Lignin‐based barrier restricts pathogens to the infection site and confers resistance in plants
Pathogenic bacteria invade plant tissues and proliferate in the extracellular space. Plants have evolved the immune system to recognize and limit the growth of pathogens. Despite substantial progress in the study of plant immunity, the mechanism by which plants limit pathogen growth remains unclear....
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creator | Lee, Myoung‐Hoon Jeon, Hwi Seong Kim, Seu Ha Chung, Joo Hee Roppolo, Daniele Lee, Hye‐Jung Cho, Hong Joo Tobimatsu, Yuki Ralph, John Park, Ohkmae K |
description | Pathogenic bacteria invade plant tissues and proliferate in the extracellular space. Plants have evolved the immune system to recognize and limit the growth of pathogens. Despite substantial progress in the study of plant immunity, the mechanism by which plants limit pathogen growth remains unclear. Here, we show that lignin accumulates in
Arabidopsis
leaves in response to incompatible interactions with bacterial pathogens in a manner dependent on Casparian strip membrane domain protein (CASP)‐like proteins (CASPLs). CASPs are known to be the organizers of the lignin‐based Casparian strip, which functions as a diffusion barrier in roots. The spread of invading avirulent pathogens is prevented by spatial restriction, which is disturbed by defects in lignin deposition. Moreover, the motility of pathogenic bacteria is negatively affected by lignin accumulation. These results suggest that the lignin‐deposited structure functions as a physical barrier similar to the Casparian strip, trapping pathogens and thereby terminating their growth.
Synopsis
Plants employ a multilayered immune system, but the exact mechanisms of how plants restrict pathogen growth remain unclear. In this study, the phenolic polymer and cell wall component lignin is shown to form a mechanical barrier against avirulent pathogens, thereby conferring disease resistance in plants.
Lignification is induced during incompatible plant‐pathogen interactions in
Arabidopsis
.
Lignin spatially restricts and encompasses bacteria in the extracellular space
Lignin deposition enhances disease resistance.
Casparian strip organizer proteins CASPL1D1 and CASPL4D1 are required for pathogen‐induced lignification.
Graphical Abstract
Lignin deposition is required for innate immune defense during incompatible plant‐pathogen interactions in a manner dependent on Casparian strip organizer proteins. |
doi_str_mv | 10.15252/embj.2019101948 |
format | Article |
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Arabidopsis
leaves in response to incompatible interactions with bacterial pathogens in a manner dependent on Casparian strip membrane domain protein (CASP)‐like proteins (CASPLs). CASPs are known to be the organizers of the lignin‐based Casparian strip, which functions as a diffusion barrier in roots. The spread of invading avirulent pathogens is prevented by spatial restriction, which is disturbed by defects in lignin deposition. Moreover, the motility of pathogenic bacteria is negatively affected by lignin accumulation. These results suggest that the lignin‐deposited structure functions as a physical barrier similar to the Casparian strip, trapping pathogens and thereby terminating their growth.
Synopsis
Plants employ a multilayered immune system, but the exact mechanisms of how plants restrict pathogen growth remain unclear. In this study, the phenolic polymer and cell wall component lignin is shown to form a mechanical barrier against avirulent pathogens, thereby conferring disease resistance in plants.
Lignification is induced during incompatible plant‐pathogen interactions in
Arabidopsis
.
Lignin spatially restricts and encompasses bacteria in the extracellular space
Lignin deposition enhances disease resistance.
Casparian strip organizer proteins CASPL1D1 and CASPL4D1 are required for pathogen‐induced lignification.
