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

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 over-expression in CCA1 over-expressing seedlings rescues root growth. Thus, a circadian rheostat orchestrates electrochemical signals to optimize source capacity with sink demand. Overall design: RNA-Seq profiling of Arabidopsis Wild-Type (Col-0) shoots and roots and their counterpart CCA1 overexpressing plants from 8-day-old seedlings under constant 15 µE of white fluorescent light at 22°C