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

High light-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, and in particular during plant recovery under growth conditions. Exposure to high light for 15 min induced a number of ¹ O ₂ - and H ₂ O ₂ -responsive genes and accumulation of an oxidative form of glutathione and ascorbate, the hallmarks of oxidative stress in cells. Prolonged exposure to high light 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, reduced glutathione and ascorbate, highlighting the critical role of jasmonic acid signaling in restoring chloroplast redox balance following high light stress. The involvement of jasmonic acid signaling in recovery-sustained gene expression was further confirmed by conducting experiments with jasmonic acid receptor mutants. High light exposure of only two min was sufficient to induce some recovery-sustained genes, indicating rapid response of plants to changing light conditions. We propose that ROS production at high light induces the signaling cascade for early oxylipin biosynthesis and 12-oxo-phytodienoic acid accumulation, while increased accumulation of jasmonic acid in recovery-phase activates the genes that fully restore the glutathione metabolism, and ultimately allow recovery from short-term high light stress.