New insights into the paradoxical distribution of IRC7 in Saccharomyces cerevisiae and its associated phenotypic and genomic landscapes

Abstract

Biotic and abiotic factors of wine fermentations have led to the accumulation of numerous genomic hallmarks of domestication in Saccharomyces cerevisiae wine strains. Here we have studied the paradoxical distribution of a dominant allele of IRC7 in wine yeast strains. This gene encodes a cysteine-S-{beta}-lyase and presents two alleles: a wild full-length allele (IRC7F) and a mutated one (IRC7S), harboring a 38bp-deletion. Interestingly, IRC7S-coding for a less active enzyme-appears in the great majority of wine strains. Studying its global distribution among phylogenetic clades, we observed that IRC7S allele is dominant just in wine strains, having a moderate presence in other domesticated clades (Beer, Bread and Wine-PDM), but being completely absent in wild clades, appearing as a new hallmark of domestication. To explain this paradoxical distribution, we performed an IRC7-rooted phenotypic-wide survey, demonstrating that IRC7S-homozygous (HS) wine strains have both fitness (lower lag phases and higher growth rates) and competitive (killer toxin resistance, pseudohyphal growth) advantages. Hence, we performed a genome-wide survey across domesticated clades, finding a set of mutations that are conserved among wine strains and potentially associated to IRC7S allele, which can help to explain the outstanding phenotype of HS strains and their dominant distribution in wines. Originality-Significance StatementS. cerevisiae is one of the best studied microbes due to its industrial importance and its use as a eukaryotic model organism. S. cerevisiae is also an interesting model for studying the effects of domestication in yeast genomic, phenotype and ecology. The study of how wild S. cerevisiae strains evolved into a greatly adapted domesticated strains and changed its lifestyle drastically is still of great interest. In the case of wine populations, strains have accumulated numerous hallmarks of domestication in their genome, related with their great phenotypic adaptation to this environment. Here, we report a new hallmark of domestication in wine strains; the IRC7 deleted allele (IRC7S) and present the first insights about its unexpected global distribution among phylogenetic clades, understanding the genomic context and the phenotypic implications of this allele in wine strains.