Unravelling the complex story of intergenomic recombination in ABB allotriploid bananas

Abstract

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.

Safeguarding and using global banana diversity: a holistic approach

“…In wild bananas, studies of whole genomes allowed to detect phenomena such as whole genome duplications and translocations (D'Hont et al 2012;Martin et al 2016;Dupouy et al 2019) as well as evidence of rapid radiation of these M. acuminata subspecies (Rouard et al 2019). In cultivated bananas, the chromosome structures of allopolyploid hybrids were explored allowing to clarify the path that led to their creation (Baurens et al 2019;Cenci et al 2019Cenci et al , 2020. Current efforts focus on resolving the mosaic structure of cultivated banana by looking at the ancestral contribution of the different M. acuminata subspecies along chromosomes (Martin et al 2020).…”

“…NGS data demonstrated their power to refine the current taxonomic classification that was established using morphological descriptors. It notably facilitates the categorization of material to the correct groups or subgroups using molecular karyotypes (Baurens et al 2019;Cenci et al 2020). Although diploid AAs and auto-triploids remain more challenging as they involve genomic sections inherited from the different M. acuminata genepools, this was recently initiated with a small number of accessions from the ITC and other banana collections (Martin et al 2020).…”

“…It offers a scalable solution to search for genotype patterns, functional annotations, or more complex filtering as well as data export in multiple format types. Datasets from several published studies have also been made available (Sardos et al 2016a, b;Cenci et al 2020).…”

A digital catalog of high‐density markers for banana germplasm collections

“…In parallel, high-throughput genotyping methods (i.e., genotypingby-sequencing (GBS) (Elshire et al, 2011) and restriction-site associated DNA markers (RADSeq) (Davey et al, 2010)) have been used to investigate single nucleotide polymorphisms (SNPs) on various panels of accessions available at the ITC genebank (Cenci et al, 2020;Sardos et al, 2016). In addition, other SNP datasets have been generated from gene expression and proteomics experiments for subsets related to drought tolerance (Cenci et al, 2019;van Wesemael et al, 2019).…”

“…Such tissue is the most convenient way to obtain DNA of an acceptable quality and quantity for high-throughput restriction enzyme-associated DNA sequencing methods, as for other omics techniques(Carpentier et al, 2007). Another advantage is that once in stock, the tissues are readily available for distribution, whereas in vitro material takes longer to obtain (i.e., an average of 2 months for proliferating tissues and 4 months for in vitro rooted plantlets).The generated sequence-short reads from Illumina sequencing machines-was processed through bioinformatics workflows composed of open source software that includes quality checks, read mapping on reference genomes, SNP calling and variant effect in genic regions as described inSardos et al, 2016;Cenci et al, 2020 andEyland et al, 2020. The outputs of the workflow are enormous text files in the variant call format (VCF).…”