Abstract

Summary 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.

Highlights

  • Plants continuously integrate information from the environment to tailor their growth, development and defensive capabilities in ways that optimize fitness

  • Growth–defense antagonism in jaz quintuple mutant (jazQ) depends on jasmonate biosynthesis and perception

  • We employed a JASMONATE ZIM-DOMAIN (JAZ)-depleted quintuple mutant to better understand how JA signaling balances growth and defense, and to identify suppressor mutations that mitigate the antagonistic relationship between leaf growth and anti-insect defense (Campos et al, 2016)

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Summary

Introduction

Plants continuously integrate information from the environment to tailor their growth, development and defensive capabilities in ways that optimize fitness. When endogenous JA levels are below a threshold concentration, the expression of JA-responsive genes is switched off through active repression of bHLH-type MYC transcription factors (TFs) (Chini et al, 2016). This repression is mediated by JASMONATE ZIM-DOMAIN (JAZ) proteins, which bind directly to MYCs to impede transcription by two distinct mechanisms (Chini et al, 2007; Thines et al, 2007; Yan et al, 2007). Transcription of JA-responsive genes is activated upon accumulation of jasmonoyl-L-isoleucine (JA-Ile), the production of which is tightly controlled by environmental and developmental cues

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