Retrograde signalling pathways that are triggered by changes in cellular redox homeostasis remain poorly understood. Transformed rice plants that are deficient in peroxisomal ascorbate peroxidase APX4 (OsAPX4-RNAi) are known to exhibit more effective protection of photosynthesis against oxidative stress than controls when catalase (CAT) is inhibited, but the mechanisms involved have not been characterized. An in-depth physiological and proteomics analysis was therefore performed on OsAPX4-RNAi CAT-inhibited rice plants. Loss of APX4 function led to an increased abundance of several proteins that are involved in essential metabolic pathways, possibly as a result of increased tissue H₂O₂ levels. Higher photosynthetic activities observed in the OsAPX4-RNAi plants under CAT inhibition were accompanied by higher levels of Rubisco, higher maximum rates of Rubisco carboxylation, and increased photochemical efficiencies, together with large increases in photosynthesis-related proteins. Large increases were also observed in the levels of proteins involved in the ascorbate/glutathione cycle and in other antioxidant-related pathways, and these changes may be important in the protection of photosynthesis in the OsAPX4-RNAi plants. Large increases in the abundance of proteins localized in the nuclei and mitochondria were also observed, together with increased levels of proteins involved in important cellular pathways, particularly protein translation. Taken together, the results show that OsAPX4-RNAi plants exhibit significant metabolic reprogramming, which incorporates a more effective antioxidant response to protect photosynthesis under conditions of impaired CAT activity.

The photosynthetic light reactions provide energy that is consumed and stored in electron sinks, the products of photosynthesis. A balance between light reactions and electron consumption in the chloroplast is vital for plants, and is protected by several photosynthetic regulation mechanisms. Photosystem I (PSI) is particularly susceptible to photoinhibition when these factors become unbalanced, which can occur in low temperatures or in high light. In this study we used the pgr5 Arabidopsis mutant that lacks ΔpH-dependent regulation of photosynthetic electron transport as a model to study the consequences of PSI photoinhibition under high light. We found that PSI damage severely inhibits carbon fixation and starch accumulation, and attenuates enzymatic oxylipin synthesis and chloroplast regulation of nuclear gene expression after high light stress. This work shows that modifications to regulation of photosynthetic light reactions, which may be designed to improve yield in crop plants, can negatively impact metabolism and signalling, and thereby threaten plant growth and stress tolerance. This article is part of the themed issue ‘Enhancing photosynthesis in crop plants: targets for improvement’.

Life on earth depends on the presence of photoautotrophic organisms that are able to input carbon into the ecosystems through the process of photosynthesis which, with a few specialized exceptions, takes place within the chloroplast. This organelle contains the most complex redox system in plants being composed of numerous players including thiol reductases, peroxidases, and glutathione-related enzymes. It seems likely that these proteins act together to adjust redox metabolism enabling plants to grow efficiently under both normal and stressed conditions. However, our knowledge concerning how these proteins interact and if they can compensate one another is relatively limited. This is in part due to the failure of considering these components from a systemic perspective. Here, we provide a systemic view of the chloroplastic-redox network highlighting how it operates and how its components co-operate to maintain efficient chloroplastic function. We further explore the cross-talk between chloroplastic-redox metabolism and that of other subcellular compartments. Given the complexity of plant redox metabolism and the compensatory role played by different redox systems, we argue that a unique possibility to understand this system is afforded by systems biology approaches and by characterizing mutants for multiple genes. Taking this into account, we highlight how gene co-expression and protein–protein network analyses coupled with different reverse genetic strategies could be used to reveal the function, potential redundancies, and complementarities among the components of the chloroplastic redox network.