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.

  • Review Article
  • Published:

Light-regulated transcriptional networks in higher plants

Nature Reviews Genetics volume 8, pages 217–230 (2007)Cite this article

Key Points

  • Light is perceived by plants through distinct families of photoreceptors and affects multiple developmental processes, including seedling photomorphogenesis, seed germination and the shade-avoidance and photoperiod responses.

  • Plants have evolved intricate light-regulated transcriptional networks that mediate these developmental changes. Recent genetic and genomic studies have greatly expanded our understanding of the components and hierarchy of these sophisticated networks.

  • Through genetic and molecular approaches, many key downstream regulators in the network have been identified. A large proportion of them are transcription factors, some of which have a role in mediating the response to a wide range of light signals, and are therefore potential integration points for light-quality-specific signals.

  • Genomic studies indicate massive reprogramming of the plant transcriptome by light; for example, at least 20% of the genome in both Arabidopsis thaliana and rice shows light-regulated differential expression during seedling development. Many of the early light-responsive genes are transcription factors.

  • Organ-specific expression profiles are observed, indicating that different transcriptional networks are recruited in different organs and cell types.

  • The integration of light signals with intrinsic signals (such as those from the circadian clock) and other environmental signals (such as temperature) is evident through research on photoperiod response and seed germination. The photoperiod response also regulates other light-controlled processes.

  • Future research will focus on identifying the direct targets of the many light-responsive transcription factors, exploring the molecular basis of organ specificity, and expanding studies on the integration of light responses with other inputs.

Abstract

Plants have evolved complex and sophisticated transcriptional networks that mediate developmental changes in response to light. These light-regulated processes include seedling photomorphogenesis, seed germination and the shade-avoidance and photoperiod responses. Understanding the components and hierarchical structure of the transcriptional networks that are activated during these processes has long been of great interest to plant scientists. Traditional genetic and molecular approaches have proved powerful in identifying key regulatory factors and their positions within these networks. Recent genomic studies have further revealed that light induces massive reprogramming of the plant transcriptome, and that the early light-responsive genes are enriched in transcription factors. These combined approaches provide new insights into light-regulated transcriptional networks.

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: General mechanisms of transcription factor regulation by light.
Figure 2: Transcriptional networks for seedling photomorphogenesis.
Figure 3: Light-responsive promoters.
Figure 4: A model for the light and temperature control of seed germination.
Figure 5: Transcriptional networks involved in the shade-avoidance response.
Figure 6: The photoperiod response in Arabidopsis thaliana.

Similar content being viewed by others

References

  1. Chen, M., Chory, J. & Fankhauser, C. Light signal transduction in higher plants. Annu. Rev. Genet. 38, 87–117 (2004). This review provides a comprehensive, up-to-date overview of plant photoreceptors.

    Article  CAS  PubMed  Google Scholar 

  2. Tepperman, J. M., Zhu, T., Chang, H.-S., Wang, X. & Quail, P. H. Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc. Natl Acad. Sci. USA 98, 9437–9442 (2001). This work identifies the transcriptional cascades that lie downstream of PHYA, which involve multiple transcription factors as primary targets.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ma, L. et al. Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13, 2589–2607 (2001). A landmark paper that demonstrates the massive effects of light on genome-wide transcription.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Jiao, Y., Ma, L., Strickland, E. & Deng, X. W. Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell 17, 3239–3256 (2005). This paper compares light-regulated transcription profiles in A. thaliana and rice. Organ specificity of the transcriptome and the evolution of the light-regulated transcriptome are also discussed.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Quail, P. H. Phytochrome photosensory signalling networks. Nature Rev. Mol. Cell Biol. 3, 85–93 (2002).

