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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Veröffentlicht in:The Plant journal : for cell and molecular biology 2020-09, Vol.104 (1), p.171-184
Hauptverfasser: Niu, Fangfang, Cui, Xing, Zhao, Peiyu, Sun, Mengting, Yang, Bo, Deyholos, Michael K., Li, Ye, Zhao, Xinjie, Jiang, Yuan‐Qing
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container_title The Plant journal : for cell and molecular biology
container_volume 104
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
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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 &amp; Sons Ltd</rights><rights>2020 Society for Experimental Biology and John Wiley &amp; Sons Ltd.</rights><rights>Copyright © 2020 Society for Experimental Biology and John Wiley &amp; 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. 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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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