Light is the primary source of energy for life on Earth. Photosynthesis is a process that converts light into chemical energy, producing sugars for living organisms. However, variations in the intensity or quality of light can be detrimental to photosynthetic organisms. To cope with these challenges, photosynthetic organisms have evolved sophisticated mechanisms to allow them to adjust the gene expression, physiology and metabolism in response to rapid changes in light conditions. These adjustments are initiated from photosynthesis and occur on short timescales and help to protect the organisms from potential damage while maintaining efficient energy production. Although acclimation to light stress, such as high light (HL) conditions, has been extensively studied, the specific roles of the light energy transducing photosystems, PSII and PSI, have remained unclear. The aim of this study was to further investigate the role of photosystems and to identify the types of signaling cascades they initiate in response to light stress. I used a PSII-deficient strain of Synechocystis sp. PCC 6803 to study the effects of PSII deficiency on thylakoid organization and gene expression. I also used Arabidopsis thaliana exposed to a light treatment that specifically inhibits PSI, to study the signaling cascades generated by compromised PSI activity. In addition, I investigated the signaling networks during recovery of plants from HL stress.

The absence of PSII leads to higher expression of genes encoding PSII components and repair proteins. Lack of PSII also leads to the accumulation of unassembled CP43 and CP47 proteins, higher PSI monomer to trimer ratio, and higher respiration. These results indicate that the PSII loss induces similar effects as the exposure of cells to HL, suggesting that PSII loss and HL-induced PSII photoinhibition trigger analogous signaling pathways, albeit with differences in the extent of photoinhibition and pigment damage.

I also provide a detailed analysis of the transcriptomic responses induced by PSI photoinhibition in plants. I show that PSI photoinhibition triggers the release of Fe from PSI FeS clusters, leading to an accumulation of excess Fe, an effect seen only under HL stress. Fe overload in chloroplast specifically upregulates genes in nucleus involved in iron homeostasis and sequestration, such as FERRITIN genes, highlighting a unique response to excess Fe stress. The Fe signaling pathway is distinct from the broader oxidative stress response observed under HL, which impacts both PSII and PSI and involves ROS production. Additionally, I show that CO2 deprivation induces the expression of genes associated with oxylipin signaling, including those involved in flavonoid synthesis.

My study culminates in the complexity of the recovery from HL stress. I show that oxidative stress induced by HL treatment leads to the accumulation of jasmonic acid (JA) during both HL and the recovery phase. JA in turn induces the accumulation of antioxidants such as glutathione (GSH) and ascorbate (AsA), which scavenge the reactive oxygen species (ROS) generated by HL stress. These findings indicate that recovery from HL stress involves more than simply reversing the effects of HL stress but involves a coordinated response involving JA-mediated antioxidant accumulation to counteract the oxidative stress sustained during HL stress.