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Genomics of sorghum local adaptation to a parasitic plant.

Identifieur interne : 000152 ( Main/Exploration ); précédent : 000151; suivant : 000153

Genomics of sorghum local adaptation to a parasitic plant.

Auteurs : Emily S. Bellis [États-Unis] ; Elizabeth A. Kelly [États-Unis] ; Claire M. Lorts [États-Unis] ; Huirong Gao [États-Unis] ; Victoria L. Deleo [États-Unis] ; Germinal Rouhan [France] ; Andrew Budden [Royaume-Uni] ; Govinal B. Bhaskara [États-Unis] ; Zhenbin Hu [États-Unis] ; Robert Muscarella [Suède] ; Michael P. Timko [États-Unis] ; Baloua Nebie [Mali] ; Steven M. Runo [Kenya] ; N Doane Chilcoat [États-Unis] ; Thomas E. Juenger [États-Unis] ; Geoffrey P. Morris [États-Unis] ; Claude W. Depamphilis [États-Unis] ; Jesse R. Lasky [États-Unis]

Source :

RBID : pubmed:32047036

Descripteurs français

English descriptors

Abstract

Host-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9-edited sorghum further indicate that the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

DOI: 10.1073/pnas.1908707117
PubMed: 32047036
PubMed Central: PMC7049153


Affiliations:


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Le document en format XML

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<name sortKey="Runo, Steven M" sort="Runo, Steven M" uniqKey="Runo S" first="Steven M" last="Runo">Steven M. Runo</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Biochemistry and Biotechnology, Kenyatta University, Nairobi, Kenya.</nlm:affiliation>
<country xml:lang="fr">Kenya</country>
<wicri:regionArea>Department of Biochemistry and Biotechnology, Kenyatta University, Nairobi</wicri:regionArea>
<wicri:noRegion>Nairobi</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Chilcoat, N Doane" sort="Chilcoat, N Doane" uniqKey="Chilcoat N" first="N Doane" last="Chilcoat">N Doane Chilcoat</name>
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</affiliation>
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<author>
<name sortKey="Juenger, Thomas E" sort="Juenger, Thomas E" uniqKey="Juenger T" first="Thomas E" last="Juenger">Thomas E. Juenger</name>
<affiliation wicri:level="2">
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<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Texas</region>
</placeName>
<wicri:cityArea>Department of Integrative Biology, University of Texas at Austin, Austin</wicri:cityArea>
</affiliation>
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<name sortKey="Morris, Geoffrey P" sort="Morris, Geoffrey P" uniqKey="Morris G" first="Geoffrey P" last="Morris">Geoffrey P. Morris</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Agronomy, Kansas State University, Manhattan, KS 66506.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Kansas</region>
</placeName>
<wicri:cityArea>Department of Agronomy, Kansas State University, Manhattan</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Depamphilis, Claude W" sort="Depamphilis, Claude W" uniqKey="Depamphilis C" first="Claude W" last="Depamphilis">Claude W. Depamphilis</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Pennsylvanie</region>
</placeName>
<wicri:cityArea>Department of Biology, The Pennsylvania State University, University Park</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Lasky, Jesse R" sort="Lasky, Jesse R" uniqKey="Lasky J" first="Jesse R" last="Lasky">Jesse R. Lasky</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Pennsylvanie</region>
</placeName>
<wicri:cityArea>Department of Biology, The Pennsylvania State University, University Park</wicri:cityArea>
</affiliation>
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<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2020" type="published">2020</date>
</imprint>
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<term>Adaptation, Physiological (MeSH)</term>
<term>Genetic Variation (MeSH)</term>
<term>Genome, Plant (MeSH)</term>
<term>Genomics (MeSH)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Weeds (genetics)</term>
<term>Plant Weeds (physiology)</term>
<term>Sorghum (genetics)</term>
<term>Sorghum (physiology)</term>
<term>Striga (genetics)</term>
<term>Striga (physiology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Adaptation physiologique (MeSH)</term>
<term>Génome végétal (MeSH)</term>
<term>Génomique (MeSH)</term>
<term>Mauvaises herbes (génétique)</term>
<term>Mauvaises herbes (physiologie)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Sorghum (génétique)</term>
<term>Sorghum (physiologie)</term>
<term>Striga (génétique)</term>
<term>Striga (physiologie)</term>
<term>Variation génétique (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Plant Weeds</term>
<term>Sorghum</term>
<term>Striga</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Mauvaises herbes</term>
<term>Protéines végétales</term>
<term>Sorghum</term>
<term>Striga</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Mauvaises herbes</term>
<term>Sorghum</term>
<term>Striga</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Plant Weeds</term>
<term>Sorghum</term>
<term>Striga</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Adaptation, Physiological</term>
<term>Genetic Variation</term>
<term>Genome, Plant</term>
<term>Genomics</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Adaptation physiologique</term>
<term>Génome végétal</term>
<term>Génomique</term>
<term>Variation génétique</term>
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<front>
<div type="abstract" xml:lang="en">Host-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop
<i>Sorghum bicolor</i>
(L.) Moench and its association with the parasitic weed
<i>Striga hermonthica</i>
(Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum
<i>LOW GERMINATION STIMULANT 1 (LGS1)</i>
are broadly distributed among African landraces and geographically associated with
<i>S. hermonthica</i>
occurrence. However, low frequency of these alleles within
<i>S. hermonthica</i>
-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation.
<i>LGS1</i>
is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding
<i>LGS1</i>
and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9-edited sorghum further indicate that the benefit of
<i>LGS1</i>
-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">32047036</PMID>
<DateCompleted>
<Year>2020</Year>
<Month>07</Month>
<Day>17</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>08</Month>
<Day>11</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1091-6490</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>117</Volume>
<Issue>8</Issue>
<PubDate>
<Year>2020</Year>
<Month>02</Month>
<Day>25</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>Genomics of sorghum local adaptation to a parasitic plant.</ArticleTitle>
<Pagination>
<MedlinePgn>4243-4251</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1908707117</ELocationID>
<Abstract>
<AbstractText>Host-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop
<i>Sorghum bicolor</i>
(L.) Moench and its association with the parasitic weed
<i>Striga hermonthica</i>
(Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum
<i>LOW GERMINATION STIMULANT 1 (LGS1)</i>
are broadly distributed among African landraces and geographically associated with
<i>S. hermonthica</i>
occurrence. However, low frequency of these alleles within
<i>S. hermonthica</i>
-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation.
<i>LGS1</i>
is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding
<i>LGS1</i>
and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9-edited sorghum further indicate that the benefit of
<i>LGS1</i>
-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Bellis</LastName>
<ForeName>Emily S</ForeName>
<Initials>ES</Initials>
<Identifier Source="ORCID">0000-0001-6066-1466</Identifier>
<AffiliationInfo>
<Affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802; ebellis@astate.edu.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Arkansas Biosciences Institute, Arkansas State University, State University, AR 72467.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Computer Science, Arkansas State University, State University, AR 72467.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kelly</LastName>
<ForeName>Elizabeth A</ForeName>
<Initials>EA</Initials>
<AffiliationInfo>
<Affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Intercollege Graduate Program in Plant Biology, The Pennsylvania State University, University Park, PA 16802.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lorts</LastName>
<ForeName>Claire M</ForeName>
<Initials>CM</Initials>
<AffiliationInfo>
<Affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gao</LastName>
<ForeName>Huirong</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Applied Science and Technology, Corteva Agriscience, Johnston, IA 50131.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>DeLeo</LastName>
<ForeName>Victoria L</ForeName>
<Initials>VL</Initials>
<AffiliationInfo>
<Affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Intercollege Graduate Program in Plant Biology, The Pennsylvania State University, University Park, PA 16802.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rouhan</LastName>
<ForeName>Germinal</ForeName>
<Initials>G</Initials>
<Identifier Source="ORCID">0000-0002-0751-5352</Identifier>
<AffiliationInfo>
<Affiliation>Institut Systématique Evolution Biodiversité, Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, École Pratique des Hautes Études, CP39, 75005 Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Budden</LastName>
<ForeName>Andrew</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Identification & Naming, Royal Botanic Gardens, Kew, TW9 3AB Richmond, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bhaskara</LastName>
<ForeName>Govinal B</ForeName>
<Initials>GB</Initials>
<Identifier Source="ORCID">0000-0002-8003-1207</Identifier>
<AffiliationInfo>
<Affiliation>Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hu</LastName>
<ForeName>Zhenbin</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>Department of Agronomy, Kansas State University, Manhattan, KS 66506.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Muscarella</LastName>
<ForeName>Robert</ForeName>
<Initials>R</Initials>
<Identifier Source="ORCID">0000-0003-3039-1076</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, SE-75236 Uppsala, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Timko</LastName>
<ForeName>Michael P</ForeName>
<Initials>MP</Initials>
<AffiliationInfo>
<Affiliation>Department of Biology, University of Virginia, Charlottesville, VA 22904.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Nebie</LastName>
<ForeName>Baloua</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>West and Central Africa Regional Program, International Crops Research Institute for the Semi-Arid Tropics, BP 320 Bamako, Mali.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Runo</LastName>
<ForeName>Steven M</ForeName>
<Initials>SM</Initials>
<AffiliationInfo>
<Affiliation>Department of Biochemistry and Biotechnology, Kenyatta University, Nairobi, Kenya.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chilcoat</LastName>
<ForeName>N Doane</ForeName>
<Initials>ND</Initials>
<AffiliationInfo>
<Affiliation>Applied Science and Technology, Corteva Agriscience, Johnston, IA 50131.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Juenger</LastName>
<ForeName>Thomas E</ForeName>
<Initials>TE</Initials>
<AffiliationInfo>
<Affiliation>Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Morris</LastName>
<ForeName>Geoffrey P</ForeName>
<Initials>GP</Initials>
<AffiliationInfo>
<Affiliation>Department of Agronomy, Kansas State University, Manhattan, KS 66506.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>dePamphilis</LastName>
<ForeName>Claude W</ForeName>
<Initials>CW</Initials>
<AffiliationInfo>
<Affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lasky</LastName>
<ForeName>Jesse R</ForeName>
<Initials>JR</Initials>
<AffiliationInfo>
<Affiliation>Department of Biology, The Pennsylvania State University, University Park, PA 16802.</Affiliation>
</AffiliationInfo>
</Author>
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<Month>02</Month>
<Day>11</Day>
</ArticleDate>
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<DescriptorName UI="D000222" MajorTopicYN="N">Adaptation, Physiological</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D014644" MajorTopicYN="N">Genetic Variation</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018745" MajorTopicYN="N">Genome, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D023281" MajorTopicYN="N">Genomics</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D057685" MajorTopicYN="N">Plant Weeds</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D045868" MajorTopicYN="N">Sorghum</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D034362" MajorTopicYN="N">Striga</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">environmental niche modeling</Keyword>
<Keyword MajorTopicYN="Y">genotype–environment association analysis</Keyword>
<Keyword MajorTopicYN="Y">species distribution modeling</Keyword>
</KeywordList>
<CoiStatement>Competing interest statement: H.G. and N.D.C. are employees of Corteva Agriscience.</CoiStatement>
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