Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants
Identifieur interne : 002443 ( Istex/Corpus ); précédent : 002442; suivant : 002444Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants
Auteurs : T. Ogata ; H. Okada ; H. Kawaide ; H. Takahashi ; S. Seo ; I. Mitsuhara ; Y. MatsushitaSource :
- Plant Biology [ 1435-8603 ] ; 2015-09.
Abstract
We previously reported that one of the ethylene response factors (ERFs), NtERF3, and other members of the subgroup VIII‐a ERFs of the AP2/ERF family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of NtERF3 in a cell death signalling pathway in tobacco plants, particularly downstream of NtSIPK/NtWIPK and NtWRKY1, which are mitogen‐activated protein kinases and a phosphorylation substrate of NtSIPK, respectively. An ERF‐associated amphiphilic repression (EAR) motif‐deficient NtERF3b mutant (NtERF3bΔEAR) that lacked cell death‐inducing ability suppressed the induction of cell death caused by NtERF3a. The transient co‐expression of NtERF3bΔEAR suppressed the hypersensitive reaction (HR)‐like cell death induced by NtSIPK and NtWRKY1. The induction of cell death by NtSIPK and NtWRKY1 was also inhibited in transgenic plants expressing NtERF3bΔEAR. Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the HR cell death signalling pathway mediated by SIPK/WIPK and WRKY1. Overall, these results suggest that NtERF3 functions downstream of NtSIPK/NtWIPK and NtWRKY1 in a cell death signalling pathway, with some feedback regulation.
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DOI: 10.1111/plb.12349
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Okada</name><affiliation><mods:affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</mods:affiliation></affiliation><affiliation><mods:affiliation>Current Address: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, KashiwaChiba, Japan</mods:affiliation></affiliation></author><author><name sortKey="Kawaide, H" sort="Kawaide, H" uniqKey="Kawaide H" first="H." last="Kawaide">H. Kawaide</name><affiliation><mods:affiliation>Institute of Agriculture, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</mods:affiliation></affiliation></author><author><name sortKey="Takahashi, H" sort="Takahashi, H" uniqKey="Takahashi H" first="H." last="Takahashi">H. Takahashi</name><affiliation><mods:affiliation>Department of Life Science, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan</mods:affiliation></affiliation></author><author><name sortKey="Seo, S" sort="Seo, S" uniqKey="Seo S" first="S." last="Seo">S. Seo</name><affiliation><mods:affiliation>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</mods:affiliation></affiliation></author><author><name sortKey="Mitsuhara, I" sort="Mitsuhara, I" uniqKey="Mitsuhara I" first="I." last="Mitsuhara">I. Mitsuhara</name><affiliation><mods:affiliation>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</mods:affiliation></affiliation></author><author><name sortKey="Matsushita, Y" sort="Matsushita, Y" uniqKey="Matsushita Y" first="Y." last="Matsushita">Y. Matsushita</name><affiliation><mods:affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</mods:affiliation></affiliation><affiliation><mods:affiliation>Y. Matsushita, Gene Research Center, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183‐8509, Japan.E‐mail:</mods:affiliation></affiliation><affiliation><mods:affiliation>E-mail: ymatsu@cc.tuat.ac.jp</mods:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">ISTEX</idno><idno type="RBID">ISTEX:DFC4A8FA17F5D73FFCDB28816C63FB2A5CDAB6DC</idno><date when="2015" year="2015">2015</date><idno type="doi">10.1111/plb.12349</idno><idno type="url">https://api.istex.fr/ark:/67375/WNG-20MF36KR-5/fulltext.pdf</idno><idno type="wicri:Area/Istex/Corpus">002443</idno><idno type="wicri:explorRef" wicri:stream="Istex" wicri:step="Corpus" wicri:corpus="ISTEX">002443</idno></publicationStmt><sourceDesc><biblStruct><analytic><title level="a" type="main">Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants</title><author><name sortKey="Ogata, T" sort="Ogata, T" uniqKey="Ogata T" first="T." last="Ogata">T. Ogata</name><affiliation><mods:affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</mods:affiliation></affiliation><affiliation><mods:affiliation>Current Address: Biological Resources and Post‐harvest Division, Japan International Research Center for Agricultural Sciences (JIRCAS), TsukubaIbaraki, Japan</mods:affiliation></affiliation></author><author><name sortKey="Okada, H" sort="Okada, H" uniqKey="Okada H" first="H." last="Okada">H. Okada</name><affiliation><mods:affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</mods:affiliation></affiliation><affiliation><mods:affiliation>Current Address: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, KashiwaChiba, Japan</mods:affiliation></affiliation></author><author><name sortKey="Kawaide, H" sort="Kawaide, H" uniqKey="Kawaide H" first="H." last="Kawaide">H. Kawaide</name><affiliation><mods:affiliation>Institute of Agriculture, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</mods:affiliation></affiliation></author><author><name sortKey="Takahashi, H" sort="Takahashi, H" uniqKey="Takahashi H" first="H." last="Takahashi">H. Takahashi</name><affiliation><mods:affiliation>Department of Life Science, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan</mods:affiliation></affiliation></author><author><name sortKey="Seo, S" sort="Seo, S" uniqKey="Seo S" first="S." last="Seo">S. Seo</name><affiliation><mods:affiliation>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</mods:affiliation></affiliation></author><author><name sortKey="Mitsuhara, I" sort="Mitsuhara, I" uniqKey="Mitsuhara I" first="I." last="Mitsuhara">I. Mitsuhara</name><affiliation><mods:affiliation>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</mods:affiliation></affiliation></author><author><name sortKey="Matsushita, Y" sort="Matsushita, Y" uniqKey="Matsushita Y" first="Y." last="Matsushita">Y. Matsushita</name><affiliation><mods:affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</mods:affiliation></affiliation><affiliation><mods:affiliation>Y. Matsushita, Gene Research Center, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183‐8509, Japan.E‐mail:</mods:affiliation></affiliation><affiliation><mods:affiliation>E-mail: ymatsu@cc.tuat.ac.jp</mods:affiliation></affiliation></author></analytic><monogr></monogr><series><title level="j" type="main">Plant Biology</title><title level="j" type="alt">PLANT BIOLOGY</title><idno type="ISSN">1435-8603</idno><idno type="eISSN">1438-8677</idno><imprint><biblScope unit="vol">17</biblScope><biblScope unit="issue">5</biblScope><biblScope unit="page" from="962">962</biblScope><biblScope unit="page" to="972">972</biblScope><biblScope unit="page-count">11</biblScope><date type="published" when="2015-09">2015-09</date></imprint><idno type="ISSN">1435-8603</idno></series></biblStruct></sourceDesc><seriesStmt><idno type="ISSN">1435-8603</idno></seriesStmt></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract">We previously reported that one of the ethylene response factors (ERFs), NtERF3, and other members of the subgroup VIII‐a ERFs of the AP2/ERF family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of NtERF3 in a cell death signalling pathway in tobacco plants, particularly downstream of NtSIPK/NtWIPK and NtWRKY1, which are mitogen‐activated protein kinases and a phosphorylation substrate of NtSIPK, respectively. An ERF‐associated amphiphilic repression (EAR) motif‐deficient NtERF3b mutant (NtERF3bΔEAR) that lacked cell death‐inducing ability suppressed the induction of cell death caused by NtERF3a. The transient co‐expression of NtERF3bΔEAR suppressed the hypersensitive reaction (HR)‐like cell death induced by NtSIPK and NtWRKY1. The induction of cell death by NtSIPK and NtWRKY1 was also inhibited in transgenic plants expressing NtERF3bΔEAR. Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the HR cell death signalling pathway mediated by SIPK/WIPK and WRKY1. Overall, these results suggest that NtERF3 functions downstream of NtSIPK/NtWIPK and NtWRKY1 in a cell death signalling pathway, with some feedback regulation.</div></front></TEI><istex><corpusName>wiley</corpusName><editor><json:item><name>G. 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Ogata</name><affiliations><json:string>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</json:string><json:string>Current Address: Biological Resources and Post‐harvest Division, Japan International Research Center for Agricultural Sciences (JIRCAS), TsukubaIbaraki, Japan</json:string></affiliations></json:item><json:item><name>H. Okada</name><affiliations><json:string>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</json:string><json:string>Current Address: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, KashiwaChiba, Japan</json:string></affiliations></json:item><json:item><name>H. Kawaide</name><affiliations><json:string>Institute of Agriculture, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</json:string></affiliations></json:item><json:item><name>H. Takahashi</name><affiliations><json:string>Department of Life Science, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan</json:string></affiliations></json:item><json:item><name>S. Seo</name><affiliations><json:string>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</json:string></affiliations></json:item><json:item><name>I. Mitsuhara</name><affiliations><json:string>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</json:string></affiliations></json:item><json:item><name>Y. Matsushita</name><affiliations><json:string>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</json:string><json:string>Y. Matsushita, Gene Research Center, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183‐8509, Japan.E‐mail:</json:string><json:string>E-mail: ymatsu@cc.tuat.ac.jp</json:string></affiliations></json:item></author><subject><json:item><lang><json:string>eng</json:string></lang><value>Ethylene response factor</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>hypersensitive reaction</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>N gene</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>salicylic acid‐induced protein kinase</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>tobacco (Nicotiana tabacum)</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>tobacco mosaic virus</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>WRKY</value></json:item></subject><articleId><json:string>PLB12349</json:string></articleId><arkIstex>ark:/67375/WNG-20MF36KR-5</arkIstex><language><json:string>eng</json:string></language><originalGenre><json:string>article</json:string></originalGenre><abstract>We previously reported that one of the ethylene response factors (ERFs), NtERF3, and other members of the subgroup VIII‐a ERFs of the AP2/ERF family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of NtERF3 in a cell death signalling pathway in tobacco plants, particularly downstream of NtSIPK/NtWIPK and NtWRKY1, which are mitogen‐activated protein kinases and a phosphorylation substrate of NtSIPK, respectively. An ERF‐associated amphiphilic repression (EAR) motif‐deficient NtERF3b mutant (NtERF3bΔEAR) that lacked cell death‐inducing ability suppressed the induction of cell death caused by NtERF3a. The transient co‐expression of NtERF3bΔEAR suppressed the hypersensitive reaction (HR)‐like cell death induced by NtSIPK and NtWRKY1. The induction of cell death by NtSIPK and NtWRKY1 was also inhibited in transgenic plants expressing NtERF3bΔEAR. Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the HR cell death signalling pathway mediated by SIPK/WIPK and WRKY1. Overall, these results suggest that NtERF3 functions downstream of NtSIPK/NtWIPK and NtWRKY1 in a cell death signalling pathway, with some feedback regulation.</abstract><qualityIndicators><score>9.172</score><pdfWordCount>8812</pdfWordCount><pdfCharCount>56307</pdfCharCount><pdfVersion>1.6</pdfVersion><pdfPageCount>11</pdfPageCount><pdfPageSize>595.276 x 799.37 pts</pdfPageSize><pdfWordsPerPage>801</pdfWordsPerPage><pdfText>true</pdfText><refBibsNative>true</refBibsNative><abstractWordCount>181</abstractWordCount><abstractCharCount>1306</abstractCharCount><keywordCount>7</keywordCount></qualityIndicators><title>Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants</title><genre><json:string>article</json:string></genre><host><title>Plant Biology</title><language><json:string>unknown</json:string></language><doi><json:string>10.1111/(ISSN)1438-8677</json:string></doi><issn><json:string>1435-8603</json:string></issn><eissn><json:string>1438-8677</json:string></eissn><publisherId><json:string>PLB</json:string></publisherId><volume>17</volume><issue>5</issue><pages><first>962</first><last>972</last><total>11</total></pages><genre><json:string>journal</json:string></genre><subject><json:item><value>Research Paper</value></json:item><json:item><value>RESEARCH PAPERS</value></json:item></subject></host><ark><json:string>ark:/67375/WNG-20MF36KR-5</json:string></ark><categories><wos><json:string>1 - science</json:string><json:string>2 - plant sciences</json:string></wos><scienceMetrix><json:string>1 - natural sciences</json:string><json:string>2 - biology</json:string><json:string>3 - plant biology & botany</json:string></scienceMetrix><scopus><json:string>1 - Life Sciences</json:string><json:string>2 - Agricultural and Biological Sciences</json:string><json:string>3 - Plant Science</json:string><json:string>1 - Life Sciences</json:string><json:string>2 - Agricultural and Biological Sciences</json:string><json:string>3 - Ecology, Evolution, Behavior and Systematics</json:string><json:string>1 - Health Sciences</json:string><json:string>2 - Medicine</json:string><json:string>3 - General Medicine</json:string></scopus><inist><json:string>1 - sciences appliquees, technologies et medecines</json:string><json:string>2 - sciences biologiques et medicales</json:string><json:string>3 - sciences biologiques fondamentales et appliquees. psychologie</json:string></inist></categories><publicationDate>2015</publicationDate><copyrightDate>2015</copyrightDate><doi><json:string>10.1111/plb.12349</json:string></doi><id>DFC4A8FA17F5D73FFCDB28816C63FB2A5CDAB6DC</id><score>1</score><fulltext><json:item><extension>pdf</extension><original>true</original><mimetype>application/pdf</mimetype><uri>https://api.istex.fr/ark:/67375/WNG-20MF36KR-5/fulltext.pdf</uri></json:item><json:item><extension>zip</extension><original>false</original><mimetype>application/zip</mimetype><uri>https://api.istex.fr/ark:/67375/WNG-20MF36KR-5/bundle.zip</uri></json:item><istex:fulltextTEI uri="https://api.istex.fr/ark:/67375/WNG-20MF36KR-5/fulltext.tei"><teiHeader><fileDesc><titleStmt><title level="a" type="main">Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants</title></titleStmt><publicationStmt><authority>ISTEX</authority><publisher ref="https://scientific-publisher.data.istex.fr/ark:/67375/H02-QW5Q88H5-V">Wiley Publishing Ltd</publisher><availability><licence>© 2015 German Botanical Society and The Royal Botanical Society of the Netherlands</licence></availability><date type="published" when="2015-09"></date></publicationStmt><notesStmt><note type="content-type" subtype="article" source="article" scheme="https://content-type.data.istex.fr/ark:/67375/XTP-6N5SZHKN-D">article</note><note type="publication-type" subtype="journal" scheme="https://publication-type.data.istex.fr/ark:/67375/JMC-0GLKJH51-B">journal</note></notesStmt><sourceDesc><biblStruct type="article"><analytic><title level="a" type="main">Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants</title><author xml:id="author-0000"><persName><forename type="first">T.</forename><surname>Ogata</surname></persName><affiliation><orgName type="division">Gene Research Center</orgName>
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<address><settlement>Fuchu</settlement>
<settlement>Tokyo</settlement>
<country key="JP" xml:lang="en">JAPAN</country></address></affiliation></author><editor xml:id="editor-0007"><persName><forename type="first">G.</forename><surname>Noctor</surname></persName></editor><idno type="istex">DFC4A8FA17F5D73FFCDB28816C63FB2A5CDAB6DC</idno><idno type="ark">ark:/67375/WNG-20MF36KR-5</idno><idno type="DOI">10.1111/plb.12349</idno><idno type="unit">PLB12349</idno><idno type="toTypesetVersion">file:PLB.PLB12349.pdf</idno></analytic><monogr><title level="j" type="main">Plant Biology</title><title level="j" type="alt">PLANT BIOLOGY</title><idno type="pISSN">1435-8603</idno><idno type="eISSN">1438-8677</idno><idno type="book-DOI">10.1111/(ISSN)1438-8677</idno><idno type="book-part-DOI">10.1111/plb.2015.17.issue-5</idno><idno type="product">PLB</idno><imprint><biblScope unit="vol">17</biblScope><biblScope unit="issue">5</biblScope><biblScope unit="page" from="962">962</biblScope><biblScope unit="page" to="972">972</biblScope><biblScope unit="page-count">11</biblScope><date type="published" when="2015-09"></date></imprint></monogr></biblStruct></sourceDesc></fileDesc><encodingDesc><schemaRef type="ODD" url="https://xml-schema.delivery.istex.fr/tei-istex.odd"></schemaRef><appInfo><application ident="pub2tei" version="1.0.10" when="2019-12-20"><label>pub2TEI-ISTEX</label><desc>A set of style sheets for converting XML documents encoded in various scientific publisher formats into a common TEI format.