    Article  CAS  Google Scholar 

  6. Lin, C. & Shalitin, D. Cryptochrome structure and signal transduction. Annu. Rev. Plant Biol. 54, 469–496 (2003).

    Article  CAS  PubMed  Google Scholar 

  7. Kleine, T., Lockhart, P. & Batschauer, A. An Arabidopsis protein closely related to Synechocystis cryptochrome is targeted to organelles. Plant J. 35, 93–103 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Kim, J.-I. et al. Phytochrome phosphorylation modulates light signaling by influencing the protein–protein interaction. Plant Cell 16, 2629–2640 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ryu, J. S. et al. Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell 120, 395–406 (2005).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  11. Yeh, K.-C. & Lagarias, J. C. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl Acad. Sci. USA 95, 13976–13981 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Matsushita, T., Mochizuki, N. & Nagatani, A. Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 424, 571–574 (2003).

    Article  CAS  PubMed  Google Scholar 

  13. Sang, Y. et al. N-terminal domain-mediated homodimerization is required for photoreceptor activity of Arabidopsis CRYPTOCHROME 1. Plant Cell 17, 1569–1584 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Christie, J. M. et al. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282, 1698–1701 (1998).

    Article  CAS  PubMed  Google Scholar 

  15. Salomon, M., Christie, J. M., Knieb, E., Lempert, U. & Briggs, W. R. Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39, 9401–9410 (2000).

    Article  CAS  PubMed  Google Scholar 

  16. Weisshaar, B., Armstrong, G. A., Block, A., da Costa e Silva, O. & Hahlbrock, K. Light-inducible and constitutively expressed DNA-binding proteins recognizing a plant promoter element with functional relevance in light responsiveness. EMBO J. 10, 1777–1786 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Feldbrugge, M. et al. Functional analysis of a light-responsive plant bZIP transcriptional regulator. Plant Cell 6, 1607–1621 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Klimczak, L. J., Schindler, U. & Cashmore, A. R. DNA binding activity of the Arabidopsis G-box binding factor GBF1 is stimulated by phosphorylation by casein kinase II from broccoli. Plant Cell 4, 87–98 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Klimczak, L. J. et al. Reconstitution of Arabidopsis casein kinase II from recombinant subunits and phosphorylation of transcription factor GBF1. Plant Cell 7, 105–115 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Harter, K. et al. Light-regulated modification and nuclear translocation of cytosolic G-box binding factors in parsley. Plant Cell 6, 545–559 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kircher, S. et al. Nuclear import of the parsley bZIP transcription factor CPRF2 is regulated by phytochrome photoreceptors. J. Cell Biol. 144, 201–211 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wellmer, F. et al. Phosphorylation of the parsley bZIP transcription factor CPRF2 is regulated by light. J. Biol. Chem. 274, 29476–29482 (1999).

    Article  CAS  PubMed  Google Scholar 

  23. Osterlund, M. T., Hardtke, C. S., Wei, N. & Deng, X. W. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405, 462–466 (2000). A landmark paper that shows that transcription factors, which are downstream of light-signalling pathways, are regulated at the level of protein degradation by COP1 and other proteins. This work demonstrates for the first time that photomorphogenesis is governed by proteolysis.

    Article  CAS  PubMed  Google Scholar 

  24. Yi, C. & Deng, X. W. COP1 — from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol. 15, 618–625 (2005).

    Article  CAS  PubMed  Google Scholar 

  25. Seo, H.-S. et al. LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423, 995–999 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. von Arnim, A. G. & Deng, X. W. Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79, 1035–1045 (1994).

    Article  CAS  PubMed  Google Scholar 

  27. Jakoby, M. et al. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7, 106–111 (2002).

    Article  CAS  PubMed  Google Scholar 

  28. Toledo-Ortiz, G., Huq, E. & Quail, P. H. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15, 1749–1770 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Holm, M., Ma, L.-G., Qu, L.-J. & Deng, X.-W. Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev. 16, 1247–1259 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Schindler, U., Menkens, A. E., Beckmann, H., Ecker, J. R. & Cashmore, A. R. Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins. EMBO J. 11, 1261–1273 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sprenger-Haussels, M. & Weisshaar B. Transactivation properties of parsley proline-rich bZIP transcription factors. Plant J. 22, 1–8 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Feldbrugge, M., Sprenger, M., Hahlbrock, K. & Weisshaar, B. PcMYB1, a novel plant protein containing a DNA-binding domain with one MYB repeat, interacts in vivo with a light-regulatory promoter unit. Plant J. 11, 1079–1093 (1997).

    Article  CAS  PubMed  Google Scholar 

  33. Zimmermann, I. M., Heim, M. A., Weisshaar, B. & Uhrig, J. F. Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J. 40, 22–34 (2004).

    Article  CAS  PubMed  Google Scholar 

  34. Terzaghi, W. B. & Cashmore, A. R. Light-regulated transcription. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 445–474 (1995).

    Article  CAS  Google Scholar 

  35. Arguello-Astorga, G. & Herrera-Estrella, L. Evolution of light-regulated plant promoters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 525–555 (1998).

    Article  CAS  PubMed  Google Scholar 

  36. Hudson, M. E. & Quail, P. H. Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol. 133, 1605–1616 (2003). This paper describes a genome-scale approach to identifying promoter cis -elements in PHYA-responding genes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jiao, Y. et al. A genome-wide analysis of blue-light regulation of Arabidopsis transcription factor gene expression during seedling development. Plant Physiol. 133, 1480–1493 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tepperman, J. M. et al. Expression profiling of PHYB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation. Plant J. 38, 725–739 (2004).

    Article  CAS  PubMed  Google Scholar 

  39. Riechmann, J. L. et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110 (2000).

    Article  CAS  PubMed  Google Scholar 

  40. Tepperman, J. M., Hwang, Y.-S. & Quail, P. H. PHYA dominates in transduction of red-light signals to rapid-responding genes at the initiation of Arabidopsis seedling deetiolation. Plant J. 48, 728–742 (2006).

    Article  CAS  PubMed  Google Scholar 

  41. Wang, H. et al. Analysis of far-red light-regulated genome expression profiles of phytochrome A pathway mutants in Arabidopsis. Plant J. 32, 723–733 (2002). This work exploits global expression analysis to understand the effects of mutations in key regulators in the PHYA-signalling pathway.

    Article  CAS  PubMed  Google Scholar 

  42. McCormac, A. C. & Terry, M. J. Light-signalling pathways leading to the co-ordinated expression of HEMA1 and Lhcb during chloroplast development in Arabidopsis thaliana. Plant J. 32, 549–559 (2002).

    Article  CAS  PubMed  Google Scholar 

  43. Hudson, M., Ringli, C., Boylan, M. T. & Quail, P. H. The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev. 13, 2017–2027 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wang, H & Deng, X. W. Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1. EMBO J. 21, 1339–1349 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Hudson, M. E., Lisch, D. R. & Quail, P. H. The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J. 34, 453–471 (2003).

    Article  CAS  PubMed  Google Scholar 

  46. Ballesteros, M. L. et al. LAF1, a MYB transcription activator for phytochrome A signaling. Genes Dev. 15, 2613–2625 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Fairchild, C. D., Schumaker, M. A. & Quail, P. H. HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev. 14, 2377–2391 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Duek, P. D. & Fankhauser, C. HFR1, a putative bHLH transcription factor, mediates both phytochrome A and cryptochrome signalling. Plant J. 34, 827–836 (2003).

    Article  CAS  PubMed  Google Scholar 

  49. Soh, M.-S., Kim, Y.-M., Han, S.-J. & Song, P.-S. REP1, a basic helix–loop–helix protein, is required for a branch pathway of phytochrome A signaling in Arabidopsis. Plant Cell 12, 2061–2074 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Spiegelman, J. I. et al. Cloning of the Arabidopsis RSF1 gene by using a mapping strategy based on high-density DNA arrays and denaturing high-performance liquid chromatography. Plant Cell 12, 2485–2498 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kim, Y.-M., Woo, J.-C., Song, P.-S. & Soh, M.-S. HFR1, a phytochrome A-signalling component, acts in a separate pathway from HY5, downstream of COP1 in Arabidopsis thaliana. Plant J. 30, 711–719 (2002).

