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

Dong Lei Yang, Jian Yao, Chuan Sheng Mei, Xiao Hong Tong, Long Jun Zeng, Qun Li, Lang Tao Xiao, Tai Ping Sun, Jigang Li, Xing Wang Deng, Chin Mei Lee, Michael F. Thomashow, Yinong Yang, Zuhua He, Sheng Yang He

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Abstract

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.

Original languageEnglish (US)
Pages (from-to)E1192-E1200
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number19
DOIs
StatePublished - May 8 2012

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Gibberellins
Plant Growth Regulators
Growth
Phytochrome
Arabidopsis
Transcription Factors
Phenotype
Angiosperms
jasmonic acid
Proteasome Endopeptidase Complex
Proteolysis
Proteins
gibberellic acid
Ligands

All Science Journal Classification (ASJC) codes

  • General

Cite this

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. / Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. In: Proceedings of the National Academy of Sciences of the United States of America. 2012 ; Vol. 109, No. 19. pp. E1192-E1200.
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title = "Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade",
abstract = "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.",
author = "Yang, {Dong Lei} and Jian Yao and Mei, {Chuan Sheng} and Tong, {Xiao Hong} and Zeng, {Long Jun} and Qun Li and Xiao, {Lang Tao} and Sun, {Tai Ping} and Jigang Li and Deng, {Xing Wang} and Lee, {Chin Mei} and Thomashow, {Michael F.} and Yinong Yang and Zuhua He and He, {Sheng Yang}",
year = "2012",
month = "5",
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doi = "10.1073/pnas.1201616109",
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Yang, DL, Yao, J, Mei, CS, Tong, XH, Zeng, LJ, Li, Q, Xiao, LT, Sun, TP, Li, J, Deng, XW, Lee, CM, Thomashow, MF, Yang, Y, He, Z & He, SY 2012, 'Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade', Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 19, pp. E1192-E1200. https://doi.org/10.1073/pnas.1201616109

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

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 19, 08.05.2012, p. E1192-E1200.

Research output: Contribution to journalArticle

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T1 - Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade

AU - Yang, Dong Lei

AU - Yao, Jian

AU - Mei, Chuan Sheng

AU - Tong, Xiao Hong

AU - Zeng, Long Jun

AU - Li, Qun

AU - Xiao, Lang Tao

AU - Sun, Tai Ping

AU - Li, Jigang

AU - Deng, Xing Wang

AU - Lee, Chin Mei

AU - Thomashow, Michael F.

AU - Yang, Yinong

AU - He, Zuhua

AU - He, Sheng Yang

PY - 2012/5/8

Y1 - 2012/5/8

N2 - 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.

AB - 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.

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