Episodes of gene flow and selection during the evolutionary history of domesticated barley.

Barley Exome sequences Fertile Crescent Gene flow Hordeum vulgare Origins of agriculture Selection Selective sweep

Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
01 Apr 2021
Historique:
received: 06 07 2020
accepted: 05 03 2021
entrez: 2 4 2021
pubmed: 3 4 2021
medline: 15 5 2021
Statut: epublish

Résumé

Barley is one of the founder crops of Neolithic agriculture and is among the most-grown cereals today. The only trait that universally differentiates the cultivated and wild subspecies is 'non-brittleness' of the rachis (the stem of the inflorescence), which facilitates harvesting of the crop. Other phenotypic differences appear to result from facultative or regional selective pressures. The population structure resulting from these regional events has been interpreted as evidence for multiple domestications or a mosaic ancestry involving genetic interaction between multiple wild or proto-domesticated lineages. However, each of the three mutations that confer non-brittleness originated in the western Fertile Crescent, arguing against multiregional origins for the crop. We examined exome data for 310 wild, cultivated and hybrid/feral barley accessions and showed that cultivated barley is structured into six genetically-defined groups that display admixture, resulting at least in part from two or more significant passages of gene flow with distinct wild populations. The six groups are descended from a single founding population that emerged in the western Fertile Crescent. Only a few loci were universally targeted by selection, the identity of these suggesting that changes in seedling emergence and pathogen resistance could represent crucial domestication switches. Subsequent selection operated on a regional basis and strongly contributed to differentiation of the genetic groups. Identification of genetically-defined groups provides clarity to our understanding of the population history of cultivated barley. Inference of population splits and mixtures together with analysis of selection sweeps indicate descent from a single founding population, which emerged in the western Fertile Crescent. This founding population underwent relatively little genetic selection, those changes that did occur affecting traits involved in seedling emergence and pathogen resistance, indicating that these phenotypes should be considered as 'domestication traits'. During its expansion out of the western Fertile Crescent, the crop underwent regional episodes of gene flow and selection, giving rise to a modern genetic signature that has been interpreted as evidence for multiple domestications, but which we show can be rationalized with a single origin.

Sections du résumé

BACKGROUND BACKGROUND
Barley is one of the founder crops of Neolithic agriculture and is among the most-grown cereals today. The only trait that universally differentiates the cultivated and wild subspecies is 'non-brittleness' of the rachis (the stem of the inflorescence), which facilitates harvesting of the crop. Other phenotypic differences appear to result from facultative or regional selective pressures. The population structure resulting from these regional events has been interpreted as evidence for multiple domestications or a mosaic ancestry involving genetic interaction between multiple wild or proto-domesticated lineages. However, each of the three mutations that confer non-brittleness originated in the western Fertile Crescent, arguing against multiregional origins for the crop.
RESULTS RESULTS
We examined exome data for 310 wild, cultivated and hybrid/feral barley accessions and showed that cultivated barley is structured into six genetically-defined groups that display admixture, resulting at least in part from two or more significant passages of gene flow with distinct wild populations. The six groups are descended from a single founding population that emerged in the western Fertile Crescent. Only a few loci were universally targeted by selection, the identity of these suggesting that changes in seedling emergence and pathogen resistance could represent crucial domestication switches. Subsequent selection operated on a regional basis and strongly contributed to differentiation of the genetic groups.
CONCLUSIONS CONCLUSIONS
Identification of genetically-defined groups provides clarity to our understanding of the population history of cultivated barley. Inference of population splits and mixtures together with analysis of selection sweeps indicate descent from a single founding population, which emerged in the western Fertile Crescent. This founding population underwent relatively little genetic selection, those changes that did occur affecting traits involved in seedling emergence and pathogen resistance, indicating that these phenotypes should be considered as 'domestication traits'. During its expansion out of the western Fertile Crescent, the crop underwent regional episodes of gene flow and selection, giving rise to a modern genetic signature that has been interpreted as evidence for multiple domestications, but which we show can be rationalized with a single origin.

Identifiants

pubmed: 33794767
doi: 10.1186/s12864-021-07511-7
pii: 10.1186/s12864-021-07511-7
pmc: PMC8015183
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

227

Subventions

Organisme : European Research Council
ID : 339941
Pays : International

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Auteurs

Peter Civáň (P)

Department of Earth and Environmental Sciences, Manchester Institute of Biotechnology, University of Manchester, Manchester, M1 7DN, UK.
INRA-Université Clermont-Auvergne, UMR 1095 GDEC, 5 Chemin de Beaulieu, 63000, Clermont-Ferrand, France.

Konstantina Drosou (K)

Department of Earth and Environmental Sciences, Manchester Institute of Biotechnology, University of Manchester, Manchester, M1 7DN, UK.
KNH Centre for Biomedical Egyptology, Faculty of Biology, Medicine and Health, University of Manchester, 99 Oxford Road, Manchester, M13 9PG, UK.

David Armisen-Gimenez (D)

INRA-Université Clermont-Auvergne, UMR 1095 GDEC, 5 Chemin de Beaulieu, 63000, Clermont-Ferrand, France.
Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, 69364, Lyon, France.

Wandrille Duchemin (W)

INRA-Université Clermont-Auvergne, UMR 1095 GDEC, 5 Chemin de Beaulieu, 63000, Clermont-Ferrand, France.
Center for Scientific Computing (sciCORE), University of Basel, Basel, Switzerland.

Jérôme Salse (J)

INRA-Université Clermont-Auvergne, UMR 1095 GDEC, 5 Chemin de Beaulieu, 63000, Clermont-Ferrand, France.

Terence A Brown (TA)

Department of Earth and Environmental Sciences, Manchester Institute of Biotechnology, University of Manchester, Manchester, M1 7DN, UK. terry.brown@manchester.ac.uk.

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