Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1997 Oct;9(10):1727–1743. doi: 10.1105/tpc.9.10.1727

Attenuation of phytochrome A and B signaling pathways by the Arabidopsis circadian clock.

S L Anderson 1, D E Somers 1, A J Millar 1, K Hanson 1, J Chory 1, S A Kay 1
PMCID: PMC157017  PMID: 9368413

Abstract

In higher plants, environmental cues such as light signals are integrated with circadian clock signals to control precisely the daily rhythms observed for many biological functions. We have used a fusion of the promoter of a chlorophyll a/b binding protein gene, CAB2, with firefly luciferase (cab2::luc) to monitor the detailed kinetics of transcription in response to photoreceptor activation in Arabidopsis. Using this marker in phototransduction and circadian-dysfunctional mutants, we studied how signals from phytochrome and the circadian clock are integrated for the regulation of CAB2 transcription. Results from these mutant studies demonstrate that similar expression features, namely, the acute and circadian responses, are present in both etiolated and green seedlings and that the acute and circadian responses are genetically separable. We also demonstrate that persistent Pfr signaling occurs in red light-pulsed etiolated seedlings, which suggests that the circadian clock antagonizes Pfr-mediated signal transduction. Based on these genetic studies, we propose a model for the regulation of CAB2 transcription in which individual photoreceptors and phototransduction components have been assigned to specific pathways for the regulation of discrete kinetic components of the CAB2 expression pattern.

