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.

East African diploid and triploid bananas: a genetic complex transported from South-East Asia.

Background and Aims: Besides bananas belonging to the AAA triploid Mutika subgroup, which predominates in the Great Lakes countries, other AAA triploids as well as edible AA diploids, locally of considerable cultural weight, are cultivated in East Africa and in the nearby Indian Ocean islands as far as Madagascar. All these varieties call for the genetic identification and characterization of their interrelations on account of their regional socio-economic significance and their potential for banana breeding strategies. Methods: An extensive sampling of all traditional bananas in East Africa and near Indian Ocean islands was genotyped with simple sequence repeat (SSR) markers, with particular emphasis on the diploid forms and on the bananas of the Indian Ocean islands, which remain poorly characterized. Key Results: All the edible AA varieties studied here are genetically homogeneous, constituting a unique subgroup, here called 'Mchare', despite high phenotypic variation and adaptions to highly diverse ecological zones. At triploid level, and besides the well-known AAA Mutika subgroup, at least two other genetically related AAA subgroups specific to this region are identified. Neither of these East African AAA genotypes can be derived directly from the local AA Mchare diploids. However, it is demonstrated that the East African diploids and triploids together belong to the same genetic complex. The geographical distribution of their wild acuminata relatives allowed identification of the original area of this complex in a restricted part of island South-East Asia. The inferred origin leads to consideration of the history of banana introduction in Africa. Linked to biological features, documentation on the embedding of bananas in founding legends and myths and convincing linguistic elements were informative regarding the period and the peoples who introduced these Asian plants into Africa. The results point to the role of Austronesian-speaking peoples who colonized the Indian Ocean islands, particularly Madagascar, and reached the East African coasts. Conclusions: Understanding of the relations between the components of this complex and identifying their Asian wild relatives and related cultivars will be a valuable asset in breeding programmes and will boost the genetic improvement of East African bananas, but also of other globally important subgroups, in particular the AAA Cavendish.

Traditional Banana Diversity in Oceania: An Endangered Heritage.

This study aims to understand the genetic diversity of traditional Oceanian starchy bananas in order to propose an efficient conservation strategy for these endangered varieties. SSR and DArT molecular markers are used to characterize a large sample of Pacific accessions, from New Guinea to Tahiti and Hawaii. All Pacific starchy bananas are shown of New Guinea origin, by interspecific hybridization between Musa acuminata (AA genome), more precisely its local subspecies M. acuminata ssp. banksii, and M. balbisiana (BB genome) generating triploid AAB Pacific starchy bananas. These AAB genotypes do not form a subgroup sensu stricto and genetic markers differentiate two subgroups across the three morphotypes usually identified: Iholena versus Popoulu and Maoli. The Popoulu/Maoli accessions, even if morphologically diverse throughout the Pacific, cluster in the same genetic subgroup. However, the subgroup is not strictly monophyletic and several close, but different genotypes are linked to the dominant genotype. One of the related genotypes is specific to New Caledonia (NC), with morphotypes close to Maoli, but with some primitive characters. It is concluded that the diffusion of Pacific starchy AAB bananas results from a series of introductions of triploids originating in New Guinea area from several sexual recombination events implying different genotypes of M. acuminata ssp. banksii. This scheme of multiple waves from the New Guinea zone is consistent with the archaeological data for peopling of the Pacific. The present geographic distribution suggests that a greater diversity must have existed in the past. Its erosion finds parallels with the erosion of cultural traditions, inexorably declining in most of the Polynesian or Melanesian Islands. Symmetrically, diversity hot spots appear linked to the local persistence of traditions: Maoli in New Caledonian Kanak traditions or Iholena in a few Polynesian islands. These results will contribute to optimizing the conservation strategy for the ex-situ Pacific Banana Collection supported collectively by the Pacific countries.

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.

Multidisciplinary perspectives on banana (Musa spp.) domestication.

Original multidisciplinary research hereby clarifies the complex geodomestication pathways that generated the vast range of banana cultivars (cvs). Genetic analyses identify the wild ancestors of modern-day cvs and elucidate several key stages of domestication for different cv groups. Archaeology and linguistics shed light on the historical roles of people in the movement and cultivation of bananas from New Guinea to West Africa during the Holocene. The historical reconstruction of domestication processes is essential for breeding programs seeking to diversify and improve banana cvs for the future.

A saturated SSR/DArT linkage map of Musa acuminata addressing genome rearrangements among bananas.

BACKGROUND: The genus Musa is a large species complex which includes cultivars at diploid and triploid levels. These sterile and vegetatively propagated cultivars are based on the A genome from Musa acuminata, exclusively for sweet bananas such as Cavendish, or associated with the B genome (Musa balbisiana) in cooking bananas such as Plantain varieties. In M. acuminata cultivars, structural heterozygosity is thought to be one of the main causes of sterility, which is essential for obtaining seedless fruits but hampers breeding. Only partial genetic maps are presently available due to chromosomal rearrangements within the parents of the mapping populations. This causes large segregation distortions inducing pseudo-linkages and difficulties in ordering markers in the linkage groups. The present study aims at producing a saturated linkage map of M. acuminata, taking into account hypotheses on the structural heterozygosity of the parents. RESULTS: An F1 progeny of 180 individuals was obtained from a cross between two genetically distant accessions of M. acuminata, 'Borneo' and 'Pisang Lilin' (P. Lilin). Based on the gametic recombination of each parent, two parental maps composed of SSR and DArT markers were established. A significant proportion of the markers (21.7%) deviated (p < 0.05) from the expected Mendelian ratios. These skewed markers were distributed in different linkage groups for each parent. To solve some complex ordering of the markers on linkage groups, we associated tools such as tree-like graphic representations, recombination frequency statistics and cytogenetical studies to identify structural rearrangements and build parsimonious linkage group order. An illustration of such an approach is given for the P. Lilin parent. CONCLUSIONS: We propose a synthetic map with 11 linkage groups containing 489 markers (167 SSRs and 322 DArTs) covering 1197 cM. This first saturated map is proposed as a "reference Musa map" for further analyses. We also propose two complete parental maps with interpretations of structural rearrangements localized on the linkage groups. The structural heterozygosity in P. Lilin is hypothesized to result from a duplication likely accompanied by an inversion on another chromosome. This paper also illustrates a methodological approach, transferable to other species, to investigate the mapping of structural rearrangements and determine their consequences on marker segregation.