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The genomics of linkage drag in sunflower

View ORCID ProfileKaichi Huang, View ORCID ProfileMojtaba Jahani, View ORCID ProfileJérôme Gouzy, Alexandra Legendre, View ORCID ProfileSebastien Carrere, View ORCID ProfileJosé Miguel Lázaro-Guevara, View ORCID ProfileEric Gerardo González Segovia, View ORCID ProfileMarco Todesco, Baptiste Mayjonade, View ORCID ProfileNathalie Rodde, View ORCID ProfileStéphane Cauet, View ORCID ProfileIsabelle Dufau, View ORCID ProfileS Evan Staton, View ORCID ProfileNicolas Pouilly, Marie-Claude Boniface, Camille Tapy, Brigitte Mangin, Alexandra Duhnen, View ORCID ProfileVéronique Gautier, View ORCID ProfileCharles Poncet, Cécile Donnadieu, Tali Mandel, View ORCID ProfileSariel Hübner, View ORCID ProfileJohn M. Burke, View ORCID ProfileSonia Vautrin, View ORCID ProfileArnaud Bellec, View ORCID ProfileGregory L. Owens, View ORCID ProfileNicolas Langlade, View ORCID ProfileStéphane Muños, View ORCID ProfileLoren H. Rieseberg
doi: https://doi.org/10.1101/2022.06.07.495047
Kaichi Huang
aDepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, V6R 2A5, Canada
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  • For correspondence: kaichi.huang@botany.ubc.ca lriesebe@mail.ubc.ca
Mojtaba Jahani
aDepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, V6R 2A5, Canada
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Jérôme Gouzy
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Alexandra Legendre
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Sebastien Carrere
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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José Miguel Lázaro-Guevara
aDepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, V6R 2A5, Canada
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Eric Gerardo González Segovia
aDepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, V6R 2A5, Canada
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Marco Todesco
aDepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, V6R 2A5, Canada
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Baptiste Mayjonade
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Nathalie Rodde
cINRAE, CNRGV French Plant Genomic Resource Center, F-31320, Castanet-Tolosan, France
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Stéphane Cauet
cINRAE, CNRGV French Plant Genomic Resource Center, F-31320, Castanet-Tolosan, France
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Isabelle Dufau
cINRAE, CNRGV French Plant Genomic Resource Center, F-31320, Castanet-Tolosan, France
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S Evan Staton
aDepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, V6R 2A5, Canada
dNRGene Canada Inc., Saskatoon, SK, S7N 3R3, Canada
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Nicolas Pouilly
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Marie-Claude Boniface
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Camille Tapy
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Brigitte Mangin
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Alexandra Duhnen
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Véronique Gautier
eGentyane Genomic Platform, INRAE, Clermont Ferrand, France
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Charles Poncet
eGentyane Genomic Platform, INRAE, Clermont Ferrand, France
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Cécile Donnadieu
fGeT-PlaGe Genomic Platform, INRAE, Toulouse, France
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Tali Mandel
gGalilee Research Institute (MIGAL), Tel-Hai Academic College, Upper Galilee, Israel
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Sariel Hübner
gGalilee Research Institute (MIGAL), Tel-Hai Academic College, Upper Galilee, Israel
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John M. Burke
hDepartment of Plant Biology, University of Georgia, Athens, GA, 30602
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Sonia Vautrin
cINRAE, CNRGV French Plant Genomic Resource Center, F-31320, Castanet-Tolosan, France
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Arnaud Bellec
cINRAE, CNRGV French Plant Genomic Resource Center, F-31320, Castanet-Tolosan, France
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Gregory L. Owens
iDepartment of Biology, University of Victoria, Victoria, BC, V8W 2Y2, Canada
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Nicolas Langlade
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Stéphane Muños
bLaboratoire des Interactions Plantes Microbes-Environnement (LIPME), CNRS, INRAE, Université de Toulouse, Castanet-Tolosan, France
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Loren H. Rieseberg
aDepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, V6R 2A5, Canada
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  • ORCID record for Loren H. Rieseberg
  • For correspondence: kaichi.huang@botany.ubc.ca lriesebe@mail.ubc.ca
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Abstract

Crop wild relatives represent valuable sources of alleles for crop improvement, including adaptation to climate change and emerging diseases. However, introgressions from wild relatives might have deleterious effects on desirable traits, including yield, due to linkage drag. Here we comprehensively analyzed the genomic and phenotypic impacts of wild introgressions into cultivated sunflower to estimate the impacts of linkage drag. First, we generated new reference sequences for seven cultivated and one wild sunflower genotype, as well as improved assemblies for two additional cultivars. Next, relying on previously generated sequences from wild donor species, we identified introgressions in the cultivated reference sequences, as well as the sequence and structural variants they contain. We then used a ridge regression model to test the effects of the introgressions on phenotypic traits in the cultivated sunflower association mapping population. We found that introgression has introduced substantial sequence and structural variation into the cultivated sunflower gene pool, including > 3,000 new genes. While introgressions reduced genetic load at protein-coding sequences and positively affected traits associated with abiotic stress resistance, they mostly had negative impacts on yield and quality traits. Introgressions found at high frequency in the cultivated gene pool had larger effects than low frequency introgressions, suggesting that the former likely were targeted by artificial selection. Also, introgressions from more distantly related species were more likely to be maladaptive than those from the wild progenitor of cultivated sunflower. Thus, pre-breeding efforts should focus, as far as possible, on closely related and fully compatible wild relatives.

Competing Interest Statement

The authors have declared no competing interest.

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The genomics of linkage drag in sunflower
Kaichi Huang, Mojtaba Jahani, Jérôme Gouzy, Alexandra Legendre, Sebastien Carrere, José Miguel Lázaro-Guevara, Eric Gerardo González Segovia, Marco Todesco, Baptiste Mayjonade, Nathalie Rodde, Stéphane Cauet, Isabelle Dufau, S Evan Staton, Nicolas Pouilly, Marie-Claude Boniface, Camille Tapy, Brigitte Mangin, Alexandra Duhnen, Véronique Gautier, Charles Poncet, Cécile Donnadieu, Tali Mandel, Sariel Hübner, John M. Burke, Sonia Vautrin, Arnaud Bellec, Gregory L. Owens, Nicolas Langlade, Stéphane Muños, Loren H. Rieseberg
bioRxiv 2022.06.07.495047; doi: https://doi.org/10.1101/2022.06.07.495047
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The genomics of linkage drag in sunflower
Kaichi Huang, Mojtaba Jahani, Jérôme Gouzy, Alexandra Legendre, Sebastien Carrere, José Miguel Lázaro-Guevara, Eric Gerardo González Segovia, Marco Todesco, Baptiste Mayjonade, Nathalie Rodde, Stéphane Cauet, Isabelle Dufau, S Evan Staton, Nicolas Pouilly, Marie-Claude Boniface, Camille Tapy, Brigitte Mangin, Alexandra Duhnen, Véronique Gautier, Charles Poncet, Cécile Donnadieu, Tali Mandel, Sariel Hübner, John M. Burke, Sonia Vautrin, Arnaud Bellec, Gregory L. Owens, Nicolas Langlade, Stéphane Muños, Loren H. Rieseberg
bioRxiv 2022.06.07.495047; doi: https://doi.org/10.1101/2022.06.07.495047

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