WRKY42 transcription factor positively regulates leaf senescence through modulating SA and ROS synthesis in Arabidopsis thaliana
SUMMARY Leaf senescence represents the final stage of leaf growth and development, and its onset and progression are strictly regulated; however, the underlying regulatory mechanisms remain largely unknown. In this study we found that WRKY42 was highly induced during leaf senescence. Loss‐of‐functio...
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creator | Niu, Fangfang Cui, Xing Zhao, Peiyu Sun, Mengting Yang, Bo Deyholos, Michael K. Li, Ye Zhao, Xinjie Jiang, Yuan‐Qing |
description | SUMMARY
Leaf senescence represents the final stage of leaf growth and development, and its onset and progression are strictly regulated; however, the underlying regulatory mechanisms remain largely unknown. In this study we found that WRKY42 was highly induced during leaf senescence. Loss‐of‐function wrky42 mutants showed delayed leaf senescence whereas the overexpression of WRKY42 accelerated senescence. Transcriptome analysis revealed 2721 differentially expressed genes between wild‐type and WRKY42‐overexpressing plants, including genes involved in salicylic acid (SA) and reactive oxygen species (ROS) synthesis as well as several senescence‐associated genes (SAGs). Moreover, WRKY42 activated the transcription of isochorismate synthase 1 (ICS1), respiratory burst oxidase homolog F (RbohF) and a few SAG genes. Consistently, the expression of these genes was reduced in wrky42 mutants but was markedly increased in transgenic Arabidopsis overexpressing WRKY42. Both in vitro electrophoretic mobility shift assays (EMSAs) and in vivo chromatin immunoprecipitation and dual luciferase assays demonstrated that WRKY42 directly bound to the promoters of ICS1 and RbohF, as well as a few SAGs, to activate their expression. Genetic analysis further showed that mutations of ICS1 and RbohF suppressed the early senescence phenotype evoked by WRKY42 overexpression. Thus, we have identified WRKY42 as a novel transcription factor positively regulating leaf senescence by directly activating the transcription of ICS1, RbohF and SAGs, without any seed yield penalty.
Significance Statement
The Arabidopsis transcription factor gene WRKY42 is induced during leaf senescence and is a senescence‐associated gene (SAG). WRKY42 positively regulates leaf senescence through activating the expression of genes implicated in salicylic acid (SA) and reactive oxygen species (ROS) synthesis, as well as the expression of several SAGs, without seed yield penalty. |
doi_str_mv | 10.1111/tpj.14914 |
format | Article |
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Leaf senescence represents the final stage of leaf growth and development, and its onset and progression are strictly regulated; however, the underlying regulatory mechanisms remain largely unknown. In this study we found that WRKY42 was highly induced during leaf senescence. Loss‐of‐function wrky42 mutants showed delayed leaf senescence whereas the overexpression of WRKY42 accelerated senescence. Transcriptome analysis revealed 2721 differentially expressed genes between wild‐type and WRKY42‐overexpressing plants, including genes involved in salicylic acid (SA) and reactive oxygen species (ROS) synthesis as well as several senescence‐associated genes (SAGs). Moreover, WRKY42 activated the transcription of isochorismate synthase 1 (ICS1), respiratory burst oxidase homolog F (RbohF) and a few SAG genes. Consistently, the expression of these genes was reduced in wrky42 mutants but was markedly increased in transgenic Arabidopsis overexpressing WRKY42. Both in vitro electrophoretic mobility shift assays (EMSAs) and in vivo chromatin immunoprecipitation and dual luciferase assays demonstrated that WRKY42 directly bound to the promoters of ICS1 and RbohF, as well as a few SAGs, to activate their expression. Genetic analysis further showed that mutations of ICS1 and RbohF suppressed the early senescence phenotype evoked by WRKY42 overexpression. Thus, we have identified WRKY42 as a novel transcription factor positively regulating leaf senescence by directly activating the transcription of ICS1, RbohF and SAGs, without any seed yield penalty.
