Abstract
The glnA gene, encoding type I glutamine synthetase (GS) in Synechocystis sp. PCC 6803, showed a high sequence similarity with other cyanobacterial glnA genes. A dramatic decrease in the amount of glnA mRNA, a single transcript of about 1.6 kb, was observed after transfer to darkness, or after incubation with the electron transport inhibitors DCMU or DBMIB. The levels of glnA transcript were fully recovered after 5 min of reillumination. The glnA mRNA was found to be equally stable both in the light and the dark (half-life about 2.5 min). Unlike the glnA messenger, the amount of GS protein was not reduced in the dark. Synthesis of the glnA transcript in the dark required the presence of glucose. In addition, glnA transcription in a Synechocystis psbE-psbF mutant lacking photosystem II required the presence of glucose even when grown in the light. These observations indicate that glnA transcription is under the control of the redox state of the cell. Finally, nitrogen starvation provoked a delay in the decrease of glnA transcript in darkness, suggesting a connection between nitrogen and redox controls of glnA transcript levels.
Similar content being viewed by others
References
Allen MM, Smith AJ: Nitrogen chlorosis in blue-green algae. Arch Microbiol 69: 114–120 (1969).
Aoki M, Katoh S: Size of the plastoquinone pool functioning in photosynthetic and respiratory electron transport of Synechococcus sp. Plant Cell Physiol 24: 1379–1386 (1983).
Cambell D, Houmard J, Tandeau de Marsac N: Electron transport regulates cellular differentiation in the filamentous cyanobacterium Calothrix. Plant Cell 5: 451–463 (1993).
Cohen-Kupiec R, Gurevitz M, Zilberstein A: Expression of glnA in the cyanobacterium Synechococcus sp. strain PCC 7942 is initiated from a single nif like promoter under various nitrogen conditions. J Bact 175: 7727–7731 (1993).
Cullimore JV, Gebhardt C, Saarelainen R, Miflin BJ, Idler KB, Barker RF: Glutamine synthetase of Phaseolus vulgaris: organ specific expression of a multigene family. J Mol Appl Genet 2: 589–599 (1987).
Chastain CJ, Brusca JS, Ramasubramanian TS, Wei T-F, Golden JW: A sequence specific DNA-binding factor (VF1) from Anabaena sp. strain PCC 7120 vegetative cells binds to three adjacent sites in the xisA upstream region. J Bact 172: 5044–5051 (1990).
Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).
Edwards JW, Coruzzi GM: Photorespiration and light act in concert to regulate the expression of the nuclear gene for chloroplast glutamine synthetase. Plant Cell 1: 241–248 (1989).
Elmorjani K, Liotenberg S, Houmard J, Tandeau du Marsac N: Molecular characterization of the gene encoding glutamine synthetase in the cyanobacterium Calothrix sp. PCC 7601. Biochem Biophys Res Comm 189: 1296–1302 (1992).
Flores E, Schmetterer G: Interaction of fructose with the glucose permease of the cyanobacterium Synechocystis sp. PCC 6803. J Bact 166: 693–696 (1984).
Forchhammer K, Tandeau de Marsac N: The PII protein in the cyanobacterium Synechococcus sp. strain 7942 is modified by serine phosphorylation and signals the cellular N-status. J Bact 176: 84–91 (1994).
Fork DC, Herbert SK: Electron transport and photophosphorylation by photosystem I in vivo in plants and cyanobacteria. Photosynth Res 36: 149–168 (1993).
Guerrero MG, Lara L: Assimilation of inorganic nitrogen. In: Fay P, VanBaalen C (eds) The Cyanobacteria, pp. 163–186. Elsevier Science Publishers, Amsterdam (1987).
Harrison MA, Keen JN, Findlay JBC, Allen JF: Modification of a glnB-like gene product by photosynthetic electron transport in the cyanobacterium Synechococcus 6301. FEBS Lett 264: 25–28 (1990).
Hirano M, Satoh K, Katoh S: Plastoquinone as a common link between photosynthesis and respiration in a blue-green alga. Photosynth Res 1: 149–162 (1980).
Jansson C, Debus R, Osiewacz HD, Gurevitz M, McIntosh L: Construction of an obligate photoheterotrophic mutant of the cyanobacterium Synechocystis 6803. Plant Physiol 85: 1021–1025 (1987).
Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685 (1970).
Lehmann M, Wöber G: Accumulation, mobilization and turnover of glycogen in the blue-green bacterium Anacystis nidulans. Arch Microbiol 111: 93–97 (1976).
Luque I, Flores E, Herreros A: Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13: 2862–2869 (1994).
Magasanik B, Neidhardt FC: Regulation of carbon and nitrogen utilization. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 1318–1325. American Society for Microbiology, Washington, DC (1987).
Marqués S, Mérida A, Candau P, Florencio FJ: Light-mediated regulation of glutamine synthetase activity in the unicellular cyanobacterium Synechococcus sp. PCC 6301. Planta 187: 247–253 (1992).
Meeks JC, Wolk CP, Lockau W, Schilling N, Shaffer PW, Chien WS: Pathways of assimilation of [13N]N2 and 13NH4 + by cyanobacteria with and without heterocysts. J Bact 134: 125–130 (1978).
Mérida A, Flores E, Florencio FJ: Regulation of Anabaena sp. PCC strain 7120 glutamine synthetase activity in a Synechocystis sp. strain PCC 6803 derivative strain bearing the Anabaena glnA gene and a mutated host glnA gene. J Bact 174: 650–654 (1992).
Mérida A, Leurentop L, Candau P, Florencio FJ: Purification and properties of glutamine synthetase from the cyanobacteria Synechocystis sp. strain PCC 6803 and Calothrix sp. strain PCC 7601. J Bact 172: 4732–4735 (1990).
Mohamed A, Eriksson J, Osiewacz HD, Jansson C: Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238: 161–168 (1993).
Mohamed A, Jansson C: Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 13: 693–700 (1989).
Mohamed A, Jansson C: Photosynthetic electron transport controls degradation but not production of psbA transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 16: 891–897 (1991).
Muro-Pastor MI, Florencio FJ: Purification and properties of NADP-isocitrate dehydrogenase from the unicellular cyanobacterium Synechocystis sp. PCC 6803. Eur J Biochem 203: 99–105 (1992).
Pahel G, Rothstein DM, Magasanik B: Complex glnA-glnL-glnG operon of Escherichia coli. J Bact 268: 469–475 (1982).
Pakrasi HB, Williams JGK, Arntzen CJ: Targeted mutagenesis of the psbE and psbF genes blocks photosynthetic electron transport: evidence for a functional role of cytochrome b559 in photosystem II. EMBO J 7: 325–332 (1988).
Peschek GA: Respiratory electron transport. In: Fay P, VanBaalen C (eds) The Cyanobacteria, pp. 119–161. Elsevier Science Publisher, Amsterdam (1987).
Peterman TK, Goodman HM: The glutamine synthetase gene family of Arabidopsis thaliana: light-regulation and differential expression in leaves, roots and seeds. Mol Gen Genet 230: 145–154 (1991).
Reyes JC, Florencio FJ: A new type of glutamine synthetase in cyanobacteria: the protein encoded by the glnN gene supports nitrogen assimilation in Synechocystis sp. PCC 6803. J Bact 176: 1260–1267 (1994).
Rich PR, Madgwick SA, Moss DA: The interactions of duroquinol, DBMIB and NQNO with the chloroplast cytochrome bf complex. Biochim Biophys Acta 108: 1188–1195 (1991).
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY: Genetics assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1–61 (1979).
Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).
Smart LB, Bowlby NB Anderson SL, Sithole I, McIntosh L: Genetic manipulation of the cyanobacterium Synechocystis sp. PCC 6803. Development of strains lacking photosystem I for the analysis of mutations in photosystem II. Plant Physiol 104: 349–354 (1994).
Smart LB, McIntosh L: Expression of photosynthesis genes in the cyanobacterium Synechocystis sp. PCC 6803: psaA-psaB and psbA transcripts accumulate in dark-grown cells. Plant Mol Biol 17: 959–971 (1991).
Smith AJ: Modes of cyanobacterial carbon metabolism. In: Carr NG, Whitton BA (eds) The Biology of Cyanobacteria, pp. 47–85. Blackwell Scientific Publications, Oxford (1982).
Stewart GR, Mann AF, Fentem PA: Enzymes of glutamate formation: glutamate dehydrogenase, glutamine synthetase and glutamate syntase. In: Stumpf K, Conn EE (eds) The Biology of Plants, vol. 5, pp. 217–237. Academic Press, New York (1980).
Tingey SV, Walker EL, Coruzzi GM: Glutamine synthetase genes of pea encode distinct polypeptides which are differentially expressed in leaves, root and nodules. EMBO J 6: 1–9 (1987).
Trebst A: Inhibitors in the electron flow. Meth Enzymol 69: 675–715 (1980).
Tsinoremas NF, Castets AM, Harrison MA, Allen JF, Tandeau de Marsac N: Photosynthetic electron transport controls nitrogen assimilation in cyanobacteria by means of posttranslational modification of the glnB gene product. Proc Natl Acad Sci USA 88: 4565–4569 (1991).
Tumer NE, Robinson SJ, Haselkorn R: Different promoters for the Anabaena glutamine synthetase gene during growth using molecular or fixed nitrogen. Nature 306: 337–342 (1983).
Vega-Palas MA, Herrero A, Flores E: NtcA, a global nitrogen regulator from the cyanobacterium Synechococcus that belongs to the Crp family of bacterial regulators. Mol Microbiol 6: 1853–1859 (1992).
Vega-Palas MA, Madueño F, Herrero A, Flores E: Identification and cloning of a regulatory gene for nitrogen assimilation in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bact 172: 643–647 (1990).
Vioque A: Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria. Nucl Acids Res 20: 6331–6337 (1992).
Wagner SJ, Thomas SP, Kaufman RI, Nixon BT, StevensJr SE: The glnA gene of the cyanobacterium Agmenellum quadruplicatum PR-6 is nonessential for ammonium assimilation. J Bact 175: 604–612 (1993).
Wei T-F, Ramasubramanian TS, Pu F, Golden JW: Anabaena sp. strain PCC 7120 bifA gene encoding a sequence-specific DNA-binding protein cloned by in vivo transcriptional interference selection. J Bact 175: 4025–4035 (1993).
Willians JGK: Construction of specific mutations in Photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Meth Enzymol 167: 766–778 (1988).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Reyes, J.C., Florencio, F.J. Electron transport controls transcription of the glutamine synthetase gene (glnA) from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 27, 789–799 (1995). https://doi.org/10.1007/BF00020231
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00020231