Abstract
Brassinosteroids (BRs) are steroid hormones that control many aspects of plant growth and development1,2. BRs bind to the plasma membrane receptor kinase BRI1, and act through a signalling pathway that involves a glycogen synthase kinase-3-like kinase (BIN2) and a serine/threonine phosphatase (BSU1)3,4,5. Previous models proposed that BIN2 negatively regulates BR signalling by controlling the stability and subcellular localization of the related transcription factors BES1 and BZR1 by phosphorylation, in a manner reminiscent of the canonical Wnt signalling pathway of metazoans6,7,8,9. Here we present strong evidence for a different mode of regulation of BR signalling. We show that BES1 is localized constitutively to the nucleus, where its activity is modulated by nuclear-localized BIN2 kinase. BIN2-mediated phosphorylation of BES1 inhibits its DNA-binding activity on BR-responsive target promoters and its transcriptional activity through impaired multimerization. Our observations demonstrate that phosphorylation-dependent inhibition of DNA binding and trans-activation is the key primary mechanism of BES1 regulation.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Change history
18 December 2023
A Correction to this paper has been published: https://doi.org/10.1038/s41586-023-06766-2
References
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)
Mandava, N. B. Plant growth-promoting brassinosteroids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 23–52 (1988)
Kinoshita, T. et al. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433, 167–171 (2005)
Li, J. & Nam, K. H. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295, 1299–1301 (2002)
Mora-Garcia, S. et al. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 18, 448–460 (2004)
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)
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)
Clouse, S. D. Brassinosteroid signal transduction: Clarifying the pathway from ligand perception to gene expression. Mol. Cell 10, 973–982 (2002)
Peng, P. & Li, J. Brassinosteroid signal transduction: A mix of conservation and novelty. J. Plant Growth Regul. 22, 298–312 (2003)
Hall, J. M., Couse, J. F. & Korach, K. S. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276, 36869–36872 (2001)
Olefsky, J. M. Nuclear receptor minireview series. J. Biol. Chem. 276, 36863–36864 (2001)
Choe, S. et al. Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3β-like kinase. Plant Physiol. 130, 1506–1515 (2002)
Perez-Perez, J. M., Ponce, M. R. & Micol, J. L. The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242, 161–173 (2002)
He, J. X. et al. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307, 1634–1638 (2005)
Yin, Y. et al. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120, 249–259 (2005)
Zhao, J. et al. Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol. 130, 1221–1229 (2002)
Salic, A., Lee, E., Mayer, L. & Kirschner, M. W. Control of β-catenin stability: Reconstitution of the cytoplasmic steps of the wnt pathway in Xenopus egg extracts. Mol. Cell 5, 523–532 (2000)
Staal, F. J., Noort Mv, M., Strous, G. J. & Clevers, H. C. Wnt signals are transmitted through N-terminally dephosphorylated β-catenin. EMBO Rep. 3, 63–68 (2002)
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)
Wang, Z. Y. et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505–513 (2002)
Wang, Z. Y., Seto, H., Fujioka, S., Yoshida, S. & Chory, J. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380–383 (2001)
Guo, H. & Ecker, J. R. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115, 667–677 (2003)
Lopez-Molina, L., Mongrand, S. & Chua, N. H. A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl Acad. Sci. USA 98, 4782–4787 (2001)
Sasaki, A. et al. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299, 1896–1898 (2003)
Gray, W. M., Kepinski, S., Rouse, D., Leyser, O. & Estelle, M. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001)
Xie, D. X., Feys, B. F., James, S., Nieto-Rostro, M. & Turner, J. G. COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094 (1998)
Friedrichsen, D. M., Joazeiro, C. A., 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)
Acknowledgements
We thank J. Nemhauser, N. Geldner and A. Nott for critical reading of the manuscript and discussions; T. Dabi and S. Palida for technical assistance; K. Chen for sharing the vectors containing NLS, nls, NES and nes; and Y. Yin for providing the BES1 antibody. This work was supported by a Human Frontier Science Program Organization long-term fellowship to G.V. and grants to J.C. from the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, and the National Science Foundation. J.C. is an investigator of the Howard Hughes Medical Institute. Author Contributions G.V. and J.C. conceived and designed the experiments. G.V. performed the experiments. G.V. and J.C. analyzed the data and wrote the paper.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
Supplementary information
Supplementary Notes
Supplementary Text, Supplementary Methods, Supplementary Figures — except movies from Supplementary Fig S6a and b. This file contains additional results and technical details of experimental methods used in this study. It also displays Supplementary Figures 1–8. (PDF 197 kb)
Supplementary Figure S6a
Vizualization over 1 hour of BES1–GFP fluorescence in the root following BL treatment. (AVI 7940 kb)
Supplementary Figure S6b
Vizualization over 1 hour of BES1–GFP fluorescence in the hypocotyl following BL treatment. (AVI 7684 kb)
Rights and permissions
About this article
Cite this article
Vert, G., Chory, J. Downstream nuclear events in brassinosteroid signalling. Nature 441, 96–100 (2006). https://doi.org/10.1038/nature04681
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature04681
This article is cited by
-
Zea mays GSK2 gene is involved in brassinosteroid signaling
Plant Growth Regulation (2022)
-
Fine mapping of the BnaC04.BIL1 gene controlling plant height in Brassica napus L
BMC Plant Biology (2021)
-
Author Correction: Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination
Nature Communications (2021)
-
Brassinosteroids suppress ethylene-induced fruitlet abscission through LcBZR1/2-mediated transcriptional repression of LcACS1/4 and LcACO2/3 in litchi
Horticulture Research (2021)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.