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The Verticillium-specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections.

Identifieur interne : 000906 ( Main/Exploration ); précédent : 000905; suivant : 000907

The Verticillium-specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections.

Auteurs : Lisha Zhang [République populaire de Chine, Allemagne] ; Hao Ni [République populaire de Chine] ; Xuan Du [République populaire de Chine] ; Sheng Wang [République populaire de Chine] ; Xiao-Wei Ma [République populaire de Chine] ; Thorsten Nürnberger [Allemagne] ; Hui-Shan Guo [République populaire de Chine] ; Chenlei Hua [République populaire de Chine, Allemagne]

Source :

RBID : pubmed:28407259

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English descriptors

Abstract

Fungal pathogens secrete effector proteins to suppress plant basal defense for successful colonization. Resistant plants, however, can recognize effectors by cognate R proteins to induce effector-triggered immunity (ETI). By analyzing secretomes of the vascular fungal pathogen Verticillium dahliae, we identified a novel secreted protein VdSCP7 that targets the plant nucleus. The green fluorescent protein (GFP)-tagged VdSCP7 gene with either a mutated nuclear localization signal motif or with additional nuclear export signal was transiently expressed in Nicotiana benthamiana, and investigated for induction of plant immunity. The role of VdSCP7 in V. dahliae pathogenicity was characterized by gene knockout and complementation, and GFP labeling. Expression of the VdSCP7 gene in N. benthamiana activated both salicylic acid and jasmonate signaling, and altered the plant's susceptibility to the pathogens Botrytis cinerea and Phytophthora capsici. The immune response activated by VdSCP7 was highly dependent on its initial extracellular secretion and subsequent nuclear localization in plants. Knockout of the VdSCP7 gene significantly enhanced V. dahliae aggressiveness on cotton. GFP-labeled VdSCP7 is secreted by V. dahliae and accumulates in the plant nucleus. We conclude that VdSCP7 is a novel effector protein that targets the host nucleus to modulate plant immunity, and suggest that plants can recognize VdSCP7 to activate ETI during fungal infection.

DOI: 10.1111/nph.14537
PubMed: 28407259


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<keywords scheme="KwdEn" xml:lang="en">
<term>Cell Nucleus (metabolism)</term>
<term>Fungal Proteins (analysis)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Fungal Proteins (physiology)</term>
<term>Gene Expression Regulation, Fungal (MeSH)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Immunity (MeSH)</term>
<term>Reactive Oxygen Species (metabolism)</term>
<term>Verticillium (metabolism)</term>
<term>Verticillium (pathogenicity)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Espèces réactives de l'oxygène (métabolisme)</term>
<term>Immunité des plantes (MeSH)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Noyau de la cellule (métabolisme)</term>
<term>Protéines fongiques (analyse)</term>
<term>Protéines fongiques (métabolisme)</term>
<term>Protéines fongiques (physiologie)</term>
<term>Régulation de l'expression des gènes fongiques (MeSH)</term>
<term>Verticillium (métabolisme)</term>
<term>Verticillium (pathogénicité)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="analysis" xml:lang="en">
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="analyse" xml:lang="fr">
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cell Nucleus</term>
<term>Fungal Proteins</term>
<term>Reactive Oxygen Species</term>
<term>Verticillium</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Espèces réactives de l'oxygène</term>
<term>Noyau de la cellule</term>
<term>Protéines fongiques</term>
<term>Verticillium</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Verticillium</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Verticillium</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="physiology" xml:lang="en">
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Expression Regulation, Fungal</term>
<term>Plant Immunity</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Immunité des plantes</term>
<term>Régulation de l'expression des gènes fongiques</term>
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<front>
<div type="abstract" xml:lang="en">Fungal pathogens secrete effector proteins to suppress plant basal defense for successful colonization. Resistant plants, however, can recognize effectors by cognate R proteins to induce effector-triggered immunity (ETI). By analyzing secretomes of the vascular fungal pathogen Verticillium dahliae, we identified a novel secreted protein VdSCP7 that targets the plant nucleus. The green fluorescent protein (GFP)-tagged VdSCP7 gene with either a mutated nuclear localization signal motif or with additional nuclear export signal was transiently expressed in Nicotiana benthamiana, and investigated for induction of plant immunity. The role of VdSCP7 in V. dahliae pathogenicity was characterized by gene knockout and complementation, and GFP labeling. Expression of the VdSCP7 gene in N. benthamiana activated both salicylic acid and jasmonate signaling, and altered the plant's susceptibility to the pathogens Botrytis cinerea and Phytophthora capsici. The immune response activated by VdSCP7 was highly dependent on its initial extracellular secretion and subsequent nuclear localization in plants. Knockout of the VdSCP7 gene significantly enhanced V. dahliae aggressiveness on cotton. GFP-labeled VdSCP7 is secreted by V. dahliae and accumulates in the plant nucleus. We conclude that VdSCP7 is a novel effector protein that targets the host nucleus to modulate plant immunity, and suggest that plants can recognize VdSCP7 to activate ETI during fungal infection.</div>
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<JournalIssue CitedMedium="Internet">
<Volume>215</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2017</Year>
<Month>Jul</Month>
</PubDate>
</JournalIssue>
<Title>The New phytologist</Title>
<ISOAbbreviation>New Phytol</ISOAbbreviation>
</Journal>
<ArticleTitle>The Verticillium-specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections.</ArticleTitle>
<Pagination>
<MedlinePgn>368-381</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.14537</ELocationID>
<Abstract>
<AbstractText>Fungal pathogens secrete effector proteins to suppress plant basal defense for successful colonization. Resistant plants, however, can recognize effectors by cognate R proteins to induce effector-triggered immunity (ETI). By analyzing secretomes of the vascular fungal pathogen Verticillium dahliae, we identified a novel secreted protein VdSCP7 that targets the plant nucleus. The green fluorescent protein (GFP)-tagged VdSCP7 gene with either a mutated nuclear localization signal motif or with additional nuclear export signal was transiently expressed in Nicotiana benthamiana, and investigated for induction of plant immunity. The role of VdSCP7 in V. dahliae pathogenicity was characterized by gene knockout and complementation, and GFP labeling. Expression of the VdSCP7 gene in N. benthamiana activated both salicylic acid and jasmonate signaling, and altered the plant's susceptibility to the pathogens Botrytis cinerea and Phytophthora capsici. The immune response activated by VdSCP7 was highly dependent on its initial extracellular secretion and subsequent nuclear localization in plants. Knockout of the VdSCP7 gene significantly enhanced V. dahliae aggressiveness on cotton. GFP-labeled VdSCP7 is secreted by V. dahliae and accumulates in the plant nucleus. We conclude that VdSCP7 is a novel effector protein that targets the host nucleus to modulate plant immunity, and suggest that plants can recognize VdSCP7 to activate ETI during fungal infection.</AbstractText>
