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Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor
Certain pathogens deliver effectors into plant cells to modify host protein targets and thereby suppress immunity. These target modifications can be detected by intracellular immune receptors, or Resistance (R) proteins, that trigger strong immune responses including localized host cell death. The a...
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Published in: | PLoS pathogens 2010-10, Vol.6 (10), p.e1001137-e1001137 |
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description | Certain pathogens deliver effectors into plant cells to modify host protein targets and thereby suppress immunity. These target modifications can be detected by intracellular immune receptors, or Resistance (R) proteins, that trigger strong immune responses including localized host cell death. The accelerated cell death 11 (acd11) "lesion mimic" mutant of Arabidopsis thaliana exhibits autoimmune phenotypes such as constitutive defense responses and cell death without pathogen perception. ACD11 encodes a putative sphingosine transfer protein, but its precise role during these processes is unknown. In a screen for lazarus (laz) mutants that suppress acd11 death we identified two genes, LAZ2 and LAZ5. LAZ2 encodes the histone lysine methyltransferase SDG8, previously shown to epigenetically regulate flowering time via modification of histone 3 (H3). LAZ5 encodes an RPS4-like R-protein, defined by several dominant negative alleles. Microarray and chromatin immunoprecipitation analyses showed that LAZ2/SDG8 is required for LAZ5 expression and H3 lysine 36 trimethylation at LAZ5 chromatin to maintain a transcriptionally active state. We hypothesize that LAZ5 triggers cell death in the absence of ACD11, and that cell death in other lesion mimic mutants may also be caused by inappropriate activation of R genes. Moreover, SDG8 is required for basal and R protein-mediated pathogen resistance in Arabidopsis, revealing the importance of chromatin remodeling as a key process in plant innate immunity. |
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These target modifications can be detected by intracellular immune receptors, or Resistance (R) proteins, that trigger strong immune responses including localized host cell death. The accelerated cell death 11 (acd11) "lesion mimic" mutant of Arabidopsis thaliana exhibits autoimmune phenotypes such as constitutive defense responses and cell death without pathogen perception. ACD11 encodes a putative sphingosine transfer protein, but its precise role during these processes is unknown. In a screen for lazarus (laz) mutants that suppress acd11 death we identified two genes, LAZ2 and LAZ5. LAZ2 encodes the histone lysine methyltransferase SDG8, previously shown to epigenetically regulate flowering time via modification of histone 3 (H3). LAZ5 encodes an RPS4-like R-protein, defined by several dominant negative alleles. Microarray and chromatin immunoprecipitation analyses showed that LAZ2/SDG8 is required for LAZ5 expression and H3 lysine 36 trimethylation at LAZ5 chromatin to maintain a transcriptionally active state. We hypothesize that LAZ5 triggers cell death in the absence of ACD11, and that cell death in other lesion mimic mutants may also be caused by inappropriate activation of R genes. Moreover, SDG8 is required for basal and R protein-mediated pathogen resistance in Arabidopsis, revealing the importance of chromatin remodeling as a key process in plant innate immunity.