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

Author summaryStudying 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, meiotic recombination is essential for gamete formation, and it 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, also known as the baker's yeast, and another close relative Lachancea kluyveri. L. waltii meiotic chromosomes are frequently devoid of crossover, suggesting the existence of an alternative mechanism that efficiently ensures gamete formation. In addition, in line with the L. waltii specific loss of several genes controlling interference between meiotic crossovers, a process promoting even crossovers spacing, we found only residual crossover interference in L. waltii. This residual crossover interference is likely the result of the modest interference existing between recombination precursors that is often disregarded. Finally, while crossover hotspots were found to be remarkably stable across the Saccharomyces species, we found here that they are not conserved between the Lachancea and the Saccharomyces clades. This shows that crossover hotspots can evolve at a rather limited evolutionary scale within budding yeasts. Meiotic recombination is a driving force for genome evolution, deeply characterized in a few model species, notably in the budding yeast Saccharomyces cerevisiae. Interestingly, Zip2, Zip3, Zip4, Spo16, Msh4, and Msh5, members of the so-called ZMM pathway that implements the interfering meiotic crossover pathway in S. cerevisiae, have been lost in Lachancea yeast species after the divergence of Lachancea kluyveri from the rest of the clade. In this context, after investigating meiosis in L. kluyveri, we determined the meiotic recombination landscape of Lachancea waltii. Attempts to generate diploid strains with fully hybrid genomes invariably resulted in strains with frequent whole-chromosome aneuploidy and multiple extended regions of loss of heterozygosity (LOH), which mechanistic origin is so far unclear. Despite the lack of multiple ZMM pro-crossover factors in L. waltii, numbers of crossovers and noncrossovers per meiosis were higher than in L. kluyveri but lower than in S. cerevisiae, for comparable genome sizes. Similar to L. kluyveri but opposite to S. cerevisiae, L. waltii exhibits an elevated frequency of zero-crossover bivalents. Lengths of gene conversion tracts for both crossovers and non-crossovers in L. waltii were comparable to those observed in S. cerevisiae and shorter than in L. kluyveri despite the lack of Mlh2, a factor limiting conversion tract size in S. cerevisiae. L. waltii recombination hotspots were 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, L. waltii crossover interference was reduced relative to S. cerevisiae, with interference being detected only in the 25 kb distance range. Detection of positive inference only at short distance scales in the absence of multiple ZMM factors required for interference-sensitive crossovers in other systems likely reflects interference between early recombination precursors such as DSBs.

Automated summary

In this study, the non-model budding yeast Lachancea waltii was used to investigate meiotic recombination. It was found that L. waltii frequently lacks crossover, suggesting the existence of an alternative mechanism for gamete formation. The interference between meiotic crossovers in L. waltii was reduced compared to S. cerevisiae, and crossover hotspots were not conserved between Lachancea and Saccharomyces clades. This study demonstrates that meiotic recombination can evolve at a limited evolutionary scale within budding yeasts.