Interspecific introgression patterns reveal the origins of worldwide cultivated bananas in New Guinea.

Hybridizations between Musa species and subspecies, enabled by their transport via human migration, were proposed to have played an important role in banana domestication. We exploited sequencing data of 226 Musaceae accessions, including wild and cultivated accessions, to characterize the inter(sub)specific hybridization pattern that gave rise to cultivated bananas. We identified 11 genetic pools that contributed to cultivars, including two contributors of unknown origin. Informative alleles for each of these genetic pools were pinpointed and used to obtain genome ancestry mosaics of accessions. Diploid and triploid cultivars had genome mosaics involving three up to possibly seven contributors. The simplest mosaics were found for some diploid cultivars from New Guinea, combining three contributors, i.e., banksii and zebrina representing Musa acuminata subspecies and, more unexpectedly, the New Guinean species Musa schizocarpa. Breakpoints of M. schizocarpa introgressions were found to be conserved between New Guinea cultivars and the other analyzed diploid and triploid cultivars. This suggests that plants bearing these M. schizocarpa introgressions were transported from New Guinea and gave rise to currently cultivated bananas. Many cultivars showed contrasted mosaics with predominant ancestry from their geographical origin across Southeast Asia to New Guinea. This revealed that further diversification occurred in different Southeast Asian regions through hybridization with other Musa (sub)species, including two unknown ancestors that we propose to be M. acuminata ssp. halabanensis and a yet to be characterized M. acuminata subspecies. These results highlighted a dynamic crop formation process that was initiated in New Guinea, with subsequent diversification throughout Southeast Asia.

Hybridization, missing wild ancestors and the domestication of cultivated diploid bananas.

Hybridization and introgressions are important evolutionary forces in plants. They contribute to the domestication of many species, including understudied clonal crops. Here, we examine their role in the domestication of a clonal crop of outmost importance, banana (Musa ssp.). We used genome-wide SNPs generated for 154 diploid banana cultivars and 68 samples of the wild M. acuminata to estimate and geo-localize the contribution of the different subspecies of M. acuminata to cultivated banana. We further investigated the wild to domesticate transition in New Guinea, an important domestication center. We found high levels of admixture in many cultivars and confirmed the existence of unknown wild ancestors with unequal contributions to cultivated diploid. In New Guinea, cultivated accessions exhibited higher diversity than their direct wild ancestor, the latter recovering from a bottleneck. Introgressions, balancing selection and positive selection were identified as important mechanisms for banana domestication. Our results shed new lights on the radiation of M. acuminata subspecies and on how they shaped banana domestication. They point candidate regions of origin for two unknown ancestors and suggest another contributor in New Guinea. This work feed research on the evolution of clonal crops and has direct implications for conservation, collection, and breeding.

State of ex situ conservation of landrace groups of 25 major crops.

Crop landraces have unique local agroecological and societal functions and offer important genetic resources for plant breeding. Recognition of the value of landrace diversity and concern about its erosion on farms have led to sustained efforts to establish ex situ collections worldwide. The degree to which these efforts have succeeded in conserving landraces has not been comprehensively assessed. Here we modelled the potential distributions of eco-geographically distinguishable groups of landraces of 25 cereal, pulse and starchy root/tuber/fruit crops within their geographic regions of diversity. We then analysed the extent to which these landrace groups are represented in genebank collections, using geographic and ecological coverage metrics as a proxy for genetic diversity. We find that ex situ conservation of landrace groups is currently moderately comprehensive on average, with substantial variation among crops; a mean of 63% ± 12.6% of distributions is currently represented in genebanks. Breadfruit, bananas and plantains, lentils, common beans, chickpeas, barley and bread wheat landrace groups are among the most fully represented, whereas the largest conservation gaps persist for pearl millet, yams, finger millet, groundnut, potatoes and peas. Geographic regions prioritized for further collection of landrace groups for ex situ conservation include South Asia, the Mediterranean and West Asia, Mesoamerica, sub-Saharan Africa, the Andean mountains of South America and Central to East Asia. With further progress to fill these gaps, a high degree of representation of landrace group diversity in genebanks is feasible globally, thus fulfilling international targets for their ex situ conservation.

Unravelling the complex story of intergenomic recombination in ABB allotriploid bananas.

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.

Effect of paleopolyploidy and allopolyploidy on gene expression in banana.

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.

Metabolite profiling characterises chemotypes of Musa diploids and triploids at juvenile and pre-flowering growth stages.

