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Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction.

Identifieur interne : 000274 ( Main/Exploration ); précédent : 000273; suivant : 000275

Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction.

Auteurs : Carlos A. Villarroel [Pays-Bas] ; Wim Jonckheere [Pays-Bas] ; Juan M. Alba [Pays-Bas] ; Joris J. Glas [Pays-Bas] ; Wannes Dermauw [Belgique] ; Michel A. Haring [Pays-Bas] ; Thomas Van Leeuwen [Pays-Bas, Belgique] ; Robert C. Schuurink [Pays-Bas] ; Merijn R. Kant [Pays-Bas]

Source :

RBID : pubmed:26946468

Descripteurs français

English descriptors

Abstract

Spider mites (Tetranychidae sp.) are widely occurring arthropod pests on cultivated plants. Feeding by the two-spotted spider mite T. urticae, a generalist herbivore, induces a defense response in plants that mainly depends on the phytohormones jasmonic acid and salicylic acid (SA). On tomato (Solanum lycopersicum), however, certain genotypes of T. urticae and the specialist species T. evansi were found to suppress these defenses. This phenomenon occurs downstream of phytohormone accumulation via an unknown mechanism. We investigated if spider mites possess effector-like proteins in their saliva that can account for this defense suppression. First we performed an in silico prediction of the T. urticae and the T. evansi secretomes, and subsequently generated a short list of candidate effectors based on additional selection criteria such as life stage-specific expression and salivary gland expression via whole mount in situ hybridization. We picked the top five most promising protein families and then expressed representatives in Nicotiana benthamiana using Agrobacterium tumefaciens transient expression assays to assess their effect on plant defenses. Four proteins from two families suppressed defenses downstream of the phytohormone SA. Furthermore, T. urticae performance on N. benthamiana improved in response to transient expression of three of these proteins and this improvement was similar to that of mites feeding on the tomato SA accumulation mutant nahG. Our results suggest that both generalist and specialist plant-eating mite species are sensitive to SA defenses but secrete proteins via their saliva to reduce the negative effects of these defenses.

DOI: 10.1111/tpj.13152
PubMed: 26946468


Affiliations:


