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

Abstract

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.

Sugarcane genome architecture decrypted with chromosome‐specific oligo probes

“…Clones with x = 10 and x = 9 are also much less frequent than those with x = 8. The chromosome rearrangements that led to x = 8 may have been associated with selective advantages and/or the rearranged chromosomes may be preferentially transmitted to the progeny and thus may have colonized the species (Martin et al ., 2017), or they may have favored further polyploidization resulting in an increased adaptability leading to expansion of the species to the south, east and west. Therefore, it is proposed that from the northern part of India S. spontaneum cytotypes with x = 8 emerged, polyploidized, and then extended largely to other areas.…”

“…Large chromosome structural variations such as the one observed between S. officinarum and S. spontaneum are known to generate unbalanced gametes. Aneuploidy or segmental aneuploidy can result from normal segregation of bivalents between chromosomes with distinct chromosome structures or from resolution of multivalent pairing and univalent (Martin et al ., 2017; Baurens et al ., 2019). This could explain the more variable chromosome copy numbers for basic chromosomes with a distinct structure between the two parental species.…”

Genome ancestry mosaics reveal multiple and cryptic contributors to cultivated banana

“…malaccensis accessions and thought to have originated in ssp. malaccensis was detected in Mchare accessions and in Cavendish (Martin et al , ). ‘Chicame’ and ‘Grande Naine’ bear large ‘malaccensis’ regions on both chromosomes 1 and 4; this is in line with the presence of these structural variations.…”

“…acuminata has been subdivided into several subspecies with a Northeast India to New Guinea distribution range, including: siamea , burmannica , burmannicoïdes , malaccensis , truncata , errans , microcarpa , zebrina and banksii (Simmonds, ; Perrier et al , ). Large chromosomal structural variations between the genomes of some of these species and subspecies have been reported (Shepherd, ; Martin et al , ; Baurens et al , ).…”

Chromosome painting in cultivated banana and their wild relatives (Musaspp.) reveals differences in chromosome structure

“…Based on morphology and geographical distribution, M. acuminata has been divided into nine subspecies (banksii, burmannica, burmannicoides, errans, malaccensis, microcarpa, siamea, truncata and zebrina) and three varieties (chinensis, sumatrana, tomentosa) (Perrier et al, 2011, Martin et al, 2017, WCSP, 2018. It has been estimated that least four subspecies of M. acuminata contributed to the origin of cultivated bananas (Perrier et al, 2011, Rouard et al, 2018.…”