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Phytophthora infestans RXLR Effectors Target Parallel Steps in an Immune Signal Transduction Pathway.

Identifieur interne : 000606 ( Main/Exploration ); précédent : 000605; suivant : 000607

Phytophthora infestans RXLR Effectors Target Parallel Steps in an Immune Signal Transduction Pathway.

Auteurs : Yajuan Ren [République populaire de Chine] ; Miles Armstrong [Royaume-Uni] ; Yetong Qi [République populaire de Chine] ; Hazel Mclellan ; Cheng Zhong [République populaire de Chine] ; Bowen Du [République populaire de Chine] ; Paul R J. Birch [Royaume-Uni] ; Zhendong Tian [République populaire de Chine]

Source :

RBID : pubmed:31217198

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English descriptors

Abstract

The potato (Solanum tuberosum) blight pathogen Phytophthora infestans delivers Arg-X-Leu-Arg (RXLR) effector proteins into host cells to subvert plant immune responses and promote colonization. We show that transient expression and stable transgenic expression of the RXLR effector Pi22926 in Nicotiana benthamiana promotes leaf colonization by P. infestans. Pi22926 suppresses cell death triggered by coexpression of the Cladosporium fulvum avirulence protein Avr4 and the tomato (Solanum lycopersicum) resistance protein Cf4. Pi22926 interacts with a potato mitogen-activated protein kinase kinase kinase, StMAP3Kβ2, in the nucleoplasm. Virus-induced gene silencing (VIGS) of the ortholog NbMAP3Kβ2 in N. benthamiana enhances P. infestans colonization and attenuates Cf4/Avr4-induced cell death, indicating that this host protein is a positive regulator of immunity. Cell death induced by Cf4/Avr4 is dependent on NbMAP3Kε and NbMAP3Kβ2, indicating that these MAP3Ks function in the same signaling pathway. VIGS of NbMAP3Kβ2 does not compromise cell death triggered by overexpression of MAP3Kε. Similarly, VIGS of NbMAP3Kε does not attenuate cell death triggered by MAP3Kβ2, demonstrating that these MAP3K proteins function in parallel. In agreement, Pi22926 or another RXLR effector, PexRD2, only suppresses cell death triggered by expression of StMAP3Kβ2 or StMAP3Kε, respectively. Our data reveal that two P. infestans effectors, PexRD2 and Pi22926, promote P. infestans colonization by targeting MAP3K proteins that act in parallel in the same signal transduction pathway.

DOI: 10.1104/pp.18.00625
PubMed: 31217198
PubMed Central: PMC6670088


Affiliations:


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Le document en format XML

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RXLR Effectors Target Parallel Steps in an Immune Signal Transduction Pathway.</title>
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RXLR Effectors Target Parallel Steps in an Immune Signal Transduction Pathway.</title>
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<term>Lycopersicon esculentum (microbiology)</term>
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<front>
<div type="abstract" xml:lang="en">The potato (
<i>Solanum tuberosum</i>
) blight pathogen
<i>Phytophthora infestans</i>
delivers Arg-X-Leu-Arg (RXLR) effector proteins into host cells to subvert plant immune responses and promote colonization. We show that transient expression and stable transgenic expression of the RXLR effector Pi22926 in
<i>Nicotiana benthamiana</i>
promotes leaf colonization by
<i>P. infestans.</i>
Pi22926 suppresses cell death triggered by coexpression of the
<i>Cladosporium fulvum</i>
avirulence protein Avr4 and the tomato (
<i>Solanum lycopersicum</i>
) resistance protein Cf4. Pi22926 interacts with a potato mitogen-activated protein kinase kinase kinase, StMAP3Kβ2, in the nucleoplasm. Virus-induced gene silencing (VIGS) of the ortholog
<i>NbMAP3Kβ2</i>
in
<i>N. benthamiana</i>
enhances
<i>P. infestans</i>
colonization and attenuates Cf4/Avr4-induced cell death, indicating that this host protein is a positive regulator of immunity. Cell death induced by Cf4/Avr4 is dependent on NbMAP3Kε and NbMAP3Kβ2, indicating that these MAP3Ks function in the same signaling pathway. VIGS of
<i>NbMAP3Kβ2</i>
does not compromise cell death triggered by overexpression of MAP3Kε. Similarly, VIGS of
<i>NbMAP3Kε</i>
does not attenuate cell death triggered by MAP3Kβ2, demonstrating that these MAP3K proteins function in parallel. In agreement, Pi22926 or another RXLR effector, PexRD2, only suppresses cell death triggered by expression of StMAP3Kβ2 or StMAP3Kε, respectively. Our data reveal that two
<i>P. infestans</i>
effectors, PexRD2 and Pi22926, promote
<i>P. infestans</i>
colonization by targeting MAP3K proteins that act in parallel in the same signal transduction pathway.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">31217198</PMID>
<DateCompleted>
<Year>2020</Year>
<Month>08</Month>
<Day>24</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>08</Month>
<Day>24</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1532-2548</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>180</Volume>
<Issue>4</Issue>
<PubDate>
<Year>2019</Year>
<Month>08</Month>
</PubDate>
</JournalIssue>
<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>
<i>Phytophthora infestans</i>
RXLR Effectors Target Parallel Steps in an Immune Signal Transduction Pathway.</ArticleTitle>
<Pagination>
<MedlinePgn>2227-2239</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.18.00625</ELocationID>
<Abstract>
<AbstractText>The potato (
<i>Solanum tuberosum</i>
) blight pathogen
<i>Phytophthora infestans</i>
delivers Arg-X-Leu-Arg (RXLR) effector proteins into host cells to subvert plant immune responses and promote colonization. We show that transient expression and stable transgenic expression of the RXLR effector Pi22926 in
<i>Nicotiana benthamiana</i>
promotes leaf colonization by
<i>P. infestans.</i>
Pi22926 suppresses cell death triggered by coexpression of the
<i>Cladosporium fulvum</i>
avirulence protein Avr4 and the tomato (
<i>Solanum lycopersicum</i>
) resistance protein Cf4. Pi22926 interacts with a potato mitogen-activated protein kinase kinase kinase, StMAP3Kβ2, in the nucleoplasm. Virus-induced gene silencing (VIGS) of the ortholog
<i>NbMAP3Kβ2</i>
in
<i>N. benthamiana</i>
enhances
<i>P. infestans</i>
colonization and attenuates Cf4/Avr4-induced cell death, indicating that this host protein is a positive regulator of immunity. Cell death induced by Cf4/Avr4 is dependent on NbMAP3Kε and NbMAP3Kβ2, indicating that these MAP3Ks function in the same signaling pathway. VIGS of
<i>NbMAP3Kβ2</i>
does not compromise cell death triggered by overexpression of MAP3Kε. Similarly, VIGS of
<i>NbMAP3Kε</i>
does not attenuate cell death triggered by MAP3Kβ2, demonstrating that these MAP3K proteins function in parallel. In agreement, Pi22926 or another RXLR effector, PexRD2, only suppresses cell death triggered by expression of StMAP3Kβ2 or StMAP3Kε, respectively. Our data reveal that two
<i>P. infestans</i>
effectors, PexRD2 and Pi22926, promote
<i>P. infestans</i>
colonization by targeting MAP3K proteins that act in parallel in the same signal transduction pathway.</AbstractText>
<CopyrightInformation>© 2019 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Ren</LastName>
