Multiple independent losses of crossover interference during yeast evolutionary history

PLoS Genet. 2024 Sep 26;20(9):e1011426. doi: 10.1371/journal.pgen.1011426. eCollection 2024 Sep.

Abstract

Meiotic recombination is essential for the accurate chromosome segregation and the generation of genetic diversity through crossover and gene conversion events. Although this process has been studied extensively in a few selected model species, understanding how its properties vary across species remains limited. For instance, the ancestral ZMM pathway that generates interference-dependent crossovers has undergone multiple losses throughout evolution, suggesting variations in the regulation of crossover formation. In this context, we first characterized the meiotic recombination landscape and properties of the Kluyveromyces lactis budding yeast. We then conducted a comprehensive analysis of 29,151 recombination events (19, 212 COs and 9, 939 NCOs) spanning 577 meioses in the five budding yeast species Saccharomyces cerevisiae, Saccharomyces paradoxus, Lachancea kluyveri, Lachancea waltii and K. lactis. Eventually, we found that the Saccharomyces yeasts displayed higher recombination rates compared to the non-Saccharomyces yeasts. In addition, bona fide crossover interference and associated crossover homeostasis were detected in the Saccharomyces species only, adding L. kluyveri and K. lactis to the list of budding yeast species that lost crossover interference. Finally, recombination hotspots, although highly conserved within the Saccharomyces yeasts are not conserved beyond the Saccharomyces genus. Overall, these results highlight great variability in the recombination landscape and properties through budding yeasts evolution.

MeSH terms

  • Chromosome Segregation / genetics
  • Crossing Over, Genetic*
  • Evolution, Molecular*
  • Gene Conversion
  • Kluyveromyces / genetics
  • Meiosis* / genetics
  • Saccharomyces / genetics
  • Saccharomyces cerevisiae* / genetics
  • Saccharomycetales / genetics

Grants and funding

Agence Nationale de la Recherche (ANR):JS ANR-18-CE12-0013; Agence Nationale de la Recherche (ANR):BL ANR-18-CE12-0013; EC | European Research Council (ERC):JS 772505 The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.