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  • Review Article
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The cell surface is the place to be for brassinosteroid perception and responses

Abstract

Adjusting the microenvironment around the cell surface is critical to responding to external cues or endogenous signals and to maintaining cell activities. In plant cells, the plasma membrane is covered by the cell wall and scaffolded with cytoskeletal networks, which altogether compose the cell surface. It has long been known that these structures mutually interact, but the mechanisms that integrate the whole system are still obscure. Here we spotlight the brassinosteroid (BR) plant hormone receptor BRASSINOSTEROID INSENSITIVE1 (BRI1) since it represents an outstanding model for understanding cell surface signalling and regulation. We summarize how BRI1 activity and dynamics are controlled by plasma membrane components and their associated factors to fine-tune signalling. The downstream signals, in turn, manipulate cell surface structures by transcriptional and post-translational mechanisms. Moreover, the changes in these architectures impact BR signalling, resulting in a feedback loop formation. This Review discusses how BRI1 and BR signalling function as central hubs to integrate cell surface regulation.

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Fig. 1: BRI1 levels and activity controls at the PM.
Fig. 2: Cell surface regulation by the BR pathway in A. thaliana seedling development.
Fig. 3: BR controls the feedback loop coupled by several mechanisms.

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References

  1. Congreve, M., de Graaf, C., Swain, N. A. & Tate, C. G. Impact of GPCR structures on drug discovery. Cell 181, 81–91 (2020).

    Article  CAS  PubMed  Google Scholar 

  2. Robinson, D. R., Wu, Y.-M. & Lin, S.-F. The protein tyrosine kinase family of the human genome. Oncogene 19, 5548–5557 (2000).

    Article  CAS  PubMed  Google Scholar 

  3. Shiu, S.-H. & Bleecker, A. B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl Acad. Sci. USA 98, 10763–10768 (2001).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Shiu, S.-H. et al. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220–1234 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Li, J. & Chory, J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929–938 (1997).

    Article  CAS  PubMed  Google Scholar 

  6. Choe, S. et al. The Arabidopsis dwf7/ste1 mutant is defective in the Δ7 Sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11, 207–221 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Nakaya, M., Tsukaya, H., Murakami, N. & Kato, M. Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant Cell Physiol. 43, 239–244 (2002).

    Article  CAS  PubMed  Google Scholar 

  8. Savaldi-Goldstein, S., Peto, C. & Chory, J. The epidermis both drives and restricts plant shoot growth. Nature 446, 199–202 (2007).

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Ye, Q. et al. Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc. Natl Acad. Sci. USA 107, 6100–6105 (2010).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  10. Vogler, F., Schmalzl, C., Englhart, M., Bircheneder, M. & Sprunck, S. Brassinosteroids promote Arabidopsis pollen germination and growth. Plant Reprod. 27, 153–167 (2014).

    Article  CAS  PubMed  Google Scholar 

  11. Krishna, P., Prasad, B. D. & Rahman, T. in Brassinosteroids: Methods and Protocols (eds Russinova, E. & Caño-Delgado, A. I.) 193–202 (Springer, 2017); https://doi.org/10.1007/978-1-4939-6813-8_16

  12. Planas-Riverola, A. et al. Brassinosteroid signaling in plant development and adaptation to stress. Development 146, dev151894 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hong, Z. et al. Loss-of-function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem. Plant J. 32, 495–508 (2002).

    Article  CAS  PubMed  Google Scholar 

  14. Mori, M. et al. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol. 130, 1152–1161 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Nakamura, A. et al. The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol. 140, 580–590 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Song, L. et al. Reducing brassinosteroid signalling enhances grain yield in semi-dwarf wheat. Nature 617, 118–124 (2023).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  17. Oh, M.-H. et al. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc. Natl Acad. Sci. USA 106, 658–663 (2009).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bojar, D. et al. Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J. 78, 31–43 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Vert, G., Nemhauser, J. L., Geldner, N., Hong, F. & Chory, J. Molecular mechanisms of steroid hormone signaling in plants. Annu. Rev. Cell Dev. Biol. 21, 177–201 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. Jaillais, Y. & Vert, G. Brassinosteroid signaling and BRI1 dynamics went underground. Curr. Opin. Plant Biol. 33, 92–100 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Nolan, T. M., Vukašinović, N., Liu, D., Russinova, E. & Yin, Y. Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell 32, 295–318 (2020).

