SignificanceThe plant hormone jasmonate promotes resistance to plant-eating organisms, ranging from pathogenic microbes to mammals. Jasmonate reprograms metabolism to fuel the production of diverse defense compounds and simultaneously inhibits plant growth. Understanding how growth is influenced across a range of defense levels remains unclear, but has important implications for optimizing crop productivity. Using a genetic approach to “tune” the jasmonate response, we assessed the physiological consequences of discrete levels of defense throughout the plant life cycle. Overactivation of jasmonate response led to carbon starvation, near loss of seed production and, under extreme conditions, lethality. Our findings explain the emergence of diverse strategies to keep jasmonate responses at bay and provide new insights into metabolic processes that underlie growth–defense trade-offs.

SummaryThe 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.

The plant hormone jasmonate (JA) promotes resistance to biotic stress by stimulating the degradation of JASMONATE ZIM-DOMAIN (JAZ) proteins, which relieves repression on MYC transcription factors that execute defense programs. JA-triggered depletion of JAZ proteins in Arabidopsis thaliana is also associated with reduced growth and seed production, but the mechanisms underlying these pleiotropic growth effects remain unclear. Here, we investigated this question using an Arabidopsis JAZ-deficient mutant (jazD; jaz1/2/3/4/5/6/7/9/10/13) that exhibits high levels of defense and strong growth inhibition. Genetic suppressor screens for mutations that uncouple growth-defense tradeoffs in the jazD mutant identified nine independent causal mutations in the red-light receptor phytochrome B (phyB). Unlike the ability of the phyB mutations to completely uncouple the mild growth-defense phenotypes in a jaz mutant (jazQ) defective in JAZ1/3/4/9/10, phyB null alleles only weakly alleviated the growth and reproductive defects in the jazD mutant. phyB-independent growth restriction of the jazD mutant was tightly correlated with upregulation of the tryptophan biosynthetic pathway but not changes in central carbon metabolism. Interestingly, jazD and jazD phyB plants were insensitive to a chemical inhibitor of tryptophan biosynthesis, which is a phenotype previously observed in plants expressing hyperactive MYC transcription factors that cannot bind JAZ repressors. These data provide evidence that the mechanisms underlying the JA-mediated growth-defense balance depend on the level of defense, and further establish an association between growth inhibition at high levels of defense and dysregulation of tryptophan biosynthesis.

As global climate change brings elevated average temperatures and more frequent and extreme weather events, pressure from biotic stresses will become increasingly compounded by harsh abiotic stress conditions. The plant hormone jasmonate (JA) promotes resilience to many environmental stresses, including attack by arthropod herbivores whose feeding activity is often stimulated by rising temperatures. How wound-induced JA signaling affects plant adaptive responses to elevated temperature (ET), however, remains largely unknown. In this study, we used the commercially important crop plant Solanum lycopersicum (cultivated tomato) to investigate the interaction between simulated heat waves and wound-inducible JA responses. We provide evidence that the heat shock protein HSP90 enhances wound responses at ET by increasing the accumulation of the JA receptor, COI1. Wound-induced JA responses directly interfered with short-term adaptation to ET by blocking leaf hyponasty and evaporative cooling. Specifically, leaf damage inflicted by insect herbivory or mechanical wounding at ET resulted in COI1-dependent stomatal closure, leading to increased leaf temperature, lower photosynthetic carbon assimilation rate, and growth inhibition. Pharmacological inhibition of HSP90 reversed these effects to recapitulate the phenotype of a JA-insensitive mutant lacking the COI1 receptor. As climate change is predicted to compound biotic stress with larger and more voracious arthropod pest populations, our results suggest that antagonistic responses resulting from a combination of insect herbivory and moderate heat stress may exacerbate crop losses.

Summary Robust plant immunity negatively affects other fitness traits, including growth and seed production. Jasmonate (JA) confers broad‐spectrum protection against plant consumers by stimulating the degradation of JASMONATE ZIM‐DOMAIN (JAZ) proteins, which in turn relieves repression on transcription factors (TFs) coincident with reduced growth and fecundity. The molecular mechanisms underlying JA‐mediated decreases in fitness remain largely unknown. To assess the contribution of MYC TFs to growth and reproductive fitness at high levels of defence, we mutated three MYC genes in a JAZ‐deficient mutant (jazD) of Arabidopsis thaliana that exhibits strong defence and low seed yield. Genetic epistasis analysis showed that de‐repression of MYC TFs in jazD not only conferred strong resistance to insect herbivory but also reduced shoot and root growth, fruit size and seed yield. We also provided evidence that the JAZ–MYC module coordinates the supply of tryptophan with the production of indole glucosinolates and the proliferation of endoplasmic reticulum bodies that metabolise glucosinolates through the action of β‐glucosidases. Our results establish MYCs as major regulators of growth‐ and reproductive–defence trade‐offs and further indicate that these factors coordinate tryptophan availability with the production of amino acid‐derived defence compounds.