Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization.
Identifieur interne : 000212 ( Main/Exploration ); précédent : 000211; suivant : 000213Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization.
Auteurs : Romain Castilleux [France] ; Barbara Plancot [France] ; Bruno Gügi [France] ; Agnès Attard [France] ; Corinne Loutelier-Bourhis [France] ; Benjamin Lefranc [France] ; Eric Nguema-Ona [France] ; Mustapha Arkoun [France] ; Jean-Claude Yvin [France] ; Azeddine Driouich [France] ; Maïté Vicré [France]Source :
- Annals of botany [ 1095-8290 ] ; 2020.
Descripteurs français
- KwdFr :
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical : Glycoproteins, Plant Proteins.
- Arabidopsis, Cell Wall, Oomycetes.
Abstract
BACKGROUND AND AIMS
Extensins are hydroxyproline-rich glycoproteins thought to strengthen the plant cell wall, one of the first barriers against pathogens, through intra- and intermolecular cross-links. The glycan moiety of extensins is believed to confer the correct structural conformation to the glycoprotein, leading to self-assembly within the cell wall that helps limit microbial adherence and invasion. However, this role is not clearly established.
METHODS
We used Arabidopsis thaliana mutants impaired in extensin arabinosylation to investigate the role of extensin arabinosylation in root-microbe interactions. Mutant and wild-type roots were stimulated to elicit an immune response with flagellin 22 and immunolabelled with a set of anti-extensin antibodies. Roots were also inoculated with a soilborne oomycete, Phytophthora parasitica, to assess the effect of extensin arabinosylation on root colonization.
KEY RESULTS
A differential distribution of extensin epitopes was observed in wild-type plants in response to elicitation. Elicitation also triggers altered epitope expression in mutant roots compared with wild-type and non-elicited roots. Inoculation with the pathogen P. parasitica resulted in enhanced root colonization for two mutants, specifically xeg113 and rra2.
CONCLUSIONS
We provide evidence for a link between extensin arabinosylation and root defence, and propose a model to explain the importance of glycosylation in limiting invasion of root cells by pathogenic oomycetes.
DOI: 10.1093/aob/mcz068
PubMed: 31242281
PubMed Central: PMC7182588
Affiliations:
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region">Haute-Normandie</region><settlement type="city">Rouen</settlement></placeName></affiliation></author><author><name sortKey="Nguema Ona, Eric" sort="Nguema Ona, Eric" uniqKey="Nguema Ona E" first="Eric" last="Nguema-Ona">Eric Nguema-Ona</name><affiliation wicri:level="1"><nlm:affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex</wicri:regionArea><wicri:noRegion>Saint Malo Cédex</wicri:noRegion><wicri:noRegion>Saint Malo Cédex</wicri:noRegion></affiliation></author><author><name sortKey="Arkoun, Mustapha" sort="Arkoun, Mustapha" uniqKey="Arkoun M" first="Mustapha" last="Arkoun">Mustapha Arkoun</name><affiliation wicri:level="1"><nlm:affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre Mondial de 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uniqKey="Castilleux R" first="Romain" last="Castilleux">Romain Castilleux</name><affiliation wicri:level="3"><nlm:affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen</wicri:regionArea><placeName><region type="region">Région Normandie</region><region type="old region">Haute-Normandie</region><settlement type="city">Rouen</settlement></placeName></affiliation></author><author><name sortKey="Plancot, Barbara" sort="Plancot, Barbara" uniqKey="Plancot B" first="Barbara" last="Plancot">Barbara Plancot</name><affiliation wicri:level="3"><nlm:affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen</wicri:regionArea><placeName><region type="region">Région Normandie</region><region type="old region">Haute-Normandie</region><settlement type="city">Rouen</settlement></placeName></affiliation></author><author><name sortKey="Gugi, Bruno" sort="Gugi, Bruno" uniqKey="Gugi B" first="Bruno" last="Gügi">Bruno Gügi</name><affiliation wicri:level="3"><nlm:affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen</wicri:regionArea><placeName><region type="region">Région Normandie</region><region type="old region">Haute-Normandie</region><settlement type="city">Rouen</settlement></placeName></affiliation></author><author><name sortKey="Attard, Agnes" sort="Attard, Agnes" uniqKey="Attard A" first="Agnès" last="Attard">Agnès Attard</name><affiliation wicri:level="1"><nlm:affiliation>INRA, CNRS, Université Côte d'Azur, ISA, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA, CNRS, Université Côte d'Azur, ISA</wicri:regionArea><wicri:noRegion>ISA</wicri:noRegion><wicri:noRegion>ISA</wicri:noRegion></affiliation></author><author><name sortKey="Loutelier Bourhis, Corinne" sort="Loutelier Bourhis, Corinne" uniqKey="Loutelier Bourhis C" first="Corinne" last="Loutelier-Bourhis">Corinne Loutelier-Bourhis</name><affiliation wicri:level="1"><nlm:affiliation>IRCOF COBRA, UMR6014 and FR3038, CNRS, Université de Rouen Normandie, Mont-Saint-Aignan Cedex, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>IRCOF COBRA, UMR6014 and FR3038, CNRS, Université de Rouen Normandie, Mont-Saint-Aignan Cedex</wicri:regionArea><wicri:noRegion>Mont-Saint-Aignan