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1001137</identifier><identifier>PMID: 20949080</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Apoptosis ; Apoptosis Regulatory Proteins - genetics ; Apoptosis Regulatory Proteins - physiology ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - immunology ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - physiology ; Arabidopsis thaliana ; Autoimmunity ; Autoimmunity - physiology ; Cell Biology/Cellular Death and Stress Responses ; Cell death ; Cell Death - genetics ; Cell Death - immunology ; Chromatin ; Chromatin Assembly and Disassembly - genetics ; Chromatin Assembly and Disassembly - immunology ; Chromatin Assembly and Disassembly - physiology ; Chromatin remodeling ; DNA ; DNA microarrays ; double prime R protein ; Enzymes ; Epigenesis, Genetic - immunology ; Epigenesis, Genetic - physiology ; Epigenetics ; Experiments ; Flowering ; Gene Expression Regulation, Plant - physiology ; Genetic aspects ; Genetics and Genomics/Epigenetics ; Genetics and Genomics/Genetics of the Immune System ; histone methyltransferase ; Histone-Lysine N-Methyltransferase - genetics ; Histone-Lysine N-Methyltransferase - metabolism ; Histone-Lysine N-Methyltransferase - physiology ; Histones ; Immune response ; Immunity ; Immunity, Innate - genetics ; Immunology/Autoimmunity ; Immunology/Innate Immunity ; Immunoprecipitation ; Lysine ; Membrane Transport Proteins - genetics ; Membrane Transport Proteins - physiology ; Methylation ; Methyltransferase ; Mutation ; Pathogens ; Perception ; Physiological aspects ; Plant Biology/Plant Genetics and Gene Expression ; Plant Biology/Plant-Biotic Interactions ; Plant cells ; Proteins ; Receptors, Immunologic - genetics ; Receptors, Immunologic - physiology ; Seeds ; Transcription ; Transcription activation</subject><ispartof>PLoS pathogens, 2010-10, Vol.6 (10), p.e1001137-e1001137</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>Palma et al. 2010</rights><rights>2010 Palma 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: Palma K, Thorgrimsen S, Malinovsky FG, Fiil BK, Nielsen HB, et al. (2010) Autoimmunity in Arabidopsis acd11 Is Mediated by Epigenetic Regulation of an Immune Receptor. PLoS Pathog 6(10): e1001137. doi:10.1371/journal.ppat.1001137</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c730t-75c9f68cd67b37a4b6e0fff11a47b17fcd37488198a300c9615b7fd14ae5ad563</citedby><cites>FETCH-LOGICAL-c730t-75c9f68cd67b37a4b6e0fff11a47b17fcd37488198a300c9615b7fd14ae5ad563</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2951382/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2951382/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,37013,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20949080$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Dangl, Jeffery L.</contributor><creatorcontrib>Palma, Kristoffer</creatorcontrib><creatorcontrib>Thorgrimsen, Stephan</creatorcontrib><creatorcontrib>Malinovsky, Frederikke Gro</creatorcontrib><creatorcontrib>Fiil, Berthe Katrine</creatorcontrib><creatorcontrib>Nielsen, H Bjørn</creatorcontrib><creatorcontrib>Brodersen, Peter</creatorcontrib><creatorcontrib>Hofius, Daniel</creatorcontrib><creatorcontrib>Petersen, Morten</creatorcontrib><creatorcontrib>Mundy, John</creatorcontrib><title>Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Certain pathogens deliver effectors into plant cells to modify host protein targets and thereby suppress immunity. These target modifications can be detected by intracellular immune receptors, or Resistance (R) proteins, that trigger strong immune responses including localized host cell death. The accelerated cell death 11 (acd11) "lesion mimic" mutant of Arabidopsis thaliana exhibits autoimmune phenotypes such as constitutive defense responses and cell death without pathogen perception. ACD11 encodes a putative sphingosine transfer protein, but its precise role during these processes is unknown. In a screen for lazarus (laz) mutants that suppress acd11 death we identified two genes, LAZ2 and LAZ5. LAZ2 encodes the histone lysine methyltransferase SDG8, previously shown to epigenetically regulate flowering time via modification