Heterothallism inSaccharomyces cerevisiaeisolates from nature: effect ofHOlocus on the mode of reproduction

Abstract

Understanding the evolution of sex and recombination, key factors in the evolution of life, is a major challenge in biology. Studies of reproduction strategies of natural populations are important to complement the theoretical and experimental models. Fungi with both sexual and asexual life cycles are an interesting system for understanding the evolution of sex. In a study of natural populations of yeast Saccharomyces cerevisiae, we found that the isolates are heterothallic, meaning their mating type is stable, while the general belief is that natural S. cerevisiae strains are homothallic (can undergo mating-type switching). Mating-type switching is a gene-conversion process initiated by a site-specific endonuclease HO; this process can be followed by mother–daughter mating. Heterothallic yeast can mate with unrelated haploids (amphimixis), or undergo mating between spores from the same tetrad (intratetrad mating, or automixis), but cannot undergo mother–daughter mating as homothallic yeasts can. Sequence analysis of HO gene in a panel of natural S. cerevisiae isolates revealed multiple mutations. Good correspondence was found in the comparison of population structure characterized using 19 microsatellite markers spread over eight chromosomes and the HO sequence. Experiments that tested whether the mating-type switching pathway upstream and downstream of HO is functional, together with the detected HO mutations, strongly suggest that loss of function of HO is the cause of heterothallism. Furthermore, our results support the hypothesis that clonal reproduction and intratetrad mating may predominate in natural yeast populations, while mother–daughter mating might not be as significant as was considered.

Improving industrial yeast strains: exploiting natural and artificial diversity

“…In this way, the haploid stage filters out lethal recessive mutations and the subsequent haplo-selfing enables recessive, heterozygous mutations to become homozygous and thus influence the phenotype. Intratetrad mating (automixis) after sporulation will have the same effect (Katz Ezov et al ., 2010). Together, this can improve cellular fitness and adaptability to the environment (Pretorius, 2000).…”

“…This is mainly due to the homothallic nature of most industrial and feral yeast strains, making them unsuited for this approach. However, it was recently described that several feral strains show a stable haploid mating type, due to a mutation in the HO endonuclease gene, a gene responsible for mating-type switching (Katz Ezov et al ., 2010), making these strains fit for cell-to-cell mating experiments. In principle, also homothallic strains would be amenable to this approach after genetically disrupting the HO endonuclease gene (van Zyl et al ., 1993; Walker et al ., 2005; Blasco et al ., 2011; Fig 3…”

Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locusSaccharomyces cerevisiaesystem

“…Genomic data indicate that, despite its benefits, switching also has been lost several other times including in the methylotrophs Kuraishia capsulata and Dekkera bruxellensis (22)(23)(24), and in the Saccharomycetaceae Lachancea kluyveri and Kazachstania africana (29,61). Null alleles of HO are frequent among natural populations of S. cerevisiae (62). Losses of switching may simply reflect life in environments that do not require frequent spore formation for survival or dispersal.…”

New Lager Brewery Strains Obtained by Crossing Techniques Using Cachaça (Brazilian Spirit) Yeasts

“…Interestingly, different data have shown that several heterothallic S. cerevisiae strains have been isolated from wine and natural sites (21,24). However, the majority of natural isolates of S. cerevisiae are considered able to undergo mating type switching and therefore be homothallic (25,26).…”

“…Among the homothallic yeast strains of our study, 12 strains presented at least one inactive copy of the HO gene (date not shown). The mutations found in the HO sequences of S. cerevisiae strains are strong indicators of a full or partial loss of endonuclease Ho function, and yeast cells are unable to switch mating type and to exhibit crossing between neighboring "sister" cells (self-diploidization) (24). On the other hand, due to its complex sexual life cycle, homothallic yeast can eliminate cells with deleterious recessive mutations from the population while generating homozygous diploid cells in which these mutations are not present (26)(27)(28).…”