A circadian rheostat drives proton electrochemical gradients to optimize cell-type-specific growth in Arabidopsis

• Antiphasic oscillation of apoplastic pH in epidermal and phloem companion cells • CCA1 lowers apoplastic pH in epidermal cells and promotes hypocotyl growth • CCA1 represses the H + -pump AHA3 , raising phloem apoplastic pH and reducing root growth • CCA1-mediated phloem pH changes affect sucrose loading, balancing shoot-root growth Antiphasic oscillation of apoplastic pH in epidermal and phloem companion cells CCA1 lowers apoplastic pH in epidermal cells and promotes hypocotyl growth CCA1 represses the H + -pump AHA3 , raising phloem apoplastic pH and reducing root growth CCA1-mediated phloem pH changes affect sucrose loading, balancing shoot-root growth Plant growth relies on the activity of key transcription factors. Here, we uncover a mechanism for organ-specific growth driven by opposing electrochemical signals that propagate in a cell-type-specific manner. Using a genetically encoded pH sensor and a pH-sensitive dye, we show that apoplastic pH in epidermal cells oscillates antiphasically relative to phloem pH. The clock component CCA1 lowers apoplastic pH in hypocotyl epidermal cells while increasing it in companion cells. This opposing regulation promotes hypocotyl growth but inhibits root elongation. Mechanistically, CCA1 activates auxin signaling in shoots while repressing sucrose transporter 2 and the electrogenic (H + )-pump ATPase AHA3 by directly binding their promoters. The repression decreases sucrose loading into the phloem and slows transport velocity. Expressing CCA1 in the phloem is sufficient to inhibit root elongation, whereas AHA3 overexpression in CCA1 overexpressing seedlings rescues root growth. Thus, a circadian rheostat orchestrates electrochemical signals to optimize source capacity with sink demand.