Ethylene‐MPK8‐ERF.C1‐PR module confers resistance against Botrytis cinerea in tomato fruit without compromising ripening

Summary The plant hormone ethylene plays a critical role in fruit defense against Botrytis cinerea attack, but the underlying mechanisms remain poorly understood. Here, we showed that ethylene response factor SlERF.C1 acts as a key regulator to trigger the ethylene‐mediated defense against B. cinere...

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Veröffentlicht in:The New phytologist 2024-04, Vol.242 (2), p.592-609
Hauptverfasser: Deng, Heng, Pei, Yangang, Xu, Xin, Du, Xiaofei, Xue, Qihan, Gao, Zhuo, Shu, Peng, Wu, Yi, Liu, Zhaoqiao, Jian, Yongfei, Wu, Mengbo, Wang, Yikui, Li, Zhengguo, Pirrello, Julien, Bouzayen, Mondher, Deng, Wei, Hong, Yiguo, Liu, Mingchun
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container_end_page 609
container_issue 2
container_start_page 592
container_title The New phytologist
container_volume 242
creator Deng, Heng
Pei, Yangang
Xu, Xin
Du, Xiaofei
Xue, Qihan
Gao, Zhuo
Shu, Peng
Wu, Yi
Liu, Zhaoqiao
Jian, Yongfei
Wu, Mengbo
Wang, Yikui
Li, Zhengguo
Pirrello, Julien
Bouzayen, Mondher
Deng, Wei
Hong, Yiguo
Liu, Mingchun
description Summary The plant hormone ethylene plays a critical role in fruit defense against Botrytis cinerea attack, but the underlying mechanisms remain poorly understood. Here, we showed that ethylene response factor SlERF.C1 acts as a key regulator to trigger the ethylene‐mediated defense against B. cinerea in tomato fruits without compromising ripening. Knockout of SlERF.C1 increased fruit susceptibility to B. cinerea with no effect on ripening process, while overexpression enhanced resistance. RNA‐Seq, transactivation assays, EMSA and ChIP‐qPCR results indicated that SlERF.C1 activated the transcription of PR genes by binding to their promoters. Moreover, SlERF.C1 interacted with the mitogen‐activated protein kinase SlMPK8 which allowed SlMPK8 to phosphorylate SlERF.C1 at the Ser174 residue and increases its transcriptional activity. Knocking out of SlMPK8 increased fruit susceptibility to B. cinerea, whereas overexpression enhanced resistance without affecting ripening. Furthermore, genetic crosses between SlMPK8‐KO and SlERF.C1‐OE lines reduced the resistance to B. cinerea attack in SlERF.C1‐OE fruits. In addition, B. cinerea infection induced ethylene production which in turn triggered SlMPK8 transcription and enhanced the phosphorylation of SlERF.C1. Overall, our findings reveal the regulatory mechanism of the ‘Ethylene‐MPK8‐ERF.C1‐PR’ module in resistance against B. cinerea and provide new insight into the manipulation of gray mold disease in fruits.
doi_str_mv 10.1111/nph.19632
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Here, we showed that ethylene response factor SlERF.C1 acts as a key regulator to trigger the ethylene‐mediated defense against B. cinerea in tomato fruits without compromising ripening. Knockout of SlERF.C1 increased fruit susceptibility to B. cinerea with no effect on ripening process, while overexpression enhanced resistance. RNA‐Seq, transactivation assays, EMSA and ChIP‐qPCR results indicated that SlERF.C1 activated the transcription of PR genes by binding to their promoters. Moreover, SlERF.C1 interacted with the mitogen‐activated protein kinase SlMPK8 which allowed SlMPK8 to phosphorylate SlERF.C1 at the Ser174 residue and increases its transcriptional activity. Knocking out of SlMPK8 increased fruit susceptibility to B. cinerea, whereas overexpression enhanced resistance without affecting ripening. Furthermore, genetic crosses between SlMPK8‐KO and SlERF.C1‐OE lines reduced the resistance to B. cinerea attack in SlERF.C1‐OE fruits. In addition, B. cinerea infection induced ethylene production which in turn triggered SlMPK8 transcription and enhanced the phosphorylation of SlERF.C1. Overall, our findings reveal the regulatory mechanism of the ‘Ethylene‐MPK8‐ERF.C1‐PR’ module in resistance against B. cinerea and provide new insight into the manipulation of gray mold disease in fruits.