<ref target="http://www.tei-c.org/">We use TEI</ref></desc></application></appInfo></encodingDesc><profileDesc><abstract style="main" xml:id="plb12349-abs-0001"><head>Abstract</head><p>We previously reported that one of the ethylene response factors (<hi rend="fc">ERF</hi>s), Nt<hi rend="fc">ERF</hi>3, and other members of the subgroup <hi rend="fc">VIII</hi>‐a <hi rend="fc">ERF</hi>s of the <hi rend="fc">AP</hi>2/<hi rend="fc">ERF</hi> family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of Nt<hi rend="fc">ERF</hi>3 in a cell death signalling pathway in tobacco plants, particularly downstream of Nt<hi rend="fc">SIPK</hi>/Nt<hi rend="fc">WIPK</hi> and Nt<hi rend="fc">WRKY</hi>1, which are mitogen‐activated protein kinases and a phosphorylation substrate of Nt<hi rend="fc">SIPK</hi>, respectively. An <hi rend="fc">ERF</hi>‐associated amphiphilic repression (<hi rend="fc">EAR</hi>) motif‐deficient <hi rend="italic">Nt<hi rend="fc">ERF</hi>3b</hi> mutant (<hi rend="italic">Nt<hi rend="fc">ERF</hi>3bΔ<hi rend="fc">EAR</hi></hi>) that lacked cell death‐inducing ability suppressed the induction of cell death caused by <hi rend="italic">Nt<hi rend="fc">ERF</hi>3a</hi>. The transient co‐expression of <hi rend="italic">Nt<hi rend="fc">ERF</hi>3bΔ<hi rend="fc">EAR</hi></hi> suppressed the hypersensitive reaction (<hi rend="fc">HR</hi>)‐like cell death induced by <hi rend="italic">Nt<hi rend="fc">SIPK</hi></hi> and <hi rend="italic">Nt<hi rend="fc">WRKY</hi>1</hi>. The induction of cell death by <hi rend="italic">Nt<hi rend="fc">SIPK</hi></hi> and <hi rend="italic">Nt<hi rend="fc">WRKY</hi>1</hi> was also inhibited in transgenic plants expressing <hi rend="italic">Nt<hi rend="fc">ERF</hi>3bΔ<hi rend="fc">EAR</hi></hi>. Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the <hi rend="fc">HR</hi> cell death signalling pathway mediated by <hi rend="fc">SIPK</hi>/<hi rend="fc">WIPK</hi> and <hi rend="fc">WRKY</hi>1. Overall, these results suggest that <hi rend="italic">Nt<hi rend="fc">ERF</hi>3</hi> functions downstream of <hi rend="italic">Nt<hi rend="fc">SIPK</hi></hi>/<hi rend="italic">Nt<hi rend="fc">WIPK</hi></hi> and <hi rend="italic">Nt<hi rend="fc">WRKY</hi>1</hi> in a cell death signalling pathway, with some feedback regulation.</p></abstract><textClass><keywords><term xml:id="plb12349-kwd-0001">Ethylene response factor</term><term xml:id="plb12349-kwd-0002">hypersensitive reaction</term><term xml:id="plb12349-kwd-0003"><hi rend="italic"><hi rend="fc">N</hi></hi> gene</term><term xml:id="plb12349-kwd-0004">salicylic acid‐induced protein kinase</term><term xml:id="plb12349-kwd-0005">tobacco (<hi rend="italic"><hi rend="fc">N</hi>icotiana tabacum</hi>)</term><term xml:id="plb12349-kwd-0006">tobacco mosaic virus</term><term xml:id="plb12349-kwd-0007"><hi rend="fc">WRKY</hi></term></keywords><keywords rend="articleCategory"><term>Research Paper</term></keywords><keywords rend="tocHeading1"><term>RESEARCH PAPERS</term></keywords></textClass><langUsage><language ident="en"></language></langUsage></profileDesc><revisionDesc><change when="2019-12-20" who="#istex" xml:id="pub2tei">formatting</change></revisionDesc></teiHeader></istex:fulltextTEI><json:item><extension>txt</extension><original>false</original><mimetype>text/plain</mimetype><uri>https://api.istex.fr/ark:/67375/WNG-20MF36KR-5/fulltext.txt</uri></json:item></fulltext><metadata><istex:metadataXml wicri:clean="Wiley, elements deleted: body"><istex:xmlDeclaration>version="1.0" encoding="UTF-8" standalone="yes"</istex:xmlDeclaration><istex:document><component type="serialArticle" version="2.0" xml:id="plb12349" xml:lang="en"><header><publicationMeta level="product"><doi origin="wiley" registered="yes">10.1111/(ISSN)1438-8677</doi><issn type="print">1435-8603</issn><issn type="electronic">1438-8677</issn><idGroup><id type="product" value="PLB"></id></idGroup><titleGroup><title sort="PLANT BIOLOGY" type="main">Plant Biology</title><title type="short">Plant Biol J</title></titleGroup></publicationMeta><publicationMeta level="part" position="50"><doi origin="wiley">10.1111/plb.2015.17.issue-5</doi><copyright ownership="thirdParty">© 2015 German Botanical Society and Royal Botanical Society of the Netherlands</copyright><numberingGroup><numbering type="journalVolume" number="17">17</numbering><numbering type="journalIssue">5</numbering></numberingGroup><coverDate startDate="2015-09">September 2015</coverDate></publicationMeta><publicationMeta level="unit" position="60" status="forIssue" type="article"><doi>10.1111/plb.12349</doi><idGroup><id type="unit" value="PLB12349"></id></idGroup><countGroup><count