Shared pedigree relationships and transmission of unreduced gametes in cultivated banana.

Musa acuminata Musa balbisiana Musa schizocarpa Mchare banana cultivars parentage polyploid unreduced gamete whole genome approach

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
25 08 2023
Historique:
received: 13 03 2023
accepted: 02 06 2023
medline: 28 8 2023
pubmed: 2 6 2023
entrez: 2 6 2023
Statut: ppublish

Résumé

Cultivated bananas resulted from inter(sub)specific hybridizations involving Musa species and subspecies (M. acuminata subspecies, M. schizocarpa, M. balbisiana) and the subsequent selection, centuries ago, of hybrids with parthenocarpic, seedless fruits. Cultivars have low fertility and are vegetatively propagated, forming groups of somaclones. Relatively few of them, mainly triploids, are grown on a large scale and characterization of their parental relationships may be useful for breeding strategies. Here we investigate parental relationships and gamete-type contributions among diploid and polyploid banana cultivars. We used SNP genotyping data from whole-genome sequencing of 178 banana individuals, including 111 cultivars, 55 wild bananas and 12 synthetic F1 hybrids. We analysed the proportion of SNP sites in accordance with direct parentage with a global statistic and along chromosomes for selected individuals. We characterized parentage relationships for 7 diploid cultivars, 11 triploid cultivars and 1 tetraploid cultivar. Results showed that both diploid and triploid cultivars could have contributed gametes to other banana cultivars. Diploids may have contributed 1x or 2x gametes and triploids 1x to 3x gametes. The Mchare diploid cultivar group, nowadays only found in East Africa, was found as parent of two diploid and eight triploid cultivars. In five of its identified triploid offspring, corresponding to main export or locally popular dessert bananas, Mchare contributed a 2x gamete with full genome restitution without recombination. Analyses of remaining haplotypes in these Mchare offspring suggested ancestral pedigree relationships between different interspecific banana cultivars. The current cultivated banana resulted from different pathways of formation, with implication of recombined or un-recombined unreduced gametes produced by diploid or triploid cultivars. Identification of dessert banana's parents and the types of gametes they contributed should support the design of breeding strategies.

Sections du résumé

BACKGROUND AND AIMS
Cultivated bananas resulted from inter(sub)specific hybridizations involving Musa species and subspecies (M. acuminata subspecies, M. schizocarpa, M. balbisiana) and the subsequent selection, centuries ago, of hybrids with parthenocarpic, seedless fruits. Cultivars have low fertility and are vegetatively propagated, forming groups of somaclones. Relatively few of them, mainly triploids, are grown on a large scale and characterization of their parental relationships may be useful for breeding strategies. Here we investigate parental relationships and gamete-type contributions among diploid and polyploid banana cultivars.
METHODS
We used SNP genotyping data from whole-genome sequencing of 178 banana individuals, including 111 cultivars, 55 wild bananas and 12 synthetic F1 hybrids. We analysed the proportion of SNP sites in accordance with direct parentage with a global statistic and along chromosomes for selected individuals.
KEY RESULTS
We characterized parentage relationships for 7 diploid cultivars, 11 triploid cultivars and 1 tetraploid cultivar. Results showed that both diploid and triploid cultivars could have contributed gametes to other banana cultivars. Diploids may have contributed 1x or 2x gametes and triploids 1x to 3x gametes. The Mchare diploid cultivar group, nowadays only found in East Africa, was found as parent of two diploid and eight triploid cultivars. In five of its identified triploid offspring, corresponding to main export or locally popular dessert bananas, Mchare contributed a 2x gamete with full genome restitution without recombination. Analyses of remaining haplotypes in these Mchare offspring suggested ancestral pedigree relationships between different interspecific banana cultivars.
CONCLUSIONS
The current cultivated banana resulted from different pathways of formation, with implication of recombined or un-recombined unreduced gametes produced by diploid or triploid cultivars. Identification of dessert banana's parents and the types of gametes they contributed should support the design of breeding strategies.

Identifiants

pubmed: 37267450
pii: 7189797
doi: 10.1093/aob/mcad065
pmc: PMC10457027
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1149-1161

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of the Annals of Botany Company.

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Auteurs

Guillaume Martin (G)

CIRAD, UMR AGAP Institut, Montpellier F-34398, France.
UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.

Franc-Christophe Baurens (FC)

CIRAD, UMR AGAP Institut, Montpellier F-34398, France.
UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.

Karine Labadie (K)

Genoscope, Institut François Jacob, CEA, Université Paris-Saclay, Evry, France.

Catherine Hervouet (C)

CIRAD, UMR AGAP Institut, Montpellier F-34398, France.
UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.

Frédéric Salmon (F)

UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.
CIRAD, UMR AGAP Institut, F-97130 Capesterre-Belle-Eau, Guadeloupe, France.

Franck Marius (F)

UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.
CIRAD, UMR AGAP Institut, F-97130 Capesterre-Belle-Eau, Guadeloupe, FranceFrance.

Nilda Paulo-de-la-Reberdiere (N)

UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.
CIRAD, UMR AGAP Institut, CRB-PT, F-97170 Roujol Petit-Bourg, Guadeloupe, FranceFrance.

Ines Van den Houwe (I)

Bioversity International, Willem De Croylaan 42, B-3001, Leuven, Belgium.

Jean-Marc Aury (JM)

Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Université Evry, Université Paris-Saclay, Evry, France.

Angélique D'Hont (A)

CIRAD, UMR AGAP Institut, Montpellier F-34398, France.
UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.

Nabila Yahiaoui (N)

CIRAD, UMR AGAP Institut, Montpellier F-34398, France.
UMR AGAP Institut, Université Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.

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