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The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease.

Identifieur interne : 000644 ( Main/Exploration ); précédent : 000643; suivant : 000645

The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease.

Auteurs : Fraser Murphy [Royaume-Uni] ; Qin He [Royaume-Uni, République populaire de Chine] ; Miles Armstrong [Royaume-Uni] ; Licida M. Giuliani [Royaume-Uni] ; Petra C. Boevink [Royaume-Uni] ; Wei Zhang [République populaire de Chine] ; Zhendong Tian [République populaire de Chine] ; Paul R J. Birch [Royaume-Uni] ; Eleanor M. Gilroy [Royaume-Uni]

Source :

RBID : pubmed:29588335

Descripteurs français

English descriptors

Abstract

Plant pathogens deliver effectors to manipulate processes in their hosts, creating a suitable environment for invasion and proliferation. Yet, little is known about the host proteins that are targeted by effectors from filamentous pathogens. Here, we show that stable transgenic expression in potato (Solanum tuberosum) and transient expression in Nicotiana benthamiana of the arginine-any amino acid-leucine-arginine effector Pi17316 enhances leaf colonization by the late blight pathogen Phytophthora infestans Expression of Pi17316 also attenuates cell death triggered by the pathogen-associated molecular pattern Infestin1 (INF1), indicating that the effector suppresses pattern-triggered immunity. However, this effector does not attenuate cell death triggered by a range of resistance proteins, showing that it specifically suppresses INF1-triggered cell death (ICD). In yeast two-hybrid assays, Pi17316 interacts directly with the potato ortholog of VASCULAR HIGHWAY1-interacting kinase (StVIK), encoding a predicted MEK kinase (MAP3K). Interaction in planta was confirmed by coimmunoprecipitation and occurs at the plant plasma membrane. Virus-induced gene silencing of VIK in N. benthamiana attenuated P. infestans colonization, whereas transient overexpression of StVIK enhanced colonization, indicating that this host protein acts as a susceptibility factor. Moreover, VIK overexpression specifically attenuated ICD, indicating that it is a negative regulator of immunity. The abilities of Pi17316 to enhance P. infestans colonization or suppress ICD were compromised significantly in NbVIK-silenced plants, demonstrating that the effector activity of Pi17316 is mediated by this MAP3K. Thus, StVIK is exploited by P. infestans as a susceptibility factor to promote late blight disease.

