Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization
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...
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Veröffentlicht in: | Annals of botany 2020-04, Vol.125 (5), p.751-763 |
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creator | Castilleux, Romain Plancot, Barbara Gügi, Bruno Attard, Agnès Loutelier-Bourhis, Corinne Lefranc, Benjamin Nguema-Ona, Eric Arkoun, Mustapha Yvin, Jean-Claude Driouich, Azeddine Vicré, Maïté |
description | 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.
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.
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.
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_str_mv | 10.1093/aob/mcz068 |
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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.
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.
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.</description><identifier>ISSN: 0305-7364</identifier><identifier>EISSN: 1095-8290</identifier><identifier>DOI: 10.1093/aob/mcz068</identifier><identifier>PMID: 31242281</identifier><language>eng</language><publisher>England: Oxford University Press (OUP)</publisher><subject>Arabidopsis ; Biochemistry ; Biochemistry, Molecular Biology ; Biotechnology ; Cell Behavior ; Cell Wall ; Cellular Biology ; Development Biology ; Genomics ; Glycoproteins ; Life Sciences ; Molecular biology ; Oomycetes ; Original ; Phytopathology and phytopharmacy ; Plant breeding ; Plant Proteins ; Subcellular Processes ; Vegetal Biology</subject><ispartof>Annals of botany, 2020-04, Vol.125 (5), p.751-763</ispartof><rights>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.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>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. 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-6b34ac221385c50ee66e3715a823ff0587b315395c39efa61f0d01236eb43b783</citedby><cites>FETCH-LOGICAL-c412t-6b34ac221385c50ee66e3715a823ff0587b315395c39efa61f0d01236eb43b783</cites><orcidid>0000-0002-0367-2414 ; 0000-0001-5184-7402 ; 0000-0002-6416-7032 ; 0000-0002-3361-1532</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7182588/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7182588/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31242281$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://normandie-univ.hal.science/hal-02173816$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Castilleux, Romain</creatorcontrib><creatorcontrib>Plancot, Barbara</creatorcontrib><creatorcontrib>Gügi, Bruno</creatorcontrib><creatorcontrib>Attard, Agnès</creatorcontrib><creatorcontrib>Loutelier-Bourhis, Corinne</creatorcontrib><creatorcontrib>Lefranc, Benjamin</creatorcontrib><creatorcontrib>Nguema-Ona, Eric</creatorcontrib><creatorcontrib>Arkoun, Mustapha</creatorcontrib><creatorcontrib>Yvin, Jean-Claude</creatorcontrib><creatorcontrib>Driouich, Azeddine</creatorcontrib><creatorcontrib>Vicré, Maïté</creatorcontrib><title>Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization</title><title>Annals of botany</title><addtitle>Ann Bot</addtitle><description>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.
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.
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.
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.</description><subject>Arabidopsis</subject><subject>Biochemistry</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biotechnology</subject><subject>Cell Behavior</subject><subject>Cell Wall</subject><subject>Cellular Biology</subject><subject>Development Biology</subject><subject>Genomics</subject><subject>Glycoproteins</subject><subject>Life Sciences</subject><subject>Molecular biology</subject><subject>Oomycetes</subject><subject>Original</subject><subject>Phytopathology and phytopharmacy</subject><subject>Plant breeding</subject><subject>Plant Proteins</subject><subject>Subcellular Processes</subject><subject>Vegetal