    Article  CAS  PubMed  Google Scholar 

  22. Li, J., Nam, K. H., Vafeados, D. & Chory, J. BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol. 127, 14–22 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. He, J.-X., Gendron, J. M., Yang, Y., Li, J. & Wang, Z.-Y. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 99, 10185–10190 (2002).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhao, J. et al. Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol. 130, 1221–1229 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Vert, G. & Chory, J. Downstream nuclear events in brassinosteroid signalling. Nature 441, 96–100 (2006).

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Gampala, S. S. et al. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 13, 177–189 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yin, Y. et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181–191 (2002).

    Article  CAS  PubMed  Google Scholar 

  28. Wang, Z. Y. et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505–513 (2002).

    Article  CAS  PubMed  Google Scholar 

  29. Ryu, H. et al. Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19, 2749–2762 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wang, R. et al. Nucleocytoplasmic trafficking and turnover mechanisms of BRASSINAZOLE RESISTANT1 in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 118, e2101838118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Li, J. et al. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213–222 (2002).

    Article  CAS  PubMed  Google Scholar 

  32. Nam, K. H. & Li, J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203–212 (2002).

    Article  CAS  PubMed  Google Scholar 

  33. Santiago, J., Henzler, C. & Hothorn, M. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341, 889–892 (2013).

    Article  ADS  CAS  PubMed  Google Scholar 

  34. Wang, X. et al. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell 15, 220–235 (2008).

    Article  CAS  PubMed  Google Scholar 

  35. Tang, W. et al. Brassinosteroid-Signaling Kinases (BSKs) mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557–560 (2008).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kim, T.-W., Guan, S., Burlingame, A. L. & Wang, Z.-Y. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 43, 561–571 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Mora-García, S. et al. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 18, 448–460 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kim, T.-W. et al. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 11, 1254–1260 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Tang, W. et al. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124–131 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Müssig, C., Fischer, S. & Altmann, T. Brassinosteroid-regulated gene expression. Plant Physiol. 129, 1241–1251 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Sun, Y. et al. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19, 765–777 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Yu, X. et al. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65, 634–646 (2011).

    Article  CAS  PubMed  Google Scholar 

  43. Kadota, Y. et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54, 43–55 (2014).

    Article  CAS  PubMed  Google Scholar 

  44. Li, L. et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15, 329–338 (2014).

    Article  CAS  PubMed  Google Scholar 

  45. Fujita, S. et al. SCHENGEN receptor module drives localized ROS production and lignification in plant roots. EMBO J. 39, e103894 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lin, W. et al. TMK-based cell-surface auxin signalling activates cell-wall acidification. Nature 599, 278–282 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  47. Li, L. et al. Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature 599, 273–277 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  48. Viotti, C. et al. Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22, 1344–1357 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Sutkeviciute, I. & Vilardaga, J.-P. Structural insights into emergent signaling modes of G protein–coupled receptors. J. Biol. Chem. 295, 11626–11642 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Di Rubbo, S. et al. The clathrin adaptor complex AP-2 mediates endocytosis of BRASSINOSTEROID INSENSITIVE1 in Arabidopsis. Plant Cell 25, 2986–2997 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Martins, S. et al. Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination. Nat. Commun. 6, 6151 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  52. Liu, D. et al. Endocytosis of BRASSINOSTEROID INSENSITIVE1 is partly driven by a canonical Tyr-based motif. Plant Cell 32, 3598–3612 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Saeed, B. et al. K63-linked ubiquitin chains are a global signal for endocytosis and contribute to selective autophagy in plants. Curr. Biol. 33, 1337–1345.e5 (2023).

