Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module

New Phytol. 2017 Sep;215(4):1533-1547. doi: 10.1111/nph.14638. Epub 2017 Jun 26.

Abstract

The plant hormone jasmonate (JA) promotes the degradation of JASMONATE ZIM-DOMAIN (JAZ) proteins to relieve repression on diverse transcription factors (TFs) that execute JA responses. However, little is known about how combinatorial complexity among JAZ-TF interactions maintains control over myriad aspects of growth, development, reproduction, and immunity. We used loss-of-function mutations to define epistatic interactions within the core JA signaling pathway and to investigate the contribution of MYC TFs to JA responses in Arabidopsis thaliana. Constitutive JA signaling in a jaz quintuple mutant (jazQ) was largely eliminated by mutations that block JA synthesis or perception. Comparison of jazQ and a jazQ myc2 myc3 myc4 octuple mutant validated known functions of MYC2/3/4 in root growth, chlorophyll degradation, and susceptibility to the pathogen Pseudomonas syringae. We found that MYC TFs also control both the enhanced resistance of jazQ leaves to insect herbivory and restricted leaf growth of jazQ. Epistatic transcriptional profiles mirrored these phenotypes and further showed that triterpenoid biosynthetic and glucosinolate catabolic genes are up-regulated in jazQ independently of MYC TFs. Our study highlights the utility of genetic epistasis to unravel the complexities of JAZ-TF interactions and demonstrates that MYC TFs exert master control over a JAZ-repressible transcriptional hierarchy that governs growth-defense balance.

Keywords: gene cluster; glucosinolate; growth-defense tradeoffs; jasmonate (JA); plant defense; plant hormone; plant-insect interaction; triterpenoid.

MeSH terms

  • Anthocyanins / metabolism
  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis / immunology*
  • Arabidopsis Proteins / metabolism*
  • Chlorophyll / metabolism
  • Cyclopentanes / pharmacology
  • Disease Resistance
  • Epistasis, Genetic
  • Flowers / physiology
  • Gene Expression Regulation, Plant
  • Mutation / genetics
  • Oxylipins / pharmacology
  • Plant Leaves / metabolism
  • Plant Roots / drug effects
  • Plant Roots / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction / drug effects
  • Transcription Factors / metabolism
  • Transcription, Genetic*

Substances

  • Anthocyanins
  • Arabidopsis Proteins
  • Cyclopentanes
  • Oxylipins
  • RNA, Messenger
  • Transcription Factors
  • Chlorophyll
  • jasmonic acid