Skip to main content
PMC home page
Protein & Cell logoLink to Protein & Cell
. 2013 May 25;4(6):475–482. doi: 10.1007/s13238-013-3027-8

Structural basis for differential recognition of brassinolide by its receptors

Ji She 1,2, Zhifu Han 3, Bin Zhou 4, Jijie Chai 3,5,✉
PMCID: PMC4875557  PMID: 23709366

Abstract

Brassinosteroids, a group of plant steroid hormones, regulate many aspects of plant growth and development. We and other have previously solved the crystal structures of BRI1(LRR) in complex with brassinolide, the most active brassinosteroid identified thus far. Although these studies provide a structural basis for the recognition of brassinolide by its receptor BRI1, it still remains poorly understood how the hormone differentiates among its conserved receptors. Here we present the crystal structure of the BRI1 homolog BRL1 in complex with brassinolide. The structure shows that subtle differences around the brassinolide binding site can generate a striking effect on its recognition by the BRI1 family of receptors. Structural comparison of BRL1 and BRI1 in their brassinolide-bound forms reveals the molecular basis for differential binding of brassinolide to its different receptors, which can be used for more efficient design of plant growth regulators for agricultural practice. On the basis of our structural studies and others’ data, we also suggest possible mechanisms for the activation of BRI1 family receptors.

Keywords: X-ray crystallography, leucine-rich repeat domain, brassinosteroid, BRL1

References

  1. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, Mc-Coy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr. 2002;58:1948–1954. doi: 10.1107/S0907444902016657. [DOI] [PubMed] [Google Scholar]
  2. Back TG, Pharis RP. Structure-activity studies of brassinosteroids and the search for novel analogues and mimetics with improved bioactivity. J Plant Growth Regul. 2003;22:350–361. doi: 10.1007/s00344-003-0057-0. [DOI] [PubMed] [Google Scholar]
  3. Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development. 2004;131:5341–5351. doi: 10.1242/dev.01403. [DOI] [PubMed] [Google Scholar]
  4. Ceserani T, Trofka A, Gandotra N, Nelson T. VH1/BRL2 receptor-like kinase interacts with vascular-specific adaptor proteins VIT and VIK to influence leaf venation. Plant J. 2009;57:1000–1014. doi: 10.1111/j.1365-313X.2008.03742.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Clay NK, Nelson T. VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in Arabidopsis. Plant Cell. 2002;14:2707–2722. doi: 10.1105/tpc.005884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clouse SD, Sasse JM. BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development. Annu Rev Plant Physiol Plant Mol Biol. 1998;49:427–451. doi: 10.1146/annurev.arplant.49.1.427. [DOI] [PubMed] [Google Scholar]
  7. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, De Lorenzo G, Tsernoglou D, Cervone F. The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci U S A. 2003;100:10124–10128. doi: 10.1073/pnas.1733690100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60:2126–2132. doi: 10.1107/S0907444904019158. [DOI] [PubMed] [Google Scholar]
  9. Eswar N, Eramian D, Webb B, Shen MY, Sali A. Protein structure modeling with MODELLER. Methods Mol Biol. 2008;426:145–159. doi: 10.1007/978-1-60327-058-8_8. [DOI] [PubMed] [Google Scholar]
  10. Friedrichsen DM, Joazeiro CA, Li J, Hunter T, Chory J. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol. 2000;123:1247–1256. doi: 10.1104/pp.123.4.1247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fukuda H. Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol. 2004;5:379–391. doi: 10.1038/nrm1364. [DOI] [PubMed] [Google Scholar]
  12. He Z, Wang ZY, Li J, Zhu Q, Lamb C, Ronald P, Chory J. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science. 2000;288:2360–2363. doi: 10.1126/science.288.5475.2360. [DOI] [PubMed] [Google Scholar]
  13. Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, Wilson IA, Chory J. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature. 2011;474:467–471. doi: 10.1038/nature10153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Huang P, Chandra V, Rastinejad F. Structural overview of the nuclear receptor superfamily: insights into physiology and therapeutics. Ann Rev Physiol. 2010;72:247–272. doi: 10.1146/annurev-physiol-021909-135917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jaillais Y, Belkhadir Y, Balsemao-Pires E, Dangl JL, Chory J. Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation. Proc Natl Acad Sci U S A. 2011;108:8503–8507. doi: 10.1073/pnas.1103556108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jaillais Y, Hothorn M, Belkhadir Y, Dabi T, Nimchuk ZL, Meyerowitz EM, Chory J. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev. 2011;25:232–237. doi: 10.1101/gad.2001911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kim TW, Wang ZY. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol. 2010;61:681–704. doi: 10.1146/annurev.arplant.043008.092057. [DOI] [PubMed] [Google Scholar]
  18. Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature. 2005;433:167–171. doi: 10.1038/nature03227. [DOI] [PubMed] [Google Scholar]
  19. Li J, Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell. 1997;90:929–938. doi: 10.1016/S0092-8674(00)80357-8. [DOI] [PubMed] [Google Scholar]
  20. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell. 2002;110:213–222. doi: 10.1016/S0092-8674(02)00812-7. [DOI] [PubMed] [Google Scholar]
  21. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007;40:658–674. doi: 10.1107/S0021889807021206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nakamura A, Fujioka S, Sunohara H, Kamiya N, Hong Z, Inukai Y, Miura K, Takatsuto S, Yoshida S, Ueguchi-Tanaka M, et al. The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol. 2006;140:580–590. doi: 10.1104/pp.105.072330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nam KH, Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell. 2002;110:203–212. doi: 10.1016/S0092-8674(02)00814-0. [DOI] [PubMed] [Google Scholar]
  24. Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Yoshida S, et al. BAS1: A gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc Natl Acad Sci U S A. 1999;96:15316–15323. doi: 10.1073/pnas.96.26.15316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Noguchi T, Fujioka S, Choe S, Takatsuto S, Yoshida S, Yuan H, Feldmann KA, Tax FE. Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol. 1999;121:743–752. doi: 10.1104/pp.121.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997;276:307–326. doi: 10.1016/S0076-6879(97)76066-X. [DOI] [PubMed] [Google Scholar]
  27. Renaud JP, Moras D. Structural studies on nuclear receptors. Cell Mol Life Sci. 2000;57:1748–1769. doi: 10.1007/PL00000656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. She J, Han Z, Kim TW, Wang J, Cheng W, Chang J, Shi S, Yang M, Wang ZY, Chai J. Structural insight into brassinosteroid perception by BRI1. Nature. 2011;474:472–476. doi: 10.1038/nature10178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shiu SH, Bleecker AB. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A. 2001;98:10763–10768. doi: 10.1073/pnas.181141598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vert G, Nemhauser JL, Geldner N, Hong F, Chory J. Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol. 2005;21:177–201. doi: 10.1146/annurev.cellbio.21.090704.151241. [DOI] [PubMed] [Google Scholar]
  31. Wang X, Chory J. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science. 2006;313:1118–1122. doi: 10.1126/science.1127593. [DOI] [PubMed] [Google Scholar]
  32. Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell. 2008;15:220–235. doi: 10.1016/j.devcel.2008.06.011. [DOI] [PubMed] [Google Scholar]
  33. Wang ZY, Bai MY, Oh E, Zhu JY. Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet. 2012;46:701–724. doi: 10.1146/annurev-genet-102209-163450. [DOI] [PubMed] [Google Scholar]
  34. Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature. 2001;410:380–383. doi: 10.1038/35066597. [DOI] [PubMed] [Google Scholar]
  35. Zhou A, Wang H, Walker JC, Li J. BRL1, a leucinerich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. Plant J. 2004;40:399–409. doi: 10.1111/j.1365-313X.2004.02214.x. [DOI] [PubMed] [Google Scholar]

Articles from Protein & Cell are provided here courtesy of Oxford University Press

RESOURCES