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Rapid and multiregional adaptation to host partial resistance in a plant pathogenic oomycete: evidence from European populations of Plasmopara viticola, the causal agent of grapevine downy mildew.

Identifieur interne : 000487 ( Main/Exploration ); précédent : 000486; suivant : 000488

Rapid and multiregional adaptation to host partial resistance in a plant pathogenic oomycete: evidence from European populations of Plasmopara viticola, the causal agent of grapevine downy mildew.

Auteurs : François Delmotte [France] ; Pere Mestre [France] ; Christophe Schneider [France] ; Hanns-Heinz Kassemeyer [Allemagne] ; Pál Kozma [Hongrie] ; Sylvie Richart-Cervera [France] ; Mélanie Rouxel [France] ; Laurent Delière [France]

Source :

RBID : pubmed:24184095

Descripteurs français

English descriptors

Abstract

Crop pathogens evolve rapidly to adapt to their hosts. The use of crops with quantitative disease resistance is expected to alter selection of pathogen life-history traits. This may result in differential adaptation of the pathogen to host cultivars and, sometimes, to the erosion of quantitative resistance. Here, we assessed the level of host adaptation in an oomycete plant pathogenic species. We analysed the phenotypic and genetic variability of 17 Plasmopara viticola isolates collected on Vitis vinifera and 35 isolates from partially resistant varieties (Regent and genotypes carrying the Rpv1 gene). Cross-inoculation experiments assessed two components of aggressiveness and a life-history trait of the pathogen: disease severity, sporangial production and sporangia size. The results contribute evidence to the emergence of P. viticola aggressive isolates presenting a high level of sporulation on the partially resistant Regent. By contrast, no adaptation to the Rpv1 gene was found in this study. The erosion of Regent resistance may have occurred in less than 5years and at least three times independently in three distant wine-producing areas. Populations from resistant varieties showed a significant increase in sporangia production capacity, indicating an absence of fitness costs for this adaptation. The increase in the number of sporangia was correlated with a reduction in sporangia size, a result which illustrates how partial plant disease resistance can impact selection of the pathogen's life-history traits. This case study on grapevine downy mildew shows how new plant pathogen populations emerge in agro-ecosystems by adapting to partial host resistance. This adaptive pattern highlights the need for wise management of plant partial disease resistance to ensure its sustainability over time.

DOI: 10.1016/j.meegid.2013.10.017
PubMed: 24184095


Affiliations:


