Abstract
During meiosis, homologous chromosomes undergo crossover recombination, which creates genetic diversity and balances homolog segregation. Despite these critical functions, crossover frequency varies extensively within and between species. Although natural crossover recombination modifier loci have been detected in plants, causal genes have remained elusive. Using natural Arabidopsis thaliana accessions, we identified two major recombination quantitative trait loci (rQTLs) that explain 56.9% of crossover variation in Col×Ler F2 populations. We mapped rQTL1 to semidominant polymorphisms in HEI10, which encodes a conserved ubiquitin E3 ligase that regulates crossovers. Null hei10 mutants are haploinsufficient, and, using genome-wide mapping and immunocytology, we show that transformation of additional HEI10 copies is sufficient to more than double euchromatic crossovers. However, heterochromatic centromeres remained recombination-suppressed. The strongest HEI10-mediated crossover increases occur in subtelomeric euchromatin, which is reminiscent of sex differences in Arabidopsis recombination. Our work reveals that HEI10 naturally limits Arabidopsis crossovers and has the potential to influence the response to selection.
Highlights
The majority of eukaryotes reproduces via the meiotic cell division, where a diploid cell replicates DNA once and segregates chromosomes twice to produce tetrads of haploid gametes (Barton and Charlesworth 1998)
We identified two major trans rQTLs on chromosomes 1 and 4, with logarithm of the odds ratio (LOD) scores of 40.2 and 53.5, which explain 23.3% and 33.6% of the variance in recombination, respectively (F-test, P < 2 × 10−16) (Fig. 2A; Supplemental Table S6). rQTL1Ler genotypes associate with low recombination, with heterozygotes showing intermediate crossover frequency (Fig. 2B), consistent with the semidominant effects observed for chromosome 1 in the chromosome substitution lines (CSLs) F1 experiments (Fig. 1E,F; Supplemental Tables S3, S4)
Fungi, and invertebrates possess a single HEI10/ RNF212 ortholog (Bhalla et al 2008; Chelysheva et al 2012; Wang et al 2012; Serrentino et al 2013; De Muyt et al 2014; Lake et al 2015), whereas vertebrates encode separate RNF212 and HEI10 proteins that function as antagonistic SUMO and ubiquitin E3 ligases (Ward et al 2007; Reynolds et al 2013; Qiao et al 2014; Gray and Cohen 2016; Rao et al 2017)
Summary
The majority of eukaryotes reproduces via the meiotic cell division, where a diploid cell replicates DNA once and segregates chromosomes twice to produce tetrads of haploid gametes (Barton and Charlesworth 1998). Despite the importance of crossovers for balanced chromosome segregation during meiosis and fertility, extensive genetic variation in recombination frequency is observed within and between species (Sanchez-Moran et al 2002; Coop and Przeworski 2006; Fledel-Alon et al 2011; Hinch et al 2011; Sandor et al 2012; Bauer et al 2013; Rodgers-Melnick et al 2015; Ziolkowski et al 2015; Johnston et al 2016). Genetic polymorphisms that modify crossover frequency can be classified as cis- or trans-acting, according to whether they control recombination on the same chromosome or throughout the genome, respectively (Coop and Przeworski 2006; Yandeau-Nelson et al 2006; Baudat and de Massy 2007; Ziolkowski et al 2015). 10 of these initiating meiotic DSBs mature into crossovers per Arabidopsis meiosis (Giraut et al 2011; Salomé et al 2012; Rowan et al 2015; Choi et al 2016)
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