Antagonistic cell surface and intracellular auxin signalling regulate plasma membrane H+-fluxes for root growth

Growth regulation tailors plant development to its environment. A showcase is adaptation to gravity, where shoots bend up and roots down. This paradox is based on opposite responses to the phytohormone auxin, which promotes cell expansion in shoots, while inhibiting it in roots via a yet unknown cellular mechanism. Here, by combining microfluidics, live imaging, genetic engineering and phospho-proteomics in Arabidopsis thaliana, we advance our understanding how auxin inhibits root growth. We show that auxin activates two distinct, antagonistically acting signalling pathways that converge on the rapid regulation of the apoplastic pH, which directly determines growth. Cell surface-based TRANSMEMBRANE KINASE 1 (TMK1) interacts with and mediates phosphorylation and activation of plasma membrane H+-ATPases for apoplast acidification, while intracellular TIR1/AFB-mediated signalling triggers net cellular H+-influx, causing apoplast alkalinisation. The simultaneous activation of these two counteracting mechanisms poises the root for a rapid, fine-tuned growth modulation to subtle changes in the environment.