Abstract

Meiotic recombination is a major factor of genome evolution, deeply characterized in only a few model species, notably the yeast Saccharomyces cerevisiae. Consequently, little is known about variations of its properties across species. In this respect, we explored the recombination landscape of Lachancea kluyveri, a protoploid yeast species that diverged from the Saccharomyces genus more than 100 million years ago and we found striking differences with S. cerevisiae. These variations include a lower recombination rate, a higher frequency of chromosomes segregating without any crossover and the absence of recombination on the chromosome arm containing the sex locus. In addition, although well conserved within the Saccharomyces clade, the S. cerevisiae recombination hotspots are not conserved over a broader evolutionary distance. Finally and strikingly, we found evidence of frequent reversal of commitment to meiosis, resulting in return to mitotic growth after allele shuffling. Identification of this major but underestimated evolutionary phenomenon illustrates the relevance of exploring non-model species.

Highlights

  • Accurate chromosome segregation at the first meiotic division often requires crossovers (COs) between homologous chromosomes [1]

  • Meiotic recombination is initiated by Spo11-catalyzed double strand breaks (DSBs) [3] within nucleosome depleted regions enriched in gene promoters [4] in the context of chromatin loops organized around the synaptonemal complex [5]

  • With the exploration of the meiotic genetic exchanges of a protoploid yeast species and its comparison to S. cerevisiae as well as other fungi (Fig 4A), we unveiled characteristics that brought a new light on the variation of the recombination landscape and its potential impact on evolution

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Summary

Introduction

Accurate chromosome segregation at the first meiotic division often requires crossovers (COs) between homologous chromosomes [1]. Meiotic COs result from the repair of programmed DNA double strand breaks (DSBs) by homologous recombination, that can yield gene conversions through non reciprocal transfer of genetic variations (GCs) [2]. The mapping of 4,163 COs and 2,126 NCOs from 46 S. cerevisiae tetrads [6] showed that the frequency of meiotic recombination events correlates with previously localized DSBs [7,8]. It was highlighted that the frequency of segregating chromosome without a CO is low in S. cerevisiae (1 out of 46 tetrads), supporting the importance of at least one CO per chromosome for accurate segregation [9,10,11]

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