of histone 3 (H3). LAZ5 encodes an RPS4-like R-protein, defined by several dominant negative alleles. Microarray and chromatin immunoprecipitation analyses showed that LAZ2/SDG8 is required for LAZ5 expression and H3 lysine 36 trimethylation at LAZ5 chromatin to maintain a transcriptionally active state. We hypothesize that LAZ5 triggers cell death in the absence of ACD11, and that cell death in other lesion mimic mutants may also be caused by inappropriate activation of R genes. Moreover, SDG8 is required for basal and R protein-mediated pathogen resistance in Arabidopsis, revealing the importance of chromatin remodeling as a key process in plant innate immunity.</description><subject>Apoptosis</subject><subject>Apoptosis Regulatory Proteins - genetics</subject><subject>Apoptosis Regulatory Proteins - physiology</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - physiology</subject><subject>Arabidopsis thaliana</subject><subject>Autoimmunity</subject><subject>Autoimmunity - physiology</subject><subject>Cell Biology/Cellular Death and Stress Responses</subject><subject>Cell death</subject><subject>Cell Death - genetics</subject><subject>Cell Death - immunology</subject><subject>Chromatin</subject><subject>Chromatin Assembly and Disassembly - genetics</subject><subject>Chromatin Assembly and Disassembly - immunology</subject><subject>Chromatin Assembly and Disassembly - physiology</subject><subject>Chromatin remodeling</subject><subject>DNA</subject><subject>DNA microarrays</subject><subject>double prime R protein</subject><subject>Enzymes</subject><subject>Epigenesis, Genetic - immunology</subject><subject>Epigenesis, Genetic - physiology</subject><subject>Epigenetics</subject><subject>Experiments</subject><subject>Flowering</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Genetic aspects</subject><subject>Genetics and Genomics/Epigenetics</subject><subject>Genetics and Genomics/Genetics of the Immune System</subject><subject>histone methyltransferase</subject><subject>Histone-Lysine N-Methyltransferase - genetics</subject><subject>Histone-Lysine N-Methyltransferase - metabolism</subject><subject>Histone-Lysine N-Methyltransferase - physiology</subject><subject>Histones</subject><subject>Immune response</subject><subject>Immunity</subject><subject>Immunity, Innate - genetics</subject><subject>Immunology/Autoimmunity</subject><subject>Immunology/Innate Immunity</subject><subject>Immunoprecipitation</subject><subject>Lysine</subject><subject>Membrane Transport Proteins - genetics</subject><subject>Membrane Transport Proteins - physiology</subject><subject>Methylation</subject><subject>Methyltransferase</subject><subject>Mutation</subject><subject>Pathogens</subject><subject>Perception</subject><subject>Physiological aspects</subject><subject>Plant Biology/Plant Genetics and Gene Expression</subject><subject>Plant Biology/Plant-Biotic Interactions</subject><subject>Plant cells</subject><subject>Proteins</subject><subject>Receptors, Immunologic - genetics</subject><subject>Receptors, Immunologic - physiology</subject><subject>Seeds</subject><subject>Transcription</subject><subject>Transcription activation</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNqVkt-L1DAQx4so3nn6H4gWfBAfds00aZO-CMvhj4VDwR9vQpgmac3SNjVJxf3vzd72jlsQRPKQ4ZvPfIeZTJY9BbIGyuH1zs1-xH49TRjXQAgk9V52DmVJV5xydv9OfJY9CmFHCAMK1cPsrCA1q4kg59n3zRydHYZ5tHGf2zHfeGysdlOwIUelAfIUDEZbjEbnzT43k-3MaKJVuTfd3GO0bsxdm-OYXxuZpCszRecfZw9a7IN5stwX2bd3b79eflhdfXq_vdxcrRSnJK54qeq2EkpXvKEcWVMZ0rYtADLeAG-VTi0IAbVASoiqKygb3mpgaErUZUUvsudH36l3QS6DCRIKURPOSlYmYnsktMOdnLwd0O-lQyuvBec7iT611BspoAGly0YRbViBtBbcKNpUlCIoI5rk9WapNjdpMMqM0WN_Ynr6MtofsnO_ZFGXQEWRDF4uBt79nE2IcrBBmb7H0bg5SEHrSrCqoP8keSkEFZzUiXxxJDtMPdixdam0OtByUzCoijpVT9T6L1Q62gxWudG0NuknCa9OEhITze_Y4RyC3H75_B_sx1OWHVnlXQjetLfjAyIP633zi_Kw3nJZ75T27O7ob5Nu9pn-AcUt9ts</recordid><startdate>20101001</startdate><enddate>20101001</enddate><creator>Palma, Kristoffer</creator><creator>Thorgrimsen, Stephan</creator><creator>Malinovsky, Frederikke