DOI: 10.1104/pp.18.00028
PubMed: 29588335
PubMed Central: PMC5933144


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Le document en format XML

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RXLR Effector Pi17316 to Promote Disease.</title>
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<name sortKey="Murphy, Fraser" sort="Murphy, Fraser" uniqKey="Murphy F" first="Fraser" last="Murphy">Fraser Murphy</name>
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<name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name>
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<nlm:affiliation>Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China.</nlm:affiliation>
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<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070</wicri:regionArea>
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<country xml:lang="fr">République populaire de Chine</country>
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<title level="j">Plant physiology</title>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Cell Death (MeSH)</term>
<term>Cell Membrane (metabolism)</term>
<term>Green Fluorescent Proteins (metabolism)</term>
<term>Mitogen-Activated Protein Kinases (metabolism)</term>
<term>Phytophthora infestans (growth & development)</term>
<term>Phytophthora infestans (pathogenicity)</term>
<term>Phytophthora infestans (physiology)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Proteins (metabolism)</term>
<term>Protein Binding (MeSH)</term>
<term>Solanum tuberosum (enzymology)</term>
<term>Solanum tuberosum (microbiology)</term>
<term>Tobacco (microbiology)</term>
<term>Virulence (MeSH)</term>
<term>Virulence Factors (metabolism)</term>
</keywords>
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<term>Facteurs de virulence (métabolisme)</term>
<term>Liaison aux protéines (MeSH)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Membrane cellulaire (métabolisme)</term>
<term>Mitogen-Activated Protein Kinases (métabolisme)</term>
<term>Mort cellulaire (MeSH)</term>
<term>Phytophthora infestans (croissance et développement)</term>
<term>Phytophthora infestans (pathogénicité)</term>
<term>Phytophthora infestans (physiologie)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Protéines à fluorescence verte (métabolisme)</term>
<term>Solanum tuberosum (enzymologie)</term>
<term>Solanum tuberosum (microbiologie)</term>
<term>Tabac (microbiologie)</term>
<term>Virulence (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Green Fluorescent Proteins</term>
<term>Mitogen-Activated Protein Kinases</term>
<term>Plant Proteins</term>
<term>Virulence Factors</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Solanum tuberosum</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Solanum tuberosum</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cell Membrane</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladies des plantes</term>
<term>Solanum tuberosum</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
<term>Solanum tuberosum</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Facteurs de virulence</term>
<term>Membrane cellulaire</term>
<term>Mitogen-Activated Protein Kinases</term>
<term>Protéines végétales</term>
<term>Protéines à fluorescence verte</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Cell Death</term>
<term>Protein Binding</term>
<term>Virulence</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Liaison aux protéines</term>
<term>Mort cellulaire</term>
<term>Virulence</term>
</keywords>
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<front>
<div type="abstract" xml:lang="en">Plant pathogens deliver effectors to manipulate processes in their hosts, creating a suitable environment for invasion and proliferation. Yet, little is known about the host proteins that are targeted by effectors from filamentous pathogens. Here, we show that stable transgenic expression in potato (
<i>Solanum tuberosum</i>
) and transient expression in
<i>Nicotiana benthamiana</i>
of the arginine-any amino acid-leucine-arginine effector Pi17316 enhances leaf colonization by the late blight pathogen
<i>Phytophthora infestans</i>
Expression of Pi17316 also attenuates cell death triggered by the pathogen-associated molecular pattern Infestin1 (INF1), indicating that the effector suppresses pattern-triggered immunity. However, this effector does not attenuate cell death triggered by a range of resistance proteins, showing that it specifically suppresses INF1-triggered cell death (ICD). In yeast two-hybrid assays, Pi17316 interacts directly with the potato ortholog of VASCULAR HIGHWAY1-interacting kinase (StVIK), encoding a predicted MEK kinase (MAP3K). Interaction in planta was confirmed by coimmunoprecipitation and occurs at the plant plasma membrane. Virus-induced gene silencing of
<i>VIK</i>
in
<i>N. benthamiana</i>
attenuated
<i>P. infestans</i>
colonization, whereas transient overexpression of
<i>StVIK</i>
enhanced colonization, indicating that this host protein acts as a susceptibility factor. Moreover,
<i>VIK</i>
overexpression specifically attenuated ICD, indicating that it is a negative regulator of immunity. The abilities of Pi17316 to enhance
<i>P. infestans</i>
colonization or suppress ICD were compromised significantly in
<i>NbVIK</i>
-silenced plants, demonstrating that the effector activity of Pi17316 is mediated by this MAP3K. Thus, StVIK is exploited by
<i>P. infestans</i>
as a susceptibility factor to promote late blight disease.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">29588335</PMID>
<DateCompleted>
<Year>2019</Year>
<Month>01</Month>
<Day>25</Day>
</DateCompleted>
<DateRevised>
<Year>2019</Year>
<Month>01</Month>
<Day>25</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1532-2548</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>177</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2018</Year>
<Month>05</Month>
</PubDate>
</JournalIssue>
<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>The Potato MAP3K StVIK Is Required for the
<i>Phytophthora infestans</i>
RXLR Effector Pi17316 to Promote Disease.</ArticleTitle>
<Pagination>
<MedlinePgn>398-410</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.18.00028</ELocationID>
<Abstract>
