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

Proc Natl Acad Sci U S A. 2012 May 8;109(19):E1192-200. doi: 10.1073/pnas.1201616109. Epub 2012 Apr 23.

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cyclopentanes / metabolism*
  • Cyclopentanes / pharmacology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • F-Box Proteins / genetics
  • F-Box Proteins / metabolism
  • Gene Expression Regulation, Plant / drug effects
  • Gibberellins / metabolism*
  • Gibberellins / pharmacology
  • Mutation
  • Oryza / genetics
  • Oryza / growth & development
  • Oryza / metabolism
  • Oxylipins / metabolism*
  • Oxylipins / pharmacology
  • Plant Development
  • Plant Growth Regulators / metabolism
  • Plant Growth Regulators / pharmacology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plants / genetics
  • Plants / metabolism*
  • Protein Binding
  • Proteolysis / drug effects
  • RNA Interference
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Seedlings / drug effects
  • Seedlings / genetics
  • Seedlings / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Signal Transduction / physiology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Two-Hybrid System Techniques

Substances

  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Basic Helix-Loop-Helix Transcription Factors
  • CONSTANS protein, Arabidopsis
  • Cyclopentanes
  • DNA-Binding Proteins
  • F-Box Proteins
  • Gibberellins
  • JAZ1 protein, Arabidopsis
  • MYC2 protein, Arabidopsis
  • Oxylipins
  • PIF3 protein, Arabidopsis
  • Plant Growth Regulators
  • Plant Proteins
  • RGL1 protein, Arabidopsis
  • Repressor Proteins
  • Transcription Factors
  • jasmonic acid

Associated data

  • GEO/GSE29577
  • GEO/GSM732294
  • GEO/GSM732295
  • GEO/GSM732296
  • GEO/GSM732297
  • GEO/GSM732298
  • GEO/GSM732299