number="11" type="pageTotal"></count></countGroup><titleGroup><title type="articleCategory">Research Paper</title><title type="tocHeading1">RESEARCH PAPERS</title></titleGroup><copyright ownership="thirdParty">© 2015 German Botanical Society and The Royal Botanical Society of the Netherlands</copyright><eventGroup><event date="2015-04-10" type="manuscriptReceived"></event><event date="2015-05-15" type="manuscriptAccepted"></event><event agent="SPS" date="2015-05-20" type="xmlCreated"></event><event type="publishedOnlineAccepted" date="2015-05-20"></event><event type="publishedOnlineEarlyUnpaginated" date="2015-06-22"></event><event type="firstOnline" date="2015-06-22"></event><event type="publishedOnlineFinalForm" date="2015-08-10"></event><event type="xmlConverted" agent="Converter:WML3G_To_WML3G version:4.7.5 mode:FullText" date="2016-01-23"></event></eventGroup><numberingGroup><numbering type="pageFirst">962</numbering><numbering type="pageLast">972</numbering></numberingGroup><correspondenceTo><lineatedText><line><b>Correspondence</b></line><line>Y. Matsushita, Gene Research Center, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183‐8509, Japan.</line><line>E‐mail: <email>ymatsu@cc.tuat.ac.jp</email></line></lineatedText></correspondenceTo><linkGroup><link type="toTypesetVersion" href="file:PLB.PLB12349.pdf"></link></linkGroup></publicationMeta><contentMeta><titleGroup><title type="main">Involvement of Nt<fc>ERF</fc>3 in the cell death signalling pathway mediated by <fc>SIPK</fc>/<fc>WIPK</fc> and <fc>WRKY</fc>1 in tobacco plants</title><title type="shortAuthors">Ogata, Okada, Kawaide, Takahashi, Seo, Mitsuhara & Matsushita</title></titleGroup><creators><creator affiliationRef="#plb12349-aff-0001" creatorRole="author" currentRef="#plb12349-curr-0001" xml:id="plb12349-cr-0001"><personName><givenNames>T.</givenNames> <familyName>Ogata</familyName></personName></creator><creator affiliationRef="#plb12349-aff-0001" creatorRole="author" currentRef="#plb12349-curr-0002" xml:id="plb12349-cr-0002"><personName><givenNames>H.</givenNames> <familyName>Okada</familyName></personName></creator><creator affiliationRef="#plb12349-aff-0002" creatorRole="author" xml:id="plb12349-cr-0003"><personName><givenNames>H.</givenNames> <familyName>Kawaide</familyName></personName></creator><creator affiliationRef="#plb12349-aff-0003" creatorRole="author" xml:id="plb12349-cr-0004"><personName><givenNames>H.</givenNames> <familyName>Takahashi</familyName></personName></creator><creator affiliationRef="#plb12349-aff-0004" creatorRole="author" xml:id="plb12349-cr-0005"><personName><givenNames>S.</givenNames> <familyName>Seo</familyName></personName></creator><creator affiliationRef="#plb12349-aff-0004" creatorRole="author" xml:id="plb12349-cr-0006"><personName><givenNames>I.</givenNames> <familyName>Mitsuhara</familyName></personName></creator><creator affiliationRef="#plb12349-aff-0001" corresponding="yes" creatorRole="author" xml:id="plb12349-cr-0007"><personName><givenNames>Y.</givenNames> <familyName>Matsushita</familyName></personName></creator><creator creatorRole="editor" xml:id="plb12349-cr-0008"><personName><givenNames>G.</givenNames> <familyName>Noctor</familyName></personName></creator></creators><affiliationGroup><affiliation countryCode="JP" type="organization" xml:id="plb12349-aff-0001"><orgDiv>Gene Research Center</orgDiv> <orgName>Tokyo University of Agriculture and Technology</orgName> <address><city>Fuchu</city> <city>Tokyo</city> <country>Japan</country></address></affiliation><affiliation countryCode="JP" type="organization" xml:id="plb12349-aff-0002"><orgDiv>Institute of Agriculture</orgDiv> <orgName>Tokyo University of Agriculture and Technology</orgName> <address><city>Fuchu</city> <city>Tokyo</city> <country>Japan</country></address></affiliation><affiliation countryCode="JP" type="organization" xml:id="plb12349-aff-0003"><orgDiv>Department of Life Science</orgDiv> <orgDiv>Graduate School of Agricultural Science</orgDiv> <orgName>Tohoku University</orgName> <address><city>Sendai</city> <country>Japan</country></address></affiliation><affiliation countryCode="JP" type="organization" xml:id="plb12349-aff-0004"><orgDiv>Plant‐Microbe Interactions Research Unit</orgDiv> <orgName>National Institute of Agrobiological Sciences</orgName> <address><city>Tsukuba</city> <city>Ibaraki</city> <country>Japan</country></address></affiliation><affiliation countryCode="JP" type="organization" xml:id="plb12349-curr-0001"><orgDiv>Biological Resources and Post‐harvest Division</orgDiv> <orgName>Japan International