<CopyrightInformation>© 2017 The Authors. New Phytologist © 2017 New Phytologist Trust.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Lisha</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Center of Plant Molecular Biology (ZMBP), Eberhard-Karls-University Tübingen, Tübingen, D-72076, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ni</LastName>
<ForeName>Hao</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100049, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Du</LastName>
<ForeName>Xuan</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100049, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Sheng</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100049, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ma</LastName>
<ForeName>Xiao-Wei</ForeName>
<Initials>XW</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100049, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Nürnberger</LastName>
<ForeName>Thorsten</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Center of Plant Molecular Biology (ZMBP), Eberhard-Karls-University Tübingen, Tübingen, D-72076, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Guo</LastName>
<ForeName>Hui-Shan</ForeName>
<Initials>HS</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>College of Life Sciences, University of the Chinese Academy of Sciences, Beijing, 100049, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hua</LastName>
<ForeName>Chenlei</ForeName>
<Initials>C</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-6630-9049</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Center of Plant Molecular Biology (ZMBP), Eberhard-Karls-University Tübingen, Tübingen, D-72076, Germany.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2017</Year>
<Month>04</Month>
<Day>13</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>New Phytol</MedlineTA>
<NlmUniqueID>9882884</NlmUniqueID>
<ISSNLinking>0028-646X</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D017382">Reactive Oxygen Species</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D002467" MajorTopicYN="N">Cell Nucleus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName>
<QualifierName UI="Q000032" MajorTopicYN="N">analysis</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015966" MajorTopicYN="N">Gene Expression Regulation, Fungal</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D057865" MajorTopicYN="N">Plant Immunity</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017382" MajorTopicYN="N">Reactive Oxygen Species</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020172" MajorTopicYN="N">Verticillium</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="Y">pathogenicity</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Gossypium hirsutum </Keyword>
<Keyword MajorTopicYN="N">Nicotiana benthamiana </Keyword>
<Keyword MajorTopicYN="N">Verticillium dahliae </Keyword>
<Keyword MajorTopicYN="N">effector</Keyword>
<Keyword MajorTopicYN="N">hypersensitive response</Keyword>
<Keyword MajorTopicYN="N">immunity</Keyword>
<Keyword MajorTopicYN="N">nuclear localization signal</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2017</Year>
<Month>01</Month>
<Day>12</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2017</Year>
<Month>02</Month>
<Day>21</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2017</Year>
<Month>4</Month>
<Day>14</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2018</Year>
<Month>5</Month>
<Day>2</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2017</Year>
<Month>4</Month>
<Day>14</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">28407259</ArticleId>
<ArticleId IdType="doi">10.1111/nph.14537</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>République populaire de Chine</li>
</country>
<region>
<li>Bade-Wurtemberg</li>
<li>District de Tübingen</li>
</region>
<settlement>
<li>Tübingen</li>
</settlement>
</list>
<tree>
<country name="République populaire de Chine">
<noRegion>
<name sortKey="Zhang, Lisha" sort="Zhang, Lisha" uniqKey="Zhang L" first="Lisha" last="Zhang">Lisha Zhang</name>
</noRegion>
<name sortKey="Du, Xuan" sort="Du, Xuan" uniqKey="Du X" first="Xuan" last="Du">Xuan Du</name>
<name sortKey="Du, Xuan" sort="Du, Xuan" uniqKey="Du X" first="Xuan" last="Du">Xuan Du</name>
<name sortKey="Guo, Hui Shan" sort="Guo, Hui Shan" uniqKey="Guo H" first="Hui-Shan" last="Guo">Hui-Shan Guo</name>
<name sortKey="Guo, Hui Shan" sort="Guo, Hui Shan" uniqKey="Guo H" first="Hui-Shan" last="Guo">Hui-Shan Guo</name>
<name sortKey="Hua, Chenlei" sort="Hua, Chenlei" uniqKey="Hua C" first="Chenlei" last="Hua">Chenlei Hua</name>
<name sortKey="Ma, Xiao Wei" sort="Ma, Xiao Wei" uniqKey="Ma X" first="Xiao-Wei" last="Ma">Xiao-Wei Ma</name>
<name sortKey="Ma, Xiao Wei" sort="Ma, Xiao Wei" uniqKey="Ma X" first="Xiao-Wei" last="Ma">Xiao-Wei Ma</name>
<name sortKey="Ni, Hao" sort="Ni, Hao" uniqKey="Ni H" first="Hao" last="Ni">Hao Ni</name>
<name sortKey="Ni, Hao" sort="Ni, Hao" uniqKey="Ni H" first="Hao" last="Ni">Hao Ni</name>
<name sortKey="Wang, Sheng" sort="Wang, Sheng" uniqKey="Wang S" first="Sheng" last="Wang">Sheng Wang</name>
<name sortKey="Wang, Sheng" sort="Wang, Sheng" uniqKey="Wang S" first="Sheng" last="Wang">Sheng Wang</name>
</country>
<country name="Allemagne">
<region name="Bade-Wurtemberg">
<name sortKey="Zhang, Lisha" sort="Zhang, Lisha" uniqKey="Zhang L" first="Lisha" last="Zhang">Lisha Zhang</name>
</region>
<name sortKey="Hua, Chenlei" sort="Hua, Chenlei" uniqKey="Hua C" first="Chenlei" last="Hua">Chenlei Hua</name>
<name sortKey="Nurnberger, Thorsten" sort="Nurnberger, Thorsten" uniqKey="Nurnberger T" first="Thorsten" last="Nürnberger">Thorsten Nürnberger</name>
</country>
</tree>
</affiliations>
</record>

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