Chromosome reciprocal translocations have accompanied subspecies evolution in bananas

Summary 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 int...

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Published in:The Plant journal : for cell and molecular biology 2020-12, Vol.104 (6), p.1698-1711
Main Authors: Martin, Guillaume, Baurens, Franc‐Christophe, Hervouet, Catherine, Salmon, Frédéric, Delos, Jean‐Marie, Labadie, Karine, Perdereau, Aude, Mournet, Pierre, Blois, Louis, Dupouy, Marion, Carreel, Françoise, Ricci, Sébastien, Lemainque, Arnaud, Yahiaoui, Nabila, D’Hont, Angélique
Format: Article
Language:English
Subjects:
Aneuploidy
Bananas
Chromosome rearrangements
chromosome segregation
Chromosome translocations
Chromosomes
Chromosomes, Plant - genetics
Colonization
Cultivars
Cultivation
Cytogenetic Analysis
Diploids
Evolution, Molecular
Fruit cultivation
genome evolution
In Situ Hybridization, Fluorescence
Life Sciences
Musa
Musa - genetics
Musa acuminata
Original
reciprocal translocation
Recombination
Speciation
Translocation
Translocation, Genetic - genetics
Vegetal Biology
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Summary:Summary 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. Significance Statement Chromosome rearrangements, the way that they emerged and their potential impact on speciation and breeding raise important questions. We report on the characterization of several large reciprocal translocations in banana, Musa acuminata, identify the genetic group in which they emerged, characterize their impacts on chromosome recombination, and explore possible mechanisms allowing their colonization.
ISSN:0960-7412
1365-313X
DOI:10.1111/tpj.15031