Comprehensive dissection of meiotic DNA double-strand breaks and crossovers in cucumber

Abstract

Abstract Meiotic recombination drives genetic diversity and crop genome optimization. In plant breeding, parents with favorable traits are crossed to create elite varieties. Different hybridizations produce diverse types of segment reshuffling between homologous chromosomes. However, little is known about the factors that cause hybrid-specific changes in crossovers (COs). Here, we constructed 2 F2 populations from crosses between a semiwild and 2 domesticated cucumber (Cucumis sativus) accessions and examined CO events. COs mainly occurred around genes and differed unevenly along chromosomes between the 2 hybrids. Fine-scale CO distributions were suppressed in regions of heterozygous structural variations (SVs) and were accelerated by high sequence polymorphism. C. sativus RADiation sensitive 51A (CsRAD51A) binding, histone H3 lysine 4 trimethylation (H3K4me3) modification, chromatin accessibility, and hypomethylation were positively associated with global CO landscapes and in local DNA double-strand break (DSB) hotspots and genes. The frequency and suppression of COs could be roughly predicted based on multiomic information. Differences in CO events between hybrids could be partially traced to distinct genetic and epigenetic features and were significantly associated with specific DSB hotspots and heterozygous SVs. Our findings identify the genomic and epigenetic features that contribute to CO formation and hybrid-specific divergence in cucumber and provide theoretical support for selecting parental combinations and manipulating recombination events at target genomic regions during plant breeding.