Role of Cis, Trans, and Inbreeding Effects on Meiotic Recombination in Saccharomyces cerevisiae

Abstract

Meiotic recombination is a major driver of genome evolution by creating new genetic combinations. To probe the factors driving variability of meiotic recombination, we used a high-throughput method to measure recombination rates in hybrids between SK1 and a total of 26 Saccharomyces cerevisiae strains from different geographic origins and habitats. Fourteen intervals were monitored for each strain, covering chromosomes VI and XI entirely, and part of chromosome I. We found an average number of crossovers per chromosome ranging between 1.0 and 9.5 across strains ("domesticated" or not), which is higher than the average between 0.5 and 1.5 found in most organisms. In the different intervals analyzed, recombination showed up to ninefold variation across strains but global recombination landscapes along chromosomes varied less. We also built an incomplete diallel experiment to measure recombination rates in one region of chromosome XI in 10 different crosses involving five parental strains. Our overall results indicate that recombination rate is increasingly positively correlated with sequence similarity between homologs (i) in DNA doublestrand-break-rich regions within intervals, (ii) in entire intervals, and (iii) at the whole genome scale. Therefore, these correlations cannot be explained by cis effects only. We also estimated that cis and trans effects explained 38 and 17%, respectively, of the variance of recombination rate. In addition, by using a quantitative genetics analysis, we identified an inbreeding effect that reduces recombination rate in homozygous genotypes, while other interaction effects (specific combining ability) or additive effects (general combining ability) are found to be weak. Finally, we measured significant crossover interference in some strains, and interference intensity was positively correlated with crossover number.

The recombination landscape of introgression in yeast

“…We detected more COs and fewer NCOs in our natural cross when compared to our fermentation cross, within a similar range of COs and NCOs per meiosis as previous studies in S. cerevisiae and S. paradoxus (Liu et al, 2019;Mancera et al, 2008). Our findings demonstrate significant differences in recombination rate between closely related strains, adding to a body of literature across plants, animals, and fungi that recombination rate can evolve rapidly (Bauer et al, 2013;Danguy des Déserts et al, 2021;Kong et al, 2014;McGaugh et al, 2012;Petit et al, 2017;Raffoux et al, 2018;Samuk et al, 2019;Sandor et al, 2012;Schreiber et al, 2022).…”

“…Yeasts provide an excellent opportunity to study DSB resolution, as we can readily isolate and collect all four meiotic products of a given meiosis and detect both CO and more elusive NCO events (Figure 1A) (Brion et al, 2017; Gerton et al, 2000; Liu et al, 2018, 2019; Mancera et al, 2008). Recombination rates vary between strains of S. cerevisiae (Cubillos et al, 2011; Raffoux et al, 2018) and between S. cerevisiae and its sister species S. paradoxus (Liu et al, 2019; Tsai et al, 2010). Strains of different Saccharomyces species have often hybridized with other species and carry introgressed DNA from these events (Albertin et al, 2018; Almeida et al, 2014; Bendixsen et al, 2022; D’Angiolo et al, 2020; Langdon et al, 2019; Stelkens & Bendixsen, 2022; Tellini et al, 2023).…”

Negative heterosis for meiotic recombination rate in spermatocytes of the domestic chicken Gallus gallus

“…Similarly, the study of recombination rate in hybrids be tween S. cerevisiae strains using highthroughput method showed a positive correlation of its level with sequence similarity between homologs at different scales (Raffoux et al, 2018). This is consistent with the finding that sequence divergence greater than about 1 % leads to the suppression of recombination due to heteroduplex rejection by the mismatch repair machinery (Chen, JinksRobertson, 1999).…”

The recombination landscape of introgression in yeast

“…Yeasts provide an excellent opportunity to study DSB resolution, as we can readily isolate and collect all four meiotic products of a given meiosis and detect both CO and more elusive NCO events (Figure 1A ) (Brion et al, 2017 ;Gerton et al, 2000 ;Liu et al, 2018Liu et al, , 2019Mancera et al, 2008 ). Recombination rates vary between strains of S. cerevisiae (Cubillos et al, 2011 ;Raffoux et al, 2018 ) and between S. cerevisiae and its sister species S. paradoxus (Liu et al, 2019 ;Tsai et al, 2010 ). Strains of different Saccharomyces species have often hybridized with other species and carry introgressed DNA from these events (Albertin et al, 2018 ;Almeida et al, 2014 ;Bendixsen et al, 2022 ;D'Angiolo et al, 2020 ;Langdon et al, 2019 ;Tellini et al, 2023 ).…”