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<nlm:affiliation>Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.</nlm:affiliation>
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<wicri:regionArea>Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam</wicri:regionArea>
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<nlm:affiliation>Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.</nlm:affiliation>
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<nlm:affiliation>Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.</nlm:affiliation>
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<title level="j">The Plant journal : for cell and molecular biology</title>
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<term>Animals (MeSH)</term>
<term>Arthropod Proteins (metabolism)</term>
<term>Herbivory (MeSH)</term>
<term>Mites (classification)</term>
<term>Mites (physiology)</term>
<term>Reproduction (MeSH)</term>
<term>Salivary Proteins and Peptides (metabolism)</term>
<term>Tobacco (immunology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux (MeSH)</term>
<term>Herbivorie (MeSH)</term>
<term>Mites (acariens) (classification)</term>
<term>Mites (acariens) (physiologie)</term>
<term>Protéines d'arthropode (métabolisme)</term>
<term>Protéines et peptides salivaires (métabolisme)</term>
<term>Reproduction (MeSH)</term>
<term>Tabac (immunologie)</term>
</keywords>
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<term>Arthropod Proteins</term>
<term>Salivary Proteins and Peptides</term>
</keywords>
<keywords scheme="MESH" qualifier="classification" xml:lang="en">
<term>Mites</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Mites (acariens)</term>
<term>Protéines d'arthropode</term>
<term>Protéines et peptides salivaires</term>
</keywords>
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<term>Mites (acariens)</term>
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<term>Mites</term>
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<keywords scheme="MESH" xml:lang="en">
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<term>Herbivory</term>
<term>Reproduction</term>
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<div type="abstract" xml:lang="en">Spider mites (Tetranychidae sp.) are widely occurring arthropod pests on cultivated plants. Feeding by the two-spotted spider mite T. urticae, a generalist herbivore, induces a defense response in plants that mainly depends on the phytohormones jasmonic acid and salicylic acid (SA). On tomato (Solanum lycopersicum), however, certain genotypes of T. urticae and the specialist species T. evansi were found to suppress these defenses. This phenomenon occurs downstream of phytohormone accumulation via an unknown mechanism. We investigated if spider mites possess effector-like proteins in their saliva that can account for this defense suppression. First we performed an in silico prediction of the T. urticae and the T. evansi secretomes, and subsequently generated a short list of candidate effectors based on additional selection criteria such as life stage-specific expression and salivary gland expression via whole mount in situ hybridization. We picked the top five most promising protein families and then expressed representatives in Nicotiana benthamiana using Agrobacterium tumefaciens transient expression assays to assess their effect on plant defenses. Four proteins from two families suppressed defenses downstream of the phytohormone SA. Furthermore, T. urticae performance on N. benthamiana improved in response to transient expression of three of these proteins and this improvement was similar to that of mites feeding on the tomato SA accumulation mutant nahG. Our results suggest that both generalist and specialist plant-eating mite species are sensitive to SA defenses but secrete proteins via their saliva to reduce the negative effects of these defenses.</div>
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<PubDate>
<Year>2016</Year>
<Month>Apr</Month>
</PubDate>
</JournalIssue>
<Title>The Plant journal : for cell and molecular biology</Title>
<ISOAbbreviation>Plant J</ISOAbbreviation>
</Journal>
<ArticleTitle>Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction.</ArticleTitle>
<Pagination>
<MedlinePgn>119-31</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/tpj.13152</ELocationID>
<Abstract>
<AbstractText>Spider mites (Tetranychidae sp.) are widely occurring arthropod pests on cultivated plants. Feeding by the two-spotted spider mite T. urticae, a generalist herbivore, induces a defense response in plants that mainly depends on the phytohormones jasmonic acid and salicylic acid (SA). On tomato (Solanum lycopersicum), however, certain genotypes of T. urticae and the specialist species T. evansi were found to suppress these defenses. This phenomenon occurs downstream of phytohormone accumulation via an unknown mechanism. We investigated if spider mites possess effector-like proteins in their saliva that can account for this defense suppression. First we performed an in silico prediction of the T. urticae and the T. evansi secretomes, and subsequently generated a short list of candidate effectors based on additional selection criteria such as life stage-specific expression and salivary gland expression via whole mount in situ hybridization. We picked the top five most promising protein families and then expressed representatives in Nicotiana benthamiana using Agrobacterium tumefaciens transient expression assays to assess their effect on plant defenses. Four proteins from two families suppressed defenses downstream of the phytohormone SA. Furthermore, T. urticae performance on N. benthamiana improved in response to transient expression of three of these proteins and this improvement was similar to that of mites feeding on the tomato SA accumulation mutant nahG. Our results suggest that both generalist and specialist plant-eating mite species are sensitive to SA defenses but secrete proteins via their saliva to reduce the negative effects of these defenses.</AbstractText>
<CopyrightInformation>© 2016 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Villarroel</LastName>
<ForeName>Carlos A</ForeName>
<Initials>CA</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jonckheere</LastName>
<ForeName>Wim</ForeName>
<Initials>W</Initials>
<AffiliationInfo>
<Affiliation>Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Alba</LastName>
<ForeName>Juan M</ForeName>
<Initials>JM</Initials>
<AffiliationInfo>
<Affiliation>Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Glas</LastName>
<ForeName>Joris J</ForeName>
<Initials>JJ</Initials>
<AffiliationInfo>
<Affiliation>Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dermauw</LastName>
<ForeName>Wannes</ForeName>
<Initials>W</Initials>
<AffiliationInfo>
<Affiliation>Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, B-9000, Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Haring</LastName>
<ForeName>Michel A</ForeName>
<Initials>MA</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Van Leeuwen</LastName>
<ForeName>Thomas</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, B-9000, Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schuurink</LastName>
<ForeName>Robert C</ForeName>
<Initials>RC</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kant</LastName>
<ForeName>Merijn R</ForeName>
<Initials>MR</Initials>
<AffiliationInfo>
<Affiliation>Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.</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>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Plant J</MedlineTA>
<NlmUniqueID>9207397</NlmUniqueID>
<ISSNLinking>0960-7412</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D060829">Arthropod Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D012471">Salivary Proteins and Peptides</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060829" MajorTopicYN="N">Arthropod Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060434" MajorTopicYN="Y">Herbivory</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008925" MajorTopicYN="N">Mites</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012098" MajorTopicYN="N">Reproduction</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012471" MajorTopicYN="N">Salivary Proteins and Peptides</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014026" MajorTopicYN="N">Tobacco</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Agrobacterium tumefaciens transient assay</Keyword>
<Keyword MajorTopicYN="N">Nicotiana benthamiana</Keyword>
<Keyword MajorTopicYN="N">Solanum lycopersicum</Keyword>
<Keyword MajorTopicYN="N">Tetranychus evansi</Keyword>
<Keyword MajorTopicYN="N">Tetranychus urticae</Keyword>
<Keyword MajorTopicYN="N">effector</Keyword>
<Keyword MajorTopicYN="N">jasmonic acid</Keyword>
<Keyword MajorTopicYN="N">nahG tomato</Keyword>
<Keyword MajorTopicYN="N">plant defense suppression</Keyword>
<Keyword MajorTopicYN="N">salicylic acid</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2015</Year>
<Month>10</Month>
<Day>06</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2016</Year>
<Month>01</Month>
<Day>29</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2016</Year>
<Month>02</Month>
<Day>19</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2016</Year>
<Month>3</Month>
<Day>7</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2016</Year>
<Month>3</Month>
<Day>8</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2017</Year>
<Month>2</Month>
<Day>22</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">26946468</ArticleId>
<ArticleId IdType="doi">10.1111/tpj.13152</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Belgique</li>
<li>Pays-Bas</li>
</country>
<region>
<li>Hollande-Septentrionale</li>
<li>Province de Flandre-Orientale</li>
<li>Région flamande</li>
</region>
<settlement>
<li>Amsterdam</li>
<li>Gand</li>
</settlement>
<orgName>
<li>Université d'Amsterdam</li>
<li>Université de Gand</li>
</orgName>
</list>
<tree>
<country name="Pays-Bas">
<region name="Hollande-Septentrionale">
<name sortKey="Villarroel, Carlos A" sort="Villarroel, Carlos A" uniqKey="Villarroel C" first="Carlos A" last="Villarroel">Carlos A. Villarroel</name>
</region>
<name sortKey="Alba, Juan M" sort="Alba, Juan M" uniqKey="Alba J" first="Juan M" last="Alba">Juan M. Alba</name>
<name sortKey="Glas, Joris J" sort="Glas, Joris J" uniqKey="Glas J" first="Joris J" last="Glas">Joris J. Glas</name>
<name sortKey="Haring, Michel A" sort="Haring, Michel A" uniqKey="Haring M" first="Michel A" last="Haring">Michel A. Haring</name>
<name sortKey="Jonckheere, Wim" sort="Jonckheere, Wim" uniqKey="Jonckheere W" first="Wim" last="Jonckheere">Wim Jonckheere</name>
<name sortKey="Kant, Merijn R" sort="Kant, Merijn R" uniqKey="Kant M" first="Merijn R" last="Kant">Merijn R. Kant</name>
<name sortKey="Schuurink, Robert C" sort="Schuurink, Robert C" uniqKey="Schuurink R" first="Robert C" last="Schuurink">Robert C. Schuurink</name>
<name sortKey="Van Leeuwen, Thomas" sort="Van Leeuwen, Thomas" uniqKey="Van Leeuwen T" first="Thomas" last="Van Leeuwen">Thomas Van Leeuwen</name>
<name sortKey="Villarroel, Carlos A" sort="Villarroel, Carlos A" uniqKey="Villarroel C" first="Carlos A" last="Villarroel">Carlos A. Villarroel</name>
</country>
<country name="Belgique">
<region name="Région flamande">
<name sortKey="Dermauw, Wannes" sort="Dermauw, Wannes" uniqKey="Dermauw W" first="Wannes" last="Dermauw">Wannes Dermauw</name>
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<name sortKey="Van Leeuwen, Thomas" sort="Van Leeuwen, Thomas" uniqKey="Van Leeuwen T" first="Thomas" last="Van Leeuwen">Thomas Van Leeuwen</name>
</country>
</tree>
</affiliations>
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