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19632</identifier><identifier>PMID: 38402567</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Botrytis - physiology ; Botrytis cinerea ; Disease Resistance - genetics ; ERF ; Ethene ; Ethylene ; Ethylenes - metabolism ; Fruit - metabolism ; Fruits ; Gene Expression Regulation, Plant ; Genes ; Grey mold ; Hormones ; Kinases ; Life Sciences ; Modules ; MPK ; Phosphorylation ; Plant Diseases - genetics ; Plant growth substances ; Plant hormones ; postharvest disease ; Regulatory mechanisms (biology) ; Ripening ; Solanum lycopersicum - genetics ; Tomatoes ; Transcription ; Vegetal Biology</subject><ispartof>The New phytologist, 2024-04, Vol.242 (2), p.592-609</ispartof><rights>2024 The Authors © 2024 New Phytologist Foundation</rights><rights>2024 The Authors New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3872-3822f85a98d3aaea650bf61c62bd2e86f69393de0af68efd3cec2f0330beeab63</citedby><cites>FETCH-LOGICAL-c3872-3822f85a98d3aaea650bf61c62bd2e86f69393de0af68efd3cec2f0330beeab63</cites><orcidid>0000-0001-6440-6972 ; 0009-0006-2382-5170 ; 0000-0001-7019-2560 ; 0000-0001-8004-1758 ; 0000-0002-8579-4983 ; 0000-0003-2091-374X ; 0000-0002-5725-885X ; 0000-0001-7630-1449</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%2Fnph.19632$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19632$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38402567$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://ut3-toulouseinp.hal.science/hal-04639780$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Deng, Heng</creatorcontrib><creatorcontrib>Pei, Yangang</creatorcontrib><creatorcontrib>Xu, Xin</creatorcontrib><creatorcontrib>Du, Xiaofei</creatorcontrib><creatorcontrib>Xue, Qihan</creatorcontrib><creatorcontrib>Gao, Zhuo</creatorcontrib><creatorcontrib>Shu, Peng</creatorcontrib><creatorcontrib>Wu, Yi</creatorcontrib><creatorcontrib>Liu, Zhaoqiao</creatorcontrib><creatorcontrib>Jian, Yongfei</creatorcontrib><creatorcontrib>Wu, Mengbo</creatorcontrib><creatorcontrib>Wang, Yikui</creatorcontrib><creatorcontrib>Li, Zhengguo</creatorcontrib><creatorcontrib>Pirrello, Julien</creatorcontrib><creatorcontrib>Bouzayen, Mondher</creatorcontrib><creatorcontrib>Deng, Wei</creatorcontrib><creatorcontrib>Hong, Yiguo</creatorcontrib><creatorcontrib>Liu, Mingchun</creatorcontrib><title>Ethylene‐MPK8‐ERF.C1‐PR module confers resistance against Botrytis cinerea in tomato fruit without compromising ripening</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary The plant hormone ethylene plays a critical role in fruit defense against Botrytis cinerea attack, but the underlying mechanisms remain poorly understood. 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Here, we showed that ethylene response factor SlERF.C1 acts as a key regulator to trigger the ethylene‐mediated defense against B. cinerea in tomato fruits without compromising ripening. Knockout of SlERF.C1 increased fruit susceptibility to B. cinerea with no effect on ripening process, while overexpression enhanced resistance. RNA‐Seq, transactivation assays, EMSA and ChIP‐qPCR results indicated that SlERF.C1 activated the transcription of PR genes by binding to their promoters. Moreover, SlERF.C1 interacted with the mitogen‐activated protein kinase SlMPK8 which allowed SlMPK8 to phosphorylate SlERF.C1 at the Ser174 residue and increases its transcriptional activity. Knocking out of SlMPK8 increased fruit susceptibility to B. cinerea, whereas overexpression enhanced resistance without affecting ripening. Furthermore, genetic crosses between SlMPK8‐KO and SlERF.C1‐OE lines reduced the resistance to B. cinerea attack in SlERF.C1‐OE fruits. 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subjects Botrytis - physiology
Botrytis cinerea
Disease Resistance - genetics
ERF
Ethene
Ethylene
Ethylenes - metabolism
Fruit - metabolism
Fruits
Gene Expression Regulation, Plant
Genes
Grey mold
Hormones
Kinases
Life Sciences
Modules
MPK
Phosphorylation
Plant Diseases - genetics
Plant growth substances
Plant hormones
postharvest disease
Regulatory mechanisms (biology)
Ripening
Solanum lycopersicum - genetics
Tomatoes
Transcription
Vegetal Biology
title Ethylene‐MPK8‐ERF.C1‐PR module confers resistance against Botrytis cinerea in tomato fruit without compromising ripening
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