Chromosome reciprocal translocations have accompanied subspecies evolution in bananas.

Chromosome rearrangements and the way that they impact genetic differentiation and speciation have long raised questions from evolutionary biologists. They are also a major concern for breeders because of their bearing on chromosome recombination. Banana is a major crop that derives from inter(sub)specific hybridizations between various once geographically isolated Musa species and subspecies. We sequenced 155 accessions, including banana cultivars and representatives of Musa diversity, and genotyped-by-sequencing 1059 individuals from 11 progenies. We precisely characterized six large reciprocal translocations and showed that they emerged in different (sub)species of Musa acuminata, the main contributor to currently cultivated bananas. Most diploid and triploid cultivars analyzed were structurally heterozygous for 1 to 4 M. acuminata translocations, highlighting their complex origin. We showed that all translocations induced a recombination reduction of variable intensity and extent depending on the translocations, involving only the breakpoint regions, a chromosome arm, or an entire chromosome. The translocated chromosomes were found preferentially transmitted in many cases. We explore and discuss the possible mechanisms involved in this preferential transmission and its impact on translocation colonization.

Genome ancestry mosaics reveal multiple and cryptic contributors to cultivated banana.

Hybridizations between closely related species commonly occur in the domestication process of many crops. Banana cultivars are derived from such hybridizations between species and subspecies of the Musa genus that have diverged in various tropical Southeast Asian regions and archipelagos. Among the diploid and triploid hybrids generated, those with seedless parthenocarpic fruits were selected by humans and thereafter dispersed through vegetative propagation. Musa acuminata subspecies contribute to most of these cultivars. We analyzed sequence data from 14 M. acuminata wild accessions and 10 M. acuminata-based cultivars, including diploids and one triploid, to characterize the ancestral origins along their chromosomes. We used multivariate analysis and single nucleotide polymorphism clustering and identified five ancestral groups as contributors to these cultivars. Four of these corresponded to known M. acuminata subspecies. A fifth group, found only in cultivars, was defined based on the 'Pisang Madu' cultivar and represented two uncharacterized genetic pools. Diverse ancestral contributions along cultivar chromosomes were found, resulting in mosaics with at least three and up to five ancestries. The commercially important triploid Cavendish banana cultivar had contributions from at least one of the uncharacterized genetic pools and three known M. acuminata subspecies. Our results highlighted that cultivated banana origins are more complex than expected - involving multiple hybridization steps - and also that major wild banana ancestors have yet to be identified. This study revealed the extent to which admixture has framed the evolution and domestication of a crop plant.

Musa balbisiana genome reveals subgenome evolution and functional divergence.

Banana cultivars (Musa ssp.) are diploid, triploid and tetraploid hybrids derived from Musa acuminata and Musa balbisiana. We presented a high-quality draft genome assembly of M. balbisiana with 430 Mb (87%) assembled into 11 chromosomes. We identified that the recent divergence of M. acuminata (A-genome) and M. balbisiana (B-genome) occurred after lineage-specific whole-genome duplication, and that the B-genome may be more sensitive to the fractionation process compared to the A-genome. Homoeologous exchanges occurred frequently between A- and B-subgenomes in allopolyploids. Genomic variation within progenitors resulted in functional divergence of subgenomes. Global homoeologue expression dominance occurred between subgenomes of the allotriploid. Gene families related to ethylene biosynthesis and starch metabolism exhibited significant expansion at the pathway level and wide homoeologue expression dominance in the B-subgenome of the allotriploid. The independent origin of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) homoeologue gene pairs and tandem duplication-driven expansion of ACO genes in the B-subgenome contributed to rapid and major ethylene production post-harvest in allotriploid banana fruits. The findings of this study provide greater context for understanding fruit biology, and aid the development of tools for breeding optimal banana cultivars.

Recombination and Large Structural Variations Shape Interspecific Edible Bananas Genomes.

Admixture and polyploidization are major recognized eukaryotic genome evolutionary processes. Their impacts on genome dynamics vary among systems and are still partially deciphered. Many banana cultivars are triploid (sometimes diploid) interspecific hybrids between Musa acuminata (A genome) and M. balbisiana (B genome). They have no or very low fertility, are vegetatively propagated and have been classified as "AB," "AAB," or "ABB" based on morphological characters. We used NGS sequence data to characterize the A versus B chromosome composition of nine diploid and triploid interspecific cultivars, to compare the chromosome structures of A and B genomes and analyze A/B chromosome segregations in a polyploid context. We showed that interspecific recombination occurred frequently between A and B chromosomes. We identified two large structural variations between A and B genomes, a reciprocal translocation and an inversion that locally affected recombination and led to segregation distortion and aneuploidy in a triploid progeny. Interspecific recombination and large structural variations explained the mosaic genomes observed in edible bananas. The unprecedented resolution in deciphering their genome structure allowed us to start revisiting the origins of banana cultivars and provided new information to gain insight into the impact of interspecificity on genome evolution. It will also facilitate much more effective assessment of breeding strategies.