<AbstractText>Plant pathogens deliver effectors to manipulate processes in their hosts, creating a suitable environment for invasion and proliferation. Yet, little is known about the host proteins that are targeted by effectors from filamentous pathogens. Here, we show that stable transgenic expression in potato (
<i>Solanum tuberosum</i>
) and transient expression in
<i>Nicotiana benthamiana</i>
of the arginine-any amino acid-leucine-arginine effector Pi17316 enhances leaf colonization by the late blight pathogen
<i>Phytophthora infestans</i>
Expression of Pi17316 also attenuates cell death triggered by the pathogen-associated molecular pattern Infestin1 (INF1), indicating that the effector suppresses pattern-triggered immunity. However, this effector does not attenuate cell death triggered by a range of resistance proteins, showing that it specifically suppresses INF1-triggered cell death (ICD). In yeast two-hybrid assays, Pi17316 interacts directly with the potato ortholog of VASCULAR HIGHWAY1-interacting kinase (StVIK), encoding a predicted MEK kinase (MAP3K). Interaction in planta was confirmed by coimmunoprecipitation and occurs at the plant plasma membrane. Virus-induced gene silencing of
<i>VIK</i>
in
<i>N. benthamiana</i>
attenuated
<i>P. infestans</i>
colonization, whereas transient overexpression of
<i>StVIK</i>
enhanced colonization, indicating that this host protein acts as a susceptibility factor. Moreover,
<i>VIK</i>
overexpression specifically attenuated ICD, indicating that it is a negative regulator of immunity. The abilities of Pi17316 to enhance
<i>P. infestans</i>
colonization or suppress ICD were compromised significantly in
<i>NbVIK</i>
-silenced plants, demonstrating that the effector activity of Pi17316 is mediated by this MAP3K. Thus, StVIK is exploited by
<i>P. infestans</i>
as a susceptibility factor to promote late blight disease.</AbstractText>
<CopyrightInformation>© 2018 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Murphy</LastName>
<ForeName>Fraser</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Division of Plant Science, University of Dundee (at James Hutton Institute), Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>He</LastName>
<ForeName>Qin</ForeName>
<Initials>Q</Initials>
<Identifier Source="ORCID">0000-0002-4957-2785</Identifier>
<AffiliationInfo>
<Affiliation>Division of Plant Science, University of Dundee (at James Hutton Institute), Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Armstrong</LastName>
<ForeName>Miles</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">0000-0002-9441-476X</Identifier>
<AffiliationInfo>
<Affiliation>Division of Plant Science, University of Dundee (at James Hutton Institute), Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Giuliani</LastName>
<ForeName>Licida M</ForeName>
<Initials>LM</Initials>
<Identifier Source="ORCID">0000-0001-6668-7501</Identifier>
<AffiliationInfo>
<Affiliation>Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Boevink</LastName>
<ForeName>Petra C</ForeName>
<Initials>PC</Initials>
<Identifier Source="ORCID">0000-0002-7021-9097</Identifier>
<AffiliationInfo>
<Affiliation>Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Wei</ForeName>
<Initials>W</Initials>
<Identifier Source="ORCID">0000-0003-2723-8257</Identifier>
<AffiliationInfo>
<Affiliation>Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tian</LastName>
<ForeName>Zhendong</ForeName>
<Initials>Z</Initials>
<Identifier Source="ORCID">0000-0002-3271-5372</Identifier>
<AffiliationInfo>
<Affiliation>Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture, Huazhong Agricultural University, Wuhan 430070, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Birch</LastName>
<ForeName>Paul R J</ForeName>
<Initials>PRJ</Initials>
<Identifier Source="ORCID">0000-0002-6559-3746</Identifier>
<AffiliationInfo>
<Affiliation>Division of Plant Science, University of Dundee (at James Hutton Institute), Invergowrie, Dundee DD2 5DA, United Kingdom p.birch@dundee.ac.uk eleanor.gilroy@hutton.ac.uk.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gilroy</LastName>
<ForeName>Eleanor M</ForeName>
<Initials>EM</Initials>
<Identifier Source="ORCID">0000-0002-5301-4268</Identifier>
<AffiliationInfo>
<Affiliation>Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom p.birch@dundee.ac.uk eleanor.gilroy@hutton.ac.uk.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>BB/G015244/1</GrantID>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
<Grant>
<GrantID>BB/L026880/1</GrantID>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
</GrantList>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2018</Year>
<Month>03</Month>
<Day>27</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Plant Physiol</MedlineTA>
<NlmUniqueID>0401224</NlmUniqueID>
<ISSNLinking>0032-0889</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D037521">Virulence Factors</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>147336-22-9</RegistryNumber>
<NameOfSubstance UI="D049452">Green Fluorescent Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 2.7.11.24</RegistryNumber>
<NameOfSubstance UI="D020928">Mitogen-Activated Protein Kinases</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D016923" MajorTopicYN="N">Cell Death</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D049452" MajorTopicYN="N">Green Fluorescent Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020928" MajorTopicYN="N">Mitogen-Activated Protein Kinases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055750" MajorTopicYN="N">Phytophthora infestans</DescriptorName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011198" MajorTopicYN="N">Solanum tuberosum</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014026" MajorTopicYN="N">Tobacco</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014774" MajorTopicYN="N">Virulence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D037521" MajorTopicYN="N">Virulence Factors</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2018</Year>
<Month>01</Month>
<Day>12</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2018</Year>
<Month>03</Month>
<Day>04</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2018</Year>
<Month>3</Month>
<Day>29</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="medline">
<Year>2019</Year>
<Month>1</Month>
<Day>27</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="entrez">
<Year>2018</Year>
<Month>3</Month>
<Day>29</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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