The leucine-rich repeat receptor kinase (LRR-RK) BRASSINOSTEROID INSENSITIVE 1 (BRI1) requires a shape-complementary SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) co-receptor for brassinosteroid sensing and receptor activation1. Interface mutations that weaken the interaction between receptor and co-receptor in vitro reduce brassinosteroid signalling responses2. The SERK3 elongated (elg) allele3,4,5 maps to the complex interface and shows enhanced brassinosteroid signalling, but surprisingly no tighter binding to the BRI1 ectodomain in vitro. Here, we report that rather than promoting the interaction with BRI1, the elg mutation disrupts the ability of the co-receptor to interact with the ectodomains of BRI1-ASSOCIATED-KINASE1 INTERACTING KINASE (BIR) receptor pseudokinases, negative regulators of LRR-RK signalling6. A conserved lateral surface patch in BIR LRR domains is required for targeting SERK co-receptors and the elg allele maps to the core of the complex interface in a 1.25 Å BIR3–SERK1 structure. Collectively, our structural, quantitative biochemical and genetic analyses suggest that brassinosteroid signalling complex formation is negatively regulated by BIR receptor ectodomains.
Subscribe to Journal
Get full journal access for 1 year
only $4.92 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.
Santiago, J., Henzler, C. & Hothorn, M. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341, 889–892 (2013).
Hohmann, U. et al. Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors. Proc. Natl Acad. Sci. USA 115, 3488–3493 (2018).
Halliday, K., Devlin, P. F., Whitelam, G. C., Hanhart, C. & Koornneef, M. The ELONGATED gene of Arabidopsis acts independently of light and gibberellins in the control of elongation growth. Plant J. 9, 305–312 (1996).
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).
Jaillais, Y., Belkhadir, Y., Balsemão-Pires, E., Dangl, J. L. & Chory, J. Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation. Proc. Natl Acad. Sci. USA 108, 8503–8507 (2011).
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).
Clouse, S. D., Langford, M. & McMorris, T. C. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111, 671–678 (1996).
Li, J. & Chory, J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929–938 (1997).
Hothorn, M. et al. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474, 467–471 (2011).
She, J. et al. Structural insight into brassinosteroid perception by BRI1. Nature 474, 472–476 (2011).
Sun, Y. et al. Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res. 23, 1326–1329 (2013).
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).
Bojar, D. et al. Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J. 78, 31–43 (2014).
Hohmann, U., Lau, K. & Hothorn, M. The structural basis of ligand perception and signal activation by receptor kinases. Annu. Rev. Plant Biol. 68, 109–137 (2017).
Belkhadir, Y. et al. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc. Natl Acad. Sci. USA 109, 297–302 (2012).
McAndrew, R. et al. Structure of the OsSERK2 leucine-rich repeat extracellular domain. Acta Crystallogr. D. Biol. Crystallogr. 70, 3080–3086 (2014).
Friedrichsen, D. M., Joazeiro, C. A. P., Li, J., Hunter, T. & Chory, J. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol. 123, 1247–1256 (2000).
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).
Ma, C. et al. Structural basis for BIR1-mediated negative regulation of plant immunity. Cell Res. 27, 1521–1524 (2017).
Santiago, J. et al. Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife 5, e15075 (2016).
Kabsch, W. & Sander, C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577–2637 (1983).
Gao, M. et al. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6, 34–44 (2009).
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. New Phytol. 212, 637–645 (2016).
Blaum, B. S. et al. Structure of the pseudokinase domain of BIR2, a regulator of BAK1-mediated immune signaling in Arabidopsis. J. Struct. Biol. 186, 112–121 (2014).
He, Z. et al. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360–2363 (2000).
Wang, Z., Meng, P., Zhang, X., Ren, D. & Yang, S. BON1 interacts with the protein kinases BIR1 and BAK1 in modulation of temperature-dependent plant growth and cell death in Arabidopsis. Plant J. 67, 1081–1093 (2011).
Li, Y., Gou, M., Sun, Q. & Hua, J. Requirement of calcium binding, myristoylation, and protein-protein interaction for the Copine BON1 function in Arabidopsis. J. Biol. Chem. 285, 29884–29891 (2010).
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).
Hashimoto, Y., Zhang, S. & Blissard, G. W. Ao38, a new cell line from eggs of the black witch moth, Ascalapha odorata (Lepidoptera: Noctuidae), is permissive for AcMNPV infection and produces high levels of recombinant proteins. BMC Biotechnol. 10, 50 (2010).
Kozma, P., Hamori, A., Cottier, K., Kurunczi, S. & Horvath, R. Grating coupled interferometry for optical sensing. Appl. Phys. B 97, 5–8 (2009).
We thank B. Kemmerling for kindly providing us with BIR2 and BIR3 polyclonal antibodies, N. Geldner for providing seeds, and the staff at beam line PXIII of the Swiss Light Source, Villigen, Switzerland, for technical assistance during data collection, J. Santiago for providing the SERK2 expression plasmid, and K. Lau for help with preparing figures. This work was supported by grant 31003A_176237 from the Swiss National Science Foundation and by an International Research Scholar Award from the Howard Hughes Medical Institute (to M.H.).
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Hohmann, U., Nicolet, J., Moretti, A. et al. The SERK3 elongated allele defines a role for BIR ectodomains in brassinosteroid signalling. Nature Plants 4, 345–351 (2018). https://doi.org/10.1038/s41477-018-0150-9
International Journal of Molecular Sciences (2020)
A strong correlation between consensus sequences and unique super secondary structures in leucine rich repeats
Proteins: Structure, Function, and Bioinformatics (2020)
Proceedings of the National Academy of Sciences (2020)
Oxidization increases the binding of EGCG to serum albumin revealed by kinetic data from label-free optical biosensor with reference channel
The Analyst (2020)
Current Opinion in Plant Biology (2020)