Research Center for Agricultural Sciences (JIRCAS)</orgName> <address><city>Tsukuba</city> <city>Ibaraki</city> <country>Japan</country></address></affiliation><affiliation countryCode="JP" type="organization" xml:id="plb12349-curr-0002"><orgDiv>Department of Integrated Biosciences</orgDiv> <orgDiv>Graduate School of Frontier Sciences</orgDiv> <orgName>University of Tokyo</orgName> <address><city>Kashiwa</city> <city>Chiba</city> <country>Japan</country></address></affiliation></affiliationGroup><keywordGroup type="author"><keyword xml:id="plb12349-kwd-0001">Ethylene response factor</keyword><keyword xml:id="plb12349-kwd-0002">hypersensitive reaction</keyword><keyword xml:id="plb12349-kwd-0003"><i><fc>N</fc></i> gene</keyword><keyword xml:id="plb12349-kwd-0004">salicylic acid‐induced protein kinase</keyword><keyword xml:id="plb12349-kwd-0005">tobacco (<i><fc>N</fc>icotiana tabacum</i>)</keyword><keyword xml:id="plb12349-kwd-0006">tobacco mosaic virus</keyword><keyword xml:id="plb12349-kwd-0007"><fc>WRKY</fc></keyword></keywordGroup><fundingInfo><fundingAgency>Japan Society for the Promotion of Science (JSPS)</fundingAgency><fundingNumber>19580045</fundingNumber></fundingInfo><fundingInfo><fundingAgency>JSPS Fellows</fundingAgency><fundingNumber>23‐8011</fundingNumber></fundingInfo><fundingInfo><fundingAgency>Collaborative Research Ring of Tokyo University of Agriculture and Technology (TUAT)</fundingAgency></fundingInfo><fundingInfo><fundingAgency>TUAT Foundation</fundingAgency></fundingInfo><supportingInformation><supportingInfoItem><mediaResource alt="supporting" mimeType="image/tiff" rendition="webOriginal" href="urn-x:wiley:14358603:media:plb12349:plb12349-sup-0001-FigS1"></mediaResource><caption><b>Fig. S1.</b> Co‐expression of <i>NtERF3bΔEAR</i> suppresses cell death induction by <i>NtERF6a</i>,<i> NtERF#111</i> and <i>NtERF#227</i>.</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting" mimeType="image/tiff" rendition="webOriginal" href="urn-x:wiley:14358603:media:plb12349:plb12349-sup-0002-FigS2"></mediaResource><caption><b>Fig. S2.</b> No inhibitory effect of <i>NtERF3bΔEAR</i> on cell death induction by <i>p50</i>.</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting" mimeType="image/tiff" rendition="webOriginal" href="urn-x:wiley:14358603:media:plb12349:plb12349-sup-0003-FigS3"></mediaResource><caption><b>Fig. S3.</b> Inhibitory effect of an EAR motif‐deficient form of <i>NtERF3b</i> on the cell death induced co‐operatively by <i>NtSIPK</i> with <i>NtWRKY</i>.</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting" mimeType="image/tiff" rendition="webOriginal" href="urn-x:wiley:14358603:media:plb12349:plb12349-sup-0004-FigS4"></mediaResource><caption><b>Fig. S4.</b> Transgenic tobacco plants harbouring 35S‐<i>NtERF3bΔEAR‐HA</i>.</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting" mimeType="image/tiff" rendition="webOriginal" href="urn-x:wiley:14358603:media:plb12349:plb12349-sup-0005-FigS5"></mediaResource><caption><b>Fig. S5.</b> The cell death‐inducing ability of <i>AtERF#080</i> in subgroup VIII‐a ERFs is affected in <i>NtWIPK</i> and <i>NtSIPK</i> double‐silenced tobacco.</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting" mimeType="image/tiff" rendition="webOriginal" href="urn-x:wiley:14358603:media:plb12349:plb12349-sup-0006-FigS6"></mediaResource><caption><b>Fig. S6.</b> Cell death induction by subgroup VIII‐a <i>ERFs</i> is not compromised at high temperature.</caption></supportingInfoItem></supportingInformation><abstractGroup><abstract type="main" xml:id="plb12349-abs-0001"><title type="main">Abstract</title><p>We previously reported that one of the ethylene response factors (<fc>ERF</fc>s), Nt<fc>ERF</fc>3, and other members of the subgroup <fc>VIII</fc>‐a <fc>ERF</fc>s of the <fc>AP</fc>2/<fc>ERF</fc> family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of Nt<fc>ERF</fc>3 in a cell death signalling pathway in tobacco plants, particularly downstream of Nt<fc>SIPK</fc>/Nt<fc>WIPK</fc> and Nt<fc>WRKY</fc>1, which are mitogen‐activated protein kinases and a phosphorylation substrate of Nt<fc>SIPK</fc>, respectively. An <fc>ERF</fc>‐associated amphiphilic repression (<fc>EAR</fc>) motif‐deficient <i>Nt<fc>ERF</fc>3b</i> mutant (<i>Nt<fc>ERF</fc>3bΔ<fc>EAR</fc></i>) that lacked cell death‐inducing ability suppressed the induction of cell death caused by <i>Nt<fc>ERF</fc>3a</i>. The transient co‐expression of <i>Nt<fc>ERF</fc>3bΔ<fc>EAR</fc></i> suppressed the hypersensitive reaction (<fc>HR</fc>)‐like cell death induced by <i>Nt<fc>SIPK</fc></i> and <i>Nt<fc>WRKY</fc>1</i>. The induction of cell death by <i>Nt<fc>SIPK</fc></i> and <i>Nt<fc>WRKY</fc>1</i> was also inhibited in transgenic plants expressing <i>Nt<fc>ERF</fc>3bΔ<fc>EAR</fc></i>. Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the <fc>HR</fc> cell death signalling pathway mediated by <fc>SIPK</fc>/<fc>WIPK</fc> and <fc>WRKY</fc>1. Overall, these results suggest that <i>Nt<fc>ERF</fc>3</i> functions downstream of <i>Nt<fc>SIPK</fc></i>/<i>Nt<fc>WIPK</fc></i> and <i>Nt<fc>WRKY</fc>1</i> in a cell death signalling pathway, with some feedback regulation.</p></abstract></abstractGroup></contentMeta></header></component></istex:document></istex:metadataXml><mods version="3.6"><titleInfo lang="en"><title>Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants</title></titleInfo><titleInfo type="alternative" contentType="CDATA" lang="en"><title>Involvement of NtERF3 in the cell death signalling pathway mediated by SIPK/WIPK and WRKY1 in tobacco plants</title></titleInfo><name type="personal"><namePart type="given">T.</namePart><namePart type="family">Ogata</namePart><affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</affiliation><affiliation>Current Address: Biological Resources and Post‐harvest Division, Japan International Research Center for Agricultural Sciences (JIRCAS), TsukubaIbaraki, Japan</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">H.</namePart><namePart type="family">Okada</namePart><affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</affiliation><affiliation>Current Address: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, KashiwaChiba, Japan</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">H.</namePart><namePart type="family">Kawaide</namePart><affiliation>Institute of Agriculture, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">H.</namePart><namePart type="family">Takahashi</namePart><affiliation>Department of Life Science, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">S.</namePart><namePart type="family">Seo</namePart><affiliation>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">I.</namePart><namePart type="family">Mitsuhara</namePart><affiliation>Plant‐Microbe Interactions Research Unit, National Institute of Agrobiological Sciences, TsukubaIbaraki, Japan</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Y.</namePart><namePart type="family">Matsushita</namePart><affiliation>Gene Research Center, Tokyo University of Agriculture and Technology, FuchuTokyo, Japan</affiliation><affiliation>Y. Matsushita, Gene Research Center, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183‐8509, Japan.E‐mail:</affiliation><affiliation>E-mail: ymatsu@cc.tuat.ac.jp</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">G.</namePart><namePart type="family">Noctor</namePart><role><roleTerm type="text">editor</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="article" displayLabel="article" authority="ISTEX" authorityURI="https://content-type.data.istex.fr" valueURI="https://content-type.data.istex.fr/ark:/67375/XTP-6N5SZHKN-D">article</genre><originInfo><publisher>Blackwell Publishing Ltd</publisher><dateIssued encoding="w3cdtf">2015-09</dateIssued><dateCreated encoding="w3cdtf">2015-05-20</dateCreated><dateCaptured encoding="w3cdtf">2015-04-10</dateCaptured><dateValid encoding="w3cdtf">2015-05-15</dateValid><copyrightDate encoding="w3cdtf">2015</copyrightDate></originInfo><language><languageTerm type="code" authority="rfc3066">en</languageTerm><languageTerm type="code" authority="iso639-2b">eng</languageTerm></language><abstract>We previously reported that one of the ethylene response factors (ERFs), NtERF3, and other members of the subgroup VIII‐a ERFs of the AP2/ERF family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of NtERF3 in a cell death signalling pathway in tobacco plants, particularly downstream of NtSIPK/NtWIPK and NtWRKY1, which are mitogen‐activated protein kinases and a phosphorylation substrate of NtSIPK, respectively. An ERF‐associated amphiphilic repression (EAR) motif‐deficient NtERF3b mutant (NtERF3bΔEAR) that lacked cell death‐inducing ability suppressed the induction of cell death caused by NtERF3a. The transient co‐expression of NtERF3bΔEAR suppressed the hypersensitive reaction (HR)‐like cell death induced by NtSIPK and NtWRKY1. The induction of cell death by NtSIPK and NtWRKY1 was also inhibited in transgenic plants expressing NtERF3bΔEAR. Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the HR cell death signalling pathway mediated by SIPK/WIPK and WRKY1. Overall, these results suggest that NtERF3 functions downstream of NtSIPK/NtWIPK and NtWRKY1 in a cell death signalling pathway, with some feedback regulation.