Bananas (Musa spp.) are consumed worldwide as dessert and cooking types. Edible banana varieties are for the most part seedless and sterile and therefore vegetatively propagated. This confers difficulties for breeding approaches against pressing biotic and abiotic threats and for the nutritional enhancement of banana pulp. A panel of banana accessions, representative of the diversity of wild and cultivated bananas, was analysed to assess the range of chemotypes available globally. The focus of this assessment was banana leaves at two growth stages (juvenile and pre-flowering), to see when during the plant growth metabolic differences can be established. The metabolic data corresponded to genomic trends reported in previous studies and demonstrated a link between metabolites/pathways and the genomes of M. acuminata and M. balbisiana. Furthermore, the vigour and resistance traits of M. balbisiana was connected to the phenolic composition and showed differences with the number of B genes in the hybrid accessions. Differences in the juvenile and pre-flowering data led to low correlation between the growth stages for prediction purposes.

Three New Genome Assemblies Support a Rapid Radiation in Musa acuminata (Wild Banana).

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.

In situ conservation-harnessing natural and human-derived evolutionary forces to ensure future crop adaptation.

Ensuring the availability of the broadest possible germplasm base for agriculture in the face of increasingly uncertain and variable patterns of biotic and abiotic change is fundamental for the world's future food supply. While ex situ conservation plays a major role in the conservation and availability of crop germplasm, it may be insufficient to ensure this. In situ conservation aims to maintain target species and the collective genotypes they represent under evolution. A major rationale for this view is based on the likelihood that continued exposure to changing selective forces will generate and favor new genetic variation and an increased likelihood that rare alleles that may be of value to future agriculture are maintained. However, the evidence that underpins this key rationale remains fragmented and has not been examined systematically, thereby decreasing the perceived value and support for in situ conservation for agriculture and food systems and limiting the conservation options available. This study reviews evidence regarding the likelihood and rate of evolutionary change in both biotic and abiotic traits for crops and their wild relatives, placing these processes in a realistic context in which smallholder farming operates and crop wild relatives continue to exist. It identifies areas of research that would contribute to a deeper understanding of these processes as the basis for making them more useful for future crop adaptation.

Evolution of the Banana Genome (Musa acuminata) Is Impacted by Large Chromosomal Translocations.

Most banana cultivars are triploid seedless parthenocarpic clones derived from hybridization between Musa acuminata subspecies and sometimes M. balbisiana. M. acuminata subspecies were suggested to differ by a few large chromosomal rearrangements based on chromosome pairing configurations in intersubspecies hybrids. 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 and 10 Mb segments from chromosomes 01 and 04, respectively, and showed that it generated high segregation distortion, reduced recombination and linkage between chromosomes 01 and 04 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 present only in wild malaccensis ssp. accessions, thus suggesting that this rearrangement occurred in M. acuminata ssp. malaccensis. We propose a mechanism for the spread of this rearrangement in Musa diversity and suggest that this rearrangement could have played a role in the emergence of triploid cultivars.

A Genome-Wide Association Study on the Seedless Phenotype in Banana (Musa spp.) Reveals the Potential of a Selected Panel to Detect Candidate Genes in a Vegetatively Propagated Crop.

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.

Towards a more holistic research approach to plant conservation: the case of rare plants on oceanic islands.

Research dedicated to rare endemic plants is usually focused on one given aspect. However, holistic studies, addressing several key issues, might be more useful, supporting management programmes while unravelling basic knowledge about ecological and population-level processes. A more comprehensive approach to research is proposed, encompassing: phylogenetics/systematics, pollination biology and seed dispersal, propagation, population genetics, species distribution models (SDMs), threats and monitoring. We present a holistic study dedicated to Veronica dabneyi Hochst. ex Seub., an endangered chamaephyte endemic to the Azores. Veronica dabneyi was mainly found associated with other endemic taxa; however, invasive plants were also present and together with introduced cattle, goats and rabbits are a major threat. Most populations grow at somewhat rocky and steep locations that appeared to work as refuges. Seed set in the wild was generally high and recruitment of young plants from seed seemed to be frequent. In the laboratory, it was possible to germinate and fully develop V. dabneyi seedlings, which were planted at their site of origin. No dormancy was detected and time for 50 % germination was affected by incubation temperature. Eight new microsatellite markers were applied to 72 individuals from 7 sites. A considerable degree of admixture was found between samples from the two islands Flores and Corvo, with 98 % of the genetic variability allocated within populations. Levels of heterozygosity were high and no evidence of inbreeding was found. Species distribution models based on climatic and topographic variables allowed the estimation of the potential distribution of V. dabneyi on Flores and Corvo using ecological niche factor analysis and Maxent. The inclusion of land-use variables only slightly increased the information explained by the models. Projection of the expected habitat in Faial largely coincided with the only historic record of V. dabneyi on that island. This research could be the basis for the design of a recovery plan, showing the pertinence of more holistic research approaches to plant conservation.