Cedex</wicri:noRegion><wicri:noRegion>Mont-Saint-Aignan Cedex</wicri:noRegion></affiliation></author><author><name sortKey="Lefranc, Benjamin" sort="Lefranc, Benjamin" uniqKey="Lefranc B" first="Benjamin" last="Lefranc">Benjamin Lefranc</name><affiliation wicri:level="3"><nlm:affiliation>INSERM U1239, Différenciation et Communication Neuronale et Neuroendocrine, Normandie Université, Rouen, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INSERM U1239, Différenciation et Communication Neuronale et Neuroendocrine, Normandie Université, Rouen</wicri:regionArea><placeName><region type="region">Région Normandie</region><region type="old region">Haute-Normandie</region><settlement type="city">Rouen</settlement></placeName></affiliation></author><author><name sortKey="Nguema Ona, Eric" sort="Nguema Ona, Eric" uniqKey="Nguema Ona E" first="Eric" last="Nguema-Ona">Eric Nguema-Ona</name><affiliation wicri:level="1"><nlm:affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex</wicri:regionArea><wicri:noRegion>Saint Malo Cédex</wicri:noRegion><wicri:noRegion>Saint Malo Cédex</wicri:noRegion></affiliation></author><author><name sortKey="Arkoun, Mustapha" sort="Arkoun, Mustapha" uniqKey="Arkoun M" first="Mustapha" last="Arkoun">Mustapha Arkoun</name><affiliation wicri:level="1"><nlm:affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex</wicri:regionArea><wicri:noRegion>Saint Malo Cédex</wicri:noRegion><wicri:noRegion>Saint Malo Cédex</wicri:noRegion></affiliation></author><author><name sortKey="Yvin, Jean Claude" sort="Yvin, Jean Claude" uniqKey="Yvin J" first="Jean-Claude" last="Yvin">Jean-Claude Yvin</name><affiliation wicri:level="1"><nlm:affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex</wicri:regionArea><wicri:noRegion>Saint Malo Cédex</wicri:noRegion><wicri:noRegion>Saint Malo Cédex</wicri:noRegion></affiliation></author><author><name sortKey="Driouich, Azeddine" sort="Driouich, Azeddine" uniqKey="Driouich A" first="Azeddine" last="Driouich">Azeddine Driouich</name><affiliation wicri:level="3"><nlm:affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen</wicri:regionArea><placeName><region type="region">Région Normandie</region><region type="old region">Haute-Normandie</region><settlement type="city">Rouen</settlement></placeName></affiliation></author><author><name sortKey="Vicre, Maite" sort="Vicre, Maite" uniqKey="Vicre M" first="Maïté" last="Vicré">Maïté Vicré</name><affiliation wicri:level="3"><nlm:affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen</wicri:regionArea><placeName><region type="region">Région Normandie</region><region type="old region">Haute-Normandie</region><settlement type="city">Rouen</settlement></placeName></affiliation></author></analytic><series><title level="j">Annals of botany</title><idno type="eISSN">1095-8290</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Arabidopsis (MeSH)</term><term>Cell Wall (MeSH)</term><term>Glycoproteins (MeSH)</term><term>Oomycetes (MeSH)</term><term>Plant Proteins (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Arabidopsis (MeSH)</term><term>Glycoprotéines (MeSH)</term><term>Oomycetes (MeSH)</term><term>Paroi cellulaire (MeSH)</term><term>Protéines végétales (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" xml:lang="en"><term>Glycoproteins</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Arabidopsis</term><term>Cell Wall</term><term>Oomycetes</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Arabidopsis</term><term>Glycoprotéines</term><term>Oomycetes</term><term>Paroi cellulaire</term><term>Protéines végétales</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND AND AIMS</b></p><p>Extensins are hydroxyproline-rich glycoproteins thought to strengthen the plant cell wall, one of the first barriers against pathogens, through intra- and intermolecular cross-links. The glycan moiety of extensins is believed to confer the correct structural conformation to the glycoprotein, leading to self-assembly within the cell wall that helps limit microbial adherence and invasion. However, this role is not clearly established.</p></div><div type="abstract" xml:lang="en"><p><b>METHODS</b></p><p>We used Arabidopsis thaliana mutants impaired in extensin arabinosylation to investigate the role of extensin arabinosylation in root-microbe interactions. Mutant and wild-type roots were stimulated to elicit an immune response with flagellin 22 and immunolabelled with a set of anti-extensin antibodies. Roots were also inoculated with a soilborne oomycete, Phytophthora parasitica, to assess the effect of extensin arabinosylation on root colonization.</p></div><div type="abstract" xml:lang="en"><p><b>KEY RESULTS</b></p><p>A differential distribution of extensin epitopes was observed in wild-type plants in response to elicitation. Elicitation also triggers altered epitope expression in mutant roots compared with wild-type and non-elicited roots. Inoculation with the pathogen P. parasitica resulted in enhanced root colonization for two mutants, specifically xeg113 and rra2.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>We provide evidence for a link between extensin arabinosylation and root defence, and propose a model to explain the importance of glycosylation in limiting invasion of root cells by pathogenic oomycetes.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Automated" Owner="NLM"><PMID Version="1">31242281</PMID><DateCompleted><Year>2020</Year><Month>07</Month><Day>13</Day></DateCompleted><DateRevised><Year>2020</Year><Month>07</Month><Day>13</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1095-8290</ISSN><JournalIssue CitedMedium="Internet"><Volume>125</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>04</Month><Day>25</Day></PubDate></JournalIssue><Title>Annals of botany</Title><ISOAbbreviation>Ann Bot</ISOAbbreviation></Journal><ArticleTitle>Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization.</ArticleTitle><Pagination><MedlinePgn>751-763</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/aob/mcz068</ELocationID><Abstract><AbstractText Label="BACKGROUND AND AIMS">Extensins are hydroxyproline-rich glycoproteins thought to strengthen the plant cell wall, one of the first barriers against pathogens, through intra- and intermolecular cross-links. The glycan moiety of extensins is believed to confer the correct structural conformation to the glycoprotein, leading to self-assembly within the cell wall that helps limit microbial adherence and invasion. However, this role is not clearly established.</AbstractText><AbstractText Label="METHODS">We used Arabidopsis thaliana mutants impaired in extensin arabinosylation to investigate the role of extensin arabinosylation in root-microbe interactions. Mutant and wild-type roots were stimulated to elicit an immune response with flagellin 22 and immunolabelled with a set of anti-extensin antibodies. Roots were also inoculated with a soilborne oomycete, Phytophthora parasitica, to assess the effect of extensin arabinosylation on root colonization.</AbstractText><AbstractText Label="KEY RESULTS">A differential distribution of extensin epitopes was observed in wild-type plants in response to elicitation. Elicitation also triggers altered epitope expression in mutant roots compared with wild-type and non-elicited roots. Inoculation with the pathogen P. parasitica resulted in enhanced root colonization for two mutants, specifically xeg113 and rra2.</AbstractText><AbstractText Label="CONCLUSIONS">We provide evidence for a link between extensin arabinosylation and root defence, and propose a model to explain the importance of glycosylation in limiting invasion of root cells by pathogenic oomycetes.</AbstractText><CopyrightInformation>© The Author(s) 2019. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Castilleux</LastName><ForeName>Romain</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Plancot</LastName><ForeName>Barbara</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gügi</LastName><ForeName>Bruno</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Attard</LastName><ForeName>Agnès</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>INRA, CNRS, Université Côte d'Azur, ISA, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Loutelier-Bourhis</LastName><ForeName>Corinne</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>IRCOF COBRA, UMR6014 and FR3038, CNRS, Université de Rouen Normandie, Mont-Saint-Aignan Cedex, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lefranc</LastName><ForeName>Benjamin</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>INSERM U1239, Différenciation et Communication Neuronale et Neuroendocrine, Normandie Université, Rouen, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nguema-Ona</LastName><ForeName>Eric</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Arkoun</LastName><ForeName>Mustapha</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yvin</LastName><ForeName>Jean-Claude</ForeName><Initials>JC</Initials><AffiliationInfo><Affiliation>Centre Mondial de l'Innovation, Groupe Roullier, Saint Malo Cédex, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Driouich</LastName><ForeName>Azeddine</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vicré</LastName><ForeName>Maïté</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Normandie Université, UNIROUEN, Laboratoire Glyco-MEV EA 4358, Fédération de Recherche 'Normandie Végétal' FED, Rouen, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Ann Bot</MedlineTA><NlmUniqueID>0372347</NlmUniqueID><ISSNLinking>0305-7364</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D006023">Glycoproteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Ann Bot. 2020 Apr 25;125(5):vii-viii</RefSource><PMID Version="1">32333011</PMID></CommentsCorrections></CommentsCorrectionsList><MeshHeadingList><MeshHeading><DescriptorName UI="D017360" MajorTopicYN="Y">Arabidopsis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002473" MajorTopicYN="N">Cell Wall</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006023" MajorTopicYN="N">Glycoproteins</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009868" MajorTopicYN="Y">Oomycetes</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Arabinosylation</Keyword><Keyword MajorTopicYN="Y">cell wall</Keyword><Keyword MajorTopicYN="Y">defence</Keyword><Keyword MajorTopicYN="Y">extensin</Keyword><Keyword MajorTopicYN="Y">immunocytochemistry</Keyword><Keyword MajorTopicYN="Y">monoclonal antibodies</Keyword><Keyword 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