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The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000
Stomata play an important role in plant innate immunity by limiting pathogen entry into leaves but molecular mechanisms regulating stomatal closure upon pathogen perception are not well understood. Here we show that the Arabidopsis thaliana L-type lectin receptor kinase-V.5 (LecRK-V.5) negatively re...
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Published in: | PLoS pathogens 2012-02, Vol.8 (2), p.e1002513-e1002513 |
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description | Stomata play an important role in plant innate immunity by limiting pathogen entry into leaves but molecular mechanisms regulating stomatal closure upon pathogen perception are not well understood. Here we show that the Arabidopsis thaliana L-type lectin receptor kinase-V.5 (LecRK-V.5) negatively regulates stomatal immunity. Loss of LecRK-V.5 function increased resistance to surface inoculation with virulent bacteria Pseudomonas syringae pv tomato DC3000. Levels of resistance were not affected after infiltration-inoculation, suggesting that LecRK-V.5 functions at an early defense stage. By contrast, lines overexpressing LecRK-V.5 were more susceptible to Pst DC3000. Enhanced resistance in lecrk-V.5 mutants was correlated with constitutive stomatal closure, while increased susceptibility phenotypes in overexpression lines were associated with early stomatal reopening. Lines overexpressing LecRK-V.5 also demonstrated a defective stomatal closure after pathogen-associated molecular pattern (PAMP) treatments. LecRK-V.5 is rapidly expressed in stomatal guard cells after bacterial inoculation or treatment with the bacterial PAMP flagellin. In addition, lecrk-V.5 mutants guard cells exhibited constitutive accumulation of reactive oxygen species (ROS) and inhibition of ROS production opened stomata of lecrk-V.5. LecRK-V.5 is also shown to interfere with abscisic acid-mediated stomatal closure signaling upstream of ROS production. These results provide genetic evidences that LecRK-V.5 negatively regulates stomatal immunity upstream of ROS biosynthesis. Our data reveal that plants have evolved mechanisms to reverse bacteria-mediated stomatal closure to prevent long-term effect on CO(2) uptake and photosynthesis. |
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Here we show that the Arabidopsis thaliana L-type lectin receptor kinase-V.5 (LecRK-V.5) negatively regulates stomatal immunity. Loss of LecRK-V.5 function increased resistance to surface inoculation with virulent bacteria Pseudomonas syringae pv tomato DC3000. Levels of resistance were not affected after infiltration-inoculation, suggesting that LecRK-V.5 functions at an early defense stage. By contrast, lines overexpressing LecRK-V.5 were more susceptible to Pst DC3000. Enhanced resistance in lecrk-V.5 mutants was correlated with constitutive stomatal closure, while increased susceptibility phenotypes in overexpression lines were associated with early stomatal reopening. Lines overexpressing LecRK-V.5 also demonstrated a defective stomatal closure after pathogen-associated molecular pattern (PAMP) treatments. LecRK-V.5 is rapidly expressed in stomatal guard cells after bacterial inoculation or treatment with the bacterial PAMP flagellin. In addition, lecrk-V.5 mutants guard cells exhibited constitutive accumulation of reactive oxygen species (ROS) and inhibition of ROS production opened stomata of lecrk-V.5. LecRK-V.5 is also shown to interfere with abscisic acid-mediated stomatal closure signaling upstream of ROS production. These results provide genetic evidences that LecRK-V.5 negatively regulates stomatal immunity upstream of ROS biosynthesis. Our data reveal that plants have evolved mechanisms to reverse bacteria-mediated stomatal closure to prevent long-term effect on CO(2) uptake and photosynthesis.