Wounding induces a peroxisomal H₂ O₂ decrease via glycolate oxidase-catalase switch dependent on glutamate...

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 (H₂ O₂ ) interplay with each other to mediate plant systemic signaling. However, the mechanisms underlying Ca²⁺ -H₂ O₂ 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 H₂ O₂ 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 H₂ O₂ levels, in contrast to a simultaneous outburst of the nicotinamide adenine dinucleotide phosphate (NADPH) oxidase-derived apoplastic H₂ O₂ . 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 H₂ O₂ levels. Our findings provide new insights into the functions of photorespiratory H₂ O₂ in plant systemic acclimation and an optimized systemic H₂ O₂ signaling via spatiotemporal interplay between the GC switch and NADPH oxidases.