Recombination suppression in heterozygotes for a pericentric inversion induces the interchromosomal effect on crossovers in Arabidopsis

During meiosis, recombination ensures allelic exchanges through crossovers (COs) between the homologous chromosomes. Advances in our understanding of the rules ofCOs have come from studies of mutations including structural chromosomal rearrangements that, when heterozygous, are known to impairCOs in various organisms. In this work, we investigate the effect of a large heterozygous pericentric inversion on male and female recombination in Arabidopsis. The inversion was discovered in theAtmcc1mutant background and was characterized through genetic and next-generation sequencing analysis. Reciprocal backcross populations, each consisting of over 400 individuals, obtained from the mutant and the wild type, both crossed with Landsbergerecta, were analyzed genome-wide by 143 single-nucleotide polymorphisms. The negative impact of inversion became evident in terms ofCOloss in the rearranged chromosome in both male and female meiosis. No single-COevent was detected within the inversion, consistent with a post-meiotic selection operating against unbalanced gametes. Cytological analysis of chiasmata in F(1)plants confirmed thatCOs were reduced in male meiosis in the chromosome with inversion. Crossover suppression on the rearranged chromosome is associated with a significant increase ofCOs in the other chromosomes, thereby maintaining unchanged the number ofCOs per cell. TheCOpattern observed in our study is consistent with the interchromosomal (IC) effect as first described inDrosophila. In contrast to male meiosis, in female meiosis noICeffect is visible. This may be related to the greater strength of interference that constrains theCOnumber in excess of the minimum value imposed byCOassurance in Arabidopsis female meiosis.