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

SUMMARY 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 (Ca 2+ ) and hydrogen peroxide (H 2 O 2 ) interplay with each other to mediate plant systemic signaling. However, the mechanisms underlying Ca 2+ -H 2 O 2 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 H 2 O 2 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 H 2 O 2 levels, in contrast to a simultaneous outburst of the nicotinamide adenine dinucleotide phosphate (NADPH) oxidase-derived apoplastic H 2 O 2 . Moreover, the systemic response of the two processes depends on the transmission of Ca 2+ signaling, mediated by glutamate-receptor-like Ca 2+ channels 3.3 and 3.6. Mechanistically, by direct binding and/or indirect mediation by some potential biochemical sensors, peroxisomal Ca 2+ regulates the GC switch states in situ , leading to changes in H 2 O 2 levels. Our findings provide new insights into the functions of photorespiratory H 2 O 2 in plant systemic acclimation and an optimized systemic H 2 O 2 signaling via spatiotemporal interplay between the GC switch and NADPH oxidases.