Jasmonic acid signaling and glutathione coordinate plant recovery from high light stress

Abstract

High light (HL)-induced chloroplast retrograde signaling originates from the photosynthetic apparatus and regulates nuclear gene expression to enhance photoprotection and coordination of cell metabolism. Here, we analyzed the transcript profiles and accumulation of ROS, stress hormones, and small molecule antioxidants to investigate the signaling mechanisms operating under HL stress, particularly during plant recovery under growth light condition. Exposure of Arabidopsis (Arabidopsis thaliana) rosettes to HL for 15 min induced several 1O2- and H2O2-responsive genes and accumulation of an oxidized form of glutathione, the hallmarks of oxidative stress in cells. Prolonged exposure to HL resulted in accumulation of transcripts encoding oxylipin biosynthesis enzymes, leading to accumulation of 12-oxo-phytodienoic acid and jasmonic acid. However, the expression of several jasmonic acid-responsive genes, already induced by HL, peaked during the recovery, together with accumulation of jasmonic acid and reduced glutathione and ascorbate, highlighting the critical role of jasmonic acid signaling in restoring chloroplast redox balance following HL stress. The involvement of jasmonic acid signaling in recovery-sustained gene expression was further confirmed via experiments with jasmonic acid receptor mutants. HL exposure of only 2 min was sufficient to induce some recovery-sustained genes, indicating the rapid response of plants to changing light conditions. We propose that ROS production at HL induces the signaling cascade for early oxylipin biosynthesis and 12-oxo-phytodienoic acid accumulation, while increased accumulation of jasmonic acid in the recovery phase activates genes that fully restore the glutathione metabolism, ultimately allowing recovery from short-term HL stress.