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Downstream nuclear events in brassinosteroid signalling

An Author Correction to this article was published on 18 December 2023

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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.

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Figure 1: GSK3 kinases act redundantly to negatively regulate BR signalling.
Figure 2: BIN2 is found and required in the nucleus for BR signalling.
Figure 3: BES1 is constitutively nuclear and its levels are unaffected by BRs.
Figure 4: BIN2-mediated phosphorylation abolishes BES1 DNA-binding and trans -activation.

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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.

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Correspondence to Joanne Chory.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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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)

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Vert, G., Chory, J. Downstream nuclear events in brassinosteroid signalling. Nature 441, 96–100 (2006). https://doi.org/10.1038/nature04681

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