    Article  CAS  PubMed  Google Scholar 

  52. Yang, K.-Y., Kim, Y.-M., Lee, S., Song, P.-S. & Soh, M.-S. Overexpression of a mutant basic helix–loop–helix protein HFR1, HFR1-dN105, activates a branch pathway of light signaling in Arabidopsis. Plant Physiol. 133, 1630–1642 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Park, D.-H. et al. The Arabidopsis COG1 gene encodes a Dof domain transcription factor and negatively regulates phytochrome signaling. Plant J. 34, 161–171 (2003).

    Article  CAS  PubMed  Google Scholar 

  54. Ward, J. M., Cufr, C. A., Denzel, M. A. & Neff, M. M. The Dof transcription factor OBP3 modulates phytochrome and cryptochrome signaling in Arabidopsis. Plant Cell 17, 475–485 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Yadav, V., Mallappa, C., Gangappa, S. N., Bhatia, S. & Chattopadhyay, S. A basic helix-loop-helix transcription factor in Arabidopsis, MYC2, acts as a repressor of blue light-mediated photomorphogenic growth. Plant Cell 17, 1953–1966 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Mallappa, C., Yadav, V., Negi, P. & Chattopadhyay, S. A bzip transcription factor, G-box binding factor 1, regulates blue light mediated photomorphogenic growth in Arabidopsis. J. Biol. Chem. 31, 22190–22199 (2006).

    Article  CAS  Google Scholar 

  57. Khanna, R. et al. A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix–loop–helix transcription factors. Plant Cell 16, 3033–3044 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ni, M., Tepperman, J. M. & Quail, P. H. PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix–loop–helix protein. Cell 95, 657–667 (1998).

    Article  CAS  PubMed  Google Scholar 

  59. Zhu, Y., Tepperman, J. M., Fairchild, C. D. & Quail, P. H. Phytochrome B binds with greater apparent affinity than phytochrome A to the basic helix–loop–helix factor PIF3 in a reaction requiring the PAS domain of PIF3. Proc. Natl Acad. Sci. USA 97, 13419–13424 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Huq, E. & Quail, P. H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21, 2441–2450 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Huq, E. et al. Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305, 1937–1941 (2004).

    Article  CAS  PubMed  Google Scholar 

  62. Oh, E. et al. PIL5, a phytochrome-interacting basic helix–loop–helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16, 3045–3058 (2004). References 61 and 62 describe the identification of an additional branch of the PHYA-signalling network, which negatively regulates chlorophyll biosynthesis and represses seed germination.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kim, J. et al. Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15, 2399–2407 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Bauer, D. et al. Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16, 1433–1445 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Fujimori, T., Yamashino, T., Kato, T. & Mizuno, T. Circadian-controlled basic/helix–loop–helix factor, PIL6, implicated in light-signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 45, 1078–1086 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Monte, E. et al. The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc. Natl Acad. Sci. USA 101, 16091–16098 (2004). A comprehensive study of the multiple facets of PIF3, a PHYA-interacting transcription factor that regulates a branch of the PHYA-signalling network.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Shen, H., Moon, J. & Huq, E. PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J. 44, 1023–1035 (2005).

    Article  CAS  PubMed  Google Scholar 

  68. Brown, B. A. et al. A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl Acad. Sci. USA 102, 18225–18230 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Oravecz, A., et al. CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18, 1975–1990 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Oyama, T., Shimura, Y. & Okada, K. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 11, 2983–2995 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Ulm, R., et al. Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc. Natl Acad. Sci. USA 101, 1397–1402 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Hardtke, C. S. et al. HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J. 19, 4997–5006 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Ang, L.-H. et al. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell 1, 213–222 (1998).

    Article  CAS  PubMed  Google Scholar 

  74. Chattopadhyay, S., Ang, L.-H., Puente, P., Deng, X.-W. & Wei, N. Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10, 673–683 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lee, J. et al. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell (in the press).