Graphical Abstract
Lignin deposition is required for innate immune defense during incompatible plant‐pathogen interactions in a manner dependent on Casparian strip organizer proteins.</description><identifier>ISSN: 0261-4189</identifier><identifier>ISSN: 1460-2075</identifier><identifier>EISSN: 1460-2075</identifier><identifier>DOI: 10.15252/embj.2019101948</identifier><identifier>PMID: 31559647</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Arabidopsis ; Arabidopsis - immunology ; Arabidopsis - metabolism ; Arabidopsis - microbiology ; Arabidopsis Proteins - metabolism ; Bacteria ; Bacterial Infections - microbiology ; Barriers ; Casparian strip ; CASPL ; Cell Wall - immunology ; Cell Wall - metabolism ; Cell Wall - microbiology ; Cell walls ; Deposition ; Diffusion barriers ; Disease resistance ; EMBO23 ; EMBO30 ; Gene Expression Regulation, Plant ; Host-Pathogen Interactions - immunology ; Immune system ; Lignin ; Lignin - metabolism ; Membrane proteins ; Pathogens ; Phenolic compounds ; Phenols ; Plant diseases ; Plant immunity ; Plant Roots - immunology ; Plant Roots - metabolism ; Plant Roots - microbiology ; Plant tissues ; Polymers ; Proteins ; Strip</subject><ispartof>The EMBO journal, 2019-12, Vol.38 (23), p.e101948-n/a</ispartof><rights>The Author(s) 2019</rights><rights>2019 The Authors</rights><rights>2019 The Authors.</rights><rights>2019 EMBO</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6128-6e803021a899545183fc499b23954b44b12f144c5d92cd6a57fdd5ce2dfd50e43</citedby><cites>FETCH-LOGICAL-c6128-6e803021a899545183fc499b23954b44b12f144c5d92cd6a57fdd5ce2dfd50e43</cites><orcidid>0000-0002-0234-6908 ; 0000000202346908</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/PMC6885736/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6885736/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,1411,1427,27901,27902,41096,42165,45550,45551,46384,46808,51551,53766,53768</link.rule.ids><linktorsrc>$$Uhttps://doi.org/10.15252/embj.2019101948$$EView_record_in_Springer_Nature$$FView_record_in_$$GSpringer_Nature</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31559647$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1566920$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Myoung‐Hoon</creatorcontrib><creatorcontrib>Jeon, Hwi Seong</creatorcontrib><creatorcontrib>Kim, Seu Ha</creatorcontrib><creatorcontrib>Chung, Joo Hee</creatorcontrib><creatorcontrib>Roppolo, Daniele</creatorcontrib><creatorcontrib>Lee, Hye‐Jung</creatorcontrib><creatorcontrib>Cho, Hong Joo</creatorcontrib><creatorcontrib>Tobimatsu, Yuki</creatorcontrib><creatorcontrib>Ralph, John</creatorcontrib><creatorcontrib>Park, Ohkmae K</creatorcontrib><title>Lignin‐based barrier restricts pathogens to the infection site and confers resistance in plants</title><title>The EMBO journal</title><addtitle>EMBO J</addtitle><addtitle>EMBO J</addtitle><description>Pathogenic bacteria invade plant tissues and proliferate in the extracellular space. Plants have evolved the immune system to recognize and limit the growth of pathogens. Despite substantial progress in the study of plant immunity, the mechanism by which plants limit pathogen growth remains unclear. Here, we show that lignin accumulates in
Arabidopsis
leaves in response to incompatible interactions with bacterial pathogens in a manner dependent on Casparian strip membrane domain protein (CASP)‐like proteins (CASPLs). CASPs are known to be the organizers of the lignin‐based Casparian strip, which functions as a diffusion barrier in roots. The spread of invading avirulent pathogens is prevented by spatial restriction, which is disturbed by defects in lignin deposition. Moreover, the motility of pathogenic bacteria is negatively affected by lignin accumulation. These results suggest that the lignin‐deposited structure functions as a physical barrier similar to the Casparian strip, trapping pathogens and thereby terminating their growth.
Synopsis
Plants employ a multilayered immune system, but the exact mechanisms of how plants restrict pathogen growth remain unclear. In this study, the phenolic polymer and cell wall component lignin is shown to form a mechanical barrier against avirulent pathogens, thereby conferring disease resistance in plants.
Lignification is induced during incompatible plant‐pathogen interactions in
Arabidopsis
.
Lignin spatially restricts and encompasses bacteria in the extracellular space
Lignin deposition enhances disease resistance.
Casparian strip organizer proteins CASPL1D1 and CASPL4D1 are required for pathogen‐induced lignification.
