Natural variation modifies centromere-proximal meiotic crossover frequency and segregation distortion in Arabidopsis...

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 12 F1 hybrids between the reference strain Col-0 and nonreference 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 7 accessions, to epigenetic patterns of CENH3 enrichment and DNA methylation. Using linear modeling, 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, which occurred with or without a simultaneous change to centromere-proximal crossover frequency. Linear modeling 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.