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1002513</identifier><identifier>PMID: 22346749</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abscisic acid ; Abscisic Acid - metabolism ; Arabidopsis ; Arabidopsis - enzymology ; Arabidopsis - genetics ; Arabidopsis - immunology ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - immunology ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Bacteria ; Bacterial infections ; Biology ; Carbon Dioxide - metabolism ; Cell Membrane - enzymology ; Disease Resistance - physiology ; Diseases and pests ; Flagellin ; Flowers & plants ; Gene Expression Regulation, Plant - physiology ; Health aspects ; Host-parasite relationships ; Kinases ; Leaves ; Lectins ; Life sciences ; Lycopersicon esculentum ; Lycopersicon esculentum - microbiology ; Models, Biological ; Mutation ; Phenotype ; Phosphotransferases ; Photosynthesis ; Physiological aspects ; Plant Diseases - immunology ; Plant Diseases - microbiology ; Plant Leaves - genetics ; Plant Leaves - immunology ; Plant Leaves - microbiology ; Plant Leaves - physiology ; Plant Stomata - genetics ; Plant Stomata - immunology ; Plant Stomata - microbiology ; Plant Stomata - physiology ; Protein-Serine-Threonine Kinases - genetics ; Protein-Serine-Threonine Kinases - immunology ; Protein-Serine-Threonine Kinases - metabolism ; Proteins ; Pseudomonas ; Pseudomonas syringae ; Pseudomonas syringae - physiology ; Reactive Oxygen Species - analysis ; Reactive Oxygen Species - metabolism ; Signal Transduction - physiology ; Tomatoes</subject><ispartof>PLoS pathogens, 2012-02, Vol.8 (2), p.e1002513-e1002513</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Desclos-Theveniau et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Desclos-Theveniau M, Arnaud D, Huang T-Y, Lin GJ-C, Chen W-Y, et al. (2012) The Arabidopsis Lectin Receptor Kinase LecRK-V.5 Represses Stomatal Immunity Induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 8(2): e1002513. doi:10.1371/journal.ppat.1002513</rights><rights>Desclos-Theveniau et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-174e681a3d1af295720496f6316561cf7d364ed911ebbce8ae115db80b3b5adb3</citedby><cites>FETCH-LOGICAL-c758t-174e681a3d1af295720496f6316561cf7d364ed911ebbce8ae115db80b3b5adb3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1289091579/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1289091579?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22346749$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>He, Shengyang</contributor><creatorcontrib>Desclos-Theveniau, Marie</creatorcontrib><creatorcontrib>Arnaud, Dominique</creatorcontrib><creatorcontrib>Huang, Ting-Yu</creatorcontrib><creatorcontrib>Lin, Grace Jui-Chih</creatorcontrib><creatorcontrib>Chen, Wei-Yen</creatorcontrib><creatorcontrib>Lin, Yi-Chia</creatorcontrib><creatorcontrib>Zimmerli, Laurent</creatorcontrib><title>The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Stomata play an important role in plant innate immunity by limiting pathogen entry into leaves but molecular mechanisms regulating stomatal closure upon pathogen perception are not well understood. Here we show that the Arabidopsis thaliana L-type lectin receptor kinase-V.5 (LecRK-V.5) negatively regulates stomatal immunity. Loss of LecRK-V.5 function increased resistance to surface inoculation with virulent bacteria Pseudomonas syringae pv tomato DC3000. Levels of resistance were not affected after infiltration-inoculation, suggesting that LecRK-V.5 functions at an early defense stage. By contrast, lines overexpressing LecRK-V.5 were more susceptible to Pst DC3000. Enhanced resistance in lecrk-V.5 mutants was correlated with constitutive stomatal closure, while increased susceptibility phenotypes in overexpression lines were associated with early stomatal reopening. Lines overexpressing LecRK-V.5 also demonstrated a defective stomatal closure after pathogen-associated molecular pattern (PAMP) treatments. LecRK-V.5 is rapidly expressed in stomatal guard cells after bacterial inoculation or treatment with the bacterial PAMP flagellin. In addition, lecrk-V.5 mutants guard cells exhibited constitutive accumulation of reactive oxygen species (ROS) and inhibition of ROS production opened stomata of lecrk-V.5. LecRK-V.5 is also shown to interfere with abscisic acid-mediated stomatal closure signaling upstream of ROS production. These results provide genetic evidences that LecRK-V.5 negatively regulates stomatal immunity upstream of ROS biosynthesis. Our data reveal that plants have evolved mechanisms to reverse bacteria-mediated stomatal closure to prevent long-term effect on CO(2) uptake and photosynthesis.