  76. Ma, L. et al. Genomic evidence for COP1 as a repressor of light-regulated gene expression and development in Arabidopsis. Plant Cell 14, 2383–2398 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Wang, Z.-Y. et al. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9, 491–507 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Schaffer, R. et al. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219–1229 (1998).

    Article  CAS  PubMed  Google Scholar 

  79. Wang, Z.-Y. & Tobin, E. M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207–1217 (1998).

    Article  CAS  PubMed  Google Scholar 

  80. Ma, L. et al. Organ-specific expression of Arabidopsis genome during development. Plant Physiol. 138, 80–91 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Khanna, R. et al. Functional profiling reveals that only a small number of phytochrome-regulated early-response genes in Arabidopsis are necessary for optimal deetiolation. Plant Cell 18, 2157–2171 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Degenhardt, J. & Tobin, E. M. A DNA binding activity for one of two closely defined phytochrome regulatory elements in an Lhcb promoter is more abundant in etiolated than in green plants. Plant Cell 8, 31–41 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Puente, P., Wei, N. & Deng, X. W. Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 15, 3732–3743 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Chattopadhyay, S., Puente, P., Deng, X. W. & Wei, N. Combinatorial interaction of light-responsive elements plays a critical role in determining the response characteristics of light-regulated promoters in Arabidopsis. Plant J. 15, 69–77 (1998).

    Article  CAS  PubMed  Google Scholar 

  85. Chua, Y.-L., Brown, A. P. & Gray, J. C. Targeted histone acetylation and altered nuclease accessibility over short regions of the pea plastocyanin gene. Plant Cell 13, 599–612 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Chua, Y.-L., Watson, L. A. & Gray, J. C. The transcriptional enhancer of the pea plastocyanin gene associates with the nuclear matrix and regulates gene expression through histone acetylation. Plant Cell 15, 1468–1479 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Bertrand, C. et al. Arabidopsis HAF2 gene encoding TATA-binding protein (TBP)-associated factor TAF1, is required to integrate light signals to regulate gene expression and growth. J. Biol. Chem. 280, 1465–1473 (2005).

    Article  CAS  PubMed  Google Scholar 

  88. Benhamed, M., Bertrand, C., Servet, C. & Zhou, D.-X. Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18, 2893–2903 (2006). This paper, with reference 87, demonstrates that an HAT and an HDAC are involved in transcriptional regulation downstream of multiple photoreceptors, indicating that chromatin remodelling is a convergence point in light-regulated transcription.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Chory, J., Peto, C., Feinbaum, R., Pratt, L. & Ausubel, F. Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58, 991–999 (1989).

    Article  CAS  PubMed  Google Scholar 

  90. Pepper, A., Delaney, T., Washburn, T., Poole, D. & Chory, J. DET1, a negative regulator of light-mediated development and gene expression in Arabidopsis, encodes a novel nuclear-localized protein. Cell 78, 109–116 (1994).

    Article  CAS  PubMed  Google Scholar 

  91. Schroeder, D. F. et al. De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr. Biol. 12, 1462–1472 (2002).

    Article  CAS  PubMed  Google Scholar 

  92. Yanagawa, Y. et al. Arabidopsis COP10 forms a complex with DDB1 and DET1 in vivo and enhances the activity of ubiquitin conjugating enzymes. Genes Dev. 18, 2172–2181 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Benvenuto, G., Formiggini, F., Laflamme, P., Malakhov, M. & Bowler, C. The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Curr Biol. 12, 1529–1534 (2002). References 91–93 describe the interaction of DET1, COP10 and DDB1 as a protein complex and suggest that chromatin remodelling might be involved in photomorphogenesis.

    Article  CAS  PubMed  Google Scholar 

  94. Berloco, M., Fanti, L., Breling, A., Orlando, V. & Pimpinelli, S. The maternal effect gene, abnormal oocyte (abo), of Drosophila melanogaster encodes a specific negative regulator of histones. Proc. Natl Acad. Sci. USA 98, 12126–12131 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Maxwell, B. B., Andersson, C. R., Poole, D. S., Kay, S. A. & Chory, J. HY5, Circadian Clock-Associated 1, and a cis-element, DET1 dark response element, mediate DET1 regulation of chlorophyll a/b-binding protein 2 expression. Plant Physiol. 133, 1565–1577 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Penfield, S. et al. Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr. Biol. 5, 378–381 (2005).

    Google Scholar 

  97. Oh, E. et al. Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J. 47, 124–139 (2006). References 96 and 97 provide evidence that light signal is transduced through a phytochrome-interacting bHLH transcription factor to control seed germination by regulating endogenous GA level.

    Article  CAS  PubMed  Google Scholar 

  98. Roig-Villanova, I., Bou, J., Sorin, C., Devlin, P. F. & Martinez-Garcia, J. F. Identification of primary target genes of phytochrome signaling. Early transcriptional control during shade avoidance responses in Arabidopsis. Plant Physiol. 141, 85–96 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Sessa, G. et al. A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev. 19, 2811–2815 (2005). This paper describes a negative regulatory mechanism in shade-avoidance response.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Carabelli, M., Sessa, G., Baima, S., Morelli, G. & Ruberti, I. The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. Plant J. 4, 469–479 (1993).

    Article  CAS  PubMed  Google Scholar 

  101. Steindler, C. et al. Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development 126, 4235–4245 (1999).

    CAS  PubMed  Google Scholar 

  102. Ohgishi, M., Oka, A., Morelli, G., Ruberti, I. & Aoyama, T. Negative autoregulation of the Arabidopsis homeobox gene ATHB-2. Plant J. 25, 389–398 (2001).

    Article  CAS  PubMed  Google Scholar 

  103. Salter, M. G., Franklin, K. A. & Whitelam, G. C. Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426, 680–683 (2003).

    Article  CAS  PubMed  Google Scholar 

  104. Devlin, P. F., Yanovsky, M. J. & Kay, S. A. A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol. 133, 1617–1629 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Yamashino, T. et al. A Link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 44, 619–629 (2003).

    Article  CAS  PubMed  Google Scholar 

  106. Locke, J. C. et al. Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol. Syst. Biol. 1, 2005.0013 (2005).

  107. Zeilinger, M. N., Farré, E. M., Taylor, S. R., Kay, S. A. & Doyle, F. J. III. A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol. Syst. Biol. 2, 58 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Locke, J. C. et al. Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2, 59 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Strayer, C. et al. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768–771 (2000).

    Article  CAS  PubMed  Google Scholar 

  110. Harmer, S. L. et al. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110–2113 (2000).

    Article  CAS  PubMed  Google Scholar 

  111. Alabadí, D. et al. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293, 880–883 (2001). A landmark paper that reports the first model for the plant circadian clock, following the observation of a reciprocal regulation between CCA1/LHY and TOC1.

    Article  PubMed  Google Scholar 

  112. Alabadí, D., Yanovsky, M. J., Más, P., Harmer, S. L. & Kay, S. A. Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr. Biol. 12, 757–761 (2002).

    Article  PubMed  Google Scholar 

  113. Doyle, M. R. et al. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419, 74–77 (2002).

    Article  CAS  PubMed  Google Scholar 

  114. Mizoguchi, T. et al. LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev. Cell 2, 629–641 (2002).

    Article  CAS  PubMed  Google Scholar 

  115. Kikis, E. A., Khanna, R. & Quail, P. H. ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. Plant J. 44, 300–313 (2005).

    Article  CAS  PubMed  Google Scholar 

  116. Mizoguchi et al. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17, 2255–2270 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Hazen, S. P. et al. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc. Natl Acad. Sci. USA 102, 10387–10392 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Onai, K. & Ishiura, M. PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes Cells 10, 963–972 (2005).

    Article  CAS  PubMed  Google Scholar 

  119. Farre, E. M., Harmer, S. L., Harmon, F. G., Yanovsky, M. J. & Kay, S. A. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 15, 47–54 (2005).