<ForeName>Yajuan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University (HZAU), Wuhan 430070, People's Republic of China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of 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 Sciences, School of Life 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>Qi</LastName>
<ForeName>Yetong</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University (HZAU), Wuhan 430070, People's Republic of China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>McLellan</LastName>
<ForeName>Hazel</ForeName>
<Initials>H</Initials>
<Identifier Source="ORCID">0000-0003-4490-7053</Identifier>
</Author>
<Author ValidYN="Y">
<LastName>Zhong</LastName>
<ForeName>Cheng</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University (HZAU), Wuhan 430070, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Du</LastName>
<ForeName>Bowen</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University (HZAU), Wuhan 430070, People's Republic of China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of 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 Sciences, School of Life 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>Tian</LastName>
<ForeName>Zhendong</ForeName>
<Initials>Z</Initials>
<Identifier Source="ORCID">0000-0002-3271-5372</Identifier>
<AffiliationInfo>
<Affiliation>Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University (HZAU), Wuhan 430070, People's Republic of China tianzhd@mail.hzau.edu.cn.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>BB/G015244/1</GrantID>
<Acronym>BB_</Acronym>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
<Grant>
<GrantID>BB/L026880/1</GrantID>
<Acronym>BB_</Acronym>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
<Grant>
<GrantID>BB/K018183/1</GrantID>
<Acronym>BB_</Acronym>
<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>2019</Year>
<Month>06</Month>
<Day>19</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>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D016923" MajorTopicYN="N">Cell Death</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002467" MajorTopicYN="N">Cell Nucleus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018551" MajorTopicYN="N">Lycopersicon esculentum</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055750" MajorTopicYN="N">Phytophthora infestans</DescriptorName>
<QualifierName UI="Q000472" MajorTopicYN="Y">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D057865" MajorTopicYN="N">Plant Immunity</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014026" MajorTopicYN="N">Tobacco</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
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<Month>06</Month>
<Day>12</Day>
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<affiliations>
<list>
<country>
<li>Royaume-Uni</li>
<li>République populaire de Chine</li>
</country>
<region>
<li>Hubei</li>
</region>
<settlement>
<li>Wuhan</li>
</settlement>
</list>
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<noCountry>
<name sortKey="Mclellan, Hazel" sort="Mclellan, Hazel" uniqKey="Mclellan H" first="Hazel" last="Mclellan">Hazel Mclellan</name>
</noCountry>
<country name="République populaire de Chine">
<region name="Hubei">
<name sortKey="Ren, Yajuan" sort="Ren, Yajuan" uniqKey="Ren Y" first="Yajuan" last="Ren">Yajuan Ren</name>
</region>
<name sortKey="Du, Bowen" sort="Du, Bowen" uniqKey="Du B" first="Bowen" last="Du">Bowen Du</name>
<name sortKey="Du, Bowen" sort="Du, Bowen" uniqKey="Du B" first="Bowen" last="Du">Bowen Du</name>
<name sortKey="Qi, Yetong" sort="Qi, Yetong" uniqKey="Qi Y" first="Yetong" last="Qi">Yetong Qi</name>
<name sortKey="Qi, Yetong" sort="Qi, Yetong" uniqKey="Qi Y" first="Yetong" last="Qi">Yetong Qi</name>
<name sortKey="Ren, Yajuan" sort="Ren, Yajuan" uniqKey="Ren Y" first="Yajuan" last="Ren">Yajuan Ren</name>
<name sortKey="Tian, Zhendong" sort="Tian, Zhendong" uniqKey="Tian Z" first="Zhendong" last="Tian">Zhendong Tian</name>
<name sortKey="Tian, Zhendong" sort="Tian, Zhendong" uniqKey="Tian Z" first="Zhendong" last="Tian">Zhendong Tian</name>
<name sortKey="Zhong, Cheng" sort="Zhong, Cheng" uniqKey="Zhong C" first="Cheng" last="Zhong">Cheng Zhong</name>
</country>
<country name="Royaume-Uni">
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<name sortKey="Armstrong, Miles" sort="Armstrong, Miles" uniqKey="Armstrong M" first="Miles" last="Armstrong">Miles Armstrong</name>
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<name sortKey="Armstrong, Miles" sort="Armstrong, Miles" uniqKey="Armstrong M" first="Miles" last="Armstrong">Miles Armstrong</name>
<name sortKey="Birch, Paul R J" sort="Birch, Paul R J" uniqKey="Birch P" first="Paul R J" last="Birch">Paul R J. Birch</name>
<name sortKey="Birch, Paul R J" sort="Birch, Paul R J" uniqKey="Birch P" first="Paul R J" last="Birch">Paul R J. Birch</name>
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</record>

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