Serveur d'exploration Phytophthora

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Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen.

Identifieur interne : 000751 ( Main/Exploration ); précédent : 000750; suivant : 000752

Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen.

Auteurs : Yasin F. Dagdas [Royaume-Uni, Autriche] ; Pooja Pandey [Royaume-Uni] ; Yasin Tumtas [Royaume-Uni] ; Nattapong Sanguankiattichai [Royaume-Uni] ; Khaoula Belhaj [Royaume-Uni] ; Cian Duggan [Royaume-Uni] ; Alexandre Y. Leary [Royaume-Uni] ; Maria E. Segretin [Argentine] ; Mauricio P. Contreras [Royaume-Uni, Argentine] ; Zachary Savage [Royaume-Uni] ; Virendrasinh S. Khandare [Royaume-Uni] ; Sophien Kamoun [Royaume-Uni] ; Tolga O. Bozkurt [Royaume-Uni]

Source :

RBID : pubmed:29932422

Descripteurs français

English descriptors

Abstract

During plant cell invasion, the oomycete Phytophthora infestans remains enveloped by host-derived membranes whose functional properties are poorly understood. P. infestans secretes a myriad of effector proteins through these interfaces for plant colonization. Recently we showed that the effector protein PexRD54 reprograms host-selective autophagy by antagonising antimicrobial-autophagy receptor Joka2/NBR1 for ATG8CL binding (Dagdas et al., 2016). Here, we show that during infection, ATG8CL/Joka2 labelled defense-related autophagosomes are diverted toward the perimicrobial host membrane to restrict pathogen growth. PexRD54 also localizes to autophagosomes across the perimicrobial membrane, consistent with the view that the pathogen remodels host-microbe interface by co-opting the host autophagy machinery. Furthermore, we show that the host-pathogen interface is a hotspot for autophagosome biogenesis. Notably, overexpression of the early autophagosome biogenesis protein ATG9 enhances plant immunity. Our results implicate selective autophagy in polarized immune responses of plants and point to more complex functions for autophagy than the widely known degradative roles.

DOI: 10.7554/eLife.37476
PubMed: 29932422
PubMed Central: PMC6029844


Affiliations:


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Le document en format XML

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<term>ATPases Associated with Diverse Cellular Activities (genetics)</term>
<term>ATPases Associated with Diverse Cellular Activities (immunology)</term>
<term>Autophagosomes (immunology)</term>
<term>Autophagosomes (parasitology)</term>
<term>Autophagy (genetics)</term>
<term>Autophagy (immunology)</term>
<term>Autophagy-Related Protein 8 Family (genetics)</term>
<term>Autophagy-Related Protein 8 Family (immunology)</term>
<term>Carrier Proteins (genetics)</term>
<term>Carrier Proteins (immunology)</term>
<term>Gene Expression Regulation (MeSH)</term>
<term>Host-Pathogen Interactions (MeSH)</term>
<term>Membrane Proteins (genetics)</term>
<term>Membrane Proteins (immunology)</term>
<term>Phytophthora infestans (genetics)</term>
<term>Phytophthora infestans (growth & development)</term>
<term>Phytophthora infestans (pathogenicity)</term>
<term>Plant Cells (immunology)</term>
<term>Plant Cells (parasitology)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Diseases (parasitology)</term>
<term>Plant Immunity (genetics)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (immunology)</term>
<term>Protein Binding (MeSH)</term>
<term>Signal Transduction (MeSH)</term>
<term>Solanum tuberosum (genetics)</term>
<term>Solanum tuberosum (immunology)</term>
<term>Solanum tuberosum (parasitology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>ATPases associated with diverse cellular activities (génétique)</term>
<term>ATPases associated with diverse cellular activities (immunologie)</term>
<term>Autophagie (génétique)</term>
<term>Autophagie (immunologie)</term>
<term>Autophagosomes (immunologie)</term>
<term>Autophagosomes (parasitologie)</term>
<term>Cellules végétales (immunologie)</term>
<term>Cellules végétales (parasitologie)</term>
<term>Famille de la protéine-8 associée à l'autophagie (génétique)</term>
<term>Famille de la protéine-8 associée à l'autophagie (immunologie)</term>
<term>Immunité des plantes (génétique)</term>
<term>Interactions hôte-pathogène (MeSH)</term>
<term>Liaison aux protéines (MeSH)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (immunologie)</term>
<term>Maladies des plantes (parasitologie)</term>
<term>Phytophthora infestans (croissance et développement)</term>
<term>Phytophthora infestans (génétique)</term>
<term>Phytophthora infestans (pathogénicité)</term>
<term>Protéines de transport (génétique)</term>
<term>Protéines de transport (immunologie)</term>
<term>Protéines membranaires (génétique)</term>
<term>Protéines membranaires (immunologie)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (immunologie)</term>
<term>Régulation de l'expression des gènes (MeSH)</term>
<term>Solanum tuberosum (génétique)</term>
<term>Solanum tuberosum (immunologie)</term>
<term>Solanum tuberosum (parasitologie)</term>
<term>Transduction du signal (MeSH)</term>
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<term>ATPases Associated with Diverse Cellular Activities</term>
<term>Autophagy-Related Protein 8 Family</term>
<term>Carrier Proteins</term>
<term>Membrane Proteins</term>
<term>Plant Proteins</term>
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<term>ATPases Associated with Diverse Cellular Activities</term>
<term>Autophagy-Related Protein 8 Family</term>
<term>Carrier Proteins</term>
<term>Membrane Proteins</term>
<term>Plant Proteins</term>
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<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Autophagy</term>
<term>Phytophthora infestans</term>
<term>Plant Diseases</term>
<term>Plant Immunity</term>
<term>Solanum tuberosum</term>
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<term>Phytophthora infestans</term>
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<term>ATPases associated with diverse cellular activities</term>
<term>Autophagie</term>
<term>Famille de la protéine-8 associée à l'autophagie</term>
<term>Immunité des plantes</term>
<term>Maladies des plantes</term>
<term>Phytophthora infestans</term>
<term>Protéines de transport</term>
<term>Protéines membranaires</term>
<term>Protéines végétales</term>
<term>Solanum tuberosum</term>
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<term>ATPases associated with diverse cellular activities</term>
<term>Autophagie</term>
<term>Autophagosomes</term>
<term>Cellules végétales</term>
<term>Famille de la protéine-8 associée à l'autophagie</term>
<term>Maladies des plantes</term>
<term>Protéines de transport</term>
<term>Protéines membranaires</term>
<term>Protéines végétales</term>
<term>Solanum tuberosum</term>
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<term>Autophagosomes</term>
<term>Autophagy</term>
<term>Plant Cells</term>
<term>Plant Diseases</term>
<term>Solanum tuberosum</term>
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<term>Autophagosomes</term>
<term>Cellules végétales</term>
<term>Maladies des plantes</term>
<term>Solanum tuberosum</term>
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<term>Autophagosomes</term>
<term>Plant Cells</term>
<term>Plant Diseases</term>
<term>Solanum tuberosum</term>
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<term>Phytophthora infestans</term>
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<term>Phytophthora infestans</term>
</keywords>
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<term>Gene Expression Regulation</term>
<term>Host-Pathogen Interactions</term>
<term>Protein Binding</term>
<term>Signal Transduction</term>
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<term>Interactions hôte-pathogène</term>
<term>Liaison aux protéines</term>
<term>Régulation de l'expression des gènes</term>
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<front>
<div type="abstract" xml:lang="en">During plant cell invasion, the oomycete
<i>Phytophthora infestans</i>
remains enveloped by host-derived membranes whose functional properties are poorly understood.
<i>P. infestans</i>
secretes a myriad of effector proteins through these interfaces for plant colonization. Recently we showed that the effector protein PexRD54 reprograms host-selective autophagy by antagonising antimicrobial-autophagy receptor Joka2/NBR1 for ATG8CL binding (Dagdas et al., 2016). Here, we show that during infection, ATG8CL/Joka2 labelled defense-related autophagosomes are diverted toward the perimicrobial host membrane to restrict pathogen growth. PexRD54 also localizes to autophagosomes across the perimicrobial membrane, consistent with the view that the pathogen remodels host-microbe interface by co-opting the host autophagy machinery. Furthermore, we show that the host-pathogen interface is a hotspot for autophagosome biogenesis. Notably, overexpression of the early autophagosome biogenesis protein ATG9 enhances plant immunity. Our results implicate selective autophagy in polarized immune responses of plants and point to more complex functions for autophagy than the widely known degradative roles.</div>
</front>
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<DateCompleted>
<Year>2019</Year>
<Month>04</Month>
<Day>10</Day>
</DateCompleted>
<DateRevised>
<Year>2019</Year>
<Month>05</Month>
<Day>23</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">2050-084X</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>7</Volume>
<PubDate>
<Year>2018</Year>
<Month>06</Month>
<Day>22</Day>
</PubDate>
</JournalIssue>
<Title>eLife</Title>
<ISOAbbreviation>Elife</ISOAbbreviation>
</Journal>
<ArticleTitle>Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen.</ArticleTitle>
<ELocationID EIdType="doi" ValidYN="Y">10.7554/eLife.37476</ELocationID>
<ELocationID EIdType="pii" ValidYN="Y">e37476</ELocationID>
<Abstract>
<AbstractText>During plant cell invasion, the oomycete
<i>Phytophthora infestans</i>
remains enveloped by host-derived membranes whose functional properties are poorly understood.
<i>P. infestans</i>
secretes a myriad of effector proteins through these interfaces for plant colonization. Recently we showed that the effector protein PexRD54 reprograms host-selective autophagy by antagonising antimicrobial-autophagy receptor Joka2/NBR1 for ATG8CL binding (Dagdas et al., 2016). Here, we show that during infection, ATG8CL/Joka2 labelled defense-related autophagosomes are diverted toward the perimicrobial host membrane to restrict pathogen growth. PexRD54 also localizes to autophagosomes across the perimicrobial membrane, consistent with the view that the pathogen remodels host-microbe interface by co-opting the host autophagy machinery. Furthermore, we show that the host-pathogen interface is a hotspot for autophagosome biogenesis. Notably, overexpression of the early autophagosome biogenesis protein ATG9 enhances plant immunity. Our results implicate selective autophagy in polarized immune responses of plants and point to more complex functions for autophagy than the widely known degradative roles.</AbstractText>
<CopyrightInformation>© 2018, Dagdas et al.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y" EqualContrib="Y">
<LastName>Dagdas</LastName>
<ForeName>Yasin F</ForeName>
<Initials>YF</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-9502-355X</Identifier>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>The Gregor Mendel Institute of Molecular Plant Biology, Vienna Biocenter, Vienna, Austria.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y" EqualContrib="Y">
<LastName>Pandey</LastName>
<ForeName>Pooja</ForeName>
<Initials>P</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-3145-7794</Identifier>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tumtas</LastName>
<ForeName>Yasin</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sanguankiattichai</LastName>
<ForeName>Nattapong</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Belhaj</LastName>
<ForeName>Khaoula</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Duggan</LastName>
<ForeName>Cian</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Leary</LastName>
<ForeName>Alexandre Y</ForeName>
<Initials>AY</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-7223-3557</Identifier>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Segretin</LastName>
<ForeName>Maria E</ForeName>
<Initials>ME</Initials>
<AffiliationInfo>
<Affiliation>INGEBI-CONICET, Ciudad Autonoma de Buenos Aires, Buenos Aires, Argentina.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Contreras</LastName>
<ForeName>Mauricio P</ForeName>
<Initials>MP</Initials>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>INGEBI-CONICET, Ciudad Autonoma de Buenos Aires, Buenos Aires, Argentina.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Savage</LastName>
<ForeName>Zachary</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Khandare</LastName>
<ForeName>Virendrasinh S</ForeName>
<Initials>VS</Initials>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kamoun</LastName>
<ForeName>Sophien</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">https://orcid.org/0000-0002-0290-0315</Identifier>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Bozkurt</LastName>
<ForeName>Tolga O</ForeName>
<Initials>TO</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-0507-6875</Identifier>
<AffiliationInfo>
<Affiliation>Department of Life Sciences, Imperial College London, London, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>BB/M002462/1</GrantID>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<Year>2018</Year>
<Month>06</Month>
<Day>22</Day>
</ArticleDate>
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<Country>England</Country>
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<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000071182" MajorTopicYN="N">Autophagosomes</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001343" MajorTopicYN="N">Autophagy</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
</MeshHeading>
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<DescriptorName UI="D000071190" MajorTopicYN="N">Autophagy-Related Protein 8 Family</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
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<DescriptorName UI="D002352" MajorTopicYN="N">Carrier Proteins</DescriptorName>
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<DescriptorName UI="D005786" MajorTopicYN="N">Gene Expression Regulation</DescriptorName>
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<DescriptorName UI="D054884" MajorTopicYN="Y">Host-Pathogen Interactions</DescriptorName>
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<DescriptorName UI="D008565" MajorTopicYN="N">Membrane Proteins</DescriptorName>
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<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
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<MeshHeading>
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<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059828" MajorTopicYN="N">Plant Cells</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName>
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<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
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<Keyword MajorTopicYN="Y">RXLR Effector</Keyword>
<Keyword MajorTopicYN="Y">autophagosome</Keyword>
<Keyword MajorTopicYN="Y">cell biology</Keyword>
<Keyword MajorTopicYN="Y">defense-related autophagy</Keyword>
<Keyword MajorTopicYN="Y">effector biology</Keyword>
<Keyword MajorTopicYN="Y">haustoria</Keyword>
<Keyword MajorTopicYN="Y">nicotiana benthamiana</Keyword>
<Keyword MajorTopicYN="Y">phytophthora infestans</Keyword>
<Keyword MajorTopicYN="Y">plant biology</Keyword>
<Keyword MajorTopicYN="Y">plant immunity</Keyword>
<Keyword MajorTopicYN="Y">selective autophagy</Keyword>
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<CoiStatement>YD, PP, YT, NS, KB, CD, AL, MS, MC, ZS, SK, TB No competing interests declared</CoiStatement>
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