</abstract><note type="additional physical form">Fig. S1. Co‐expression of NtERF3bΔEAR suppresses cell death induction by NtERF6a, NtERF#111 and NtERF#227.Fig. S2. No inhibitory effect of NtERF3bΔEAR on cell death induction by p50.Fig. S3. Inhibitory effect of an EAR motif‐deficient form of NtERF3b on the cell death induced co‐operatively by NtSIPK with NtWRKY.Fig. S4. Transgenic tobacco plants harbouring 35S‐NtERF3bΔEAR‐HA.Fig. S5. The cell death‐inducing ability of AtERF#080 in subgroup VIII‐a ERFs is affected in NtWIPK and NtSIPK double‐silenced tobacco.Fig. S6. Cell death induction by subgroup VIII‐a ERFs is not compromised at high temperature.</note><note type="funding">Japan Society for the Promotion of Science (JSPS) - No. 19580045; </note><note type="funding">JSPS Fellows - No. 23‐8011; </note><note type="funding">Collaborative Research Ring of Tokyo University of Agriculture and Technology (TUAT)</note><note type="funding">TUAT Foundation</note><subject><genre>keywords</genre><topic>Ethylene response factor</topic><topic>hypersensitive reaction</topic><topic>N gene</topic><topic>salicylic acid‐induced protein kinase</topic><topic>tobacco (Nicotiana tabacum)</topic><topic>tobacco mosaic virus</topic><topic>WRKY</topic></subject><relatedItem type="host"><titleInfo><title>Plant Biology</title></titleInfo><titleInfo type="abbreviated"><title>Plant Biol J</title></titleInfo><genre type="journal" authority="ISTEX" authorityURI="https://publication-type.data.istex.fr" valueURI="https://publication-type.data.istex.fr/ark:/67375/JMC-0GLKJH51-B">journal</genre><subject><genre>article-category</genre><topic>Research Paper</topic><topic>RESEARCH PAPERS</topic></subject><identifier type="ISSN">1435-8603</identifier><identifier type="eISSN">1438-8677</identifier><identifier type="DOI">10.1111/(ISSN)1438-8677</identifier><identifier type="PublisherID">PLB</identifier><part><date>2015</date><detail type="volume"><caption>vol.</caption><number>17</number></detail><detail type="issue"><caption>no.</caption><number>5</number></detail><extent unit="pages"><start>962</start><end>972</end><total>11</total></extent></part></relatedItem><relatedItem type="references" displayLabel="plb12349-cit-0001"><titleInfo><title>Constitutive expression of ETHYLENE‐RESPONSE‐FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi</title></titleInfo><name type="personal"><namePart type="given">M.</namePart><namePart type="family">Berrocal‐Lobo</namePart><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">A.</namePart><namePart type="family">Molina</namePart><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">R.</namePart><namePart type="family">Solano</namePart><role><roleTerm type="text">author</roleTerm></role></name><genre>journal-article</genre><note type="citation/reference">Berrocal‐Lobo M., Molina A., Solano R. 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PLoS Pathogens, 6, e1000844.</note><part><date>2010</date><detail type="volume"><caption>vol.</caption><number>6</number></detail><extent unit="pages"><start>e1000844</start></extent></part><relatedItem type="host"><titleInfo><title>PLoS Pathogens</title></titleInfo><part><date>2010</date><detail type="volume"><caption>vol.</caption><number>6</number></detail><extent unit="pages"><start>e1000844</start></extent></part></relatedItem></relatedItem><identifier type="istex">DFC4A8FA17F5D73FFCDB28816C63FB2A5CDAB6DC</identifier><identifier type="ark">ark:/67375/WNG-20MF36KR-5</identifier><identifier type="DOI">10.1111/plb.12349</identifier><identifier type="ArticleID">PLB12349</identifier><accessCondition type="use and reproduction" contentType="copyright">© 2015 German Botanical Society and Royal Botanical Society of the Netherlands© 2015 German Botanical Society and The Royal Botanical Society of the Netherlands</accessCondition><recordInfo><recordContentSource authority="ISTEX" authorityURI="https://loaded-corpus.data.istex.fr" valueURI="https://loaded-corpus.data.istex.fr/ark:/67375/XBH-L0C46X92-X">wiley</recordContentSource><recordOrigin>Converted from (version ) to MODS version 3.6.</recordOrigin><recordCreationDate encoding="w3cdtf">2019-11-16</recordCreationDate></recordInfo></mods><json:item><extension>json</extension><original>false</original><mimetype>application/json</mimetype><uri>https://api.istex.fr/ark:/67375/WNG-20MF36KR-5/record.json</uri></json:item></metadata><serie></serie></istex></record>Pour manipuler ce document sous Unix (Dilib)
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