenotypic diversity de novo [6, 7]

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