Growth regulation tailors plant development to its environment. A showcase is response to gravity, where shoots bend up and roots down1. This paradox is based on opposite effects of the phytohormone auxin, which promotes cell expansion in shoots, while inhibiting it in roots via a yet unknown cellular mechanism2. 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, a causative growth determinant. Cell surface-based TRANSMEMBRANE KINASE1 (TMK1) interacts with and mediates phosphorylation and activation of plasma membrane H+-ATPases for apoplast acidification, while intracellular canonical auxin signalling promotes 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 while navigating complex soil environment.
We thank Nataliia Gnyliukh and Lukas Hörmayer for technical assistance and Nadine Paris for sharing PM-Cyto seeds. We gratefully acknowledge Life Science, Machine Shop and Bioimaging Facilities of IST Austria. This project has received funding from the European Research Council Advanced Grant (ETAP-742985) and the Austrian Science Fund (FWF) I 3630-B25 to J.F., the National Institutes of Health (GM067203) to W.M.G., the Netherlands Organization for Scientific Research (NWO; VIDI-864.13.001.), the Research Foundation-Flanders (FWO; Odysseus II G0D0515N) and a European Research Council Starting Grant (TORPEDO-714055) to W.S. and B.D.R., the VICI grant (865.14.001) from the Netherlands Organization for Scientific Research to M.R and D.W., the Australian Research Council and China National Distinguished Expert Project (WQ20174400441) to S.S., the MEXT/JSPS KAKENHI to K.T. (20K06685) and T.K. (20H05687 and 20H05910), the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant Agreement No. 665385 and the DOC Fellowship of the Austrian Academy of Sciences to L.L., the China Scholarship Council to J.C.
Li L, Verstraeten I, Roosjen M, et al. Cell surface and intracellular auxin signalling for H+-fluxes in root growth. Research Square. doi:10.21203/rs.3.rs-266395/v3
Li, L., Verstraeten, I., Roosjen, M., Takahashi, K., Rodriguez Solovey, L., Merrin, J., … Friml, J. (n.d.). Cell surface and intracellular auxin signalling for H+-fluxes in root growth. Research Square. https://doi.org/10.21203/rs.3.rs-266395/v3
Li, Lanxin, Inge Verstraeten, Mark Roosjen, Koji Takahashi, Lesia Rodriguez Solovey, Jack Merrin, Jian Chen, et al. “Cell Surface and Intracellular Auxin Signalling for H+-Fluxes in Root Growth.” Research Square, n.d. https://doi.org/10.21203/rs.3.rs-266395/v3.
L. Li et al., “Cell surface and intracellular auxin signalling for H+-fluxes in root growth,” Research Square. .
Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez Solovey L, Merrin J, Chen J, Shabala L, Smet W, Ren H, Vanneste S, Shabala S, De Rybel B, Weijers D, Kinoshita T, Gray WM, Friml J. Cell surface and intracellular auxin signalling for H+-fluxes in root growth. Research Square, 266395.
Li, Lanxin, et al. “Cell Surface and Intracellular Auxin Signalling for H+-Fluxes in Root Growth.” Research Square, 266395, doi:10.21203/rs.3.rs-266395/v3.
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