Apoplastic pH is a chemical switch for extracellular H₂O₂ signaling in abscisic acid-mediated inhibition of cotyledon greening

The apoplastic pH (pH_Apo) in plants is susceptible to environmental stimuli. However, the biological implications of pH_Apo variation have remained largely unknown. The universal stress phytohormone abscisic acid (ABA) as well as the major environmental stimuli drought and salinity were selected as representative cases to investigate how changes in pH_Apo relate to plant behaviors in Arabidopsis. Variations in pH_Apo negatively regulated the cotyledon greening inhibition to the universal stress hormone ABA or environmental stimuli through the action of extracellular hydrogen peroxide (eH₂O₂). Further studies revealed that an increase in pH_Apo diminishes the chemical reactivity of eH₂O₂, effectively functioning as an 'off' switch for its action in oxidizing thiols of plasma membrane proteins. Consequently, this suppresses the eH₂O₂-mediated cotyledon greening inhibition to environmental stimuli and ABA, alongside inhibiting the eH₂O₂-mediated intracellular Ca²⁺ signaling. Conversely, a decrease in pH_Apo serves as an 'on' switch for the action of eH₂O₂. In summary, the pH_Apo is a crucial messenger and chemical switch for eH₂O₂ in signal transduction, notwithstanding the apparent simplicity of the underlying mechanism. Our findings provide a novel fundamental biological insight into the significance of pH.