Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses

Nature Cell Biology volume 14, pages 802–809 (2012)Cite this article

Subjects

Abstract

Plant growth is coordinately regulated by environmental and hormonal signals. Brassinosteroid (BR) plays essential roles in growth regulation by light and temperature, but the interactions between BR and these environmental signals remain poorly understood at the molecular level. Here, we show that direct interaction between the dark- and heat-activated transcription factor phytochrome-interacting factor 4 (PIF4) and the BR-activated transcription factor BZR1 integrates the hormonal and environmental signals. BZR1 and PIF4 interact with each other in vitro and in vivo, bind to nearly 2,000 common target genes, and synergistically regulate many of these target genes, including the PRE family helix–loop–helix factors required for promoting cell elongation. Genetic analysis indicates that BZR1 and PIFs are interdependent in promoting cell elongation in response to BR, darkness or heat. These results show that the BZR1–PIF4 interaction controls a core transcription network, enabling plant growth co-regulation by the steroid and environmental signals.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: BZR1 interacts with PIF4.
Figure 2: BZR1 and PIFs act interdependently in promoting hypocotyl elongation.
Figure 3: BZR1 and PIF4 share a large number of genomic targets.
Figure 4: BZR1 and PIF4 regulate different genes interdependently and independently.
Figure 5: PREs promote hypocotyl elongation downstream of BZR1 and PIF4.
Figure 6: High temperature promotion of hypocotyl elongation requires both BZR1 and PIF4.

Similar content being viewed by others

Accession codes

Primary accessions

Gene Expression Omnibus

References

  1. Depuydt, S. & Hardtke, C. S. Hormone signalling crosstalk in plant growth regulation. Curr. Biol. 21, R365–R373 (2011).

    Article  CAS  Google Scholar 

  2. Vert, G. & Chory, J. Crosstalk in cellular signaling: background noise or the real thing? Dev. Cell 21, 985–991 (2011).

    Article  CAS  Google Scholar 

  3. Li, J., Nagpal, P., Vitart, V., McMorris, T. C. & Chory, J. A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272, 398–401 (1996).

    Article  CAS  Google Scholar 

  4. Szekeres, M. et al. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85, 171–182 (1996).

    Article  CAS  Google Scholar 

  5. Nemhauser, J. L., Mockler, T. C. & Chory, J. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol. 2, E258 (2004).

    Article  Google Scholar 

  6. Kozuka, T. et al. Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol. 153, 1608–1618 (2010).

    Article  CAS  Google Scholar 

  7. Stavang, J. A. et al. Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60, 589–601 (2009).

    Article  CAS  Google Scholar 

  8. Leivar, P. & Quail, P. H. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16, 19–28 (2011).

    Article  CAS  Google Scholar 

  9. Chen, M. & Chory, J. Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 21, 664–671 (2011).

    Article  CAS  Google Scholar 

  10. Al-Sady, B., Ni, W., Kircher, S., Schafer, E. & Quail, P. H. Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell 23, 439–446 (2006).

    Article  CAS  Google Scholar 

  11. Shin, J. et al. Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proc. Natl Acad. Sci. USA 106, 7660–7665 (2009).

    Article  CAS  Google Scholar 

  12. Leivar, P. et al. Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell. 21, 3535–3553 (2009).

    Article  CAS  Google Scholar 

  13. Feng, S. et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475–479 (2008).

    Article  CAS  Google Scholar 

  14. De Lucas, M. et al. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480–484 (2008).

    Article  CAS  Google Scholar 

  15. Nozue, K. et al. Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358–361 (2007).

    Article  CAS  Google Scholar 

  16. Foreman, J. et al. Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J. 65, 441–452 (2011).

    Article  CAS  Google Scholar 

  17. Koini, M. A. et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408–413 (2009).

    Article  CAS  Google Scholar 

  18. Song, L. et al. Genome-wide analysis revealed the complex regulatory network of brassinosteroid effects in photomorphogenesis. Mol. Plant 2, 755–772 (2009).

    Article  CAS  Google Scholar 

  19. 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).

    Article  CAS  Google Scholar 

  20. Gray, W. M., Ostin, A., Sandberg, G., Romano, C. P. & Estelle, M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl Acad. Sci. USA 95, 7197–7202 (1998).

    Article  CAS  Google Scholar 

  21. Kim, T. W. & Wang, Z. Y. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61, 681–704 (2010).

    Article  CAS  Google Scholar 

  22. Tang, W. et al. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124–131 (2011).

    Article  CAS  Google Scholar 

  23. Wang, Z. Y. et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505–513 (2002).

    Article  CAS  Google Scholar 

  24. Gampala, S. S. et al. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 13, 177–189 (2007).

    Article  CAS  Google Scholar 

  25. Luo, X-M. et al. Integration of light and brassinosteroid signaling pathways by a GATA transcription factor in Arabidopsis. Dev. Cell 19, 872–883 (2010).

    Article  CAS  Google Scholar 

  26. Fan, X. Y. et al. BZS1, a B-box protein, promotes photomorphogenesis downstream of both brassinosteroid and light signaling pathways. Mol. Plant 5, 65–74 (2012).

