Chromosome reciprocal translocations have accompanied subspecies evolution in bananas

Abstract

Chromosome rearrangements and the way that they impact genetic differentiation and speciation have long raised questions from evolutionary biologists. They are also a major concern for breeders because of their bearing on chromosome recombination. Banana is a major crop that derives from inter(sub)specific hybridizations between various once geographically isolated Musa species and subspecies. We sequenced 155 accessions, including banana cultivars and representatives of Musa diversity, and genotyped-by-sequencing 1059 individuals from 11 progenies. We precisely characterized six large reciprocal translocations and showed that they emerged in different (sub)species of Musa acuminata, the main contributor to currently cultivated bananas. Most diploid and triploid cultivars analyzed were structurally heterozygous for 1 to 4 M. acuminata translocations, highlighting their complex origin. We showed that all translocations induced a recombination reduction of variable intensity and extent depending on the translocations, involving only the breakpoint regions, a chromosome arm, or an entire chromosome. The translocated chromosomes were found preferentially transmitted in many cases. We explore and discuss the possible mechanisms involved in this preferential transmission and its impact on translocation colonization.

Reassessing Banana Phylogeny and Organelle Inheritance Modes Using Genome Skimming Data

“…However, the complex breeding history of bananas may further complicate efforts to identify accessions and trace their origins. For example, extensive studies showed frequent occurrences of chromosomal recombination (e.g., reciprocal translocation or chromosomal inversion) in bananas (Baurens et al, 2018 ; Martin et al, 2020a , b ; Cenci et al, 2021 ). These genome structural diversities have been applied to study the origins of banana cultivars and Musa evolution (Martin et al, 2020b ).…”

Male meiosis and pollen morphology in diploid Indonesian wild bananas and cultivars

“…In the recent studies that used the sequencing database of M. acuminata ssp. malaccensis reverence chromosomes [26] and chromosome painting [43], a translocation event between chromosomes 1 and 4 was present in ssp. malaccensis.…”

Wild to domesticates: genomes of edible diploid bananas hold traces of several undefined genepools

“…The range of M. acuminata spans from India at the west to north Australia at the east. It is divided into several subspecies that are geographically segregated and show unique features, morphologically (Simmonds 1956), genetically (Hippolyte et al 2012) and at the genome level (Martin, Baurens, et al 2020). The AA bananas were first hypothesized originating in Malaysia (Simmonds and Shepherd 1955) but molecular studies comparing edible AAs with different M. acuminata subspecies later pointed at the Philippines -New Guinea (NG) region as the centre of origin for the crop (Carreel et al 2002).…”