Biology</subject><issn>0305-7364</issn><issn>1095-8290</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkcGKFDEQhoMo7rh68QEkRxXaTVKd7vRFWJbVFQa86DmkM9VuJJ0ak8zg7NPb46yLekr48-Urip-xl1K8k2KAC0fjxezvRGcesdWS6MaoQTxmKwFCNz107Rl7Vsp3IYTqBvmUnYFUrVJGrpi__lkxlZC4y24Micohuhoo8VB4SHuKe9wsF56JKs9YtpQK8kocY_ChUi7cpQ2PYQ61cKL54LEi9xQphbvfqufsyeRiwRf35zn7-uH6y9VNs_788dPV5brxrVS16UZonVdKgtFeC8SuQ-ildkbBNAlt-hGkhkF7GHBynZzERkgFHY4tjL2Bc_b-5N3uxhk3HlPNLtptDrPLB0su2H9fUri132hve2mUNkfBm5Pg9r9vN5dre8yEkj0Y2e3lwr6-H5bpxw5LtXMoHmN0CWlXrFKtgR6EEQv69oT6TKVknB7cUthjg3Zp0J4aXOBXfy_xgP6pDH4BrHaZqg</recordid><startdate>20200425</startdate><enddate>20200425</enddate><creator>Castilleux, Romain</creator><creator>Plancot, Barbara</creator><creator>Gügi, Bruno</creator><creator>Attard, Agnès</creator><creator>Loutelier-Bourhis, Corinne</creator><creator>Lefranc, Benjamin</creator><creator>Nguema-Ona, Eric</creator><creator>Arkoun, Mustapha</creator><creator>Yvin, Jean-Claude</creator><creator>Driouich, Azeddine</creator><creator>Vicré, Maïté</creator><general>Oxford University Press (OUP)</general><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0367-2414</orcidid><orcidid>https://orcid.org/0000-0001-5184-7402</orcidid><orcidid>https://orcid.org/0000-0002-6416-7032</orcidid><orcidid>https://orcid.org/0000-0002-3361-1532</orcidid></search><sort><creationdate>20200425</creationdate><title>Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization</title><author>Castilleux, Romain ; Plancot, Barbara ; Gügi, Bruno ; Attard, Agnès ; Loutelier-Bourhis, Corinne ; Lefranc, Benjamin ; Nguema-Ona, Eric ; Arkoun, Mustapha ; Yvin, Jean-Claude ; Driouich, Azeddine ; Vicré, Maïté</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-6b34ac221385c50ee66e3715a823ff0587b315395c39efa61f0d01236eb43b783</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Arabidopsis</topic><topic>Biochemistry</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biotechnology</topic><topic>Cell Behavior</topic><topic>Cell Wall</topic><topic>Cellular Biology</topic><topic>Development Biology</topic><topic>Genomics</topic><topic>Glycoproteins</topic><topic>Life Sciences</topic><topic>Molecular biology</topic><topic>Oomycetes</topic><topic>Original</topic><topic>Phytopathology and phytopharmacy</topic><topic>Plant breeding</topic><topic>Plant Proteins</topic><topic>Subcellular Processes</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Castilleux, Romain</creatorcontrib><creatorcontrib>Plancot, Barbara</creatorcontrib><creatorcontrib>Gügi, Bruno</creatorcontrib><creatorcontrib>Attard, Agnès</creatorcontrib><creatorcontrib>Loutelier-Bourhis, Corinne</creatorcontrib><creatorcontrib>Lefranc, Benjamin</creatorcontrib><creatorcontrib>Nguema-Ona, Eric</creatorcontrib><creatorcontrib>Arkoun, Mustapha</creatorcontrib><creatorcontrib>Yvin, Jean-Claude</creatorcontrib><creatorcontrib>Driouich, Azeddine</creatorcontrib><creatorcontrib>Vicré, Maïté</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Annals of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Castilleux, Romain</au><au>Plancot, Barbara</au><au>Gügi, Bruno</au><au>Attard, Agnès</au><au>Loutelier-Bourhis, Corinne</au><au>Lefranc, Benjamin</au><au>Nguema-Ona, Eric</au><au>Arkoun, Mustapha</au><au>Yvin, Jean-Claude</au><au>Driouich, Azeddine</au><au>Vicré, Maïté</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization</atitle><jtitle>Annals of botany</jtitle><addtitle>Ann Bot</addtitle><date>2020-04-25</date><risdate>2020</risdate><volume>125</volume><issue>5</issue><spage>751</spage><epage>763</epage><pages>751-763</pages><issn>0305-7364</issn><eissn>1095-8290</eissn><abstract>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.
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.
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.
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.</abstract><cop>England</cop><pub>Oxford University Press (OUP)</pub><pmid>31242281</pmid><doi>10.1093/aob/mcz068</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-0367-2414</orcidid><orcidid>https://orcid.org/0000-0001-5184-7402</orcidid><orcidid>https://orcid.org/0000-0002-6416-7032</orcidid><orcidid>https://orcid.org/0000-0002-3361-1532</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Biochemistry Biochemistry, Molecular Biology Biotechnology Cell Behavior Cell Wall Cellular Biology Development Biology Genomics Glycoproteins Life Sciences Molecular biology Oomycetes Original Phytopathology and phytopharmacy Plant breeding Plant Proteins Subcellular Processes Vegetal Biology |
title | Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization |
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