Plants are able to orient their growth according to gravity, which ultimately controls both shoot and root architecture.1 Gravitropism is a dynamic process whereby gravistimulation induces the asymmetric distribution of the plant hormone auxin, leading to asymmetric growth, organ bending, and subsequent reset of auxin distribution back to the original pre-gravistimulation situation.1, 2, 3 Differential auxin accumulation during the gravitropic response depends on the activity of polarly localized PIN-FORMED (PIN) auxin-efflux carriers.1, 2, 3, 4 In particular, the timing of this dynamic response is regulated by PIN2,5,6 but the underlying molecular mechanisms are poorly understood. Here, we show that MEMBRANE ASSOCIATED KINASE REGULATOR2 (MAKR2) controls the pace of the root gravitropic response. We found that MAKR2 is required for the PIN2 asymmetry during gravitropism by acting as a negative regulator of the cell-surface signaling mediated by the receptor-like kinase TRANSMEMBRANE KINASE1 (TMK1).2,7, 8, 9, 10 Furthermore, we show that the MAKR2 inhibitory effect on TMK1 signaling is antagonized by auxin itself, which triggers rapid MAKR2 membrane dissociation in a TMK1-dependent manner. Our findings suggest that the timing of the root gravitropic response is orchestrated by the reversible inhibition of the TMK1 signaling pathway at the cell surface.
We thank the SiCE group for discussions and comments; S. Yalovsky, B. Scheres, and the NASC/ABRC collection for providing transgenic Arabidopsis lines and plasmids; L. Kalmbach and M. Barberon for the gift of pLOK180_pFR7m34GW; A. Lacroix, J. Berger, and P. Bolland for plant care; and M. Fendrych for help with microfluidics in the J.F. lab. We acknowledge the contribution of the SFR Biosciences (UMS3444/CNRS, US8/Inser m, ENS de Lyon, UCBL) facilities: C. Lionet, E. Chatre, and J. Brocard at LBIPLATIM-MICROSCOPY for assistance with imaging, and V. GuegenChaignon and A. Page at the Protein Science Facility (PSF) for assistance with protein purification and mass spectrometry. Y.J. was funded by ERC grant 3363360-APPL under FP/2007–2013. Y.J. and Z.L.N. were funded by an ANR- and NSF-supported ERA-CAPS project (SICOPID: ANR-17-CAPS0003-01/NSF PGRP IOS-1841917). A.I.C.-D. is funded by an ERC consolidator grant (ERC-2015-CoG–683163) and BIO2016-78955 grant from the Spanish Ministry of Economy and Competitiveness. Exchanges between the Y.J. and T.B. laboratories were funded by Tournesol grant 35656NB. B.K.M. was funded by the Omics@vib Marie Curie COFUND and Research Foundation Flanders for a postdoctoral fellowship.
Marquès-Bueno M, Armengot L, Noack L, et al. Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. Current Biology. 2021;31(1). doi:10.1016/j.cub.2020.10.011
Marquès-Bueno, M., Armengot, L., Noack, L., Bareille, J., Rodriguez Solovey, L., Platre, M., … Jaillais, Y. (2021). Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. Current Biology. Elsevier. https://doi.org/10.1016/j.cub.2020.10.011
Marquès-Bueno, MM, L Armengot, LC Noack, J Bareille, Lesia Rodriguez Solovey, MP Platre, V Bayle, et al. “Auxin-Regulated Reversible Inhibition of TMK1 Signaling by MAKR2 Modulates the Dynamics of Root Gravitropism.” Current Biology. Elsevier, 2021. https://doi.org/10.1016/j.cub.2020.10.011.
M. Marquès-Bueno et al., “Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism,” Current Biology, vol. 31, no. 1. Elsevier, 2021.
Marquès-Bueno M, Armengot L, Noack L, Bareille J, Rodriguez Solovey L, Platre M, Bayle V, Liu M, Opdenacker D, Vanneste S, Möller B, Nimchuk Z, Beeckman T, Caño-Delgado A, Friml J, Jaillais Y. 2021. Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. Current Biology. 31(1).
Marquès-Bueno, MM, et al. “Auxin-Regulated Reversible Inhibition of TMK1 Signaling by MAKR2 Modulates the Dynamics of Root Gravitropism.” Current Biology, vol. 31, no. 1, Elsevier, 2021, doi:10.1016/j.cub.2020.10.011.
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