Graphical Abstract
Lignin deposition is required for innate immune defense during incompatible plant‐pathogen interactions in a manner dependent on Casparian strip organizer proteins.</description><subject>Arabidopsis</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - microbiology</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Bacteria</subject><subject>Bacterial Infections - microbiology</subject><subject>Barriers</subject><subject>Casparian strip</subject><subject>CASPL</subject><subject>Cell Wall - immunology</subject><subject>Cell Wall - metabolism</subject><subject>Cell Wall - microbiology</subject><subject>Cell walls</subject><subject>Deposition</subject><subject>Diffusion barriers</subject><subject>Disease resistance</subject><subject>EMBO23</subject><subject>EMBO30</subject><subject>Gene Expression Regulation, Plant</subject><subject>Host-Pathogen Interactions - immunology</subject><subject>Immune system</subject><subject>Lignin</subject><subject>Lignin - metabolism</subject><subject>Membrane proteins</subject><subject>Pathogens</subject><subject>Phenolic compounds</subject><subject>Phenols</subject><subject>Plant diseases</subject><subject>Plant immunity</subject><subject>Plant Roots - immunology</subject><subject>Plant Roots - metabolism</subject><subject>Plant Roots - microbiology</subject><subject>Plant tissues</subject><subject>Polymers</subject><subject>Proteins</subject><subject>Strip</subject><issn>0261-4189</issn><issn>1460-2075</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc2OFCEUhYnROO3o3pUhunFTI1BAQWIm0cn4lzZudE0o6lY3nWpogdbMzkfwGX0SaWuccUyMC0KA7xzuuRehh5ScUMEEewbbfnPCCNW0Lq5uoQXlkjSMdOI2WhAmacOp0kfoXs4bQohQHb2LjloqhJa8WyC79Kvgw49v33ubYcC9TclDwglySd6VjHe2rOMKQsYl4rIG7MMIrvgYcPYFsA0DdrHepXxQ-VxscAcK7yYbSr6P7ox2yvDgcj9Gn16dfzx70yw_vH579mLZOEmZaiQo0hJGrdJacEFVOzqudc_aeuw57ykbKedODJq5QVrRjcMgHLBhHAQB3h6j09l3t--3MDgIJdnJ7JLf2nRhovXm5kvwa7OKX4xUSnStrAaPZ4OYizfZ1XBuXZOFmtZQIaVmpEJPL39J8fO-NslsfXYw1agQ99kwpjXljHNd0Sd_oZu4T6H2wLCWkYq1nFaKzJRLMecE41XFlJhfQzaHIZvrIVfJoz-TXgl-T7UCz2fgq5_g4r-G5vz9y3c3_Oksz1UZVpCuC_9nTT8B-rXF9A</recordid><startdate>20191202</startdate><enddate>20191202</enddate><creator>Lee, Myoung‐Hoon</creator><creator>Jeon, Hwi Seong</creator><creator>Kim, Seu Ha</creator><creator>Chung, Joo Hee</creator><creator>Roppolo, Daniele</creator><creator>Lee, Hye‐Jung</creator><creator>Cho, Hong Joo</creator><creator>Tobimatsu, Yuki</creator><creator>Ralph, John</creator><creator>Park, Ohkmae K</creator><general>Nature Publishing Group UK</general><general>Springer Nature B.V</general><general>Nature Publishing Group</general><general>John Wiley and Sons Inc</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>OTOTI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0234-6908</orcidid><orcidid>https://orcid.org/0000000202346908</orcidid></search><sort><creationdate>20191202</creationdate><title>Lignin‐based barrier restricts pathogens to the infection site and confers resistance in plants</title><author>Lee, Myoung‐Hoon ; Jeon, Hwi Seong ; Kim, Seu Ha ; Chung, Joo Hee ; Roppolo, Daniele ; Lee, Hye‐Jung ; Cho, Hong Joo ; Tobimatsu, Yuki ; Ralph, John ; Park, Ohkmae K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6128-6e803021a899545183fc499b23954b44b12f144c5d92cd6a57fdd5ce2dfd50e43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - immunology</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - microbiology</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Bacteria</topic><topic>Bacterial Infections - microbiology</topic><topic>Barriers</topic><topic>Casparian strip</topic><topic>CASPL</topic><topic>Cell Wall - immunology</topic><topic>Cell Wall - metabolism</topic><topic>Cell Wall - microbiology</topic><topic>Cell walls</topic><topic>Deposition</topic><topic>Diffusion barriers</topic><topic>Disease resistance</topic><topic>EMBO23</topic><topic>EMBO30</topic><topic>Gene Expression Regulation, Plant</topic><topic>Host-Pathogen Interactions - immunology</topic><topic>Immune system</topic><topic>Lignin</topic><topic>Lignin - metabolism</topic><topic>Membrane proteins</topic><topic>Pathogens</topic><topic>Phenolic compounds</topic><topic>Phenols</topic><topic>Plant diseases</topic><topic>Plant immunity</topic><topic>Plant Roots - immunology</topic><topic>Plant Roots - metabolism</topic><topic>Plant Roots - microbiology</topic><topic>Plant tissues</topic><topic>Polymers</topic><topic>Proteins</topic><topic>Strip</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Myoung‐Hoon</creatorcontrib><creatorcontrib>Jeon, Hwi Seong</creatorcontrib><creatorcontrib>Kim, Seu Ha</creatorcontrib><creatorcontrib>Chung, Joo Hee</creatorcontrib><creatorcontrib>Roppolo, Daniele</creatorcontrib><creatorcontrib>Lee, Hye‐Jung</creatorcontrib><creatorcontrib>Cho, Hong Joo</creatorcontrib><creatorcontrib>Tobimatsu, Yuki</creatorcontrib><creatorcontrib>Ralph, John</creatorcontrib><creatorcontrib>Park, Ohkmae K</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The EMBO journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Lee, Myoung‐Hoon</au><au>Jeon, Hwi Seong</au><au>Kim, Seu Ha</au><au>Chung, Joo Hee</au><au>Roppolo, Daniele</au><au>Lee, Hye‐Jung</au><au>Cho, Hong Joo</au><au>Tobimatsu, Yuki</au><au>Ralph, John</au><au>Park, Ohkmae K</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lignin‐based barrier restricts pathogens to the infection site and confers resistance in plants</atitle><jtitle>The EMBO journal</jtitle><stitle>EMBO J</stitle><addtitle>EMBO J</addtitle><date>2019-12-02</date><risdate>2019</risdate><volume>38</volume><issue>23</issue><spage>e101948</spage><epage>n/a</epage><pages>e101948-n/a</pages><issn>0261-4189</issn><issn>1460-2075</issn><eissn>1460-2075</eissn><abstract>Pathogenic bacteria invade plant tissues and proliferate in the extracellular space. Plants have evolved the immune system to recognize and limit the growth of pathogens. Despite substantial progress in the study of plant immunity, the mechanism by which plants limit pathogen growth remains unclear. Here, we show that lignin accumulates in
Arabidopsis
leaves in response to incompatible interactions with bacterial pathogens in a manner dependent on Casparian strip membrane domain protein (CASP)‐like proteins (CASPLs). CASPs are known to be the organizers of the lignin‐based Casparian strip, which functions as a diffusion barrier in roots. The spread of invading avirulent pathogens is prevented by spatial restriction, which is disturbed by defects in lignin deposition. Moreover, the motility of pathogenic bacteria is negatively affected by lignin accumulation. These results suggest that the lignin‐deposited structure functions as a physical barrier similar to the Casparian strip, trapping pathogens and thereby terminating their growth.
Synopsis
Plants employ a multilayered immune system, but the exact mechanisms of how plants restrict pathogen growth remain unclear. In this study, the phenolic polymer and cell wall component lignin is shown to form a mechanical barrier against avirulent pathogens, thereby conferring disease resistance in plants.
Lignification is induced during incompatible plant‐pathogen interactions in
Arabidopsis
.
Lignin spatially restricts and encompasses bacteria in the extracellular space
Lignin deposition enhances disease resistance.
Casparian strip organizer proteins CASPL1D1 and CASPL4D1 are required for pathogen‐induced lignification.
Graphical Abstract
Lignin deposition is required for innate immune defense during incompatible plant‐pathogen interactions in a manner dependent on Casparian strip organizer proteins.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31559647</pmid><doi>10.15252/embj.2019101948</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-0234-6908</orcidid><orcidid>https://orcid.org/0000000202346908</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Arabidopsis - immunology Arabidopsis - metabolism Arabidopsis - microbiology Arabidopsis Proteins - metabolism Bacteria Bacterial Infections - microbiology Barriers Casparian strip CASPL Cell Wall - immunology Cell Wall - metabolism Cell Wall - microbiology Cell walls Deposition Diffusion barriers Disease resistance EMBO23 EMBO30 Gene Expression Regulation, Plant Host-Pathogen Interactions - immunology Immune system Lignin Lignin - metabolism Membrane proteins Pathogens Phenolic compounds Phenols Plant diseases Plant immunity Plant Roots - immunology Plant Roots - metabolism Plant Roots - microbiology Plant tissues Polymers Proteins Strip |
title | Lignin‐based barrier restricts pathogens to the infection site and confers resistance in plants |
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