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Phytophthora infestans RXLR-WY Effector AVR3a Associates with Dynamin-Related Protein 2 Required for Endocytosis of the Plant Pattern Recognition Receptor FLS2.

Identifieur interne : 000D96 ( Main/Exploration ); précédent : 000D95; suivant : 000D97

Phytophthora infestans RXLR-WY Effector AVR3a Associates with Dynamin-Related Protein 2 Required for Endocytosis of the Plant Pattern Recognition Receptor FLS2.

Auteurs : Angela Chaparro-Garcia [Royaume-Uni] ; Simon Schwizer [Royaume-Uni] ; Jan Sklenar [Royaume-Uni] ; Kentaro Yoshida [Royaume-Uni] ; Benjamin Petre [Royaume-Uni] ; Jorunn I B. Bos [Royaume-Uni] ; Sebastian Schornack [Royaume-Uni] ; Alexandra M E. Jones [Royaume-Uni] ; Tolga O. Bozkurt [Royaume-Uni] ; Sophien Kamoun [Royaume-Uni]

Source :

RBID : pubmed:26348328

Descripteurs français

English descriptors

Abstract

Pathogens utilize effectors to suppress basal plant defense known as PTI (Pathogen-associated molecular pattern-triggered immunity). However, our knowledge of PTI suppression by filamentous plant pathogens, i.e. fungi and oomycetes, remains fragmentary. Previous work revealed that the co-receptor BAK1/SERK3 contributes to basal immunity against the potato pathogen Phytophthora infestans. Moreover BAK1/SERK3 is required for the cell death induced by P. infestans elicitin INF1, a protein with characteristics of PAMPs. The P. infestans host-translocated RXLR-WY effector AVR3a is known to supress INF1-mediated cell death by binding the plant E3 ligase CMPG1. In contrast, AVR3aKI-Y147del, a deletion mutant of the C-terminal tyrosine of AVR3a, fails to bind CMPG1 and does not suppress INF1-mediated cell death. Here, we studied the extent to which AVR3a and its variants perturb additional BAK1/SERK3-dependent PTI responses in N. benthamiana using the elicitor/receptor pair flg22/FLS2 as a model. We found that all tested variants of AVR3a suppress defense responses triggered by flg22 and reduce internalization of activated FLS2. Moreover, we discovered that AVR3a associates with the Dynamin-Related Protein 2 (DRP2), a plant GTPase implicated in receptor-mediated endocytosis. Interestingly, silencing of DRP2 impaired ligand-induced FLS2 internalization but did not affect internalization of the growth receptor BRI1. Our results suggest that AVR3a associates with a key cellular trafficking and membrane-remodeling complex involved in immune receptor-mediated endocytosis. We conclude that AVR3a is a multifunctional effector that can suppress BAK1/SERK3-mediated immunity through at least two different pathways.

DOI: 10.1371/journal.pone.0137071
PubMed: 26348328
PubMed Central: PMC4562647


Affiliations:


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Le document en format XML

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<term>Arabidopsis Proteins (immunology)</term>
<term>Arabidopsis Proteins (metabolism)</term>
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<term>Dynamins (immunology)</term>
<term>Dynamins (metabolism)</term>
<term>Endocytosis (immunology)</term>
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<term>Pathogen-Associated Molecular Pattern Molecules (metabolism)</term>
<term>Phytophthora infestans (genetics)</term>
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<term>Protein-Serine-Threonine Kinases (genetics)</term>
<term>Protein-Serine-Threonine Kinases (immunology)</term>
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<term>Dynamines (immunologie)</term>
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<term>Molécules contenant des motifs associés aux pathogènes (métabolisme)</term>
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<term>Phytophthora infestans (immunologie)</term>
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<term>Voies et réseaux métaboliques (MeSH)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
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<term>Arabidopsis</term>
<term>Arabidopsis Proteins</term>
<term>Dynamins</term>
<term>Endocytosis</term>
<term>Phytophthora infestans</term>
<term>Protein Kinases</term>
<term>Protein-Serine-Threonine Kinases</term>
<term>Tobacco</term>
<term>Virulence Factors</term>
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<term>Arabidopsis Proteins</term>
<term>Dynamins</term>
<term>Pathogen-Associated Molecular Pattern Molecules</term>
<term>Proteins</term>
<term>Ubiquitin-Protein Ligases</term>
<term>Virulence Factors</term>
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<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Arabidopsis</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Arabidopsis</term>
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<term>Protéines</term>
<term>Protéines d'Arabidopsis</term>
<term>Ubiquitin-protein ligases</term>
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<term>Plants, Genetically Modified</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Voies et réseaux métaboliques</term>
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<div type="abstract" xml:lang="en">Pathogens utilize effectors to suppress basal plant defense known as PTI (Pathogen-associated molecular pattern-triggered immunity). However, our knowledge of PTI suppression by filamentous plant pathogens, i.e. fungi and oomycetes, remains fragmentary. Previous work revealed that the co-receptor BAK1/SERK3 contributes to basal immunity against the potato pathogen Phytophthora infestans. Moreover BAK1/SERK3 is required for the cell death induced by P. infestans elicitin INF1, a protein with characteristics of PAMPs. The P. infestans host-translocated RXLR-WY effector AVR3a is known to supress INF1-mediated cell death by binding the plant E3 ligase CMPG1. In contrast, AVR3aKI-Y147del, a deletion mutant of the C-terminal tyrosine of AVR3a, fails to bind CMPG1 and does not suppress INF1-mediated cell death. Here, we studied the extent to which AVR3a and its variants perturb additional BAK1/SERK3-dependent PTI responses in N. benthamiana using the elicitor/receptor pair flg22/FLS2 as a model. We found that all tested variants of AVR3a suppress defense responses triggered by flg22 and reduce internalization of activated FLS2. Moreover, we discovered that AVR3a associates with the Dynamin-Related Protein 2 (DRP2), a plant GTPase implicated in receptor-mediated endocytosis. Interestingly, silencing of DRP2 impaired ligand-induced FLS2 internalization but did not affect internalization of the growth receptor BRI1. Our results suggest that AVR3a associates with a key cellular trafficking and membrane-remodeling complex involved in immune receptor-mediated endocytosis. We conclude that AVR3a is a multifunctional effector that can suppress BAK1/SERK3-mediated immunity through at least two different pathways. </div>
</front>
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<Abstract>
<AbstractText>Pathogens utilize effectors to suppress basal plant defense known as PTI (Pathogen-associated molecular pattern-triggered immunity). However, our knowledge of PTI suppression by filamentous plant pathogens, i.e. fungi and oomycetes, remains fragmentary. Previous work revealed that the co-receptor BAK1/SERK3 contributes to basal immunity against the potato pathogen Phytophthora infestans. Moreover BAK1/SERK3 is required for the cell death induced by P. infestans elicitin INF1, a protein with characteristics of PAMPs. The P. infestans host-translocated RXLR-WY effector AVR3a is known to supress INF1-mediated cell death by binding the plant E3 ligase CMPG1. In contrast, AVR3aKI-Y147del, a deletion mutant of the C-terminal tyrosine of AVR3a, fails to bind CMPG1 and does not suppress INF1-mediated cell death. Here, we studied the extent to which AVR3a and its variants perturb additional BAK1/SERK3-dependent PTI responses in N. benthamiana using the elicitor/receptor pair flg22/FLS2 as a model. We found that all tested variants of AVR3a suppress defense responses triggered by flg22 and reduce internalization of activated FLS2. Moreover, we discovered that AVR3a associates with the Dynamin-Related Protein 2 (DRP2), a plant GTPase implicated in receptor-mediated endocytosis. Interestingly, silencing of DRP2 impaired ligand-induced FLS2 internalization but did not affect internalization of the growth receptor BRI1. Our results suggest that AVR3a associates with a key cellular trafficking and membrane-remodeling complex involved in immune receptor-mediated endocytosis. We conclude that AVR3a is a multifunctional effector that can suppress BAK1/SERK3-mediated immunity through at least two different pathways. </AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Chaparro-Garcia</LastName>