    Article  CAS  PubMed  Google Scholar 

  54. Geldner, N., Hyman, D. L., Wang, X., Schumacher, K. & Chory, J. Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21, 1598–1602 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Neubus Claus, L. A. et al. BRASSINOSTEROID INSENSITIVE1 internalization can occur independent of ligand binding. Plant Physiol. https://doi.org/10.1093/plphys/kiad005 (2023).

  56. Russinova, E. et al. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216–3229 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Robatzek, S., Chinchilla, D. & Boller, T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537–542 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Doblas, V. G. et al. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355, 280–284 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  59. Zhou, J. et al. Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination. Proc. Natl Acad. Sci. USA 115, E1906–E1915 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhang, L. et al. SYP22 and VAMP727 regulate BRI1 plasma membrane targeting to control plant growth in Arabidopsis. N. Phytol. 223, 1059–1065 (2019).

    Article  Google Scholar 

  61. Gadeyne, A. et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 156, 691–704 (2014).

    Article  CAS  PubMed  Google Scholar 

  62. Wang, L. et al. Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells. Mol. Plant 8, 1334–1349 (2015).

    Article  CAS  PubMed  Google Scholar 

  63. Yoshinari, A. et al. Polar localization of the borate exporter BOR1 requires AP2-dependent endocytosis. Plant Physiol. 179, 1569–1580 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Leitner, J. et al. Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc. Natl Acad. Sci. USA 109, 8322–8327 (2012).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  65. Johnson, A. & Vert, G. Unraveling K63 polyubiquitination networks by sensor-based proteomics. Plant Physiol. 171, 1808–1820 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Dubeaux, G., Neveu, J., Zelazny, E. & Vert, G. Metal sensing by the IRT1 transporter-receptor orchestrates its own degradation and plant metal nutrition. Mol. Cell 69, 953–964.e5 (2018).

    Article  CAS  PubMed  Google Scholar 

  67. Luo, Y. et al. Deubiquitinating enzymes UBP12 and UBP13 stabilize the brassinosteroid receptor BRI1. EMBO Rep. 23, e53354 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lu, D. et al. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332, 1439–1442 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  69. Martins, S. et al. Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature. Nat. Commun. 8, 309 (2017).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  70. Naranjo-Arcos, M. et al. SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature. Proc. Natl Acad. Sci. USA 120, e2217255120 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Orosa, B. et al. SUMO conjugation to the pattern recognition receptor FLS2 triggers intracellular signalling in plant innate immunity. Nat. Commun. 9, 5185 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  72. Lin, W. et al. Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1. Proc. Natl Acad. Sci. USA 110, 12114–12119 (2013).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  73. Heinemann, B., Künzler, P., Eubel, H., Braun, H.-P. & Hildebrandt, T. M. Estimating the number of protein molecules in a plant cell: protein and amino acid homeostasis during drought. Plant Physiol. 185, 385–404 (2021).

    CAS  PubMed  Google Scholar 

  74. Platre, M. P. et al. Developmental control of plant Rho GTPase nano-organization by the lipid phosphatidylserine. Science 364, 57–62 (2019).

    Article  ADS  CAS  PubMed  Google Scholar 

  75. Smokvarska, M. et al. A plasma membrane nanodomain ensures signal specificity during osmotic signaling in plants. Curr. Biol. 30, 4654–4664.e4 (2020).

    Article  CAS  PubMed  Google Scholar 

  76. Gronnier, J. et al. Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors. eLife 11, e74162 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500 (2007).

    Article  ADS  CAS  PubMed  Google Scholar 

  78. Heese, A. et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl Acad. Sci. USA 104, 12217–12222 (2007).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  79. Schulze, B. et al. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444–9451 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Belkhadir, Y., Yang, L., Hetzel, J., Dangl, J. L. & Chory, J. The growth–defense pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem. Sci. 39, 447–456 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Ortiz-Morea, F. A., He, P., Shan, L. & Russinova, E. It takes two to tango—molecular links between plant immunity and brassinosteroid signalling. J. Cell Sci. 133, jcs246728 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Bücherl, C. A. et al. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife 6, e25114 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  83. Su, B. et al. Dynamic spatial reorganization of BSK1 complexes in the plasma membrane underpins signal-specific activation for growth and immunity. Mol. Plant 14, 588–603 (2021).