Significance Statement
The Arabidopsis transcription factor gene WRKY42 is induced during leaf senescence and is a senescence‐associated gene (SAG). WRKY42 positively regulates leaf senescence through activating the expression of genes implicated in salicylic acid (SA) and reactive oxygen species (ROS) synthesis, as well as the expression of several SAGs, without seed yield penalty.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.14914</identifier><identifier>PMID: 32634860</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Aging - genetics ; Aging - metabolism ; Arabidopsis ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Arabidopsis Proteins - metabolism ; Arabidopsis Proteins - physiology ; Chromatin ; Electrophoretic mobility ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Plant ; Genes ; Genes, Plant - physiology ; Genetic analysis ; Homology ; Immunoprecipitation ; Isochorismate synthase ; leaf senescence ; Leaves ; Mutants ; Mutation ; Phenotypes ; Plant Growth Regulators - metabolism ; Plant Leaves - metabolism ; Plant Leaves - physiology ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Regulatory mechanisms (biology) ; Respiratory burst oxidase ; Salicylic acid ; Salicylic Acid - metabolism ; Senescence ; Synthesis ; Transcription factors ; Transcription Factors - metabolism ; Transcription Factors - physiology ; WRKY42</subject><ispartof>The Plant journal : for cell and molecular biology, 2020-09, Vol.104 (1), p.171-184</ispartof><rights>2020 Society for Experimental Biology and John Wiley & Sons Ltd</rights><rights>2020 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2020 Society for Experimental Biology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3534-118cf0fec830a962b1aa961420447ada60eb2fb60ac965ad277a3f494d8a9f5a3</citedby><cites>FETCH-LOGICAL-c3534-118cf0fec830a962b1aa961420447ada60eb2fb60ac965ad277a3f494d8a9f5a3</cites><orcidid>0000-0003-4205-3891 ; 0000-0003-1367-922X ; 0000-0002-0421-3754</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.14914$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.14914$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32634860$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Niu, Fangfang</creatorcontrib><creatorcontrib>Cui, Xing</creatorcontrib><creatorcontrib>Zhao, Peiyu</creatorcontrib><creatorcontrib>Sun, Mengting</creatorcontrib><creatorcontrib>Yang, Bo</creatorcontrib><creatorcontrib>Deyholos, Michael K.</creatorcontrib><creatorcontrib>Li, Ye</creatorcontrib><creatorcontrib>Zhao, Xinjie</creatorcontrib><creatorcontrib>Jiang, Yuan‐Qing</creatorcontrib><title>WRKY42 transcription factor positively regulates leaf senescence through modulating SA and ROS synthesis in Arabidopsis thaliana</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Leaf senescence represents the final stage of leaf growth and development, and its onset and progression are strictly regulated; however, the underlying regulatory mechanisms remain largely unknown. In this study we found that WRKY42 was highly induced during leaf senescence. Loss‐of‐function wrky42 mutants showed delayed leaf senescence whereas the overexpression of WRKY42 accelerated senescence. Transcriptome analysis revealed 2721 differentially expressed genes between wild‐type and WRKY42‐overexpressing plants, including genes involved in salicylic acid (SA) and reactive oxygen species (ROS) synthesis as well as several senescence‐associated genes (SAGs). Moreover, WRKY42 activated the transcription of isochorismate synthase 1 (ICS1), respiratory burst oxidase homolog F (RbohF) and a few SAG genes. Consistently, the expression of these genes was reduced in wrky42 mutants but was markedly increased in transgenic Arabidopsis overexpressing WRKY42. Both in vitro electrophoretic mobility shift assays (EMSAs) and in vivo chromatin immunoprecipitation and dual luciferase assays demonstrated that WRKY42 directly bound to the promoters of ICS1 and RbohF, as well as a few SAGs, to activate their expression. Genetic analysis further showed that mutations of ICS1 and RbohF suppressed the early senescence phenotype evoked by WRKY42 overexpression. Thus, we have identified WRKY42 as a novel transcription factor positively regulating leaf senescence by directly activating the transcription of ICS1, RbohF and SAGs, without any seed yield penalty.
