Non-random distribution of extensive chromosome rearrangements in Brassica napus depends on genome organization

Chromosome rearrangements are common, but their dynamics over time, mechanisms of occurrence and the genomic features that shape their distribution and rate are still poorly understood. We used allohaploid Brassica napus (AC, n = 19) as a model to analyze the effect of genomic features on the formation and diversity of meiotically driven chromosome rearrangements. We showed that allohaploid B. napus meiosis leads to extensive new structural diversity. Almost every allohaploid offspring carried a unique combination of multiple rearrangements throughout the genome, and was thus structurally differentiated from both its haploid parent and its sister plants. This large amount of genome reshuffling was remarkably well-tolerated in the heterozygous state, as neither male nor female fertility were strongly reduced, and meiosis behavior was normal in most cases. We also used a quantitative statistical model, which accounted for 75% of the observed variation in rearrangement rates, to show that the distribution of meiotically driven chromosome rearrangements was not random but was shaped by three principal genomic features. In descending order of importance, the rate of marker loss increased strongly with genetic distance from the centromere, the degree of collinearity between chromosomes, and the genome of origin (A < C). Overall, our results demonstrate that B. napus accumulates a large number of genetic changes, but these rearrangements are not randomly distributed in the genome. The structural genetic diversity produced by the allohaploid pathway and its role in the evolution of polyploid species compared to diploid meiosis are discussed.