    Article  CAS  PubMed  Google Scholar 

  120. Nakamichi, N. et al. The Arabidopsis pseudo-response regulators, PRR5 and PRR7, coordinately play essential roles for circadian clock function. Plant Cell Physiol. 46, 609–619 (2005).

    Article  CAS  PubMed  Google Scholar 

  121. Nakamichi, N., Kita, M., Ito, S., Yamashino, T. & Mizuno, T. PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. 46, 686–698 (2005).

    Article  CAS  PubMed  Google Scholar 

  122. Liu, X.-L., Covington, M. F., Fankhauser, C., Chory, J. & Wagner, D. R. ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13, 1293–1304 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Covington, M. F. et al. ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell 13, 1305–1315 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Allen, T. et al. Arabidopsis FHY3 specifically gates phytochrome signaling to the circadian clock. Plant Cell 18, 2506–2516 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Viczián, A. et al. Functional characterization of phytochrome interacting factor 3 for the Arabidopsis thaliana circadian clockwork. Plant Cell Physiol. 46, 1591–1602 (2005).

    Article  CAS  PubMed  Google Scholar 

  126. Somers, D. E., Schultz, T. F., Milnamow, M. & Kay, S. A. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101, 319–329 (2000).

    Article  CAS  PubMed  Google Scholar 

  127. Jarillo, J. A. et al. An Arabidopsis circadian clock component interacts with both CRY1 and PHYB. Nature 410, 487–490 (2001).

    Article  CAS  PubMed  Google Scholar 

  128. Schultz, T. F., Kiyosue, T., Yanovsky, M., Wada, M. & Kay, S. A. A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13, 2659–2670 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Más, P., Kim, W.-Y., Somers, D. E. & Kay, S. A. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567–570 (2003).

    Article  CAS  PubMed  Google Scholar 

  130. Han, L., Mason, M., Risseeuw, E. P., Crosby, W. L. & Somers, D. E. Formation of an SCFZTL complex is required for proper regulation of circadian timing. Plant J. 40, 291–301 (2004).

    Article  CAS  PubMed  Google Scholar 

  131. Imaizumi, T., Tran, H. G., Swartz, T. E., Briggs, W. R. & Kay, S. A. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302–306 (2003).

    Article  CAS  PubMed  Google Scholar 

  132. Millar, A. J. & Kay, S. A. Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. Proc. Natl Acad. Sci. USA 93, 15491–15496 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Huq, E., Tepperman, J. M. & Quail, P. H. GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc. Natl Acad. Sci. USA 97, 9789–9794 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Michael, T. P., Salome, P. A. & McClung, C. R. Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc. Natl Acad. Sci. USA 100, 6878–6883 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Salome, P. A. & McClung, C. R. PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17, 791–803 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Gould, P. D. et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18, 1177–1187 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Halliday, K. J. & Whitelam, G. C. Changes in photoperiod or temperature alter the functional relationships between phytochromes and reveal roles for PHYD and PHYE. Plant Physiol. 131, 1913–1920 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Mathews, S. & Sharrock, R. A. The phytochrome gene family in grasses (Poaceae): a phylogeny and evidence that grasses have a subset of the loci found in dicot angiosperms. Mol. Biol. Evol. 13, 1141–1150 (1996).

    Article  CAS  PubMed  Google Scholar 

  139. Sharrock, R. A. & Clack, T. Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol. 130, 442–456 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Krall, L. & Reed, J. W. The histidine kinase-related domain participates in phytochrome B function but is dispensable. Proc. Natl Acad. Sci. USA 97, 8169–8174 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Brudler, R. et al. Identification of a new cryptochrome class. Structure, function, and evolution. Mol. Cell 11, 59–67 (2003).

    Article  CAS  PubMed  Google Scholar 

  142. Partch, C. L., Clarkson, M. W., Ozgur, S., Lee, A.-L. & Sancar, A. Role of structural plasticity in signal transduction by the cryptochrome blue-light photoreceptor. Biochemistry 44, 3795–3805 (2005).

