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Background and Aims: Bananas (Musa spp.) are a major staple food for hundreds of millions of people in developing countries. The cultivated varieties are seedless and parthenocarpic clones of which the ancestral origin remains to be clarified. The most important cultivars are triploids with an AAA, AAB or ABB genome constitution, with A and B genomes provided by M. acuminata and M. balbisiana, respectively. Previous studies suggested that inter-genome recombinations were relatively common in banana cultivars and that triploids were more likely to have passed through an intermediate hybrid. In this study, we investigated the chromosome structure within the ABB group, composed of starchy cooking bananas that play an important role in food security., Methods: Using SNP markers called from RADSeq data, we studied the chromosome structure of 36 ABB genotypes spanning defined taxonomic subgroups. To complement our understanding, we searched for similar events within nine AB hybrid genotypes., Key Results: Recurrent homologous exchanges (HEs), i.e. chromatin exchanges between A and B subgenomes, were unravelled with at least nine founding events (HE patterns) at the origin of ABB bananas prior to clonal diversification. Two independent founding events were found for Pisang Awak genotypes. Two HE patterns, corresponding to genotypes Pelipita and Klue Teparod, show an over-representation of B genome contribution. Three HE patterns mainly found in Indian accessions shared some recombined regions and two additional patterns did not correspond to any known subgroups., Conclusions: The discovery of the nine founding events allowed an investigation of the possible routes that led to the creation of the different subgroups, which resulted in new hypotheses. Based on our observations, we suggest different routes that gave rise to the current diversity in the ABB cultivars, routes involving primary AB hybrids, routes leading to shared HEs and routes leading to a B excess ratio. Genetic fluxes took place between M. acuminata and M. balbisiana, particularly in India, where these unbalanced AB hybrids and ABB allotriploids originated, and where cultivated M. balbisiana are abundant. The result of this study clarifies the classification of ABB cultivars, possibly leading to the revision of the classification of this subgroup., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company.)

Background: Bananas (Musa spp.) are an important crop worldwide. Most modern cultivars resulted from a complex polyploidization history that comprised three whole genome duplications (WGDs) shaping the haploid Musa genome, followed by inter- and intra-specific crosses between Musa acuminata and M. balbisiana (A and B genome, respectively). Unresolved hybridizations finally led to banana diversification into several autotriploid (AAA) and allotriploid cultivars (AAB and ABB). Using transcriptomic data, we investigated the impact of the genome structure on gene expression patterns in roots of 12 different triploid genotypes covering AAA, AAB and ABB subgenome constitutions., Results: We demonstrate that (i) there are different genome structures, (ii) expression patterns go beyond the predicted genomic groups, and (iii) the proportion of the B genome influences the gene expression. The presence of the B genome is associated with a higher expression of genes involved in flavonoid biosynthesis, fatty acid metabolism, amino sugar and nucleotide sugar metabolism and oxidative phosphorylation. There are cultivar-specific chromosome regions with biased B:A gene expression ratios that demonstrate homoeologous exchanges (HE) between A and B sub-genomes. In two cultivars, aneuploidy was detected. We identified 3674 genes with a different expression level between allotriploid and autotriploid with ~ 57% having recently duplicated copies (paralogous). We propose a Paralog Inclusive Expression (PIE) analysis that appears to be suitable for genomes still in a downsizing and fractionation process following whole genome duplications. Our approach allows highlighting the genes with a maximum likelihood to affect the plant phenotype., Conclusions: This study on banana is a good case to investigate the effects of alloploidy in crops. We conclude that allopolyploidy triggered changes in the genome structure of a crop and it clearly influences the gene.

Edible bananas result from interspecific hybridization between Musa acuminata and Musa balbisiana, as well as among subspecies in M. acuminata. Four particular M. acuminata subspecies have been proposed as the main contributors of edible bananas, all of which radiated in a short period of time in southeastern Asia. Clarifying the evolution of these lineages at a whole-genome scale is therefore an important step toward understanding the domestication and diversification of this crop. This study reports the de novo genome assembly and gene annotation of a representative genotype from three different subspecies of M. acuminata. These data are combined with the previously published genome of the fourth subspecies to investigate phylogenetic relationships. Analyses of shared and unique gene families reveal that the four subspecies are quite homogenous, with a core genome representing at least 50% of all genes and very few M. acuminata species-specific gene families. Multiple alignments indicate high sequence identity between homologous single copy-genes, supporting the close relationships of these lineages. Interestingly, phylogenomic analyses demonstrate high levels of gene tree discordance, due to both incomplete lineage sorting and introgression. This pattern suggests rapid radiation within Musa acuminata subspecies that occurred after the divergence with M. balbisiana. Introgression between M. a. ssp. malaccensis and M. a. ssp. burmannica was detected across the genome, though multiple approaches to resolve the subspecies tree converged on the same topology. To support evolutionary and functional analyses, we introduce the PanMusa database, which enables researchers to exploration of individual gene families and trees.

The fate of doubled genes, from allopolyploid or autopolyploid origin, is controlled at multiple levels, resulting in the modern day cultivars. We studied the root growth of 3 different triploid banana cultivars under control and osmotic stress conditions. The root growth of the allopolyploid ABB cultivar was 42% higher under control and 61% higher under osmotic stress. By integrating transcriptomics and proteomics, we studied the gene expression of all 3 cultivars, resulting in 2,749 identified root proteins. 383 gene loci displayed genotype specific differential expression whereof 252 showed at least one Single Amino Acid Polymorphism (SAAP). In the ABB cultivar, allele expressions supposedly follow a 1/3 and 2/3 pattern for respectively the A and the B allele. Using transcriptome read alignment to assess the homeoallelic contribution we found that 63% of the allele specific genes deviated from this expectation. 32 gene loci even did not express the A allele. The identified ABB allele- specific proteins correlate well with the observed growth phenotype as they are enriched in energy related functions such as ATP metabolic processes, nicotinamide nucleotide metabolic processes, and glycolysis.

Banana (Musa sp.) is a vegetatively propagated, low fertility, potentially hybrid and polyploid crop. These qualities make the breeding and targeted genetic improvement of this crop a difficult and long process. The Genome-Wide Association Study (GWAS) approach is becoming widely used in crop plants and has proven efficient to detecting candidate genes for traits of interest, especially in cereals. GWAS has not been applied yet to a vegetatively propagated crop. However, successful GWAS in banana would considerably help unravel the genomic basis of traits of interest and therefore speed up this crop improvement. We present here a dedicated panel of 105 accessions of banana, freely available upon request, and their corresponding GBS data. A set of 5,544 highly reliable markers revealed high levels of admixture in most accessions, except for a subset of 33 individuals from Papua. A GWAS on the seedless phenotype was then successfully applied to the panel. By applying the Mixed Linear Model corrected for both kinship and structure as implemented in TASSEL, we detected 13 candidate genomic regions in which we found a number of genes potentially linked with the seedless phenotype (i.e. parthenocarpy combined with female sterility). An additional GWAS performed on the unstructured Papuan subset composed of 33 accessions confirmed six of these regions as candidate. Out of both sets of analyses, one strong candidate gene for female sterility, a putative orthologous gene to Histidine Kinase CKI1, was identified. The results presented here confirmed the feasibility and potential of GWAS when applied to small sets of banana accessions, at least for traits underpinned by a few loci. As phenotyping in banana is extremely space and time-consuming, this latest finding is of particular importance in the context of banana improvement.