Significance Statement
The Arabidopsis transcription factor gene WRKY42 is induced during leaf senescence and is a senescence‐associated gene (SAG). WRKY42 positively regulates leaf senescence through activating the expression of genes implicated in salicylic acid (SA) and reactive oxygen species (ROS) synthesis, as well as the expression of several SAGs, without seed yield penalty.</description><subject>Aging - genetics</subject><subject>Aging - metabolism</subject><subject>Arabidopsis</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis Proteins - physiology</subject><subject>Chromatin</subject><subject>Electrophoretic mobility</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genes, Plant - physiology</subject><subject>Genetic analysis</subject><subject>Homology</subject><subject>Immunoprecipitation</subject><subject>Isochorismate synthase</subject><subject>leaf senescence</subject><subject>Leaves</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Phenotypes</subject><subject>Plant Growth Regulators - metabolism</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Leaves - physiology</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Regulatory mechanisms (biology)</subject><subject>Respiratory burst oxidase</subject><subject>Salicylic acid</subject><subject>Salicylic Acid - metabolism</subject><subject>Senescence</subject><subject>Synthesis</subject><subject>Transcription factors</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription Factors - physiology</subject><subject>WRKY42</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10U2LFDEQBuAgijuuHvwDEvCih97NV6enj8Pi98LK7op6aqrTlZkMPUmbpJW5-dPNOKsHwVyKwMNLFS8hTzk74-Wd52l7xlXL1T2y4FLXleTyy32yYK1mVaO4OCGPUtoyxhup1UNyIoWWaqnZgvz8fP3hqxI0R_DJRDdlFzy1YHKIdArJZfcdxz2NuJ5HyJjoiGBpQo_JoDdI8yaGeb2huzAchPNrerOi4Ad6fXVD097nDSaXqPN0FaF3Q5gO37yB0YGHx-SBhTHhk7t5Sj69fnV78ba6vHrz7mJ1WRlZS1VxvjSWWTRLyaDVoudQBleCKdXAAJphL2yvGZhW1zCIpgFpVauGJbS2BnlKXhxzpxi-zZhyt3PlgnEEj2FOnVCCKy1aLgt9_g_dhjn6sl1Rqqk1l-1BvTwqE0NKEW03RbeDuO846w61dKWW7nctxT67S5z7HQ5_5Z8eCjg_gh9uxP3_k7rbj--Pkb8A4hSYQg</recordid><startdate>202009</startdate><enddate>202009</enddate><creator>Niu, Fangfang</creator><creator>Cui, Xing</creator><creator>Zhao, Peiyu</creator><creator>Sun, Mengting</creator><creator>Yang, Bo</creator><creator>Deyholos, Michael K.</creator><creator>Li, Ye</creator><creator>Zhao, Xinjie</creator><creator>Jiang, Yuan‐Qing</creator><general>Blackwell Publishing Ltd</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-4205-3891</orcidid><orcidid>https://orcid.org/0000-0003-1367-922X</orcidid><orcidid>https://orcid.org/0000-0002-0421-3754</orcidid></search><sort><creationdate>202009</creationdate><title>WRKY42 transcription factor positively regulates leaf senescence through modulating SA and ROS synthesis in Arabidopsis thaliana</title><author>Niu, Fangfang ; Cui, Xing ; Zhao, Peiyu ; Sun, Mengting ; Yang, Bo ; Deyholos, Michael K. ; Li, Ye ; Zhao, Xinjie ; Jiang, Yuan‐Qing</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3534-118cf0fec830a962b1aa961420447ada60eb2fb60ac965ad277a3f494d8a9f5a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Aging - genetics</topic><topic>Aging - metabolism</topic><topic>Arabidopsis</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis Proteins - physiology</topic><topic>Chromatin</topic><topic>Electrophoretic mobility</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Genes, Plant - physiology</topic><topic>Genetic analysis</topic><topic>Homology</topic><topic>Immunoprecipitation</topic><topic>Isochorismate synthase</topic><topic>leaf senescence</topic><topic>Leaves</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Phenotypes</topic><topic>Plant Growth Regulators - metabolism</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Leaves - physiology</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Regulatory mechanisms (biology)</topic><topic>Respiratory burst oxidase</topic><topic>Salicylic acid</topic><topic>Salicylic Acid - metabolism</topic><topic>Senescence</topic><topic>Synthesis</topic><topic>Transcription factors</topic><topic>Transcription Factors - metabolism</topic><topic>Transcription Factors - physiology</topic><topic>WRKY42</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Niu, Fangfang</creatorcontrib><creatorcontrib>Cui, Xing</creatorcontrib><creatorcontrib>Zhao, Peiyu</creatorcontrib><creatorcontrib>Sun, Mengting</creatorcontrib><creatorcontrib>Yang, Bo</creatorcontrib><creatorcontrib>Deyholos, Michael K.</creatorcontrib><creatorcontrib>Li, Ye</creatorcontrib><creatorcontrib>Zhao, Xinjie</creatorcontrib><creatorcontrib>Jiang, Yuan‐Qing</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Niu, Fangfang</au><au>Cui, Xing</au><au>Zhao, Peiyu</au><au>Sun, Mengting</au><au>Yang, Bo</au><au>Deyholos, Michael K.</au><au>Li, Ye</au><au>Zhao, Xinjie</au><au>Jiang, Yuan‐Qing</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>WRKY42 transcription factor positively regulates leaf senescence through modulating SA and ROS synthesis in Arabidopsis thaliana</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2020-09</date><risdate>2020</risdate><volume>104</volume><issue>1</issue><spage>171</spage><epage>184</epage><pages>171-184</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Leaf senescence represents the final stage of leaf growth and development, and its onset and progression are strictly regulated; however, the underlying regulatory mechanisms remain largely unknown. In this study we found that WRKY42 was highly induced during leaf senescence. Loss‐of‐function wrky42 mutants showed delayed leaf senescence whereas the overexpression of WRKY42 accelerated senescence. Transcriptome analysis revealed 2721 differentially expressed genes between wild‐type and WRKY42‐overexpressing plants, including genes involved in salicylic acid (SA) and reactive oxygen species (ROS) synthesis as well as several senescence‐associated genes (SAGs). Moreover, WRKY42 activated the transcription of isochorismate synthase 1 (ICS1), respiratory burst oxidase homolog F (RbohF) and a few SAG genes. Consistently, the expression of these genes was reduced in wrky42 mutants but was markedly increased in transgenic Arabidopsis overexpressing WRKY42. Both in vitro electrophoretic mobility shift assays (EMSAs) and in vivo chromatin immunoprecipitation and dual luciferase assays demonstrated that WRKY42 directly bound to the promoters of ICS1 and RbohF, as well as a few SAGs, to activate their expression. Genetic analysis further showed that mutations of ICS1 and RbohF suppressed the early senescence phenotype evoked by WRKY42 overexpression. Thus, we have identified WRKY42 as a novel transcription factor positively regulating leaf senescence by directly activating the transcription of ICS1, RbohF and SAGs, without any seed yield penalty.
Significance Statement
The Arabidopsis transcription factor gene WRKY42 is induced during leaf senescence and is a senescence‐associated gene (SAG). WRKY42 positively regulates leaf senescence through activating the expression of genes implicated in salicylic acid (SA) and reactive oxygen species (ROS) synthesis, as well as the expression of several SAGs, without seed yield penalty.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32634860</pmid><doi>10.1111/tpj.14914</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-4205-3891</orcidid><orcidid>https://orcid.org/0000-0003-1367-922X</orcidid><orcidid>https://orcid.org/0000-0002-0421-3754</orcidid></addata></record> |
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subjects | Aging - genetics Aging - metabolism Arabidopsis Arabidopsis - metabolism Arabidopsis - physiology Arabidopsis Proteins - metabolism Arabidopsis Proteins - physiology Chromatin Electrophoretic mobility Gene expression Gene Expression Profiling Gene Expression Regulation, Plant Genes Genes, Plant - physiology Genetic analysis Homology Immunoprecipitation Isochorismate synthase leaf senescence Leaves Mutants Mutation Phenotypes Plant Growth Regulators - metabolism Plant Leaves - metabolism Plant Leaves - physiology Reactive oxygen species Reactive Oxygen Species - metabolism Regulatory mechanisms (biology) Respiratory burst oxidase Salicylic acid Salicylic Acid - metabolism Senescence Synthesis Transcription factors Transcription Factors - metabolism Transcription Factors - physiology WRKY42 |
title | WRKY42 transcription factor positively regulates leaf senescence through modulating SA and ROS synthesis in Arabidopsis thaliana |
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