    Article  CAS  PubMed  Google Scholar 

  143. Yang, H.-Q. et al. The C termini of Arabidopsis cryptochromes mediate a constitutive light response. Cell 103, 815–827 (2000).

    Article  CAS  PubMed  Google Scholar 

  144. Wang, H., Ma, L.-G., Li, J.-M., Zhao, H.-Y. & Deng, X.-W. Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294, 154–158 (2001).

    Article  CAS  PubMed  Google Scholar 

  145. Yang, H.-Q., Tang, R.-H. & Cashmore, A. R. The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell 13, 2573–2587 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Briggs, W. R. & Christie, J. M. Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 7, 204–210 (2002).

    Article  CAS  PubMed  Google Scholar 

  147. Koornneef, M., Bentsink, L. & Hilhorst, H. Seed dormancy and germination. Curr. Opin. Plant Biol. 5, 33–36 (2002).

    Article  CAS  PubMed  Google Scholar 

  148. Takano, M. et al. Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 17, 3311–3125 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Saijo, Y. et al. The COP1–SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev. 17, 2642–2647 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This area of research in the authors' laboratory has been supported by a US National Institutes of Health grant to X.W.D.

Author information

Authors and Affiliations

  1. Department of Molecular, Cellular and Developmental Biology, 165 Prospect Street, Yale University, New Haven, 06520-8104, Connecticut, USA

    Yuling Jiao, On Sun Lau & Xing Wang Deng

Authors
  1. Yuling Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. On Sun Lau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xing Wang Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xing Wang Deng.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Tair

CCA1

COP1

CRY1

CRY2

DET1

FAR1

FHY3

GCN5

HAF2

HD1

HFR1

HY5

LAF1

LHY

SPA1

PIF3

PHOT1

PHOT2

PHYA

PHYB

FURTHER INFORMATION

Deng laboratory homepage

Glossary

Phototropism

Directional plant growth that is determined by the direction of the light source.

Gravitropism

A growth movement in response to gravity.

Chromophore

The part of a molecule that absorbs specific wavelengths of light and is responsible for its colour.

Proplastid

Precursors of plastids, which are plant organelles that include chloroplasts.

Etioplast

An immature chloroplast that has not been exposed to light.

Ubiquitin E3 ligase

Enzymes that covalently attach ubiquitin to a lysine residue on a target protein.

26S proteasome

A large, ATP-dependent, multicatalytic protease, which degrades ubiquitylated proteins to short peptides.

Hypocotyl

The part of the stem of a young seedling that is situated underneath the cotyledon (the seed leaves) and above the root.

Apical zone

The apical part of a seedling that includes the apical hook and the cotyledon.

Hook opening

The unbending of the apical hook during seedling photomorphogenesis.

Chromatin immunoprecipitation

A technique that is used to determine whether a particular protein, for example, a transcription factor, can bind to a specific region on a chromatin in vivo.

Nuclear matrix

The network of fibres found throughout the inside of a cell nucleus.

Histone acetyltransferase

A type of enzyme that acetylates conserved lysine amino acids on histones by transferring an acetyl group from acetyl CoA to lysine to form ε-N-acetyl lysine.

Histone deacetylase

A type of enzyme that removes an acetyl group from histones, which usually allows histones to bind DNA and inhibit gene transcription.

Gibberellic acid

A phytohormone involved in promoting stem elongation, seed germination, mobilization of food reserves in seeds and other processes.

Cold stratification

A dormancy-breaking process of treating seeds with a period of moist cold, which a seed must endure before germination.

Fluence rate

The light irradiance that is incident from all angles onto a small region of space.

Subjective day

An artificially defined daytime in circadian experiments.

Thermocycles

Alternating warm and cool conditions.

ChIP-on-chip approach

A method that combines chromatin immunoprecipitation with microarray technology to identify in vivo targets of a transcription factor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiao, Y., Lau, O. & Deng, X. Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8, 217–230 (2007). https://doi.org/10.1038/nrg2049

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg2049

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