Brassinosteroids are essential phytohormones that have crucial roles in plant growth and development. Perception of brassinosteroids requires an active complex of BRASSINOSTEROID-INSENSITIVE 1 (BRI1) and BRI1-ASSOCIATED KINASE 1 (BAK1). Recognized by the extracellular leucine-rich repeat (LRR) domain of BRI1, brassinosteroids induce a phosphorylation-mediated cascade to regulate gene expression. Here we present the crystal structures of BRI1(LRR) in free and brassinolide-bound forms. BRI1(LRR) exists as a monomer in crystals and solution independent of brassinolide. It comprises a helical solenoid structure that accommodates a separate insertion domain at its concave surface. Sandwiched between them, brassinolide binds to a hydrophobicity-dominating surface groove on BRI1(LRR). Brassinolide recognition by BRI1(LRR) is through an induced-fit mechanism involving stabilization of two interdomain loops that creates a pronounced non-polar surface groove for the hormone binding. Together, our results define the molecular mechanisms by which BRI1 recognizes brassinosteroids and provide insight into brassinosteroid-induced BRI1 activation.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Clouse, S. D. & Sasse, J. M. BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 427–451 (1998)
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)
Li, J. & Chory, J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929–938 (1997)
Li, J. et al. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213–222 (2002)
Nam, K. H. & Li, J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203–212 (2002)
Li, J. & Nam, K. H. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295, 1299–1301 (2002)
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)
Wang, X. & Chory, J. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313, 1118–1122 (2006)
Tang, W. et al. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis . Science 321, 557–560 (2008)
Shiu, S. H. et al. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220–1234 (2004)
He, Z. et al. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360–2363 (2000)
Kinoshita, T. et al. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433, 167–171 (2005)
Li, J. Brassinosteroid signaling: from receptor kinases to transcription factors. Curr. Opin. Plant Biol. 8, 526–531 (2005)
Kim, T. W. & Wang, Z. Y. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61, 681–704 (2010)
Russinova, E. et al. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216–3229 (2004)
Wang, X. et al. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell 8, 855–865 (2005)
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)
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)
J aillais, Y. et al. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev. 25, 232–237 (2011)
Kajava, A. V. Structural diversity of leucine-rich repeat proteins. J. Mol. Biol. 277, 519–527 (1998)
Di Matteo, A. et al. The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc. Natl Acad. Sci. USA 100, 10124–10128 (2003)
Hink, M. A., Shah, K., Russinova, E., de Vries, S. C. & Visser, A. J. Fluorescence fluctuation analysis of Arabidopsis thaliana somatic embryogenesis receptor-like kinase and brassinosteroid insensitive 1 receptor oligomerization. Biophys. J. 94, 1052–1062 (2008)
Zullo, M. T. A. & Adam, G. Brassinosteroid phytohormones—structure, bioactivity and applications. Braz. J. Plant Physiol. 14, 143–181 (2002)
Li, J., Lease, K. A., Tax, F. E. & Walker, J. C. BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana . Proc. Natl Acad. Sci. USA 98, 5916–5921 (2001)
Liu, L. et al. Structural basis of Toll-like receptor 3 signaling with double-stranded RNA. Science 320, 379–381 (2008)
Park, B. S. et al. The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex. Nature 458, 1191–1195 (2009)
Whippo, C. W. & Hangarter, R. P. A brassinosteroid-hypersensitive mutant of BAK1 indicates that a convergence of photomorphogenic and hormonal signaling modulates phototropism. Plant Physiol. 139, 448–457 (2005)
Yun, H. S. et al. Analysis of phosphorylation of the BRI1/BAK1 complex in Arabidopsis reveals amino acid residues critical for receptor formation and activation of BR signaling. Mol. Cells 27, 183–190 (2009)
Sheard, L. B. & Zheng, N. Plant biology: signal advance for abscisic acid. Nature 462, 575–576 (2009)
Sheard, L. B. et al. Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor. Nature 468, 400–405 (2010)
Otwinowski, Z. &. Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997)
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658–674 (2007)
Schubert, W. D. et al. Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111, 825–836 (2002)
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004)
Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948–1954 (2002)
DeLano, W. L. PyMOL molecular viewer 〈http://www.pymol.org〉 (2002)
We thank S. Huang and J. He at Shanghai Synchrotron Radiation Facility (SSRF) for assistance with data collection; J. Chory from the Salk Institute for providing the tritium-labelled brassinolide. This research was funded by the National Outstanding Young Scholar Science Foundation of National Natural Science Foundation of China grant no. 20101331722 to J. Chai and NIH R01GM066258 to Z.-Y.W.
The authors declare no competing financial interests.
About this article
Cite this article
She, J., Han, Z., Kim, T. et al. Structural insight into brassinosteroid perception by BRI1. Nature 474, 472–476 (2011). https://doi.org/10.1038/nature10178
Brassinosteroids regulate outer ovule integument growth in part via the control of INNER NO OUTER by BRASSINOZOLE‐RESISTANT family transcription factors
Journal of Integrative Plant Biology (2020)
Frontiers in Plant Science (2020)
Current Biology (2020)
The Journal of Physical Chemistry B (2020)
Plant Biology (2020)