Abstract
The plant photoreceptor phytochrome A utilizes three signal transduction pathways, dependent upon calcium and/or cGMP, to activate genes in the light. In this report, we have studied the phytochrome A regulation of a gene that is down-regulated by light, asparagine synthetase (AS1). We show that AS1 is expressed in the dark and repressed in the light. Repression of AS1 in the light is likely controlled by the same calcium/cGMP-dependent pathway that is used to activate other light responses. The use of the same signal transduction pathway for both activating and repressing different responses provides an interesting mechanism for phytochrome action. Using complementary loss- and gain-of-function experiments we have identified a 17 bp cis-element within the AS1 promoter that is both necessary and sufficient for this regulation. This sequence is likely to be the target for a highly conserved phytochrome-generated repressor whose activity is regulated by both calcium and cGMP.
Full Text
The Full Text of this article is available as a PDF (226.6 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bowler C., Chua N. H. Emerging themes of plant signal transduction. Plant Cell. 1994 Nov;6(11):1529–1541. doi: 10.1105/tpc.6.11.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bowler C., Neuhaus G., Yamagata H., Chua N. H. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell. 1994 Apr 8;77(1):73–81. doi: 10.1016/0092-8674(94)90236-4. [DOI] [PubMed] [Google Scholar]
- 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. 1993 Sep;4(3):469–479. doi: 10.1046/j.1365-313x.1993.04030469.x. [DOI] [PubMed] [Google Scholar]
- Colbert J. T., Costigan S. A., Zhao Z. Photoregulation of beta-Tubulin mRNA Abundance in Etiolated Oat and Barley Seedlings. Plant Physiol. 1990 Jul;93(3):1196–1202. doi: 10.1104/pp.93.3.1196. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dehesh K., Franci C., Sharrock R. A., Somers D. E., Welsch J. A., Quail P. H. The Arabidopsis phytochrome A gene has multiple transcription start sites and a promoter sequence motif homologous to the repressor element of monocot phytochrome A genes. Photochem Photobiol. 1994 Mar;59(3):379–384. doi: 10.1111/j.1751-1097.1994.tb05051.x. [DOI] [PubMed] [Google Scholar]
- Fluhr Robert, Moses Phyllis, Morelli Giorgio, Coruzzi Gloria, Chua Nam-Hai. Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J. 1986 Sep;5(9):2063–2071. doi: 10.1002/j.1460-2075.1986.tb04467.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hershey H. P., Barker R. F., Idler K. B., Lissemore J. L., Quail P. H. Analysis of cloned cDNA and genomic sequences for phytochrome: complete amino acid sequences for two gene products expressed in etiolated Avena. Nucleic Acids Res. 1985 Dec 9;13(23):8543–8559. doi: 10.1093/nar/13.23.8543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang J., Nasr M., Kim Y., Matthews H. R. Genistein inhibits protein histidine kinase. J Biol Chem. 1992 Aug 5;267(22):15511–15515. [PubMed] [Google Scholar]
- Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kay S. A., Keith B., Shinozaki K., Chua N. H. The sequence of the rice phytochrome gene. Nucleic Acids Res. 1989 Apr 11;17(7):2865–2866. doi: 10.1093/nar/17.7.2865. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lam E., Chua N. H. GT-1 binding site confers light responsive expression in transgenic tobacco. Science. 1990 Apr 27;248(4954):471–474. doi: 10.1126/science.2330508. [DOI] [PubMed] [Google Scholar]