Full Text

The Full Text of this article is available as a PDF (3.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson S. L., Kay S. A. Functional dissection of circadian clock- and phytochrome-regulated transcription of the Arabidopsis CAB2 gene. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1500–1504. doi: 10.1073/pnas.92.5.1500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson S. L., Kay S. A. Phototransduction and circadian clock pathways regulating gene transcription in higher plants. Adv Genet. 1997;35:1–34. doi: 10.1016/s0065-2660(08)60446-0. [DOI] [PubMed] [Google Scholar]
  3. Anderson S. L., Teakle G. R., Martino-Catt S. J., Kay S. A. Circadian clock- and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of the Arabidopsis CAB2 promoter. Plant J. 1994 Oct;6(4):457–470. doi: 10.1046/j.1365-313x.1994.6040457.x. [DOI] [PubMed] [Google Scholar]
  4. Arpaia G., Loros J. J., Dunlap J. C., Morelli G., Macino G. Light induction of the clock-controlled gene ccg-1 is not transduced through the circadian clock in Neurospora crassa. Mol Gen Genet. 1995 Apr 20;247(2):157–163. doi: 10.1007/BF00705645. [DOI] [PubMed] [Google Scholar]
  5. Arpaia G., Loros J. J., Dunlap J. C., Morelli G., Macino G. The interplay of light and the circadian clock. Independent dual regulation of clock-controlled gene ccg-2(eas). Plant Physiol. 1993 Aug;102(4):1299–1305. doi: 10.1104/pp.102.4.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Beator J., Pötter E., Kloppstech K. The effect of heat shock on morphogenesis in barley : coordinated circadian regulation of mRNA levels for light-regulated genes and of the capacity for accumulation of chlorophyll protein complexes. Plant Physiol. 1992 Dec;100(4):1780–1786. doi: 10.1104/pp.100.4.1780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bent A. F., Kunkel B. N., Dahlbeck D., Brown K. L., Schmidt R., Giraudat J., Leung J., Staskawicz B. J. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science. 1994 Sep 23;265(5180):1856–1860. doi: 10.1126/science.8091210. [DOI] [PubMed] [Google Scholar]
  8. Bowler C., Yamagata H., Neuhaus G., Chua N. H. Phytochrome signal transduction pathways are regulated by reciprocal control mechanisms. Genes Dev. 1994 Sep 15;8(18):2188–2202. doi: 10.1101/gad.8.18.2188. [DOI] [PubMed] [Google Scholar]
  9. Boylan M. T., Quail P. H. Phytochrome a overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10806–10810. doi: 10.1073/pnas.88.23.10806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carre I. A., Kay S. A. Multiple DNA-Protein Complexes at a Circadian-Regulated Promoter Element. Plant Cell. 1995 Dec;7(12):2039–2051. doi: 10.1105/tpc.7.12.2039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chory J., Peto C. A., Ashbaugh M., Saganich R., Pratt L., Ausubel F. Different Roles for Phytochrome in Etiolated and Green Plants Deduced from Characterization of Arabidopsis thaliana Mutants. Plant Cell. 1989 Sep;1(9):867–880. doi: 10.1105/tpc.1.9.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Daniels S. M., Quail P. H. Monoclonal antibodies to three separate domains on 124 kilodalton phytochrome from Avena. Plant Physiol. 1984 Nov;76(3):622–626. doi: 10.1104/pp.76.3.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Giuliano G., Hoffman N. E., Ko K., Scolnik P. A., Cashmore A. R. A light-entrained circadian clock controls transcription of several plant genes. EMBO J. 1988 Dec 1;7(12):3635–3642. doi: 10.1002/j.1460-2075.1988.tb03244.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hicks K. A., Millar A. J., Carré I. A., Somers D. E., Straume M., Meeks-Wagner D. R., Kay S. A. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science. 1996 Nov 1;274(5288):790–792. doi: 10.1126/science.274.5288.790. [DOI] [PubMed] [Google Scholar]
  15. Kay S. A., Nagatani A., Keith B., Deak M., Furuya M., Chua N. H. Rice Phytochrome Is Biologically Active in Transgenic Tobacco. Plant Cell. 1989 Aug;1(8):775–782. doi: 10.1105/tpc.1.8.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kay S. A. Shedding light on clock controlled cab gene transcription in higher plants. Semin Cell Biol. 1993 Apr;4(2):81–86. doi: 10.1006/scel.1993.1010. [DOI] [PubMed] [Google Scholar]
  17. Kunkel T., Neuhaus G., Batschauer A., Chua N. H., Schäfer E. Functional analysis of yeast-derived phytochrome A and B phycocyanobilin adducts. Plant J. 1996 Oct;10(4):625–636. doi: 10.1046/j.1365-313x.1996.10040625.x. [DOI] [PubMed] [Google Scholar]
  18. Lee M. K., Tuttle J. B., Rebhun L. I., Cleveland D. W., Frankfurter A. The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton. 1990;17(2):118–132. doi: 10.1002/cm.970170207. [DOI] [PubMed] [Google Scholar]
  19. Millar A. J., Carré I. A., Strayer C. A., Chua N. H., Kay S. A. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science. 1995 Feb 24;267(5201):1161–1163. doi: 10.1126/science.7855595. [DOI] [PubMed] [Google Scholar]
  20. Millar A. J., Short S. R., Chua N. H., Kay S. A. A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell. 1992 Sep;4(9):1075–1087. doi: 10.1105/tpc.4.9.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Millar A. J., Straume M., Chory J., Chua N. H., Kay S. A. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science. 1995 Feb 24;267(5201):1163–1166. doi: 10.1126/science.7855596. [DOI] [PubMed] [Google Scholar]
  22. Neuhaus G., Bowler C., Kern R., Chua N. H. Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell. 1993 Jun 4;73(5):937–952. doi: 10.1016/0092-8674(93)90272-r. [DOI] [PubMed] [Google Scholar]
  23. Parks B. M., Quail P. H., Hangarter R. P. Phytochrome A regulates red-light induction of phototropic enhancement in Arabidopsis. Plant Physiol. 1996 Jan;110(1):155–162. doi: 10.1104/pp.110.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Quail P. H., Briggs W. R., Chory J., Hangarter R. P., Harberd N. P., Kendrick R. E., Koornneef M., Parks B., Sharrock R. A., Schafer E. Spotlight on Phytochrome Nomenclature. Plant Cell. 1994 Apr;6(4):468–471. doi: 10.1105/tpc.6.4.468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Reed J. W., Nagpal P., Poole D. S., Furuya M., Chory J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell. 1993 Feb;5(2):147–157. doi: 10.1105/tpc.5.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Somers D. E., Sharrock R. A., Tepperman J. M., Quail P. H. The hy3 Long Hypocotyl Mutant of Arabidopsis Is Deficient in Phytochrome B. Plant Cell. 1991 Dec;3(12):1263–1274. doi: 10.1105/tpc.3.12.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sun L., Tobin E. M. Phytochrome-regulated expression of genes encoding light-harvesting chlorophyll a/b-protein in two long hypocotyl mutants and wild type plants of Arabidopsis thaliana. Photochem Photobiol. 1990 Jul;52(1):51–56. doi: 10.1111/j.1751-1097.1990.tb01754.x. [DOI] [PubMed] [Google Scholar]
  28. Teakle G. R., Kay S. A. The GATA-binding protein CGF-1 is closely related to GT-1. Plant Mol Biol. 1995 Dec;29(6):1253–1266. doi: 10.1007/BF00020466. [DOI] [PubMed] [Google Scholar]
  29. Wagner D., Tepperman J. M., Quail P. H. Overexpression of Phytochrome B Induces a Short Hypocotyl Phenotype in Transgenic Arabidopsis. Plant Cell. 1991 Dec;3(12):1275–1288. doi: 10.1105/tpc.3.12.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wang Z. Y., Kenigsbuch D., Sun L., Harel E., Ong M. S., Tobin E. M. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell. 1997 Apr;9(4):491–507. doi: 10.1105/tpc.9.4.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wu Y., Hiratsuka K., Neuhaus G., Chua N. H. Calcium and cGMP target distinct phytochrome-responsive elements. Plant J. 1996 Dec;10(6):1149–1154. doi: 10.1046/j.1365-313x.1996.10061149.x. [DOI] [PubMed] [Google Scholar]
  32. Zagotta M. T., Hicks K. A., Jacobs C. I., Young J. C., Hangarter R. P., Meeks-Wagner D. R. The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J. 1996 Oct;10(4):691–702. doi: 10.1046/j.1365-313x.1996.10040691.x. [DOI] [PubMed] [Google Scholar]
  33. Zhong H. H., McClung C. R. The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol Gen Genet. 1996 May 23;251(2):196–203. doi: 10.1007/BF02172918. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES