Natural variation and dosage of the HEI10 meiotic E$_{3}$ ligase control $\textit{Arabidopsis}$ crossover recombination

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 $\textit{Arabidopsis thaliana}$ accessions, we identified two major recombination quantitative trait loci (rQTLs) that explain 56.9% of crossover variation in Col×Ler F${2}$ populations. We mapped rQTL1 to semidominant polymorphisms in HEI10, which encodes a conserved ubiquitin E${3}$ 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 $\textit{Arabidopsis}$ recombination. Our work reveals that HEI10 naturally limits $\textit{Arabidopsis}$ crossovers and has the potential to influence the response to selection.