Wounding induces a peroxisomal H2O2 decrease via glycolate oxidase-catalase switch dependent on glutamate receptor-like channel-supported Ca2+ signaling in plants

Abstract

Sensing of environmental challenges, such as mechanical injury, by a single plant tissue results in the activation of systemic signaling, which attunes the plant's physiology and morphology for better survival and reproduction. As key signals, both calcium ions (Ca2+) and hydrogen peroxide (H2O2) interplay with each other to mediate plant systemic signaling. However, the mechanisms underlying Ca2+-H2O2 crosstalk are not fully revealed. Our previous study showed that the interaction between glycolate oxidase and catalase, key enzymes of photorespiration, serves as a molecular switch (GC switch) to dynamically modulate photorespiratory H2O2 fluctuations via metabolic channeling. In this study, we further demonstrate that local wounding induces a rapid shift of the GC switch to a more interactive state in systemic leaves, resulting in a sharp decrease in peroxisomal H2O2 levels, in contrast to a simultaneous outburst of the nicotinamide adenine dinucleotide phosphate (NADPH) oxidase-derived apoplastic H2O2. Moreover, the systemic response of the two processes depends on the transmission of Ca2+ signaling, mediated by glutamate-receptor-like Ca2+ channels 3.3 and 3.6. Mechanistically, by direct binding and/or indirect mediation by some potential biochemical sensors, peroxisomal Ca2+ regulates the GC switch states in situ, leading to changes in H2O2 levels. Our findings provide new insights into the functions of photorespiratory H2O2 in plant systemic acclimation and an optimized systemic H2O2 signaling via spatiotemporal interplay between the GC switch and NADPH oxidases.