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
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 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
References
Depuydt, S. & Hardtke, C. S. Hormone signalling crosstalk in plant growth regulation. Curr. Biol. 21, R365–R373 (2011).
Vert, G. & Chory, J. Crosstalk in cellular signaling: background noise or the real thing? Dev. Cell 21, 985–991 (2011).
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).
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).
Nemhauser, J. L., Mockler, T. C. & Chory, J. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol. 2, E258 (2004).
Kozuka, T. et al. Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol. 153, 1608–1618 (2010).
Stavang, J. A. et al. Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60, 589–601 (2009).
Leivar, P. & Quail, P. H. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16, 19–28 (2011).
Chen, M. & Chory, J. Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 21, 664–671 (2011).
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).
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).
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).
Feng, S. et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475–479 (2008).
De Lucas, M. et al. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480–484 (2008).
Nozue, K. et al. Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358–361 (2007).
Foreman, J. et al. Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J. 65, 441–452 (2011).
Koini, M. A. et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408–413 (2009).
Song, L. et al. Genome-wide analysis revealed the complex regulatory network of brassinosteroid effects in photomorphogenesis. Mol. Plant 2, 755–772 (2009).
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).
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).
Kim, T. W. & Wang, Z. Y. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61, 681–704 (2010).
Tang, W. et al. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124–131 (2011).
Wang, Z. Y. et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505–513 (2002).
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).
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).
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).
He, J-X. et al. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307, 1634–1638 (2005).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Waters, M. T. et al. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell. 21, 1109–1128 (2009).
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).
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).
Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616–629 (2006).
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).
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).
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).
Machanick, P. & Bailey, T. L. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27, 1696–1697 (2011).
Furlan-Magaril, M., Rincon-Arano, H. & Recillas-Targa, F. Sequential chromatin immunoprecipitation protocol: ChIP–reChIP. Methods Mol. Biol. 543, 253–266 (2009).
Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25, 1105–1111 (2009).
Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
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
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
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
(PDF 785 kb)
Supplementary Table 1
(XLSX 57 kb)
Supplementary Table 2
(XLSX 185 kb)
Supplementary Table 3
(XLSX 50 kb)
Supplementary Table 4
(XLSX 225 kb)
Supplementary Table 5
(XLSX 159 kb)
Supplementary Table 6
(XLSX 29 kb)
Supplementary Table 7
(XLS 28 kb)
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ncb2545
This article is cited by
-
Natural genetic variation in GLK1-mediated photosynthetic acclimation in response to light
BMC Plant Biology (2024)
-
Natural variation of STKc_GSK3 kinase TaSG-D1 contributes to heat stress tolerance in Indian dwarf wheat
Nature Communications (2024)
-
Regulation of chloroplast biogenesis, development, and signaling by endogenous and exogenous cues
Physiology and Molecular Biology of Plants (2024)
-
Plants and global warming: challenges and strategies for a warming world
Plant Cell Reports (2024)
-
Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize
Genome Biology (2023)