    Article  CAS  PubMed  Google Scholar 

  84. Good, M. C., Zalatan, J. G. & Lim, W. A. Scaffold proteins: hubs for controlling the flow of cellular information. Science 332, 680–686 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  85. Amorim-Silva, V. et al. TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in Arabidopsis. Plant Cell 31, 1807–1828 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Ren, H. et al. Brassinosteroid-signaling kinase 3, a plasma membrane-associated scaffold protein involved in early brassinosteroid signaling. PLoS Genet. 15, e1007904 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Lakhssassi, N. et al. The Arabidopsis tetratricopeptide thioredoxin-like gene family is required for osmotic stress tolerance and male sporogenesis. Plant Physiol. 158, 1252–1266 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Kesten, C. et al. Peripheral membrane proteins modulate stress tolerance by safeguarding cellulose synthases. Sci. Adv. 8, eabq6971 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  89. Wang, X. et al. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell 8, 855–865 (2005).

    Article  CAS  PubMed  Google Scholar 

  90. Hothorn, M. et al. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474, 467–471 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Hink, M. A., Shah, K., Russinova, E., de Vries, S. C. & Visser, A. J. W. G. Fluorescence fluctuation analysis of Arabidopsis thaliana somatic embryogenesis receptor-like kinase and brassinosteroid insensitive 1 receptor oligomerization. Biophys. J. 94, 1052–1062 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Wang, X. et al. Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis brassinosteroid-insensitive1 receptor kinase. Plant Cell 17, 1685–1703 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Oh, M.-H., Wang, X., Clouse, S. D. & Huber, S. C. Deactivation of the Arabidopsis brassinosteroid insensitive 1 (BRI1) receptor kinase by autophosphorylation within the glycine-rich loop. Proc. Natl Acad. Sci. USA 109, 327–332 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  94. Liu, Y., Huang, X., Li, M., He, P. & Zhang, Y. Loss-of-function of Arabidopsis receptor-like kinase BIR1 activates cell death and defense responses mediated by BAK1 and SOBIR1. N. Phytol. 212, 637–645 (2016).

    Article  CAS  Google Scholar 

  95. Ma, C. et al. Structural basis for BIR1-mediated negative regulation of plant immunity. Cell Res. 27, 1521–1524 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Halter, T. et al. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr. Biol. 24, 134–143 (2014).

    Article  CAS  PubMed  Google Scholar 

  97. Hohmann, U., Nicolet, J., Moretti, A., Hothorn, L. A. & Hothorn, M. The SERK3 elongated allele defines a role for BIR ectodomains in brassinosteroid signalling. Nat. Plants 4, 345–351 (2018).

    Article  CAS  PubMed  Google Scholar 

  98. Imkampe, J. et al. The Arabidopsis leucine-rich repeat receptor kinase BIR3 negatively regulates BAK1 receptor complex formation and stabilizes BAK1. Plant Cell 29, 2285–2303 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Wang, X. & Chory, J. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313, 1118–1122 (2006).

    Article  ADS  CAS  PubMed  Google Scholar 

  100. Jaillais, Y. et al. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev. 25, 232–237 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Simon, M. L. A. et al. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nat. Plants 2, 16089 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Kang, Y. H. & Hardtke, C. S. Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling. EMBO Rep. 17, 1145–1154 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Marquès-Bueno, M. M. et al. Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. Curr. Biol. 31, 228–237.e10 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Wang, D. et al. BKI1 regulates plant architecture through coordinated inhibition of the brassinosteroid and ERECTA signaling pathways in Arabidopsis. Mol. Plant 10, 297–308 (2017).