- Leu W. M., Cao X. L., Wilson T. J., Snustad D. P., Chua N. H. Phytochrome A and phytochrome B mediate the hypocotyl-specific downregulation of TUB1 by light in arabidopsis. Plant Cell. 1995 Dec;7(12):2187–2196. doi: 10.1105/tpc.7.12.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lissemore J. L., Quail P. H. Rapid transcriptional regulation by phytochrome of the genes for phytochrome and chlorophyll a/b-binding protein in Avena sativa. Mol Cell Biol. 1988 Nov;8(11):4840–4850. doi: 10.1128/mcb.8.11.4840. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Massom L., Lee H., Jarrett H. W. Trifluoperazine binding to porcine brain calmodulin and skeletal muscle troponin C. Biochemistry. 1990 Jan 23;29(3):671–681. doi: 10.1021/bi00455a012. [DOI] [PubMed] [Google Scholar]
- Millar A. J., McGrath R. B., Chua N. H. Phytochrome phototransduction pathways. Annu Rev Genet. 1994;28:325–349. doi: 10.1146/annurev.ge.28.120194.001545. [DOI] [PubMed] [Google Scholar]
- Mösinger E., Batschauer A., Schäfer E., Apel K. Phytochrome control of in vitro transcription of specific genes in isolated nuclei from barley (Hordeum vulgare). Eur J Biochem. 1985 Feb 15;147(1):137–142. doi: 10.1111/j.1432-1033.1985.tb08729.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Neuhaus G., Neuhaus-Url G., Katagiri F., Seipel K., Chua N. H. Tissue-Specific Expression of as-1 in Transgenic Tobacco. Plant Cell. 1994 Jun;6(6):827–834. doi: 10.1105/tpc.6.6.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quail P. H., Boylan M. T., Parks B. M., Short T. W., Xu Y., Wagner D. Phytochromes: photosensory perception and signal transduction. Science. 1995 May 5;268(5211):675–680. doi: 10.1126/science.7732376. [DOI] [PubMed] [Google Scholar]
- Reed J. W., Nagatani A., Elich T. D., Fagan M., Chory J. Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development. Plant Physiol. 1994 Apr;104(4):1139–1149. doi: 10.1104/pp.104.4.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnorf M., Potrykus I., Neuhaus G. Microinjection technique: routine system for characterization of microcapillaries by bubble pressure measurement. Exp Cell Res. 1994 Feb;210(2):260–267. doi: 10.1006/excr.1994.1038. [DOI] [PubMed] [Google Scholar]
- Sharma R., López-Juez E., Nagatani A., Furuya M. Identification of photo-inactive phytochrome A in etiolated seedlings and photo-active phytochrome B in green leaves of the aurea mutant of tomato. Plant J. 1993 Dec;4(6):1035–1042. doi: 10.1046/j.1365-313x.1993.04061035.x. [DOI] [PubMed] [Google Scholar]
- Sharrock R. A., Quail P. H. Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Dev. 1989 Nov;3(11):1745–1757. doi: 10.1101/gad.3.11.1745. [DOI] [PubMed] [Google Scholar]
- Tonoike H., Han I. S., Jongewaard I., Doyle M., Guiltinan M., Fosket D. E. Hypocotyl expression and light downregulation of the soybean tubulin gene, tubB1. Plant J. 1994 Mar;5(3):343–351. doi: 10.1111/j.1365-313x.1994.00343.x. [DOI] [PubMed] [Google Scholar]
- Tsai F. Y., Coruzzi G. M. Dark-induced and organ-specific expression of two asparagine synthetase genes in Pisum sativum. EMBO J. 1990 Feb;9(2):323–332. doi: 10.1002/j.1460-2075.1990.tb08114.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsai F. Y., Coruzzi G. Light represses transcription of asparagine synthetase genes in photosynthetic and nonphotosynthetic organs of plants. Mol Cell Biol. 1991 Oct;11(10):4966–4972. doi: 10.1128/mcb.11.10.4966. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Von Arnim Albrecht, Deng Xing-Wang. LIGHT CONTROL OF SEEDLING DEVELOPMENT. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):215–243. doi: 10.1146/annurev.arplant.47.1.215. [DOI] [PubMed] [Google Scholar]
- 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]
- van Tuinen A., Kerckhoffs L. H., Nagatani A., Kendrick R. E., Koornneef M. Far-red light-insensitive, phytochrome A-deficient mutants of tomato. Mol Gen Genet. 1995 Jan 20;246(2):133–141. doi: 10.1007/BF00294675. [DOI] [PubMed] [Google Scholar]