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<div type="abstract" xml:lang="en">Crop pathogens evolve rapidly to adapt to their hosts. The use of crops with quantitative disease resistance is expected to alter selection of pathogen life-history traits. This may result in differential adaptation of the pathogen to host cultivars and, sometimes, to the erosion of quantitative resistance. Here, we assessed the level of host adaptation in an oomycete plant pathogenic species. We analysed the phenotypic and genetic variability of 17 Plasmopara viticola isolates collected on Vitis vinifera and 35 isolates from partially resistant varieties (Regent and genotypes carrying the Rpv1 gene). Cross-inoculation experiments assessed two components of aggressiveness and a life-history trait of the pathogen: disease severity, sporangial production and sporangia size. The results contribute evidence to the emergence of P. viticola aggressive isolates presenting a high level of sporulation on the partially resistant Regent. By contrast, no adaptation to the Rpv1 gene was found in this study. The erosion of Regent resistance may have occurred in less than 5years and at least three times independently in three distant wine-producing areas. Populations from resistant varieties showed a significant increase in sporangia production capacity, indicating an absence of fitness costs for this adaptation. The increase in the number of sporangia was correlated with a reduction in sporangia size, a result which illustrates how partial plant disease resistance can impact selection of the pathogen's life-history traits. This case study on grapevine downy mildew shows how new plant pathogen populations emerge in agro-ecosystems by adapting to partial host resistance. This adaptive pattern highlights the need for wise management of plant partial disease resistance to ensure its sustainability over time. </div>
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<AbstractText>Crop pathogens evolve rapidly to adapt to their hosts. The use of crops with quantitative disease resistance is expected to alter selection of pathogen life-history traits. This may result in differential adaptation of the pathogen to host cultivars and, sometimes, to the erosion of quantitative resistance. Here, we assessed the level of host adaptation in an oomycete plant pathogenic species. We analysed the phenotypic and genetic variability of 17 Plasmopara viticola isolates collected on Vitis vinifera and 35 isolates from partially resistant varieties (Regent and genotypes carrying the Rpv1 gene). Cross-inoculation experiments assessed two components of aggressiveness and a life-history trait of the pathogen: disease severity, sporangial production and sporangia size. The results contribute evidence to the emergence of P. viticola aggressive isolates presenting a high level of sporulation on the partially resistant Regent. By contrast, no adaptation to the Rpv1 gene was found in this study. The erosion of Regent resistance may have occurred in less than 5years and at least three times independently in three distant wine-producing areas. Populations from resistant varieties showed a significant increase in sporangia production capacity, indicating an absence of fitness costs for this adaptation. The increase in the number of sporangia was correlated with a reduction in sporangia size, a result which illustrates how partial plant disease resistance can impact selection of the pathogen's life-history traits. This case study on grapevine downy mildew shows how new plant pathogen populations emerge in agro-ecosystems by adapting to partial host resistance. This adaptive pattern highlights the need for wise management of plant partial disease resistance to ensure its sustainability over time. </AbstractText>
<CopyrightInformation>Copyright © 2013 Elsevier B.V. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Delmotte</LastName>
<ForeName>François</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>INRA, Institut des Sciences de la Vigne et du Vin, UMR1065 Santé et Agroécologie du Vignoble, F-33883 Villenave d'Ornon, France; Université de Bordeaux, ISVV, UMR1065 SAVE, F-33883 Villenave d'Ornon, France. Electronic address: delmotte@bordeaux.inra.fr.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Mestre</LastName>
<ForeName>Pere</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>INRA, UMR 1131 Santé de la Vigne et Qualité du Vin, F-68000 Colmar, France; Université de Strasbourg, UMR 1131 Santé de la Vigne et Qualité du Vin, F-68000 Colmar, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schneider</LastName>
<ForeName>Christophe</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>INRA, UMR 1131 Santé de la Vigne et Qualité du Vin, F-68000 Colmar, France; Université de Strasbourg, UMR 1131 Santé de la Vigne et Qualité du Vin, F-68000 Colmar, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kassemeyer</LastName>
<ForeName>Hanns-Heinz</ForeName>
<Initials>HH</Initials>
<AffiliationInfo>
<Affiliation>Staatliches Weinbauinstitut, Merzhauser Strasse 119, 79100 Freiburg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kozma</LastName>
<ForeName>Pál</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>University of Pécs, Research Institute for Viticulture and Oenology, H-7634 Pécs, Pázmány Péter u.4, Hungary.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Richart-Cervera</LastName>
<ForeName>Sylvie</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>INRA, Institut des Sciences de la Vigne et du Vin, UMR1065 Santé et Agroécologie du Vignoble, F-33883 Villenave d'Ornon, France; Université de Bordeaux, ISVV, UMR1065 SAVE, F-33883 Villenave d'Ornon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rouxel</LastName>
<ForeName>Mélanie</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>INRA, Institut des Sciences de la Vigne et du Vin, UMR1065 Santé et Agroécologie du Vignoble, F-33883 Villenave d'Ornon, France; Université de Bordeaux, ISVV, UMR1065 SAVE, F-33883 Villenave d'Ornon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Delière</LastName>
<ForeName>Laurent</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>INRA, Institut des Sciences de la Vigne et du Vin, UMR1065 Santé et Agroécologie du Vignoble, F-33883 Villenave d'Ornon, France; Université de Bordeaux, ISVV, UMR1065 SAVE, F-33883 Villenave d'Ornon, France.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2013</Year>
<Month>10</Month>
<Day>30</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>Netherlands</Country>
<MedlineTA>Infect Genet Evol</MedlineTA>
<NlmUniqueID>101084138</NlmUniqueID>
<ISSNLinking>1567-1348</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D060467" MajorTopicYN="Y">Disease Resistance</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005843" MajorTopicYN="N">Geography</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D054884" MajorTopicYN="Y">Host-Pathogen Interactions</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009868" MajorTopicYN="Y">Oomycetes</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D027843" MajorTopicYN="N">Vitis</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Aggressiveness</Keyword>
<Keyword MajorTopicYN="N">Erosion of quantitative host resistance</Keyword>
<Keyword MajorTopicYN="N">Fungal plant pathogen</Keyword>
<Keyword MajorTopicYN="N">Life-history traits</Keyword>
<Keyword MajorTopicYN="N">Regent grape cultivar</Keyword>
<Keyword MajorTopicYN="N">Vitis vinifera</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2013</Year>
<Month>07</Month>
<Day>03</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2013</Year>
<Month>10</Month>
<Day>17</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2013</Year>
<Month>10</Month>
<Day>21</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2013</Year>
<Month>11</Month>
<Day>5</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2013</Year>
<Month>11</Month>
<Day>5</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2016</Year>
<Month>5</Month>
<Day>12</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">24184095</ArticleId>
<ArticleId IdType="pii">S1567-1348(13)00389-4</ArticleId>
<ArticleId IdType="doi">10.1016/j.meegid.2013.10.017</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>France</li>
<li>Hongrie</li>
</country>
<region>
<li>Alsace (région administrative)</li>
<li>Aquitaine</li>
<li>Bade-Wurtemberg</li>
<li>District de Fribourg-en-Brisgau</li>
<li>Grand Est</li>
<li>Nouvelle-Aquitaine</li>
</region>
<settlement>
<li>Colmar</li>
<li>Fribourg-en-Brisgau</li>
<li>Villenave d'Ornon</li>
</settlement>
<orgName>
<li>Université de Bordeaux</li>
<li>Université de Strasbourg</li>
</orgName>
</list>
<tree>
<country name="France">
<region name="Nouvelle-Aquitaine">
<name sortKey="Delmotte, Francois" sort="Delmotte, Francois" uniqKey="Delmotte F" first="François" last="Delmotte">François Delmotte</name>
</region>
<name sortKey="Deliere, Laurent" sort="Deliere, Laurent" uniqKey="Deliere L" first="Laurent" last="Delière">Laurent Delière</name>
<name sortKey="Mestre, Pere" sort="Mestre, Pere" uniqKey="Mestre P" first="Pere" last="Mestre">Pere Mestre</name>
<name sortKey="Richart Cervera, Sylvie" sort="Richart Cervera, Sylvie" uniqKey="Richart Cervera S" first="Sylvie" last="Richart-Cervera">Sylvie Richart-Cervera</name>
<name sortKey="Rouxel, Melanie" sort="Rouxel, Melanie" uniqKey="Rouxel M" first="Mélanie" last="Rouxel">Mélanie Rouxel</name>
<name sortKey="Schneider, Christophe" sort="Schneider, Christophe" uniqKey="Schneider C" first="Christophe" last="Schneider">Christophe Schneider</name>
</country>
<country name="Allemagne">
<region name="Bade-Wurtemberg">
<name sortKey="Kassemeyer, Hanns Heinz" sort="Kassemeyer, Hanns Heinz" uniqKey="Kassemeyer H" first="Hanns-Heinz" last="Kassemeyer">Hanns-Heinz Kassemeyer</name>
</region>
</country>
<country name="Hongrie">
<noRegion>
<name sortKey="Kozma, Pal" sort="Kozma, Pal" uniqKey="Kozma P" first="Pál" last="Kozma">Pál Kozma</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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