    Article  PubMed  Google Scholar 

  105. Wu, G. et al. Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci. Signal. 4, ra29 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  106. Wang, R. et al. The brassinosteroid-activated BRI1 receptor kinase is switched off by dephosphorylation mediated by cytoplasm-localized PP2A B′ subunits. Mol. Plant 9, 148–157 (2016).

    Article  CAS  PubMed  Google Scholar 

  107. Liu, X. et al. Salicylic acid attenuates brassinosteroid signaling via protein de-S-acylation. EMBO J. 42, e112998 (2023).

    Article  CAS  PubMed  Google Scholar 

  108. Wang, H. et al. Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Mol. Plant 11, 315–325 (2018).

    Article  ADS  CAS  PubMed  Google Scholar 

  109. Kost, B. & Chua, N.-H. The plant cytoskeleton: vacuoles and cell walls make the difference. Cell 108, 9–12 (2002).

    Article  CAS  PubMed  Google Scholar 

  110. Hamant, O. et al. Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650–1655 (2008).

    Article  ADS  CAS  PubMed  Google Scholar 

  111. Fujita, S. et al. An atypical tubulin kinase mediates stress-induced microtubule depolymerization in Arabidopsis. Curr. Biol. 23, 1969–1978 (2013).

    Article  CAS  PubMed  Google Scholar 

  112. Oda, Y. & Fukuda, H. Initiation of cell wall pattern by a rho- and microtubule-driven symmetry breaking. Science 337, 1333–1336 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  113. Lindeboom, J. J. et al. A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342, 1245533 (2013).

    Article  PubMed  Google Scholar 

  114. Qian, D. et al. Arabidopsis ADF5 promotes stomatal closure by regulating actin cytoskeleton remodeling in response to ABA and drought stress. J. Exp. Bot. 70, 435–446 (2019).

    Article  CAS  PubMed  Google Scholar 

  115. Takatani, S. et al. Microtubule response to tensile stress is curbed by NEK6 to buffer growth variation in the Arabidopsis hypocotyl. Curr. Biol. 30, 1491–1503.e2 (2020).

    Article  CAS  PubMed  Google Scholar 

  116. Catterou, M. et al. Brassinosteroids, microtubules and cell elongation in Arabidopsis thaliana. II. Effects of brassinosteroids on microtubules and cell elongation in the bul1 mutant. Planta 212, 673–683 (2001).

    Article  CAS  PubMed  Google Scholar 

  117. Lanza, M. et al. Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Dev. Cell 22, 1275–1285 (2012).

    Article  CAS  PubMed  Google Scholar 

  118. de Bang, L. et al. Brassinosteroids inhibit autotropic root straightening by modifying filamentous-actin organization and dynamics. Front. Plant Sci. 11, 5 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Blume, Ya. B., Krasylenko, Yu. A. & Yemets, A. I. Effects of phytohormones on the cytoskeleton of the plant cell. Russ. J. Plant Physiol. 59, 515–529 (2012).

    Article  CAS  Google Scholar 

  120. Wang, X. et al. Arabidopsis microtubule destabilizing protein40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24, 4012–4025 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Wang, J. et al. Brassinosteroid signals cooperate with katanin-mediated microtubule severing to control stamen filament elongation. EMBO J. 42, e111883 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  122. Ambrose, C., Allard, J. F., Cytrynbaum, E. N. & Wasteneys, G. O. A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis. Nat. Commun. 2, 430 (2011).

    Article  ADS  PubMed  Google Scholar 

  123. Ruan, Y. et al. The microtubule-associated protein CLASP sustains cell proliferation through a brassinosteroid signaling negative feedback loop. Curr. Biol. 28, 2718–2729.e5 (2018).

    Article  CAS  PubMed  Google Scholar 

  124. Ambrose, C. et al. CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev. Cell 24, 649–659 (2013).

    Article  CAS  PubMed  Google Scholar 

  125. Jaillais, Y., Fobis-Loisy, I., Miège, C. & Gaude, T. Evidence for a sorting endosome in Arabidopsis root cells. Plant J. 53, 237–247 (2008).

