Autoinhibition of plasma membrane H+-ATPase1 regulates systemic herbivore defense in Arabidopsis

Autoinhibited plasma membrane H+-ATPases1 (AHA1) plays a crucial role in wound-induced systemic signaling, yet its role in insect resistance has not been fully explored. Prior research on fungal and plant AHAs has identified an extended carboxy-terminal tail (C-tail), which forms a regulatory apparatus involving an autoinhibitory domain. Here, we show that truncation of the C-tail of AHA1 increases pump activity and reduces the duration of repolarization after wounding. This also led to reduced expression of the jasmonate pathway marker gene JAZ10 in both wounded and systemic leaves. By specifically increasing AHA1 activity in phloem cells, we further highlighted the essential role of sieve tube elements in mediating electrical signaling and defense responses. Metabolomic analysis showed that AHA1 influences a broad spectrum of metabolites, including amino acids, sugars, and organic acids. Notably, organosulfur compounds like glucosinolates were strongly accumulated in aha1-7 mutants but not in C-tail truncated lines. Collectively, our study identifies the autoinhibitory C-tail of AHA1 as a key regulator that regulates proton pump activity to coordinate electrical signaling, hormonal regulation, and insect defense. These results provide a mechanistic framework for engineering AHA activity to strengthen crop resilience against herbivory.