Population Genomics Reveals Chromosome-Scale Heterogeneous Evolution in a Protoploid Yeast

Abstract

Yeast species represent an ideal model system for population genomic studies but large-scale polymorphism surveys have only been reported for species of the Saccharomyces genus so far. Hence, little is known about intraspecific diversity and evolution in yeast. To obtain a new insight into the evolutionary forces shaping natural populations, we sequenced the genomes of an expansive worldwide collection of isolates from a species distantly related to Saccharomyces cerevisiae: Lachancea kluyveri (formerly S. kluyveri). We identified 6.5 million single nucleotide polymorphisms and showed that a large introgression event of 1 Mb of GC-rich sequence in the chromosomal arm probably occurred in the last common ancestor of all L. kluyveri strains. Our population genomic data clearly revealed that this 1-Mb region underwent a molecular evolution pattern very different from the rest of the genome. It is characterized by a higher recombination rate, with a dramatically elevated A:T → G:C substitution rate, which is the signature of an increased GC-biased gene conversion. In addition, the predicted base composition at equilibrium demonstrates that the chromosome-scale compositional heterogeneity will persist after the genome has reached mutational equilibrium. Altogether, the data presented herein clearly show that distinct recombination and substitution regimes can coexist and lead to different evolutionary patterns within a single genome.

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

“…We confirmed that the orthologs of LIF1 and NEJ1 were missing from the L. kluyveri reference genome (Fig. 2) and from the 28 sequenced strains of L. kluyveri (Friedrich et al 2015). A relic of NEJ1 was found next to a rearrangement breakpoint in the L. kluyveri genome, suggesting that the loss of NEJ1 resulted from a gene disruption event (Supplemental Fig.…”

“…In L. kluyveri, a region of 1 Mb containing the MAT locus and covering almost the whole left arm of chromosome C, has an average GC content of 52.9%, which is significantly higher than the 40.4% global GC content of the rest of the genome (Payen et al 2009;Souciet et al 2009). The orthologous counterpart of this chromosomal region is found in all other Lachancea species, but none of them presented the GC content heterogeneity characterized in L. kluyveri, reinforcing the hypothesis of an introgression event at the origin of this chromosomal arm (Friedrich et al 2015).…”

“…With 131 predicted genes, the L. kluyveri branch encompasses the highest number of species-specific singleton genes. We used the available population genomic data (Friedrich et al 2015) to check whether these CDS are conserved between the genomes of L. kluyveri isolates we recently sequenced. We found that 114 CDS have homologs conserved in several strains and, therefore, probably correspond to real genes.…”

“…For the 127 L. kluyveri-specific TRGs, the CDS were considered physically absent from a given L. kluyveri strain if their sequencing coverage (estimated by mpileup in samtools) in the BAM files from the 28 sequenced L. kluyveri strains (Friedrich et al 2015) was lower than the mean coverage minus two standard deviations for the core genome of that strain (L. kluyveri syntenic homologs).…”

Experimental evolution of the model eukaryote Saccharomyces cerevisiae yields insight into the molecular mechanisms underlying adaptation

“…Subsequent technological advances made it possible to sequence other fungal genomes [2][3][4][5][6]. This in turn allowed researchers to compare the genomes of different yeast species, investigate the specific order of genes and study the organization and evolution of biological pathways and regulatory modules [7,8].…”