Control of Chloroplast Integrity by the Jasmonate Signaling Pathway is Linked to Growth-Defense Balance

Chloroplasts play a central role in plant responses to environmental stress. Little is known, however, about how chloroplast homeostasis is maintained during stress responses that place high metabolic and bioenergetic demands on the cell. As a chloroplast-derived retrograde signal, jasmonate (JA) promotes broad-spectrum immunity by triggering the degradation of JAZ transcriptional repressors that act in the nucleus to control chloroplast metabolism. Here, we manipulated JAZ abundance to investigate how chloroplast integrity and function is maintained at high levels of defense. A jaz decuple mutant (jazD) lacking 10 of 13 JAZs exhibited strong growth-defense antagonism without loss of photosynthetic efficiency. Treatment of jazD with the JA-receptor agonist coronatine triggered rapid loss of chlorophyll and the turnover of chloroplast proteins and lipids, leading to the collapse of photosynthetic activity and cell death. These findings were supported by global transcript and metabolite profiling over a time course of coronatine treatment. Genetic screens identified MYC2 and the JAZ-destabilizing F-box protein, COI1, as positive regulators of coronatine-induced chloroplast dismantling in jazD plants. These results demonstrate how the progressive loss of JAZ repression drives a continuum of MYC2-dependent growth-defense tradeoffs, including disassembly of the photosynthetic apparatus as a terminal response. In highlighting the critical role for JAZ proteins in maintaining chloroplast integrity at high levels of defense, our results provide insight into the general mechanism by which jasmonate governs chloroplast metabolism to balance growth and stress responses.