<ForeName>Angela</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schwizer</LastName>
<ForeName>Simon</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sklenar</LastName>
<ForeName>Jan</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yoshida</LastName>
<ForeName>Kentaro</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Petre</LastName>
<ForeName>Benjamin</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bos</LastName>
<ForeName>Jorunn I B</ForeName>
<Initials>JI</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schornack</LastName>
<ForeName>Sebastian</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Jones</LastName>
<ForeName>Alexandra M E</ForeName>
<Initials>AM</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Bozkurt</LastName>
<ForeName>Tolga O</ForeName>
<Initials>TO</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kamoun</LastName>
<ForeName>Sophien</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
</GrantList>
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<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2015</Year>
<Month>09</Month>
<Day>08</Day>
</ArticleDate>
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<Country>United States</Country>
<MedlineTA>PLoS One</MedlineTA>
<NlmUniqueID>101285081</NlmUniqueID>
<ISSNLinking>1932-6203</ISSNLinking>
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<NameOfSubstance UI="C562170">AVR3a protein, Phytophthora infestans</NameOfSubstance>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D029681">Arabidopsis Proteins</NameOfSubstance>
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<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D037521">Virulence Factors</NameOfSubstance>
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<Chemical>
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<NameOfSubstance UI="C085101">elicitin, Phytophthora</NameOfSubstance>
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<Chemical>
<RegistryNumber>EC 2.3.2.27</RegistryNumber>
<NameOfSubstance UI="D044767">Ubiquitin-Protein Ligases</NameOfSubstance>
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<Chemical>
<RegistryNumber>EC 2.7.-</RegistryNumber>
<NameOfSubstance UI="D011494">Protein Kinases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 2.7.1.-</RegistryNumber>
<NameOfSubstance UI="C463660">BAK1 protein, Arabidopsis</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 2.7.1.-</RegistryNumber>
<NameOfSubstance UI="C411853">FLS2 protein, Arabidopsis</NameOfSubstance>
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<Chemical>
<RegistryNumber>EC 2.7.11.1</RegistryNumber>
<NameOfSubstance UI="D017346">Protein-Serine-Threonine Kinases</NameOfSubstance>
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<Chemical>
<RegistryNumber>EC 3.6.1.-</RegistryNumber>
<NameOfSubstance UI="C434467">ADL6 protein, Arabidopsis</NameOfSubstance>
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<RegistryNumber>EC 3.6.5.5</RegistryNumber>
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<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
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<DescriptorName UI="D029681" MajorTopicYN="N">Arabidopsis Proteins</DescriptorName>
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<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
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<DescriptorName UI="D016923" MajorTopicYN="N">Cell Death</DescriptorName>
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<DescriptorName UI="D034281" MajorTopicYN="N">Dynamins</DescriptorName>
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<DescriptorName UI="D053858" MajorTopicYN="N">Metabolic Networks and Pathways</DescriptorName>
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<DescriptorName UI="D000069452" MajorTopicYN="N">Pathogen-Associated Molecular Pattern Molecules</DescriptorName>
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<DescriptorName UI="D057865" MajorTopicYN="N">Plant Immunity</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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<DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName>
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<DescriptorName UI="D011494" MajorTopicYN="N">Protein Kinases</DescriptorName>
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<DescriptorName UI="D017346" MajorTopicYN="N">Protein-Serine-Threonine Kinases</DescriptorName>
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<DescriptorName UI="D011506" MajorTopicYN="N">Proteins</DescriptorName>
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<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
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<DescriptorName UI="D044767" MajorTopicYN="N">Ubiquitin-Protein Ligases</DescriptorName>
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