Genome evolution across 1,011 Saccharomyces cerevisiae isolates

Abstract

Large-scale population genomic surveys are essential to explore the phenotypic diversity of natural populations. Here we report the whole-genome sequencing and phenotyping of 1,011 Saccharomyces cerevisiae isolates, which together provide an accurate evolutionary picture of the genomic variants that shape the species-wide phenotypic landscape of this yeast. Genomic analyses support a single 'out-of-China' origin for this species, followed by several independent domestication events. Although domesticated isolates exhibit high variation in ploidy, aneuploidy and genome content, genome evolution in wild isolates is mainly driven by the accumulation of single nucleotide polymorphisms. A common feature is the extensive loss of heterozygosity, which represents an essential source of inter-individual variation in this mainly asexual species. Most of the single nucleotide polymorphisms, including experimentally identified functional polymorphisms, are present at very low frequencies. The largest numbers of variants identified by genome-wide association are copy-number changes, which have a greater phenotypic effect than do single nucleotide polymorphisms. This resource will guide future population genomics and genotype-phenotype studies in this classic model system.The budding yeast S. cerevisiae is a powerful model system for understanding eukaryotic biology at the cellular, molecular and genomic levels 1,2 . S. cerevisiae has recently emerged as a model in population genomics [3][4][5] , because it can be found worldwide in a broad array of human-associated (for example, wine, sake, beer and other fermented beverages) and wild (for example, plant, soil and insect) biotopes. Recent years have seen a spike in the number of published S. cerevisiae genome sequences, which together have revealed a high level of genetic diversity and a complex population structure in this yeast [6][7][8][9][10][11][12] . However, the number of available sequenced genomes from natural isolates remains limited and stands in contrast to the wealth of data on Arabidopsis thaliana 13 and humans 14,15

Compensatorytrans-regulatory alleles minimizing variation inTDH3expression are common withinSaccharomyces cerevisiae

“…; Peter et al. ). For each strain, we measured YFP fluorescence in 12 biological replicate populations grown in rich media and used the measured YFP fluorescence to estimate changes in TDH3 mRNA levels due to differences in trans ‐regulation among strains (Duveau et al.…”

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

“…One attractive hypothesis, whose testing will require even denser taxon sampling, is that generalist lineages with less reduced genomes and more metabolic capabilities are more likely to produce new species and less likely to go extinct. Evolutionary dynamics favoring generalists over specialists could conceivably play out over geological time through some form of clade selection (Stanley, 1975; Williams, 1992), by drawing from the considerable genetic variation segregating within species (Hittinger et al, 2010; Peter et al, 2018), or both.…”

“…This diverse group, whose genetic diversity is on par with the plant and animal lineages (Figure 1), includes the baker’s yeast and premier eukaryotic model system Saccharomyces cerevisiae (Peter et al, 2018), the common human commensal and opportunistic pathogen Candida albicans, and over 1,000 other known species with more continuing to be discovered (Dujon and Louis, 2017; Hittinger et al, 2015; Kurtzman et al, 2011). …”

The Smell of Synthetic Biology: Engineering Strategies for Aroma Compound Production in Yeast

“…The initial reasons why researchers opted for S. cerevisiae remains true, i.e. this yeast species is by far the best-studied unicellular eukaryote with the genomes of several of its strains fully sequenced [12]; it is a non-pathogen that enjoys GRAS (generally recognised as safe) status; and it is amenable to genetic manipulation with a wide range of genetic tools available to alter the genetic make-up of the yeast. S. cerevisiae also possesses an efficient homologous recombination machinery, which greatly assists stable integration of genetic elements.…”