Phytonematode peptide effectors exploit a host post-translational trafficking mechanism to the ER using a novel translocation signal.
Identifieur interne : 000083 ( Main/Exploration ); précédent : 000082; suivant : 000084Phytonematode peptide effectors exploit a host post-translational trafficking mechanism to the ER using a novel translocation signal.
Auteurs : Jianying Wang [États-Unis] ; Andi Dhroso [États-Unis] ; Xunliang Liu [États-Unis] ; Thomas J. Baum [États-Unis] ; Richard S. Hussey [États-Unis] ; Eric L. Davis [États-Unis] ; Xiaohong Wang [États-Unis] ; Dmitry Korkin [États-Unis] ; Melissa G. Mitchum [États-Unis]Source :
- The New phytologist [ 1469-8137 ] ; 2020.
Abstract
Cyst nematodes induce a multicellular feeding site within roots called a syncytium. It remains unknown how root cells are primed for incorporation into the developing syncytium. Furthermore, it is unclear how CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide effectors secreted into the cytoplasm of the initial feeding cell could have an effect on plant cells so distant from where the nematode is feeding as the syncytium expands. Here we describe a novel translocation signal within nematode CLE effectors that is recognized by plant cell secretory machinery to redirect these peptides from the cytoplasm to the apoplast of plant cells. We show that the translocation signal is functionally conserved across CLE effectors identified in nematode species spanning three genera and multiple plant species, operative across plant cell types, and can traffic other unrelated small peptides from the cytoplasm to the apoplast of host cells via a previously unknown post-translational mechanism of endoplasmic reticulum (ER) translocation. Our results uncover a mechanism of effector trafficking that is unprecedented in any plant pathogen to date, andthey illustrate how phytonematodes can deliver effector proteins into host cells and then hijack plant cellular processes for their export back out of the cell to function as external signaling molecules to distant cells.
DOI: 10.1111/nph.16765
PubMed: 32569394
Affiliations:
- États-Unis
- Iowa, État de New York
- Ames (Iowa), Ithaca (New York)
- Université Cornell, Université d'État de l'Iowa
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Holley Center for Agriculture and Health, US Department of Agriculture, Agricultural Research Service and School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853</wicri:regionArea><orgName type="university">Université Cornell</orgName><placeName><settlement type="city">Ithaca (New York)</settlement><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Korkin, Dmitry" sort="Korkin, Dmitry" uniqKey="Korkin D" first="Dmitry" last="Korkin">Dmitry Korkin</name><affiliation wicri:level="1"><nlm:affiliation>Department of Computer Science and Bioinformatics and Computational Biology Program, Worcester Polytechnic Institute, Worcester, MA, 01609, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Computer Science and Bioinformatics and Computational Biology Program, Worcester Polytechnic Institute, Worcester, MA, 01609</wicri:regionArea><wicri:noRegion>01609</wicri:noRegion></affiliation></author><author><name sortKey="Mitchum, Melissa G" sort="Mitchum, Melissa G" uniqKey="Mitchum M" first="Melissa G" last="Mitchum">Melissa G. Mitchum</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology and Institute of Plant Breeding, Genetics, and Genomics, Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology and Institute of Plant Breeding, Genetics, and Genomics, Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602</wicri:regionArea><wicri:noRegion>30602</wicri:noRegion></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Cyst nematodes induce a multicellular feeding site within roots called a syncytium. It remains unknown how root cells are primed for incorporation into the developing syncytium. Furthermore, it is unclear how CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide effectors secreted into the cytoplasm of the initial feeding cell could have an effect on plant cells so distant from where the nematode is feeding as the syncytium expands. Here we describe a novel translocation signal within nematode CLE effectors that is recognized by plant cell secretory machinery to redirect these peptides from the cytoplasm to the apoplast of plant cells. We show that the translocation signal is functionally conserved across CLE effectors identified in nematode species spanning three genera and multiple plant species, operative across plant cell types, and can traffic other unrelated small peptides from the cytoplasm to the apoplast of host cells via a previously unknown post-translational mechanism of endoplasmic reticulum (ER) translocation. Our results uncover a mechanism of effector trafficking that is unprecedented in any plant pathogen to date, andthey illustrate how phytonematodes can deliver effector proteins into host cells and then hijack plant cellular processes for their export back out of the cell to function as external signaling molecules to distant cells.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32569394</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Jun</Month><Day>22</Day></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Phytonematode peptide effectors exploit a host post-translational trafficking mechanism to the ER using a novel translocation signal.