Natural variation modifies centromere-proximal meiotic crossover frequency and segregation distortion in <i>Arabidopsis thaliana</i>

Eukaryotic centromeres mediate chromosome segregation during cell division. Plant centromeres are loaded with CENH3-variant nucleosomes, which direct kinetochore formation and spindle-microtubule interaction. Centromeres are frequently composed of megabase-scale satellite repeat arrays, or retrotransposon nests. In monocentric genomes, such as the model plant Arabidopsis thaliana, pericentromeric heterochromatin surrounds the CENH3-occupied satellite arrays. A zone of suppressed meiotic crossover recombination contains the centromere and extends into the pericentromeres. Here, we explore how natural variation in Arabidopsis influences centromere-proximal crossover frequency, and segregation distortion, when centromeres are heterozygous. We used fluorescent crossover reporters to quantify the effect of genetic variation on centromere-proximal recombination in twelve F1 hybrids between the reference strain Col-0 and non-reference accessions that captured Eurasian and relict diversity, and in total we measured 3,037,802 meioses. The majority of the F1 hybrids (49 of 60) had significantly higher or lower centromere-proximal crossover frequency than inbreds. We relate hybrid crossover frequencies to patterns of nucleotide diversity and centromeric structural variation, and in a subset of seven accessions, to epigenetic patterns of CENH3 enrichment and DNA methylation. Using linear modelling, we observed that chromosome and accession, and their interaction, together explained 85% of variation in crossover frequency, consistent with cis- and trans-acting modifying effects. The fluorescent reporters also allow segregation distortion through meiosis to be quantified between hybrids and inbreds. We observed a minority of hybrids (18 of 60) with distorted segregation through meiosis compared to inbreds, that occurred with or without simultaneous change to centromere-proximal crossover frequency. Linear modelling revealed that 56% of variation in segregation distortion is explained by chromosome and accession, but with a stronger effect of accession compared to crossover frequency. We discuss how Arabidopsis centromeric structural heterozygosity may modify recombination, and cause segregation distortion through meiosis.