    Article  CAS  PubMed  Google Scholar 

  126. De Rybel, B. et al. Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling. Chem. Biol. 16, 594–604 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  127. Min, Y. K. et al. New lead compounds for brassinosteroid biosynthesis inhibitors. Bioorg. Med. Chem. Lett. 9, 425–430 (1999).

    Article  CAS  PubMed  Google Scholar 

  128. Liu, X. et al. Brassinosteroids regulate pavement cell growth by mediating BIN2-induced microtubule stabilization. J. Exp. Bot. 69, 1037–1049 (2018).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  129. Zhang, C. et al. ROPGAP-dependent interaction between brassinosteroid and ROP2–GTPase signaling controls pavement cell shape in Arabidopsis. Curr. Biol. 32, 518–531.e6 (2022).

    Article  CAS  PubMed  Google Scholar 

  130. Lauster, T. et al. Arabidopsis pavement cell shape formation involves spatially confined ROPGAP regulators. Curr. Biol. 32, 532–544.e7 (2022).

    Article  CAS  PubMed  Google Scholar 

  131. Feiguelman, G., Fu, Y. & Yalovsky, S. ROP GTPases structure–function and signaling pathways. Plant Physiol. 176, 57–79 (2018).

    Article  CAS  PubMed  Google Scholar 

  132. Fu, Y., Gu, Y., Zheng, Z., Wasteneys, G. & Yang, Z. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120, 687–700 (2005).

    Article  CAS  PubMed  Google Scholar 

  133. Lin, D. et al. Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr. Biol. 23, 290–297 (2013).

    Article  CAS  PubMed  Google Scholar 

  134. Deng, Z. et al. A proteomic study of brassinosteroid response in Arabidopsis. Mol. Cell. Proteom. 6, 2058–2071 (2007).

    Article  CAS  Google Scholar 

  135. Kim, T.-W. et al. Mapping the signaling network of BIN2 kinase using TurboID-mediated biotin labeling and phosphoproteomics. Plant Cell 35, 975–993 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  136. Sánchez-Rodríguez, C. et al. Brassinosteroid insensitive2 negatively regulates cellulose synthesis in Arabidopsis by phosphorylating cellulose synthase 1. Proc. Natl Acad. Sci. USA 114, 3533–3538 (2017).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  137. Somssich, M. et al. Brassinosteroids influence Arabidopsis hypocotyl graviresponses through changes in mannans and cellulose. Plant Cell Physiol. 62, 678–692 (2021).

    Article  CAS  PubMed  Google Scholar 

  138. Wang, W., Sun, Y., Li, G. & Zhang, S. Brassinosteroids promote parenchyma cell and secondary xylem development in sugar beet (Beta vulgaris L.) root. Plant Direct 5, e340 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Li, M. et al. Brassinosteroid signaling restricts root lignification by antagonizing SHORT-ROOT function in Arabidopsis. Plant Physiol. 190, 1182–1198 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Zhuang, Y. et al. MYB42 inhibits hypocotyl cell elongation by coordinating brassinosteroid homeostasis and signalling in Arabidopsis thaliana. Ann. Bot. 129, 403–413 (2021).

    Article  PubMed Central  Google Scholar 

  141. Vatén, A. et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21, 1144–1155 (2011).

    Article  PubMed  Google Scholar 

  142. Sager, R. E. & Lee, J.-Y. Plasmodesmata at a glance. J. Cell Sci. 131, jcs209346 (2018).

    Article  PubMed  Google Scholar 

  143. Wang, Y. et al. Plasmodesmata mediate cell-to-cell transport of brassinosteroid hormones. Nat. Chem. Biol. https://doi.org/10.1038/s41589-023-01346-x (2023).

  144. Clouse, S. D. Brassinosteroids. Arabidopsis Book 1, e0009 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Vukašinović, N. et al. Local brassinosteroid biosynthesis enables optimal root growth. Nat. Plants 7, 619–632 (2021).