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16765</ELocationID><Abstract><AbstractText>Cyst nematodes induce a multicellular feeding site within roots called a syncytium. It remains unknown how root cells are primed for incorporation into the developing syncytium. Furthermore, it is unclear how CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide effectors secreted into the cytoplasm of the initial feeding cell could have an effect on plant cells so distant from where the nematode is feeding as the syncytium expands. Here we describe a novel translocation signal within nematode CLE effectors that is recognized by plant cell secretory machinery to redirect these peptides from the cytoplasm to the apoplast of plant cells. We show that the translocation signal is functionally conserved across CLE effectors identified in nematode species spanning three genera and multiple plant species, operative across plant cell types, and can traffic other unrelated small peptides from the cytoplasm to the apoplast of host cells via a previously unknown post-translational mechanism of endoplasmic reticulum (ER) translocation. Our results uncover a mechanism of effector trafficking that is unprecedented in any plant pathogen to date, andthey illustrate how phytonematodes can deliver effector proteins into host cells and then hijack plant cellular processes for their export back out of the cell to function as external signaling molecules to distant cells.</AbstractText><CopyrightInformation>© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Jianying</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-4991-8328</Identifier><AffiliationInfo><Affiliation>Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dhroso</LastName><ForeName>Andi</ForeName><Initials>A</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-6117-0607</Identifier><AffiliationInfo><Affiliation>Department of Computer Science and Bioinformatics and Computational Biology Program, Worcester Polytechnic Institute, Worcester, MA, 01609, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Xunliang</ForeName><Initials>X</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-0445-0343</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology and Institute of Plant Breeding, Genetics, and Genomics, Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baum</LastName><ForeName>Thomas J</ForeName><Initials>TJ</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-9241-3141</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hussey</LastName><ForeName>Richard S</ForeName><Initials>RS</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-2293-6067</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology, University of Georgia, Athens, GA, 30602, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Davis</LastName><ForeName>Eric L</ForeName><Initials>EL</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-8025-3742</Identifier><AffiliationInfo><Affiliation>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Xiaohong</ForeName><Initials>X</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-1790-4084</Identifier><AffiliationInfo><Affiliation>Robert W. Holley Center for Agriculture and Health, US Department of Agriculture, Agricultural Research Service and School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Korkin</LastName><ForeName>Dmitry</ForeName><Initials>D</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-3875-9085</Identifier><AffiliationInfo><Affiliation>Department of Computer Science and Bioinformatics and Computational Biology Program, Worcester Polytechnic Institute, Worcester, MA, 01609, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mitchum</LastName><ForeName>Melissa G</ForeName><Initials>MG</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-9086-6312</Identifier><AffiliationInfo><Affiliation>Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Pathology and Institute of Plant Breeding, Genetics, and Genomics, Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>2009-35302-05304</GrantID><Agency>USDA-NIFA-AFRI</Agency><Country></Country></Grant><Grant><GrantID>2012-67013-19345</GrantID><Agency>USDA-NIFA-AFRI</Agency><Country></Country></Grant><Grant><GrantID>2015-67013-23511</GrantID><Agency>USDA-NIFA-AFRI</Agency><Country></Country></Grant><Grant><GrantID>IOS-1456047</GrantID><Agency>National Science Foundation</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Globodera
</Keyword><Keyword MajorTopicYN="N">Heterodera
</Keyword><Keyword MajorTopicYN="N">CLAVATA3/ESR (CLE)</Keyword><Keyword MajorTopicYN="N">cyst nematode</Keyword><Keyword MajorTopicYN="N">effector</Keyword><Keyword MajorTopicYN="N">endoplasmic reticulum (ER) secretory pathway</Keyword><Keyword MajorTopicYN="N">peptide signaling</Keyword><Keyword MajorTopicYN="N">syncytium</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>05</Month><Day>14</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>6</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>6</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>6</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32569394</ArticleId><ArticleId IdType="doi">10.1111/nph.16765</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Alenda C, Gallot-LeGrand A, Fouville D, Grenier E. 2013. 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Davis</name><name sortKey="Dhroso, Andi" sort="Dhroso, Andi" uniqKey="Dhroso A" first="Andi" last="Dhroso">Andi Dhroso</name><name sortKey="Hussey, Richard S" sort="Hussey, Richard S" uniqKey="Hussey R" first="Richard S" last="Hussey">Richard S. Hussey</name><name sortKey="Korkin, Dmitry" sort="Korkin, Dmitry" uniqKey="Korkin D" first="Dmitry" last="Korkin">Dmitry Korkin</name><name sortKey="Liu, Xunliang" sort="Liu, Xunliang" uniqKey="Liu X" first="Xunliang" last="Liu">Xunliang Liu</name><name sortKey="Mitchum, Melissa G" sort="Mitchum, Melissa G" uniqKey="Mitchum M" first="Melissa G" last="Mitchum">Melissa G. Mitchum</name><name sortKey="Mitchum, Melissa G" sort="Mitchum, Melissa G" uniqKey="Mitchum M" first="Melissa G" last="Mitchum">Melissa G. Mitchum</name><name sortKey="Wang, Xiaohong" sort="Wang, Xiaohong" uniqKey="Wang X" first="Xiaohong" last="Wang">Xiaohong Wang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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