Skip to main content
NCBI home page
The Plant Cell logoLink to The Plant Cell
. 1989 Feb;1(2):241–248. doi: 10.1105/tpc.1.2.241

Photorespiration and light act in concert to regulate the expression of the nuclear gene for chloroplast glutamine synthetase.

J W Edwards 1, G M Coruzzi 1
PMCID: PMC159756  PMID: 2577725

Abstract

In Pisum sativum, distinct chloroplast and cytosolic forms of glutamine synthetase (GS) are encoded by homologous nuclear genes that are differentially expressed in vivo (Tingey, S. V., Tsai, F.-Y., Edwards, J. W., Walker, E. L., and Coruzzi, G. M. [1988]. J. Biol. Chem. 263, 9651-9657). In leaves, light selectively affects the expression of the nuclear gene for chloroplast GS2. Differences in the maximal levels of GS2 mRNA in etiolated plants treated with red or white light indicate that only part of the white-light-induced accumulation of GS2 mRNA is due to a phytochrome-mediated response. The kinetics of GS2 mRNA accumulation in response to white-light illumination of etiolated or dark-adapted green plants indicates that GS2 mRNA accumulates more rapidly in plants containing mature, photosynthetically competent chloroplasts. Other evidence that GS2 mRNA levels are affected by the metabolic status of chloroplasts concerns the selective induction of GS2 mRNA in plants grown under conditions that result in the production of photorespiratory ammonia. These results indicate that the light-induced accumulation of GS2 mRNA in leaves results from the action of phytochrome as well as light-induced changes in chloroplast metabolism.

Full Text

The Full Text of this article is available as a PDF (2.1 MB).

Selected References

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

  1. Back E., Burkhart W., Moyer M., Privalle L., Rothstein S. Isolation of cDNA clones coding for spinach nitrite reductase: complete sequence and nitrate induction. Mol Gen Genet. 1988 Apr;212(1):20–26. doi: 10.1007/BF00322440. [DOI] [PubMed] [Google Scholar]
  2. Baim S. B., Sherman F. mRNA structures influencing translation in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1988 Apr;8(4):1591–1601. doi: 10.1128/mcb.8.4.1591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blake M. S., Johnston K. H., Russell-Jones G. J., Gotschlich E. C. A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal Biochem. 1984 Jan;136(1):175–179. doi: 10.1016/0003-2697(84)90320-8. [DOI] [PubMed] [Google Scholar]
  5. Carmichael G. G., McMaster G. K. The analysis of nucleic acids in gels using glyoxal and acridine orange. Methods Enzymol. 1980;65(1):380–391. doi: 10.1016/s0076-6879(80)65049-6. [DOI] [PubMed] [Google Scholar]
  6. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  7. Crawford N. M., Campbell W. H., Davis R. W. Nitrate reductase from squash: cDNA cloning and nitrate regulation. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8073–8076. doi: 10.1073/pnas.83.21.8073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  9. Donahue T. F., Daves R. S., Lucchini G., Fink G. R. A short nucleotide sequence required for regulation of HIS4 by the general control system of yeast. Cell. 1983 Jan;32(1):89–98. doi: 10.1016/0092-8674(83)90499-3. [DOI] [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  11. Fluhr R., Chua N. H. Developmental regulation of two genes encoding ribulose-bisphosphate carboxylase small subunit in pea and transgenic petunia plants: Phytochrome response and blue-light induction. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2358–2362. doi: 10.1073/pnas.83.8.2358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gebhardt C., Oliver J. E., Forde B. G., Saarelainen R., Miflin B. J. Primary structure and differential expression of glutamine synthetase genes in nodules, roots and leaves of Phaseolus vulgaris. EMBO J. 1986 Jul;5(7):1429–1435. doi: 10.1002/j.1460-2075.1986.tb04379.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hayward B. E., Hussain A., Wilson R. H., Lyons A., Woodcock V., McIntosh B., Harris T. J. The cloning and nucleotide sequence of cDNA for an amplified glutamine synthetase gene from the Chinese hamster. Nucleic Acids Res. 1986 Jan 24;14(2):999–1008. doi: 10.1093/nar/14.2.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hirel B., Bouet C., King B., Layzell D., Jacobs F., Verma D. P. Glutamine synthetase genes are regulated by ammonia provided externally or by symbiotic nitrogen fixation. EMBO J. 1987 May;6(5):1167–1171. doi: 10.1002/j.1460-2075.1987.tb02350.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hirel B., Weatherley C., Cretin C., Bergounioux C., Gadal P. Multiple Subunit Composition of Chloroplastic Glutamine Synthetase of Nicotiana tabacum L. Plant Physiol. 1984 Feb;74(2):448–450. doi: 10.1104/pp.74.2.448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hope I. A., Struhl K. GCN4 protein, synthesized in vitro, binds HIS3 regulatory sequences: implications for general control of amino acid biosynthetic genes in yeast. Cell. 1985 Nov;43(1):177–188. doi: 10.1016/0092-8674(85)90022-4. [DOI] [PubMed] [Google Scholar]
  17. Kaufman L. S., Roberts L. L., Briggs W. R., Thompson W. F. Phytochrome Control of Specific mRNA levels in Developing Pea Buds : Kinetics of Accumulation, Reciprocity, and Escape Kinetics of the Low Fluence Response. Plant Physiol. 1986 Aug;81(4):1033–1038. doi: 10.1104/pp.81.4.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Lara M., Porta H., Padilla J., Folch J., Sánchez F. Heterogeneity of Glutamine Synthetase Polypeptides in Phaseolus vulgaris L. Plant Physiol. 1984 Dec;76(4):1019–1023. doi: 10.1104/pp.76.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miflin B. J. The location of nitrite reductase and other enzymes related to amino Acid biosynthesis in the plastids of root and leaves. Plant Physiol. 1974 Oct;54(4):550–555. doi: 10.1104/pp.54.4.550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Penn M. D., Galgoci B., Greer H. Identification of AAS genes and their regulatory role in general control of amino acid biosynthesis in yeast. Proc Natl Acad Sci U S A. 1983 May;80(9):2704–2708. doi: 10.1073/pnas.80.9.2704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sanders P. G., Wilson R. H. Amplification and cloning of the Chinese hamster glutamine synthetase gene. EMBO J. 1984 Jan;3(1):65–71. doi: 10.1002/j.1460-2075.1984.tb01762.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Silverman S. J., Rose M., Botstein D., Fink G. R. Regulation of HIS4-lacZ fusions in Saccharomyces cerevisiae. Mol Cell Biol. 1982 Oct;2(10):1212–1219. doi: 10.1128/mcb.2.10.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Smith D. D., Jr, Campbell J. W. Subcellular location of chicken brain glutamine synthetase and comparison with chicken liver mitochondrial glutamine synthetase. J Biol Chem. 1983 Oct 25;258(20):12265–12268. [PubMed] [Google Scholar]
  25. Struhl K. The DNA-binding domains of the jun oncoprotein and the yeast GCN4 transcriptional activator protein are functionally homologous. Cell. 1987 Sep 11;50(6):841–846. doi: 10.1016/0092-8674(87)90511-3. [DOI] [PubMed] [Google Scholar]
  26. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tingey S. V., Coruzzi G. M. Glutamine Synthetase of Nicotiana plumbaginifolia: Cloning and in Vivo Expression. Plant Physiol. 1987 Jun;84(2):366–373. doi: 10.1104/pp.84.2.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tingey S. V., Tsai F. Y., Edwards J. W., Walker E. L., Coruzzi G. M. Chloroplast and cytosolic glutamine synthetase are encoded by homologous nuclear genes which are differentially expressed in vivo. J Biol Chem. 1988 Jul 15;263(20):9651–9657. [PubMed] [Google Scholar]
  29. Vogt P. K., Bos T. J., Doolittle R. F. Homology between the DNA-binding domain of the GCN4 regulatory protein of yeast and the carboxyl-terminal region of a protein coded for by the oncogene jun. Proc Natl Acad Sci U S A. 1987 May;84(10):3316–3319. doi: 10.1073/pnas.84.10.3316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wallsgrove R. M., Turner J. C., Hall N. P., Kendall A. C., Bright S. W. Barley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis. Plant Physiol. 1987 Jan;83(1):155–158. doi: 10.1104/pp.83.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zalkin H., Yanofsky C. Yeast gene TRP5: structure, function, regulation. J Biol Chem. 1982 Feb 10;257(3):1491–1500. [PubMed] [Google Scholar]

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

RESOURCES