    Article  CAS  Google Scholar 

  27. He, J-X. et al. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307, 1634–1638 (2005).

    Article  CAS  Google Scholar 

  28. Ji, H., Jiang, H., Ma, W. & Wong, W. H. Using CisGenome to analyze ChIP-chip and ChIP-seq data. Curr. Protoc. Bioinformatics 33, 2.13.1–2.13.45 (2011).

    Google Scholar 

  29. Muino, J. M., Hoogstraat, M., van Ham, R. C. & van Dijk, A. D. PRI-CAT: a web-tool for the analysis, storage and visualization of plant ChIP-seq experiments. Nucleic Acids Res. 39, W524–W527 (2011).

    Article  CAS  Google Scholar 

  30. Richter, R., Behringer, C., Muller, I. K. & Schwechheimer, C. The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes Dev. 24, 2093–2104 (2010).

    Article  CAS  Google Scholar 

  31. Lorrain, S., Trevisan, M., Pradervand, S. & Fankhauser, C. Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 60, 449–461 (2009).

    Article  CAS  Google Scholar 

  32. Nozue, K., Harmer, S. L. & Maloof, J. N. Genomic analysis of circadian clock-, light-, and growth-correlated genes reveals PHYTOCHROME-INTERACTING FACTOR5 as a modulator of auxin signaling in Arabidopsis. Plant Physiol. 156, 357–372 (2011).

    Article  CAS  Google Scholar 

  33. Martinez-Garcia, J. F., Huq, E. & Quail, P. H. Direct targeting of light signals to a promoter element-bound transcription factor. Science 288, 859–863 (2000).

    Article  CAS  Google Scholar 

  34. Oh, E. et al. Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell. 21, 403–419 (2009).

    Article  CAS  Google Scholar 

  35. Lee, S. et al. Overexpression of PRE1 and its homologous genes activates Gibberellin-dependent responses in Arabidopsis thaliana. Plant Cell Physiol. 47, 591–600 (2006).

    Article  CAS  Google Scholar 

  36. Zhang, L. Y. et al. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell. 21, 3767–3780 (2009).

    Article  CAS  Google Scholar 

  37. 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).

    Article  CAS  Google Scholar 

  38. Wang, H., Zhu, Y., Fujioka, S., Asami, T. & Li, J. Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell. 21, 3781–3791 (2009).

    Article  CAS  Google Scholar 

  39. Hao, Y., Oh, E., Choi, G., Liang, Z. & Wang, Z. Y. Interactions between HLH and bHLH factors modulate light-regulated plant development. Mol. Plant 5, 162–171 (2012).

    Article  CAS  Google Scholar 

  40. Waters, M. T., Moylan, E. C. & Langdale, J. A. GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J. 56, 432–444 (2008).

    Article  CAS  Google Scholar 

  41. Waters, M. T. et al. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell. 21, 1109–1128 (2009).

    Article  CAS  Google Scholar 

  42. Fitter, D. W., Martin, D. J., Copley, M. J., Scotland, R. W. & Langdale, J. A. GLK gene pairs regulate chloroplast development in diverse plant species. Plant J. 31, 713–727 (2002).

    Article  CAS  Google Scholar 

  43. Yu, X. et al. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65, 634–646 (2011).

    Article  CAS  Google Scholar 

  44. Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616–629 (2006).

    Article  CAS  Google Scholar 

  45. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell. 18, 1121–1133 (2006).

    Article  CAS  Google Scholar 

  46. Wu, F. H. et al. Tape-Arabidopsis Sandwich—a simpler Arabidopsis protoplast isolation method. Plant Methodshttp://dx.doi.org/10.1186/1746-4811-5-16 (2009).

  47. Nakagawa, T. et al. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34–41 (2007).

    Article  CAS  Google Scholar 

  48. Machanick, P. & Bailey, T. L. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27, 1696–1697 (2011).

    Article  CAS  Google Scholar 

  49. Furlan-Magaril, M., Rincon-Arano, H. & Recillas-Targa, F. Sequential chromatin immunoprecipitation protocol: ChIP–reChIP. Methods Mol. Biol. 543, 253–266 (2009).

    Article  CAS  Google Scholar 

  50. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25, 1105–1111 (2009).

    Article  CAS  Google Scholar 

  51. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Stanford Center for Genomics and Personalized Medicine (SCGPM) service centre led by M. Snyder and A. Sidow for the sequencing service, Z. Wen for carrying out the sequencing, Y. Bai for help with genomic data analysis and Y. Hao for experimental assistance. Research was primarily supported by a grant from the NIH (R01GM066258).

Author information

Authors and Affiliations

  1. Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA

    Eunkyoo Oh, Jia-Ying Zhu & Zhi-Yong Wang

Authors
  1. Eunkyoo Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jia-Ying Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhi-Yong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.O. and J-Y.Z. carried out experiments. E.O. analysed data and wrote the manuscript. Z-Y.W. designed experiments, analysed data and wrote the manuscript.

Corresponding author

Correspondence to Zhi-Yong Wang.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oh, E., Zhu, JY. & Wang, ZY. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14, 802–809 (2012). https://doi.org/10.1038/ncb2545

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ncb2545

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing