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

Abstract

• 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.