Pattern of local adaptation to quantitative host resistance in a major pathogen of a perennial crop.

Understanding the mechanisms involved in pathogen adaptation to quantitative resistance in plants has a key role to play in establishing durable strategies for resistance deployment, especially in perennial crops. The erosion of quantitative resistance has been recently suspected in Cuba and the Dominican Republic for a major fungal pathogen of such a crop: Pseudocercospora fijiensis, causing black leaf streak disease on banana. This study set out to test whether such erosion has resulted from an adaptation of P. fijiensis populations, and to determine whether or not the adaptation is local. Almost 600 P. fijiensis isolates from Cuba and the Dominican Republic were sampled using a paired-population sampling design on resistant and susceptible banana varieties. A low genetic structure of the P. fijiensis populations was detected in each country using 16 microsatellite markers. Cross-inoculation experiments using isolates from susceptible and resistant cultivars were carried out, measuring a quantitative trait (the diseased leaf area) related to pathogen fitness on three varieties. A further analysis based on those data suggested the existence of a local pattern of adaptation to resistant cultivars in both of the study countries, due to the existence of specific (or genotype by genotype) host-pathogen interactions. However, neither cost nor benefit effects for adapted populations were found on the widely used "Cavendish" banana group. These results highlight the need to study specific host-pathogen interactions and pathogen adaptation on a wide range of quantitative resistance phenotypes in banana, in order to develop durable strategies for resistance deployment.

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.

The banana (Musa acuminata) genome and the evolution of monocotyledonous plants.

Bananas (Musa spp.), including dessert and cooking types, are giant perennial monocotyledonous herbs of the order Zingiberales, a sister group to the well-studied Poales, which include cereals. Bananas are vital for food security in many tropical and subtropical countries and the most popular fruit in industrialized countries. The Musa domestication process started some 7,000 years ago in Southeast Asia. It involved hybridizations between diverse species and subspecies, fostered by human migrations, and selection of diploid and triploid seedless, parthenocarpic hybrids thereafter widely dispersed by vegetative propagation. Half of the current production relies on somaclones derived from a single triploid genotype (Cavendish). Pests and diseases have gradually become adapted, representing an imminent danger for global banana production. Here we describe the draft sequence of the 523-megabase genome of a Musa acuminata doubled-haploid genotype, providing a crucial stepping-stone for genetic improvement of banana. We detected three rounds of whole-genome duplications in the Musa lineage, independently of those previously described in the Poales lineage and the one we detected in the Arecales lineage. This first monocotyledon high-continuity whole-genome sequence reported outside Poales represents an essential bridge for comparative genome analysis in plants. As such, it clarifies commelinid-monocotyledon phylogenetic relationships, reveals Poaceae-specific features and has led to the discovery of conserved non-coding sequences predating monocotyledon-eudicotyledon divergence.