Growth regulation tailors development in plants to their environment. A prominent example of this is the response to gravity, in which shoots bend up and roots bend 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 phosphoproteomics in Arabidopsis thaliana, we advance understanding of how auxin inhibits root growth. We show that auxin activates two distinct, antagonistically acting signalling pathways that converge on rapid regulation of apoplastic pH, a causative determinant of growth. 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 alkalinization. Simultaneous activation of these two counteracting mechanisms poises roots for rapid, fine-tuned growth modulation in navigating complex soil environments.
We thank N. Gnyliukh and L. Hörmayer for technical assistance and N. Paris for sharing PM-Cyto seeds. We gratefully acknowledge the 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) under 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), 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 Marie Skłodowska-Curie grant agreement no. 665385 and the DOC Fellowship of the Austrian Academy of Sciences to L.L., and 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. Nature. 2021;599(7884):273-277. doi:10.1038/s41586-021-04037-6
Li, L., Verstraeten, I., Roosjen, M., Takahashi, K., Rodriguez Solovey, L., Merrin, J., … Friml, J. (2021). Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature. Springer Nature. https://doi.org/10.1038/s41586-021-04037-6
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.” Nature. Springer Nature, 2021. https://doi.org/10.1038/s41586-021-04037-6.
L. Li et al., “Cell surface and intracellular auxin signalling for H+ fluxes in root growth,” Nature, vol. 599, no. 7884. Springer Nature, pp. 273–277, 2021.
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. 2021. Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature. 599(7884), 273–277.
Li, Lanxin, et al. “Cell Surface and Intracellular Auxin Signalling for H+ Fluxes in Root Growth.” Nature, vol. 599, no. 7884, Springer Nature, 2021, pp. 273–77, doi:10.1038/s41586-021-04037-6.
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