Gro</creator><creator>Fiil, Berthe Katrine</creator><creator>Nielsen, H Bjørn</creator><creator>Brodersen, Peter</creator><creator>Hofius, Daniel</creator><creator>Petersen, Morten</creator><creator>Mundy, John</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>7X8</scope><scope>7T5</scope><scope>7TM</scope><scope>H94</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20101001</creationdate><title>Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor</title><author>Palma, Kristoffer ; Thorgrimsen, Stephan ; Malinovsky, Frederikke Gro ; Fiil, Berthe Katrine ; Nielsen, H Bjørn ; Brodersen, Peter ; Hofius, Daniel ; Petersen, Morten ; Mundy, John</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c730t-75c9f68cd67b37a4b6e0fff11a47b17fcd37488198a300c9615b7fd14ae5ad563</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Apoptosis</topic><topic>Apoptosis Regulatory Proteins - genetics</topic><topic>Apoptosis Regulatory Proteins - physiology</topic><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - immunology</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - physiology</topic><topic>Arabidopsis thaliana</topic><topic>Autoimmunity</topic><topic>Autoimmunity - physiology</topic><topic>Cell Biology/Cellular Death and Stress Responses</topic><topic>Cell death</topic><topic>Cell Death - genetics</topic><topic>Cell Death - immunology</topic><topic>Chromatin</topic><topic>Chromatin Assembly and Disassembly - genetics</topic><topic>Chromatin Assembly and Disassembly - immunology</topic><topic>Chromatin Assembly and Disassembly - physiology</topic><topic>Chromatin remodeling</topic><topic>DNA</topic><topic>DNA microarrays</topic><topic>double prime R protein</topic><topic>Enzymes</topic><topic>Epigenesis, Genetic - immunology</topic><topic>Epigenesis, Genetic - physiology</topic><topic>Epigenetics</topic><topic>Experiments</topic><topic>Flowering</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>Genetic aspects</topic><topic>Genetics and Genomics/Epigenetics</topic><topic>Genetics and Genomics/Genetics of the Immune System</topic><topic>histone methyltransferase</topic><topic>Histone-Lysine N-Methyltransferase - genetics</topic><topic>Histone-Lysine N-Methyltransferase - metabolism</topic><topic>Histone-Lysine N-Methyltransferase - physiology</topic><topic>Histones</topic><topic>Immune response</topic><topic>Immunity</topic><topic>Immunity, Innate - genetics</topic><topic>Immunology/Autoimmunity</topic><topic>Immunology/Innate Immunity</topic><topic>Immunoprecipitation</topic><topic>Lysine</topic><topic>Membrane Transport Proteins - genetics</topic><topic>Membrane Transport Proteins - physiology</topic><topic>Methylation</topic><topic>Methyltransferase</topic><topic>Mutation</topic><topic>Pathogens</topic><topic>Perception</topic><topic>Physiological aspects</topic><topic>Plant Biology/Plant Genetics and Gene Expression</topic><topic>Plant Biology/Plant-Biotic Interactions</topic><topic>Plant cells</topic><topic>Proteins</topic><topic>Receptors, Immunologic - genetics</topic><topic>Receptors, Immunologic - physiology</topic><topic>Seeds</topic><topic>Transcription</topic><topic>Transcription activation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Palma, Kristoffer</creatorcontrib><creatorcontrib>Thorgrimsen, Stephan</creatorcontrib><creatorcontrib>Malinovsky, Frederikke Gro</creatorcontrib><creatorcontrib>Fiil, Berthe Katrine</creatorcontrib><creatorcontrib>Nielsen, H Bjørn</creatorcontrib><creatorcontrib>Brodersen, Peter</creatorcontrib><creatorcontrib>Hofius, Daniel</creatorcontrib><creatorcontrib>Petersen, Morten</creatorcontrib><creatorcontrib>Mundy, John</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Palma, Kristoffer</au><au>Thorgrimsen, Stephan</au><au>Malinovsky, Frederikke Gro</au><au>Fiil, Berthe Katrine</au><au>Nielsen, H Bjørn</au><au>Brodersen, Peter</au><au>Hofius, Daniel</au><au>Petersen, Morten</au><au>Mundy, John</au><au>Dangl, Jeffery L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2010-10-01</date><risdate>2010</risdate><volume>6</volume><issue>10</issue><spage>e1001137</spage><epage>e1001137</epage><pages>e1001137-e1001137</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Certain pathogens deliver effectors into plant cells to modify host protein targets and thereby suppress immunity. These target modifications can be detected by intracellular immune receptors, or Resistance (R) proteins, that trigger strong immune responses including localized host cell death. The accelerated cell death 11 (acd11) "lesion mimic" mutant of Arabidopsis thaliana exhibits autoimmune phenotypes such as constitutive defense responses and cell death without pathogen perception. ACD11 encodes a putative sphingosine transfer protein, but its precise role during these processes is unknown. In a screen for lazarus (laz) mutants that suppress acd11 death we identified two genes, LAZ2 and LAZ5. LAZ2 encodes the histone lysine methyltransferase SDG8, previously shown to epigenetically regulate flowering time via modification of histone 3 (H3). LAZ5 encodes an RPS4-like R-protein, defined by several dominant negative alleles. Microarray and chromatin immunoprecipitation analyses showed that LAZ2/SDG8 is required for LAZ5 expression and H3 lysine 36 trimethylation at LAZ5 chromatin to maintain a transcriptionally active state. We hypothesize that LAZ5 triggers cell death in the absence of ACD11, and that cell death in other lesion mimic mutants may also be caused by inappropriate activation of R genes. Moreover, SDG8 is required for basal and R protein-mediated pathogen resistance in Arabidopsis, revealing the importance of chromatin remodeling as a key process in plant innate immunity.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20949080</pmid><doi>10.1371/journal.ppat.1001137</doi><oa>free_for_read</oa></addata></record> |
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subjects | Apoptosis Apoptosis Regulatory Proteins - genetics Apoptosis Regulatory Proteins - physiology Arabidopsis Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - metabolism Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - physiology Arabidopsis thaliana Autoimmunity Autoimmunity - physiology Cell Biology/Cellular Death and Stress Responses Cell death Cell Death - genetics Cell Death - immunology Chromatin Chromatin Assembly and Disassembly - genetics Chromatin Assembly and Disassembly - immunology Chromatin Assembly and Disassembly - physiology Chromatin remodeling DNA DNA microarrays double prime R protein Enzymes Epigenesis, Genetic - immunology Epigenesis, Genetic - physiology Epigenetics Experiments Flowering Gene Expression Regulation, Plant - physiology Genetic aspects Genetics and Genomics/Epigenetics Genetics and Genomics/Genetics of the Immune System histone methyltransferase Histone-Lysine N-Methyltransferase - genetics Histone-Lysine N-Methyltransferase - metabolism Histone-Lysine N-Methyltransferase - physiology Histones Immune response Immunity Immunity, Innate - genetics Immunology/Autoimmunity Immunology/Innate Immunity Immunoprecipitation Lysine Membrane Transport Proteins - genetics Membrane Transport Proteins - physiology Methylation Methyltransferase Mutation Pathogens Perception Physiological aspects Plant Biology/Plant Genetics and Gene Expression Plant Biology/Plant-Biotic Interactions Plant cells Proteins Receptors, Immunologic - genetics Receptors, Immunologic - physiology Seeds Transcription Transcription activation |
title | Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor |
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