</description><subject>Abscisic acid</subject><subject>Abscisic Acid - metabolism</subject><subject>Arabidopsis</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - immunology</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Bacteria</subject><subject>Bacterial infections</subject><subject>Biology</subject><subject>Carbon Dioxide - metabolism</subject><subject>Cell Membrane - enzymology</subject><subject>Disease Resistance - physiology</subject><subject>Diseases and pests</subject><subject>Flagellin</subject><subject>Flowers & plants</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Health aspects</subject><subject>Host-parasite relationships</subject><subject>Kinases</subject><subject>Leaves</subject><subject>Lectins</subject><subject>Life sciences</subject><subject>Lycopersicon esculentum</subject><subject>Lycopersicon esculentum - microbiology</subject><subject>Models, Biological</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Phosphotransferases</subject><subject>Photosynthesis</subject><subject>Physiological aspects</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - immunology</subject><subject>Plant Leaves - microbiology</subject><subject>Plant Leaves - physiology</subject><subject>Plant Stomata - genetics</subject><subject>Plant Stomata - immunology</subject><subject>Plant Stomata - microbiology</subject><subject>Plant Stomata - physiology</subject><subject>Protein-Serine-Threonine Kinases - genetics</subject><subject>Protein-Serine-Threonine Kinases - immunology</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Proteins</subject><subject>Pseudomonas</subject><subject>Pseudomonas syringae</subject><subject>Pseudomonas syringae - physiology</subject><subject>Reactive Oxygen Species - analysis</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Signal Transduction - physiology</subject><subject>Tomatoes</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqVk01v1DAQhiMEoqXwDxBY4oA4bPBX4uRSabV8rVgBKoWr5diTrZckDnZSsRd-O95uWnVRJYR8sOV53teeGU2SPCU4JUyQ1xs3-k41ad-rISUY04ywe8kxyTI2E0zw-7fOR8mjEDYYc8JI_jA5opTxXPDyOPl9fgFo7lVljeuDDagBPdgOedDQD86jH7ZTAdAK9NnH2fc0i5HeQwgQUBhcqwbVINu2Y2eHLbKdGTUYVG3RlwCjca2LahS23nZrBai_TNGVyKE3C4Yxfpw8qFUT4Mm0nyTf3r09X3yYrT6_Xy7mq5kWWTHMiOCQF0QxQ1RNy0xQzMu8zmM2WU50LQzLOZiSEKgqDYUCQjJTFbhiVaZMxU6S53vfvnFBTqULktCixCXJRBmJ5Z4wTm1k722r_FY6ZeXVhfNrqfxgdQOS0kwTzDiva8EVL5TWlNGSl8wUIuMsep1Or41VC0ZDN3jVHJgeRjp7IdfuUjIqYkIiGrycDLz7OUIYZGuDhqZRHbgxyDIWQ-A8tvefJI2Wkdx96sVf5N1lmKi1ipnarnbxg3rnKee0oDgvRE4jld5BxWWgtdp1UNt4fyB4dSCIzAC_hrUaQ5DLr2f_wX46ZPme1d6F4KG-KTLBcjcm10nK3ZjIaUyi7NntBt2IrueC_QFU1Qzy</recordid><startdate>20120201</startdate><enddate>20120201</enddate><creator>Desclos-Theveniau, Marie</creator><creator>Arnaud, Dominique</creator><creator>Huang, Ting-Yu</creator><creator>Lin, Grace Jui-Chih</creator><creator>Chen, Wei-Yen</creator><creator>Lin, Yi-Chia</creator><creator>Zimmerli, Laurent</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>7T5</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20120201</creationdate><title>The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000</title><author>Desclos-Theveniau, Marie ; Arnaud, Dominique ; Huang, Ting-Yu ; Lin, Grace Jui-Chih ; Chen, Wei-Yen ; Lin, Yi-Chia ; Zimmerli, Laurent</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-174e681a3d1af295720496f6316561cf7d364ed911ebbce8ae115db80b3b5adb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Abscisic