Brassinosteroid Sensing and Signaling in Plants

  • Ulrich Hohmann
  • Michael HothornEmail author


Brassinosteroids (BRs) are a class of growth-promoting steroid hormones in plants, which are sensed by the membrane receptor kinase BRASSINOSTEROID INSENSITIVE 1 (BRI1). BR binding to the extracellular domain of BRI1 creates a docking platform for shape-complementary co-receptor kinases of the SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) family. Ligand-induced hetero-dimerization of BRI1 with a SERK co-receptor at the cell surface renders their cytoplasmic kinase domains competent to trans-phosphorylate and activate each other. The fully active BRI1 kinase domain can then initiate a cytoplasmic signaling cascade, leading to substantial changes in gene expression. Here, we summarize our current mechanistic understanding of brassinosteroid sensing and BRI1 receptor activation.



Financial support by the Swiss National Science Foundation (grant number 156920) is gratefully acknowledged.


  1. Back TG, Pharis RP (2003) Structure-activity studies of brassinosteroids and the search for novel analogues and mimetics with improved bioactivity. J Plant Growth Regul 22:350–361. CrossRefPubMedGoogle Scholar
  2. Bajguz A (2007) Metabolism of brassinosteroids in plants. Plant Physiol Biochem PPB 45:95–107. CrossRefPubMedGoogle Scholar
  3. Bajwa VS, Wang X, Blackburn RK et al (2013) Identification and functional analysis of tomato BRI1 and BAK1 receptor kinase phosphorylation sites. Plant Physiol 163:30–42. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Belkhadir Y, Jaillais Y, Epple P et al (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci U S A 109:297–302. CrossRefPubMedGoogle Scholar
  5. Bojar D, Martinez J, Santiago J et al (2014) Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J 78:31–43. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brandt B, Hothorn M (2016) SERK co-receptor kinases. Curr Biol CB 26:R225–R226. CrossRefPubMedGoogle Scholar
  7. Choe J, Kelker MS, Wilson IA (2005) Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 309:581–585. CrossRefPubMedGoogle Scholar
  8. Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Friedrichsen DM, Joazeiro CAP, Li J et al (2000) Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol 123:1247–1256. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Gampala SS, Kim T-W, He J-X et al (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13:177–189. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Geldner N, Hyman DL, Wang X et al (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21:1598–1602. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gou X, Yin H, He K et al (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet 8:e1002452. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Grove MD, Spencer GF, Rohwedder WK et al (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216–217. CrossRefGoogle Scholar
  14. Gruszka D, Szarejko I, Maluszynski M (2011) New allele of HvBRI1 gene encoding brassinosteroid receptor in barley. J Appl Genet. 52(3):257–68.
  15. He Z, Wang ZY, Li J et al (2000) Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288:2360–2363CrossRefPubMedGoogle Scholar
  16. He K, Gou X, Yuan T et al (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol CB 17:1109–1115. CrossRefPubMedGoogle Scholar
  17. Hohmann U, Santiago J, Nicolet J, Olsson V, Spiga FM, Ludwig Hothorn A, Butenko MA, Hothorn M (2018) Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors. Proc Natl Acad Sci 115(13):3488–3493Google Scholar
  18. Hong Z, Jin H, Tzfira T, Li J (2008) Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20:3418–3429. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hothorn M, Belkhadir Y, Dreux M et al (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474:467–471. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Jaillais Y, Belkhadir Y, Balsemão-Pires E et al (2011a) Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation. Proc Natl Acad Sci U S A 108:8503–8507. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jaillais Y, Hothorn M, Belkhadir Y et al (2011b) Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev 25:232–237. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kajava AV (1998) Structural diversity of leucine-rich repeat proteins. J Mol Biol 277:519–527. CrossRefPubMedGoogle Scholar
  23. Karlova R, Boeren S, Russinova E et al (2006) The Arabidopsis somatic embryogenesis receptor-like kinase1 protein complex includes brassinosteroid-insensitive1. Plant Cell 18:626–638. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kim T-W, Guan S, Burlingame AL, Wang Z-Y (2011) The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol Cell 43:561–571. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kinoshita T, Caño-Delgado A, Seto H et al (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171. CrossRefPubMedGoogle Scholar
