Evolution of the banana genome is impacted by large chromosomal translocations

ost banana cultivars are triploid derived from Musa acuminata (2n=2x=22), sometimes combined with Musa balbisiana (2n=2x=22). These species and subspecies diverged following geographical isolation in distinct Southeast Asian continental regions and islands. Contact between them was made possible by human migration and led to the selection of seedless parthenocarpic hybrids. M. acuminata subspecies were suggested to differ by a few large chromosomal rearrangements based on chromosome pairing configurations in inter-subspecies hybrids. The precise nature of these rearrangements, their distribution in the diversity and their consequence on chromosomal segregation in structural heterozygote remained to be documented. We searched for large chromosomal rearrangements in a seedy M. acuminata ssp. malaccensis banana accession through mate-pair sequencing, BAC-FISH, targeted PCR and marker (DArTseq) segregation in its progeny. We identified a heterozygous reciprocal translocation involving two distal 3 Mb and 10 Mb segments from chromosomes 01 and 04, respectively, and showed that it locally generated high segregation distortions and reduced recombinations in its progeny. The two chromosome structures were found to be mutually exclusive in gametes and the rearranged structure was preferentially transmitted to the progeny. The rearranged chromosome structure was frequently found in triploid cultivars but within the wild accessions, it was only found within malaccensis sub-species accessions, thus suggesting that this rearrangement occurred in this sub-species. We propose mechanisms for the spread of this rearrangement in Musa diversity and propose that this structure may have played a role in the emergence of triploid cultivars. Knowledge on these structures and their impact on chromosomal recombination and segregation will now allow to take them into account for the genetic analysis of traits of agronomic interest (QTL, GWAS) and for the choice of crosses in breeding programs. (Texte intégral