Cytosolic APX2 is a pleiotropic protein involved in H2O2 homeostasis, chloroplast protection, plant architecture and fertility maintenance.

KEY MESSAGE: Rice cytoplasmic APX2 is a pleiotropic protein, densely distributed around chloroplasts. It plays key roles in H2O2 homeostasis and chloroplast protection, and is related to plant architecture and fertility regulation. Ascorbate peroxidases (APXs) catalyze the conversion of H2O2 into H2O. In this report, we systematically investigated the function of cytosolic APX2 using a T-DNA knockout mutant. Loss of OsAPX2 altered rice architecture including shoot height and leaf inclination, resulting in shoot dwarfing, leaf dispersion and fertility decline. Sixty-five differentially expressed proteins were identified in flag leaves of the milk-ripe stage, mainly involved in photosynthesis, glycolysis and TCA cycle, redox homeostasis, and defense. The absence of APX2 severely impacted the stability of chloroplast proteins, and dramatically reduced their expression levels. Subcellular localization showed that APX2 was enriched around each chloroplast to form a high concentration sphere, highlighting chloroplasts as key targets protected by the protein. Accumulation of H2O2 was suppressed in the KO-APX2 mutant, which may benefit from increased CAT activity and functional complementation of APX family members. Unexpectedly, the accumulation of soluble sugar, especially sucrose increased significantly, suggesting that APX2 was involved in regulation of sugar metabolism. Obviously, roles of the cytosolic APX2 are very profound and complex in rice. It can be concluded that the cytosolic APX2 is a pleiotropic protein and an important regulator in ROS homeostasis, chloroplast protection, carbohydrate metabolism as well as plant architecture and fertility maintenance.