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Abstract
Hybrids between diverged lineages contain novel genetic combinations but an impaired meiosis often makes them evolutionary dead ends. Here, we explore to what extent an aborted meiosis followed by a return-to-growth (RTG) promotes recombination across a panel of 20 Saccharomyces cerevisiae and S. paradoxus diploid hybrids with different genomic structures and levels of sterility. Genome analyses of 275 clones reveal that RTG promotes recombination and generates extensive regions of loss-of-heterozygosity in sterile hybrids with either a defective meiosis or a heavily rearranged karyotype, whereas RTG recombination is reduced by high sequence divergence between parental subgenomes. The RTG recombination preferentially arises in regions with low local heterozygosity and near meiotic recombination hotspots. The loss-of-heterozygosity has a profound impact on sexual and asexual fitness, and enables genetic mapping of phenotypic differences in sterile lineages where linkage analysis would fail. We propose that RTG gives sterile yeast hybrids access to a natural route for genome recombination and adaptation.
Highlights
Hybrids between diverged lineages contain novel genetic combinations but an impaired meiosis often makes them evolutionary dead ends
We probed whether RTG allows S. cerevisiae (Sc) to the bypass mutational barriers in meiosis by deleting NDT80, the master regulator of middle and late meiotic genes, in an otherwise fertile ScS288C/ScSK1 intraspecies lab-hybrid
We confirmed by DAPI staining that ndt80Δ cells were all arrested before the first meiotic division (MI) after 8 h of sporulation induction, whereas ≥50% of the wild-type ScS288C/ScSK1 cells had already completed MI (≥ 2 nuclei) at this time-point
Summary
Hybrids between diverged lineages contain novel genetic combinations but an impaired meiosis often makes them evolutionary dead ends. Saccharomyces interspecies hybrids produce inviable gametes because of the large DNA sequence divergence between parental subgenomes, namely heterozygosity, which suppresses recombination and leads to chromosome missegregation[14]. As in most eukaryotes[18], a homolog of an archaea DNA topoisomerase VI, Spo11p in yeast, generates genome-wide double-strand breaks (DSBs)[19] The repair of these DSBs produces joint DNA molecules and leads to recombination through chromosomal crossover (CO) and non-crossover (NCO) events. RTG cells repair the DSBs, budlike mitotic cells and segregate their recombined chromatids with no further DNA replication[22] This process generates a mother and a daughter cell that both maintain the parental diploid state, as they do not complete the two chromosomal segregation events that occur in complete meiosis, but contain different rearranged genotypes. We show that RTG allows recombination in Saccharomyces hybrids that are sterile due to common reproductive barriers, and we propose RTG as a powerful alternative to completed meiosis that may play an unanticipated role in the evolution of yeast hybrid genomes in nature
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