Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade

Plants must effectively defend against biotic and abiotic stresses to survive in nature. However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question....

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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2012-05, Vol.109 (19), p.E1192-E1200
Hauptverfasser: Yang, Dong-Lei, Yao, Jian, Mei, Chuan-Sheng, Tong, Xiao-Hong, Zeng, Long-Jun, Li, Qun, Xiao, Lang-Tao, Sun, Tai-ping, Li, Jigang, Deng, Xing-Wang, Lee, Chin Mei, Thomashow, Michael F, Yang, Yinong, He, Zuhua, He, Sheng Yang
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container_issue 19
container_start_page E1192
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 109
creator Yang, Dong-Lei
Yao, Jian
Mei, Chuan-Sheng
Tong, Xiao-Hong
Zeng, Long-Jun
Li, Qun
Xiao, Lang-Tao
Sun, Tai-ping
Li, Jigang
Deng, Xing-Wang
Lee, Chin Mei
Thomashow, Michael F
Yang, Yinong
He, Zuhua
He, Sheng Yang
description Plants must effectively defend against biotic and abiotic stresses to survive in nature. However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question. Jasmonate (JA) and gibberellic acid (GA) are important plant hormones that mediate defense and growth, respectively. Binding of bioactive JA or GA ligands to cognate receptors leads to proteasome-dependent degradation of specific transcriptional repressors (the JAZ or DELLA family of proteins), which, at the resting state, represses cognate transcription factors involved in defense (e.g., MYCs) or growth [e.g. phytochrome interacting factors (PIFs)]. In this study, we found that the coi1 JA receptor mutants of rice (a domesticated monocot crop) and Arabidopsis (a model dicot plant) both exhibit hallmark phenotypes of GA-hypersensitive mutants. JA delays GA-mediated DELLA protein degradation, and the della mutant is less sensitive to JA for growth inhibition. Overexpression of a selected group of JAZ repressors in Arabidopsis plants partially phenocopies GA-associated phenotypes of the coi1 mutant, and JAZ9 inhibits RGA (a DELLA protein) interaction with transcription factor PIF3. Importantly, the pif quadruple (pifq) mutant no longer responds to JA-induced growth inhibition, and overexpression of PIF3 could partially overcome JA-induced growth inhibition. Thus, a molecular cascade involving the COI1–JAZ–DELLA–PIF signaling module, by which angiosperm plants prioritize JA-mediated defense over growth, has been elucidated.
doi_str_mv 10.1073/pnas.1201616109
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However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question. Jasmonate (JA) and gibberellic acid (GA) are important plant hormones that mediate defense and growth, respectively. Binding of bioactive JA or GA ligands to cognate receptors leads to proteasome-dependent degradation of specific transcriptional repressors (the JAZ or DELLA family of proteins), which, at the resting state, represses cognate transcription factors involved in defense (e.g., MYCs) or growth [e.g. phytochrome interacting factors (PIFs)]. In this study, we found that the coi1 JA receptor mutants of rice (a domesticated monocot crop) and Arabidopsis (a model dicot plant) both exhibit hallmark phenotypes of GA-hypersensitive mutants. JA delays GA-mediated DELLA protein degradation, and the della mutant is less sensitive to JA for growth inhibition. Overexpression of a selected group of JAZ repressors in Arabidopsis plants partially phenocopies GA-associated phenotypes of the coi1 mutant, and JAZ9 inhibits RGA (a DELLA protein) interaction with transcription factor PIF3. Importantly, the pif quadruple (pifq) mutant no longer responds to JA-induced growth inhibition, and overexpression of PIF3 could partially overcome JA-induced growth inhibition. 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However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question. Jasmonate (JA) and gibberellic acid (GA) are important plant hormones that mediate defense and growth, respectively. Binding of bioactive JA or GA ligands to cognate receptors leads to proteasome-dependent degradation of specific transcriptional repressors (the JAZ or DELLA family of proteins), which, at the resting state, represses cognate transcription factors involved in defense (e.g., MYCs) or growth [e.g. phytochrome interacting factors (PIFs)]. In this study, we found that the coi1 JA receptor mutants of rice (a domesticated monocot crop) and Arabidopsis (a model dicot plant) both exhibit hallmark phenotypes of GA-hypersensitive mutants. JA delays GA-mediated DELLA protein degradation, and the della mutant is less sensitive to JA for growth inhibition. Overexpression of a selected group of JAZ repressors in Arabidopsis plants partially phenocopies GA-associated phenotypes of the coi1 mutant, and JAZ9 inhibits RGA (a DELLA protein) interaction with transcription factor PIF3. Importantly, the pif quadruple (pifq) mutant no longer responds to JA-induced growth inhibition, and overexpression of PIF3 could partially overcome JA-induced growth inhibition. Thus, a molecular cascade involving the COI1–JAZ–DELLA–PIF signaling module, by which angiosperm plants prioritize JA-mediated defense over growth, has been elucidated.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth &amp; development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors</subject><subject>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - metabolism</subject><subject>Basic Helix-Loop-Helix Transcription Factors</subject><subject>Basic Helix-Loop-Helix Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Binding sites</subject><subject>Biological Sciences</subject><subject>Cyclopentanes</subject><subject>Cyclopentanes - metabolism</subject><subject>Cyclopentanes - pharmacology</subject><subject>DNA-Binding Proteins</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>drug effects</subject><subject>F-Box Proteins</subject><subject>F-Box Proteins - genetics</subject><subject>F-Box Proteins - metabolism</subject><subject>Flowers &amp; plants</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>gene overexpression</subject><subject>genetics</subject><subject>gibberellic acid</subject><subject>Gibberellins</subject><subject>Gibberellins - metabolism</subject><subject>Gibberellins - pharmacology</subject><subject>growth &amp; development</subject><subject>growth retardation</subject><subject>Hormones</subject><subject>jasmonic acid</subject><subject>Liliopsida</subject><subject>metabolism</subject><subject>mutants</subject><subject>Mutation</subject><subject>Oryza</subject><subject>Oryza - genetics</subject><subject>Oryza - growth &amp; development</subject><subject>Oryza - metabolism</subject><subject>Oxylipins</subject><subject>Oxylipins - metabolism</subject><subject>Oxylipins - pharmacology</subject><subject>pharmacology</subject><subject>phenotype</subject><subject>physiology</subject><subject>Plant Development</subject><subject>Plant growth</subject><subject>Plant Growth Regulators</subject><subject>Plant Growth Regulators - metabolism</subject><subject>Plant Growth Regulators - pharmacology</subject><subject>Plant Proteins</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants</subject><subject>Plants - genetics</subject><subject>Plants - metabolism</subject><subject>PNAS Plus</subject><subject>Protein Binding</subject><subject>protein degradation</subject><subject>Proteins</subject><subject>Proteolysis</subject><subject>Proteolysis - drug effects</subject><subject>receptors</subject><subject>Repressor Proteins</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>rice</subject><subject>RNA Interference</subject><subject>Seedlings</subject><subject>Seedlings - drug effects</subject><subject>Seedlings - genetics</subject><subject>Seedlings - metabolism</subject><subject>Signal Transduction</subject><subject>Signal Transduction - drug effects</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - physiology</subject><subject>transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Two-Hybrid System Techniques</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkl1vVCEQhonR2LV67Z2SeOPNaQc4X9yYNE39SJpoor0mHHY4y-YsrHC2Tf31zmbXVoWECfDMy7wZGHst4ExAp8630ZYzIUG0NEE_YQtaRdXWGp6yBYDsqr6W9Ql7UcoaAHTTw3N2ImUjterbBQvfJhtnvkp5kyLytS0U7Yx8m0PKYQ6_sPAleowFebrFzMec7uYVH-55iDNmjznEkd8FOhvDMGDGaQqRlzBGO-2vnC3OLvEle-btVPDVMZ6ym49XPy4_V9dfP325vLiuXANqrobGqR5aLQb0nXddK2mjyaDrluC8dfXg5RJ163XjG91YsuF7rK3uQNZyUKfsw0F3uxs2uHQY52wnQ342Nt-bZIP59yaGlRnTrVGq6XvdkcD7o0BOP3dYZrMJxZErGzHtihGaRtMqVRP67j90nXaZfBMFQgqAWiiizg-Uy6mUjP6hGAFm30azb6N5bCNlvPnbwwP_p28E8COwz3yU01SduRJCS0LeHhBvk7FjDsXcfKcnavoGvejaVv0G5YivOw</recordid><startdate>20120508</startdate><enddate>20120508</enddate><creator>Yang, Dong-Lei</creator><creator>Yao, Jian</creator><creator>Mei, Chuan-Sheng</creator><creator>Tong, Xiao-Hong</creator><creator>Zeng, Long-Jun</creator><creator>Li, Qun</creator><creator>Xiao, Lang-Tao</creator><creator>Sun, Tai-ping</creator><creator>Li, Jigang</creator><creator>Deng, Xing-Wang</creator><creator>Lee, Chin Mei</creator><creator>Thomashow, Michael F</creator><creator>Yang, Yinong</creator><creator>He, Zuhua</creator><creator>He, Sheng Yang</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20120508</creationdate><title>Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade</title><author>Yang, Dong-Lei ; Yao, Jian ; Mei, Chuan-Sheng ; Tong, Xiao-Hong ; Zeng, Long-Jun ; Li, Qun ; Xiao, Lang-Tao ; Sun, Tai-ping ; Li, Jigang ; Deng, Xing-Wang ; Lee, Chin Mei ; Thomashow, Michael F ; Yang, Yinong ; He, Zuhua ; He, Sheng Yang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c503t-b5c380691bef7fc7620699016c7d0cfac4bf2de96f95f595a386f8e4a970242b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth &amp; development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors</topic><topic>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - metabolism</topic><topic>Basic Helix-Loop-Helix Transcription Factors</topic><topic>Basic Helix-Loop-Helix Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Binding sites</topic><topic>Biological Sciences</topic><topic>Cyclopentanes</topic><topic>Cyclopentanes - metabolism</topic><topic>Cyclopentanes - pharmacology</topic><topic>DNA-Binding Proteins</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>drug effects</topic><topic>F-Box Proteins</topic><topic>F-Box Proteins - genetics</topic><topic>F-Box Proteins - metabolism</topic><topic>Flowers &amp; 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However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question. Jasmonate (JA) and gibberellic acid (GA) are important plant hormones that mediate defense and growth, respectively. Binding of bioactive JA or GA ligands to cognate receptors leads to proteasome-dependent degradation of specific transcriptional repressors (the JAZ or DELLA family of proteins), which, at the resting state, represses cognate transcription factors involved in defense (e.g., MYCs) or growth [e.g. phytochrome interacting factors (PIFs)]. In this study, we found that the coi1 JA receptor mutants of rice (a domesticated monocot crop) and Arabidopsis (a model dicot plant) both exhibit hallmark phenotypes of GA-hypersensitive mutants. JA delays GA-mediated DELLA protein degradation, and the della mutant is less sensitive to JA for growth inhibition. Overexpression of a selected group of JAZ repressors in Arabidopsis plants partially phenocopies GA-associated phenotypes of the coi1 mutant, and JAZ9 inhibits RGA (a DELLA protein) interaction with transcription factor PIF3. Importantly, the pif quadruple (pifq) mutant no longer responds to JA-induced growth inhibition, and overexpression of PIF3 could partially overcome JA-induced growth inhibition. Thus, a molecular cascade involving the COI1–JAZ–DELLA–PIF signaling module, by which angiosperm plants prioritize JA-mediated defense over growth, has been elucidated.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>22529386</pmid><doi>10.1073/pnas.1201616109</doi><oa>free_for_read</oa></addata></record>
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1091-6490
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3358897
source MEDLINE; Jstor Complete Legacy; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry
subjects Arabidopsis
Arabidopsis - genetics
Arabidopsis - growth & development
Arabidopsis - metabolism
Arabidopsis Proteins
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - genetics
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - metabolism
Basic Helix-Loop-Helix Transcription Factors
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Binding sites
Biological Sciences
Cyclopentanes
Cyclopentanes - metabolism
Cyclopentanes - pharmacology
DNA-Binding Proteins
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
drug effects
F-Box Proteins
F-Box Proteins - genetics
F-Box Proteins - metabolism
Flowers & plants
Gene Expression Regulation, Plant
Gene Expression Regulation, Plant - drug effects
gene overexpression
genetics
gibberellic acid
Gibberellins
Gibberellins - metabolism
Gibberellins - pharmacology
growth & development
growth retardation
Hormones
jasmonic acid
Liliopsida
metabolism
mutants
Mutation
Oryza
Oryza - genetics
Oryza - growth & development
Oryza - metabolism
Oxylipins
Oxylipins - metabolism
Oxylipins - pharmacology
pharmacology
phenotype
physiology
Plant Development
Plant growth
Plant Growth Regulators
Plant Growth Regulators - metabolism
Plant Growth Regulators - pharmacology
Plant Proteins
Plant Proteins - genetics
Plant Proteins - metabolism
Plants
Plants - genetics
Plants - metabolism
PNAS Plus
Protein Binding
protein degradation
Proteins
Proteolysis
Proteolysis - drug effects
receptors
Repressor Proteins
Repressor Proteins - genetics
Repressor Proteins - metabolism
Reverse Transcriptase Polymerase Chain Reaction
rice
RNA Interference
Seedlings
Seedlings - drug effects
Seedlings - genetics
Seedlings - metabolism
Signal Transduction
Signal Transduction - drug effects
Signal Transduction - genetics
Signal Transduction - physiology
transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Two-Hybrid System Techniques
title Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade
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