  26. Kobe B, Deisenhofer J (1993) Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature 366:751–756. CrossRefPubMedGoogle Scholar
  27. Leonard JN, Ghirlando R, Askins J et al (2008) The TLR3 signaling complex forms by cooperative receptor dimerization. Proc Natl Acad Sci U S A 105:258–263. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938CrossRefPubMedGoogle Scholar
  29. Li J, Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295:1299–1301. CrossRefPubMedGoogle Scholar
  30. Li J, Nam KH, Vafeados D, Chory J (2001) BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol 127:14–22CrossRefPubMedPubMedCentralGoogle Scholar
  31. Li J, Wen J, Lease KA et al (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222CrossRefPubMedGoogle Scholar
  32. Liu L, Botos I, Wang Y et al (2008) Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320:379–381. CrossRefPubMedPubMedCentralGoogle Scholar
  33. McAndrew R, Pruitt RN, Kamita SG et al (2014) Structure of the OsSERK2 leucine-rich repeat extracellular domain. Acta Crystallogr D Biol Crystallogr 70:3080–3086. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mora-García S, Vert G, Yin Y et al (2004) Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev 18:448–460. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212CrossRefPubMedGoogle Scholar
  36. Noguchi T, Fujioka S, Choe S et al (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol 121:743–752CrossRefPubMedPubMedCentralGoogle Scholar
  37. Oh MH, Ray WK, Huber SC et al (2000) Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol 124:751–766CrossRefPubMedPubMedCentralGoogle Scholar
  38. Oh M-H, Wang X, Kota U et al (2009) Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc Natl Acad Sci U S A 106:658–663. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Santiago J, Henzler C, Hothorn M (2013) Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341:889–892. CrossRefPubMedGoogle Scholar
  40. She J, Han Z, Kim T-W et al (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474:472–476. CrossRefPubMedPubMedCentralGoogle Scholar
  41. She J, Han Z, Zhou B, Chai J (2013) Structural basis for differential recognition of brassinolide by its receptors. Protein Cell 4:475–482. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A 98:10763–10768. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Sun Y, Han Z, Tang J et al (2013) Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res 23:1326–1329. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Tang W, Kim T-W, Oses-Prieto JA et al (2008) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321:557–560. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signalling. Nature 441:96–100. CrossRefPubMedGoogle Scholar
  46. Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313:1118–1122. CrossRefPubMedGoogle Scholar
  47. Wang ZY, Seto H, Fujioka S et al (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–383. CrossRefPubMedGoogle Scholar
  48. Wang ZY, Nakano T, Gendron J et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2:505–513CrossRefPubMedGoogle Scholar
  49. Wang X, Goshe MB, Soderblom EJ et al (2005a) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor kinase. Plant Cell 17:1685–1703. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wang X, Li X, Meisenhelder J et al (2005b) Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev Cell 8:855–865. CrossRefPubMedGoogle Scholar
  51. Wang Z, Liu J, Sudom A et al (2006) Crystal structures of IRAK-4 kinase in complex with inhibitors: a serine/threonine kinase with tyrosine as a gatekeeper. Struct Lond Engl 1993 14:1835–1844. CrossRefGoogle Scholar
  52. Wang X, Kota U, He K et al (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15:220–235. CrossRefPubMedGoogle Scholar
  53. Wang J, Jiang J, Wang J et al (2014) Structural insights into the negative regulation of BRI1 signaling by BRI1-interacting protein BKI1. Cell Res 24:1328–1341. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Wang R, Liu M, Yuan M et al (2016) The brassinosteroid-activated BRI1 receptor kinase is switched off by dephosphorylation mediated by cytoplasm-localized PP2A B’ subunits. Mol Plant 9:148–157. CrossRefPubMedGoogle Scholar
  55. Xu W, Huang J, Li B et al (2008) Is kinase activity essential for biological functions of BRI1? Cell Res 18:472–478. CrossRefPubMedGoogle Scholar
  56. Yan L, Ma Y, Liu D et al (2012) Structural basis for the impact of phosphorylation on the activation of plant receptor-like kinase BAK1. Cell Res 22:1304–1308. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Yin Y, Wang ZY, Mora-Garcia S et al (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181–191CrossRefPubMedGoogle Scholar
  58. Zhao J, Peng P, Schmitz RJ et al (2002) Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol 130:1221–1229. CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Structural Plant Biology Laboratory, Department of Botany and Plant BiologyUniversity of GenevaGenevaSwitzerland

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