acid</topic><topic>Abscisic Acid - 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Academic</collection><collection>Immunology Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJÂ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Desclos-Theveniau, Marie</au><au>Arnaud, Dominique</au><au>Huang, Ting-Yu</au><au>Lin, Grace Jui-Chih</au><au>Chen, Wei-Yen</au><au>Lin, Yi-Chia</au><au>Zimmerli, Laurent</au><au>He, Shengyang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2012-02-01</date><risdate>2012</risdate><volume>8</volume><issue>2</issue><spage>e1002513</spage><epage>e1002513</epage><pages>e1002513-e1002513</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Stomata play an important role in plant innate immunity by limiting pathogen entry into leaves but molecular mechanisms regulating stomatal closure upon pathogen perception are not well understood. Here we show that the Arabidopsis thaliana L-type lectin receptor kinase-V.5 (LecRK-V.5) negatively regulates stomatal immunity. Loss of LecRK-V.5 function increased resistance to surface inoculation with virulent bacteria Pseudomonas syringae pv tomato DC3000. Levels of resistance were not affected after infiltration-inoculation, suggesting that LecRK-V.5 functions at an early defense stage. By contrast, lines overexpressing LecRK-V.5 were more susceptible to Pst DC3000. Enhanced resistance in lecrk-V.5 mutants was correlated with constitutive stomatal closure, while increased susceptibility phenotypes in overexpression lines were associated with early stomatal reopening. Lines overexpressing LecRK-V.5 also demonstrated a defective stomatal closure after pathogen-associated molecular pattern (PAMP) treatments. LecRK-V.5 is rapidly expressed in stomatal guard cells after bacterial inoculation or treatment with the bacterial PAMP flagellin. In addition, lecrk-V.5 mutants guard cells exhibited constitutive accumulation of reactive oxygen species (ROS) and inhibition of ROS production opened stomata of lecrk-V.5. LecRK-V.5 is also shown to interfere with abscisic acid-mediated stomatal closure signaling upstream of ROS production. These results provide genetic evidences that LecRK-V.5 negatively regulates stomatal immunity upstream of ROS biosynthesis. Our data reveal that plants have evolved mechanisms to reverse bacteria-mediated stomatal closure to prevent long-term effect on CO(2) uptake and photosynthesis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22346749</pmid><doi>10.1371/journal.ppat.1002513</doi><oa>free_for_read</oa></addata></record> |
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subjects | Abscisic acid Abscisic Acid - metabolism Arabidopsis Arabidopsis - enzymology Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - immunology Arabidopsis Proteins - metabolism Arabidopsis thaliana Bacteria Bacterial infections Biology Carbon Dioxide - metabolism Cell Membrane - enzymology Disease Resistance - physiology Diseases and pests Flagellin Flowers & plants Gene Expression Regulation, Plant - physiology Health aspects Host-parasite relationships Kinases Leaves Lectins Life sciences Lycopersicon esculentum Lycopersicon esculentum - microbiology Models, Biological Mutation Phenotype Phosphotransferases Photosynthesis Physiological aspects Plant Diseases - immunology Plant Diseases - microbiology Plant Leaves - genetics Plant Leaves - immunology Plant Leaves - microbiology Plant Leaves - physiology Plant Stomata - genetics Plant Stomata - immunology Plant Stomata - microbiology Plant Stomata - physiology Protein-Serine-Threonine Kinases - genetics Protein-Serine-Threonine Kinases - immunology Protein-Serine-Threonine Kinases - metabolism Proteins Pseudomonas Pseudomonas syringae Pseudomonas syringae - physiology Reactive Oxygen Species - analysis Reactive Oxygen Species - metabolism Signal Transduction - physiology Tomatoes |
title | The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000 |
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