Lessons from the meiotic recombination landscape of the ZMM deficient budding yeast Lachancea waltii

Abstract

AbstractMeiotic recombination has been deeply characterized in a few model species only, notably in the budding yeast Saccharomyces cerevisiae. Interestingly, most members of the ZMM pathway that implements meiotic crossover interference in S. cerevisiae have been lost in Lachancea yeast species after the divergence of Lachancea kluyveri from the rest of the clade. This suggests major differences in the control of crossover distribution. After investigating meiosis in L. kluyveri, we determined the meiotic recombination landscape of Lachancea waltii and identified several characteristics that should help understand better the underlying mechanisms. Such characteristics include systematic regions of loss of heterozygosity (LOH) in L. waltii hybrids, compatible with dysregulated Spo11-mediated DNA double strand breaks (DSB) independently of meiosis. They include a higher recombination rate in L. waltii than in L. kluyveri despite the lack of multiple ZMM pro-crossover factors. L. waltii exhibits an elevated frequency of zero-crossover bivalents as L. kluyveri but opposite to S. cerevisiae. L. waltii gene conversion tracts lengths are comparable to those observed in S. cerevisiae and shorter than in L. kluyveri despite the lack of Mlh2, a factor limiting conversion tracts size in S. cerevisiae. L. waltii recombination hotspots are not shared with either S. cerevisiae or L. kluyveri, showing that meiotic recombination hotspots can evolve at a rather limited evolutionary scale within budding yeasts. Finally, in line with the loss of several ZMM genes, we found only residual crossover interference in L. waltii likely coming from the modest interference existing between recombination precursors.Significance statementStudying non-model species is relevant to understand better biological processes by shedding light on their evolutionary variations. Here we chose the non-model budding yeast Lachancea waltii to study meiotic recombination. In sexually reproducing organisms, meiotic recombination shuffles parental genetic combinations notably by crossovers that cluster in hotspots at the population level. We found remarkable variations compared to both the canonical Saccharomyces cerevisiae model and another close relative Lachancea kluyveri. Such variations notably include the loss in L. waltii of a layer of regulation of crossover distribution that is otherwise conserved in budding yeasts and mammals. They also include the lack of conservation of crossover hotspots across the Lachancea species while crossover hotspots are remarkably stable across the Saccharomyces species.Highlights-Extensive LOH events in L. waltii intraspecific hybrids-No conservation of the recombination hotspots across the Lachancea genus-Reduced but not suppressed crossover interference in the absence of the ZMM pathway-Similar gene conversion tract lengths in L. waltii, S. cerevisiae, and L. kluyveri despite the lack of MLH2 in L. waltii