Chromosomal breakage in Arabidopsis thaliana neo-polyploids occurs preferentially at candidate fragile sites colocalized with ancient genome rearrangements

Newly formed polyploids often suffer extensive aneuploidy and chromosome rearrangement. We explored whether these are predictable and conserved across genotypes. We quantified whole-chromosome and segmental aneuploidy in progeny arrays of neo-polyploid Arabidopsis thaliana from two accessions (Col-0 and Ler). 29% of progeny had whole-chromosome and/or segmental aneuploidies. Strikingly, segmental aneuploidy arose exclusively from Ler, preferentially maternally, showing that genotype and sex of origin matter. Breakpoints of segmental aneuploidies were non-random, with over 2/3 mapping to five potentially fragile regions (PFRs). Two PFRs overlap with junctions of ancient chromosomal fusions that differentiate the A. thaliana genome from that of its relatives and also overlap more broadly with hotspots of recurrent chromosomal rearrangements differentiating species in the Brassicaceae family. Several PFRs overlap with large tandemly repeated disease resistance gene clusters. Our results support the hypothesis of a link between ancestral genome rearrangements and present-day chromosome fragility. Polyploidy serving as a context that makes aneuploidies more likely to arise and survive, with fragile sites lending a degree of predictability.