    Article  PubMed  Google Scholar 

  146. Takahashi, K., Hirata, S., Kido, N. & Katou, K. Wall-yielding properties of cell walls from elongating cucumber hypocotyls in relation to the action of expansin. Plant Cell Physiol. 47, 1520–1529 (2006).

    Article  CAS  PubMed  Google Scholar 

  147. Friml, J. et al. ABP1–TMK auxin perception for global phosphorylation and auxin canalization. Nature 609, 575–581 (2022).

    Article  ADS  CAS  PubMed  Google Scholar 

  148. Spartz, A. K. et al. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26, 2129–2142 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Caesar, K. et al. A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana. Plant J. 66, 528–540 (2011).

    Article  CAS  PubMed  Google Scholar 

  150. Minami, A., Takahashi, K., Inoue, S., Tada, Y. & Kinoshita, T. Brassinosteroid induces phosphorylation of the plasma membrane H+-ATPase during hypocotyl elongation in Arabidopsis thaliana. Plant Cell Physiol. 60, 935–944 (2019).

    Article  CAS  PubMed  Google Scholar 

  151. Li, M. et al. SAUR15 interaction with BRI1 activates plasma membrane H+-ATPase to promote organ development of Arabidopsis. Plant Physiol. 189, 2454–2466 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  152. Großeholz, R. et al. Computational modeling and quantitative physiology reveal central parameters for brassinosteroid-regulated early cell physiological processes linked to elongation growth of the Arabidopsis root. eLife 11, e73031 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  153. Liu, L. et al. Extracellular pH sensing by plant cell-surface peptide-receptor complexes. Cell 185, 3341–3355.e13 (2022).

    Article  CAS  PubMed  Google Scholar 

  154. Diaz-Ardila, H. N., Gujas, B., Wang, Q., Moret, B. & Hardtke, C. S. pH-dependent CLE peptide perception permits phloem differentiation in Arabidopsis roots. Curr. Biol. 33, 597–605.e3 (2023).

    Article  CAS  PubMed  Google Scholar 

  155. Doblas, V. G., Gonneau, M. & Höfte, H. Cell wall integrity signaling in plants: malectin-domain kinases and lessons from other kingdoms. Cell Surf. 3, 1–11 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  156. Mishra, R., Minc, N. & Peter, M. Cells under pressure: how yeast cells respond to mechanical forces. Trends Microbiol. 30, 495–510 (2022).

    Article  CAS  PubMed  Google Scholar 

  157. Engelsdorf, T. et al. The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in Arabidopsis thaliana. Sci. Signal. 11, eaao3070 (2018).

    Article  PubMed  Google Scholar 

  158. Wolf, S. Cell wall signaling in plant development and defense. Annu. Rev. Plant Biol. 73, 323–353 (2022).

    Article  CAS  PubMed  Google Scholar 

  159. Haswell, E. S., Peyronnet, R., Barbier-Brygoo, H., Meyerowitz, E. M. & Frachisse, J.-M. Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr. Biol. 18, 730–734 (2008).

    Article  CAS  PubMed  Google Scholar 

  160. Mecchia, M. A. et al. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358, 1600–1603 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  161. Wolf, S. et al. A receptor-like protein mediates the response to pectin modification by activating brassinosteroid signaling. Proc. Natl Acad. Sci. USA 111, 15261–15266 (2014).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  162. Ge, Z. et al. LLG2/3 are co-receptors in BUPS/ANX–RALF signaling to regulate Arabidopsis pollen tube integrity. Curr. Biol. 29, 3256–3265.e5 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Hématy, K. et al. A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17, 922–931 (2007).

    Article  PubMed  Google Scholar 

  164. Miyazaki, S. et al. ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr. Biol. 19, 1327–1331 (2009).

    Article  CAS  PubMed  Google Scholar 

  165. Tang, W. et al. Mechano-transduction via the pectin–FERONIA complex activates ROP6 GTPase signaling in Arabidopsis pavement cell morphogenesis. Curr. Biol. 32, 508–517.e3 (2022).

