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Abstract
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.
Highlights
Plant peroxisomes are the most important cellular site for hydrogen peroxide (H2O2) production in C3 plants exposed to light
The silencing resulted in a decrease in abundance of the APX4 protein by about 60% in the OsAPX4-RNAi line compared with non-transformed (NT) controls, which was reduced to a 40% decrease when plants were exposed to 3-AT (Fig. 1).These changes in APX4
After NT and OsAPX4RNAi plants were treated with 10 mM 3-AT, rapid inhibition of CAT was observed, with almost 100% inhibition occurring after 90 min (Fig. 2).This treatment regime provided simultaneous deficiencies of peroxisomal APX (pAPX) and CAT in the transgenic plants and CAT deficiency alone in the NT plants for about 24 h, which was enough to affect the translation mechanisms and the proteomic profiles
Summary
Plant peroxisomes are the most important cellular site for hydrogen peroxide (H2O2) production in C3 plants exposed to light. Peroxisomal isoforms of ascorbate peroxidase (APX, EC 1.11.1.11) are generally regarded as the most important plant peroxidases related to compensation and/or supplementation of CAT activity (Yamaguchi et al, 1995; Mullen et al, 1999; Wang et al, 1999; Kavitha et al, 2008; Xu et al, 2008); there is no consensus about this, since some studies employing Arabidopsis and rice plants deficient in peroxisomal APX (pAPX) have suggested only minor importance for these proteins as H2O2 scavengers (Narendra et al, 2006; Sousa et al, 2015) It remains unclear whether the different proteins of the peroxisomal redox network can compensate for each other
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