Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars

Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucle...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 110; no. 20; pp. 8057 - 8062
Main Authors Cavanagh, Colin R., Chao, Shiaoman, Wang, Shichen, Huang, Bevan Emma, Stephen, Stuart, Kiani, Seifollah, Forrest, Kerrie, Saintenac, Cyrille, Brown-Guedira, Gina L., Akhunova, Alina, See, Deven, Bai, Guihua, Pumphrey, Michael, Tomar, Luxmi, Wong, Debbie, Kong, Stephan, Reynolds, Matthew, da Silva, Marta Lopez, Bockelman, Harold, Talbert, Luther, Anderson, James A., Dreisigacker, Susanne, Baenziger, Stephen, Carter, Arron, Korzun, Viktor, Morrell, Peter Laurent, Dubcovsky, Jorge, Morell, Matthew K., Sorrells, Mark E., Hayden, Matthew J., Akhunov, Eduard
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 14.05.2013
National Acad Sciences
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Online AccessGet full text
ISSN0027-8424
1091-6490
1091-6490
DOI10.1073/pnas.1217133110

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Abstract Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucleotide polymorphisms (SNP) in a worldwide sample of 2,994 accessions of hexaploid wheat including landraces and modern cultivars. Using a SNP-based diversity map we characterized the impact of crop improvement on genomic and geographic patterns of genetic diversity. We found evidence of a small population bottleneck and extensive use of ancestral variation often traceable to founders of cultivars from diverse geographic regions. Analyzing genetic differentiation among populations and the extent of haplotype sharing, we identified allelic variants subjected to selection during improvement Selective sweeps were found around genes involved in the regulation of flowering time and phenology. An introgression of a wild relative-derived gene conferring resistance to a fungal pathogen was detected by haplotype-based analysis. Comparing selective sweeps identified in different populations, we show that selection likely acts on distinct targets or multiple functionally equivalent alleles in different portions of the geographic range of wheat. The majority of the selected alleles were present at low frequency in local populations, suggesting either weak selection pressure or temporal variation in the targets of directional selection during breeding probably associated with changing agricultural practices or environmental conditions. The developed SNP chip and map of genetic variation provide a resource for advancing wheat breeding and supporting future population genomic and genome-wide association studies in wheat.
AbstractList Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucleotide polymorphisms (SNP) in a worldwide sample of 2,994 accessions of hexaploid wheat including landraces and modern cultivars. Using a SNP-based diversity map we characterized the impact of crop improvement on genomic and geographic patterns of genetic diversity. We found evidence of a small population bottleneck and extensive use of ancestral variation often traceable to founders of cultivars from diverse geographic regions. Analyzing genetic differentiation among populations and the extent of haplotype sharing, we identified allelic variants subjected to selection during improvement. Selective sweeps were found around genes involved in the regulation of flowering time and phenology. An introgression of a wild relative-derived gene conferring resistance to a fungal pathogen was detected by haplotype-based analysis. Comparing selective sweeps identified in different populations, we show that selection likely acts on distinct targets or multiple functionally equivalent alleles in different portions of the geographic range of wheat. The majority of the selected alleles were present at low frequency in local populations, suggesting either weak selection pressure or temporal variation in the targets of directional selection during breeding probably associated with changing agricultural practices or environmental conditions. The developed SNP chip and map of genetic variation provide a resource for advancing wheat breeding and supporting future population genomic and genome-wide association studies in wheat.
Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucleotide polymorphisms (SNP) in a worldwide sample of 2,994 accessions of hexaploid wheat including landraces and modern cultivars. Using a SNP-based diversity map we characterized the impact of crop improvement on genomic and geographic patterns of genetic diversity. We found evidence of a small population bottleneck and extensive use of ancestral variation often traceable to founders of cultivars from diverse geographic regions. Analyzing genetic differentiation among populations and the extent of haplotype sharing, we identified allelic variants subjected to selection during improvement. Selective sweeps were found around genes involved in the regulation of flowering time and phenology. An introgression of a wild relative-derived gene conferring resistance to a fungal pathogen was detected by haplotype-based analysis. Comparing selective sweeps identified in different populations, we show that selection likely acts on distinct targets or multiple functionally equivalent alleles in different portions of the geographic range of wheat. The majority of the selected alleles were present at low frequency in local populations, suggesting either weak selection pressure or temporal variation in the targets of directional selection during breeding probably associated with changing agricultural practices or environmental conditions. The developed SNP chip and map of genetic variation provide a resource for advancing wheat breeding and supporting future population genomic and genome-wide association studies in wheat.Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucleotide polymorphisms (SNP) in a worldwide sample of 2,994 accessions of hexaploid wheat including landraces and modern cultivars. Using a SNP-based diversity map we characterized the impact of crop improvement on genomic and geographic patterns of genetic diversity. We found evidence of a small population bottleneck and extensive use of ancestral variation often traceable to founders of cultivars from diverse geographic regions. Analyzing genetic differentiation among populations and the extent of haplotype sharing, we identified allelic variants subjected to selection during improvement. Selective sweeps were found around genes involved in the regulation of flowering time and phenology. An introgression of a wild relative-derived gene conferring resistance to a fungal pathogen was detected by haplotype-based analysis. Comparing selective sweeps identified in different populations, we show that selection likely acts on distinct targets or multiple functionally equivalent alleles in different portions of the geographic range of wheat. The majority of the selected alleles were present at low frequency in local populations, suggesting either weak selection pressure or temporal variation in the targets of directional selection during breeding probably associated with changing agricultural practices or environmental conditions. The developed SNP chip and map of genetic variation provide a resource for advancing wheat breeding and supporting future population genomic and genome-wide association studies in wheat.
Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucleotide polymorphisms (SNP) in a worldwide sample of 2,994 accessions of hexaploid wheat including landraces and modern cultivars. Using a SNP-based diversity map we characterized the impact of crop improvement on genomic and geographic patterns of genetic diversity. We found evidence of a small population bottleneck and extensive use of ancestral variation often traceable to founders of cultivars from diverse geographic regions. Analyzing genetic differentiation among populations and the extent of haplotype sharing, we identified allelic variants subjected to selection during improvement. Selective sweeps were found around genes involved in the regulation of flowering time and phenology. An introgression of a wild relative-derived gene conferring resistance to a fungal pathogen was detected by haplotype-based analysis. Comparing selective sweeps identified in different populations, we show that selection likely acts on distinct targets or multiple functionally equivalent alleles in different portions of the geographic range of wheat. The majority of the selected alleles were present at low frequency in local populations, suggesting either weak selection pressure or temporal variation in the targets of directional selection during breeding probably associated with changing agricultural practices or environmental conditions. The developed SNP chip and map of genetic variation provide a resource for advancing wheat breeding and supporting future population genomic and genome-wide association studies in wheat. [PUBLICATION ABSTRACT]
Author Wong, Debbie
Morell, Matthew K.
Brown-Guedira, Gina L.
Hayden, Matthew J.
Reynolds, Matthew
Saintenac, Cyrille
Wang, Shichen
Chao, Shiaoman
Talbert, Luther
Forrest, Kerrie
Tomar, Luxmi
See, Deven
Akhunova, Alina
Huang, Bevan Emma
da Silva, Marta Lopez
Bockelman, Harold
Akhunov, Eduard
Stephen, Stuart
Kong, Stephan
Anderson, James A.
Kiani, Seifollah
Korzun, Viktor
Carter, Arron
Dubcovsky, Jorge
Dreisigacker, Susanne
Sorrells, Mark E.
Bai, Guihua
Pumphrey, Michael
Morrell, Peter Laurent
Cavanagh, Colin R.
Baenziger, Stephen
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/23630259$$D View this record in MEDLINE/PubMed
https://hal.inrae.fr/hal-02651659$$DView record in HAL
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DocumentTitleAlternate Comparative population genomics of hexaploid wheat
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Keywords polyploid wheat
selection scans
wheat improvement
SNP genotyping
breeding history
Language English
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Author contributions: M.J.H. and E.A. designed research; C.R.C., S.C., S.S., S. Kiani, K.F., C.S., G.L.B.-G., A.A., D.S., G.B., M.P., L. Tomar, D.W., S. Kong, M.R., M.L.d.S., H.B., L. Talbert, J.A.A., S.D., S.B., A.C., V.K., P.L.M., J.D., M.K.M., M.E.S., M.J.H., and E.A. performed research; S.W. and B.E.H. contributed new reagents/analytic tools; C.R.C., S.C., S.W., B.E.H., S. Kiani, K.F., C.S., A.C., J.D., M.J.H., and E.A. analyzed data; and C.R.C., P.L.M., M.J.H., and E.A. wrote the paper.
Edited by Katrien M. Devos, University of Georgia, Athens, GA, and accepted by the Editorial Board April 5, 2013 (received for review October 4, 2012)
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Snippet Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the...
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StartPage 8057
SubjectTerms Agricultural practices
Alleles
artificial selection
Biological Sciences
Crop improvement
crops
Crops, Agricultural - genetics
Cultivars
disease resistance
Environmental conditions
environmental factors
flowering
fungal diseases of plants
fungi
Gene Frequency
Genes, Plant
Genetic diversity
genetic improvement
Genetic loci
Genetic Variation
Genome, Plant
Genomes
Genomics
Genotype
Haplotypes
hexaploidy
high-yielding varieties
introgression
landraces
Life Sciences
Local population
Oligonucleotide Array Sequence Analysis
pathogens
phenology
Plant breeding
Ploidies
Polymorphism
Polymorphism, Single Nucleotide
Population genetics
sampling
single nucleotide polymorphism
temporal variation
Triticum - genetics
Triticum aestivum
Wheat
wild relatives
Winter
Title Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars
URI https://www.jstor.org/stable/42656636
http://www.pnas.org/content/110/20/8057.abstract
https://www.ncbi.nlm.nih.gov/pubmed/23630259
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https://www.proquest.com/docview/1352279045
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https://hal.inrae.fr/hal-02651659
https://pubmed.ncbi.nlm.nih.gov/PMC3657823
Volume 110
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