    Article  CAS  PubMed  Google Scholar 

  166. Ge, Z. et al. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358, 1596–1600 (2017).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  167. Haas, K. T., Wightman, R., Meyerowitz, E. M. & Peaucelle, A. Pectin homogalacturonan nanofilament expansion drives morphogenesis in plant epidermal cells. Science 367, 1003–1007 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  168. Wolf, S., Mravec, J., Greiner, S., Mouille, G. & Höfte, H. Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Curr. Biol. 22, 1732–1737 (2012).

    Article  CAS  PubMed  Google Scholar 

  169. Holzwart, E. et al. A mutant allele uncouples the brassinosteroid-dependent and independent functions of brassinosteroid insensitive 11. Plant Physiol. 182, 669–678 (2020).

    Article  CAS  PubMed  Google Scholar 

  170. Garnelo Gómez, B., Holzwart, E., Shi, C., Lozano-Durán, R. & Wolf, S. Phosphorylation-dependent routing of RLP44 towards brassinosteroid or phytosulfokine signalling. J. Cell Sci. 134, jcs259134 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  171. Holzwart, E. et al. BRI1 controls vascular cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling. Proc. Natl Acad. Sci. USA 115, 11838–11843 (2018).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  172. Yue, Z.-L. et al. The receptor kinase OsWAK11 monitors cell wall pectin changes to fine-tune brassinosteroid signaling and regulate cell elongation in rice. Curr. Biol. 32, 2454–2466.e7 (2022).

    Article  CAS  PubMed  Google Scholar 

  173. Huerta, A. I. et al. The WAK-like protein RFO1 acts as a sensor of the pectin methylation status in Arabidopsis cell walls to modulate root growth and defense. Mol. Plant 16, 865–881 (2023).

    Article  CAS  PubMed  Google Scholar 

  174. Ubeda-Tomás, S. et al. Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat. Cell Biol. 10, 625–628 (2008).

    Article  PubMed  Google Scholar 

  175. Uchida, N. et al. Regulation of inflorescence architecture by intertissue layer ligand–receptor communication between endodermis and phloem. Proc. Natl Acad. Sci. USA 109, 6337–6342 (2012).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  176. Fridman, Y. et al. Root growth is modulated by differential hormonal sensitivity in neighboring cells. Genes Dev. 28, 912–920 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Fridman, Y. et al. The root meristem is shaped by brassinosteroid control of cell geometry. Nat. Plants 7, 1475–1484 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Kelly-Bellow, R. et al. Brassinosteroid coordinates cell layer interactions in plants via cell wall and tissue mechanics. Science 380, 1275–1281 (2023).

    Article  ADS  CAS  PubMed  Google Scholar 

  179. Azpiroz, R., Wu, Y., LoCascio, J. C. & Feldmann, K. A. An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10, 219–230 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Choe, S. et al. The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22alpha-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10, 231–243 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  181. Grove, M. D. et al. Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281, 216–217 (1979).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We apologize to authors whose work is related to BR-driven cell surface regulation but could not be cited because of either our oversight or space limitation. We thank S. Moussu for the critical reading of the manuscript. This work was supported by a PhD fellowship from the University Toulouse 3-Paul Sabatier to C.D., research grants from Agence Nationale de la Recherche (ANR-17-CE20-0026-01 to G.V. and ANR-22-CE13-0021-01 to S.F.) and the French Laboratory of Excellence (project ‘TULIP’ grant nos ANR-10-LABX-41 and ANR-11-IDEX-0002-02 to G.V.).

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C.D., G.V. and S.F. conceptualized the structure of the paper. C.D. wrote the original draft of the paper. C.D., G.V. and S.F. reviewed and edited the manuscript. C.D. and S.F. produced the figures. S.F. and G.V. supervised the manuscript.

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Correspondence to Satoshi Fujita.

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Delesalle, C., Vert, G. & Fujita, S. The cell surface is the place to be for brassinosteroid perception and responses. Nat. Plants 10, 206–218 (2024). https://doi.org/10.1038/s41477-024-01621-2

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