Abstract
Glutamine synthetase (GS) activity increased over three-fold in developing primary leaves of Phaseolus vulgaris L. This increase was shown to be the result of differential expression of three members of the GS gene family: gln-α and gln-β, which encode cytosolic GS polypeptides, and gln-δ, which encodes the chloroplast-located GS. The gln-δ gene was the most highly expressed GS gene and was regulated in a complex manner with two different transcripts accumulating differentially during leaf development. This gene was expressed weakly in the dark and was induced strongly by lingt; this induction was shown not to be an indirect effect of photorespiration. In the long term, gln-δ showed increased expression in photorespiring compared with non-photorespiring leaves. However, in the short term, there was no induction of gln-δ following transfer of plants to photorespiratory conditions. These results suggest that regulation of gln-δ by photorespiration was the result of indirect, long-term effects on cellular metabolism. In general, in all these experiments, analysis of cytosolic versus chloroplastic GS polypeptides and of the GS isoenzyme profiles showed the same pattern of changes in abundance as that observed for the mRNAs suggesting that regulation of GS gene expression occurred primarily at the mRNA level. However, it was noteworthy that the δ isoenzyme remained at a high abundance in older leaves, grown in both light and dark, despite a decrease in abundance of gln-δ mRNA.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Apel, K: Phytochrome induced appearance of mRNA activity for the apoprotein of the light-harvesting chlorophyll a/b-protein of barley (Hordeum vulgare). Eur J Biochem 97: 183–188 (1979).
Axelos, M, Bardet, C, Liboz, T, Le Van, Thai, A, Curie, C, Lescure, B: The gene family encoding the Arabidopsis thaliana translation elongation factor EF-1α: molecular cloning, characterzation and expression. Mol Gen Genet 219: 106–112 (1989).
Bennett, MJ, Cullimore, JV: Glutamine synthetase isoenzymes of Phaseolus vulgaris L.: subunit composition in developing root nodules and plumules. Planta 179: 433–440 (1989).
Bennett, MJ, Lightfoot, DA, Cullimore, JV: cDNA sequence and differential expression of gene encoding the glutamine synthetase γ polypeptide of Phaseolus vulgaris L. Plant Mol Biol 12: 553–565 (1989).
Blackwell, RD, Murray, AJS, Lea, PJ: Inhibition of photosynthesis in barley with decreased levels of chloroplastic glutamine synthetase activity. J Exp Bot 38: 1799–1809 (1987).
Bradbeer, JW: The synthesis of chloroplast enzymes. In: Milborrow, BV (ed) Biosynthesis and its Control in Plants; pp. 279–302. Academic Press, London (1973).
Bradbeer, JW, Ireland, HMM, Smith, JW, Rest, J, Edge, HJW: Plastid development in primary leaves of Phaseolus vulgaris. New Phytol 73: 263–270 (1974).
Bradford, MM: A rapid and sensitive method for the determination of μg quantities of protein using the principle of protein-dye binding. Analyt Biochem 72: 248–254 (1976).
Chaillou, S, Morot-Gaudry, J-F, Lesaint, C, Salsac, L, Jolivet, E: Nitrate or ammonium nutrition in french bean. Plant Soil 91: 363–365 (1986).
Chen, F-L, Cullimore, JV: Two isoenzymes of NADH-dependent g glutamate synthase in root nodules of Phaseolus vulgaris L. Plant Physiol 88: 1411–1417 (1988).
Cock, JM, Mould, RM, Bennett, MJ, Cullimore, JV: Expression of glutamine synthetase genes in roots and nodules of Phaseolus vulgaris following changes in the ammonium supply and infection with various Rhizobium mutants. Plant Mol Biol 14: 549–560 (1990).
Cullimore, JV, Sims, AP: An association between photorespiration and protein catabolism: studies with Chlamydomonas. Planta 150: 392–396 (1980).
Cullimore, JV, Bennettt, MJ: The molecular biology of plant glutamine synthetase from root nodules of Phaseolus vulgaris L. and other legumes. J Plant Physiol 132: 387–393 (1988).
Cumming, AC, Bennett, J: Biosynthesis of the lightharvesting chlorophyll a/b protein: control of mRNA activity by light. Eur J Biochem 118: 71–80 (1981).
Dale, JE: Leaf growth in Phaseolus vulgaris. Ann Bot 28: 579–589 (1964).
Edwards, K, Cramer, CL, Bolwell, GP, Dixon, RA, Schuch, W, Lamb, CJ: Rapid transient induction of phenylalanine ammonia-lyase mRNA in elicitor-treated bean cells. Proc Natl Acad Sci USA 82: 6731–6735 (1985).
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).
Edwards, JW, Walker, EL, Coruzzi, GM: Cell-specific expression in transgenic plants reveals non-overlapping roles for chloroplast and cytosolic glutamine synthetase. Proc Natl Acad Sci USA 87: 3459–3463 (1990).
Forde, BG, Cullimore, JV: Molecular biology of glutamine synthetase. Oxford Surv Plant Mol Cell Biol 6: 247–296 (1989).
Forde, BG, Day, HM, Turton, JF, Shen, W-J, Cullimore, JV, Oliver, JE: Two glutamine synthetase genes from Phaseolus vulgaris L. display contrasting developmental and spatial patterns of expression in transgenic Lotus corniculatus plants. Plant Cell 1: 391–401 (1989).
Freeman, J, Marquez, AJ, Wallsgrove, RM, Saarelainen, R, Forde, BG: Molecular analysis of barley mutants deficient in chloroplast glutamine synthetase. Plant Mol Biol 14: 297–311 (1990).
Gebhardt, C, Oliver, JE, Forde, BG, Saarelainen, R, Miflin, BJ: Primary structure and differential expression of glutamine synthetase genes in nodules, roots and leaves of Phaseolus vulgaris. EMBO J 5: 1429–1435 (1986).
Givan, CV, Joy, KW, Kleczkowski, LA: A decade of photorespiratory nitrogen cycling. TIBS 13: 433–437 (1988).
Kreig, PA, Melton, DA: In vitro synthesis with SP6 RNA polymerase. Meth Enzymol 155: 397–415 (1987).
Lea, PJ, Joy, KW: Amino acid interconversion in germinating seeds. In: Nozzolillo, C, Lea, PJ, Loewus, FA (eds) Mobilization of Reserves in Germination, pp. 77–109. Plenum Press, New York/London (1983).
Leech RM, Baker NR: The development of photosynthetic capacity in leaves. In: The Growth and Functioning of Leaves, pp. 271–301 (1983).
Lightfoot, DA, Green, NK, Cullimore, JV: The chloroplastlocated glutamine synthetase of Phaseolus vulgaris L.: nucleotide sequence, expression in different organs and uptake into isolated chloroplasts. Plant Mol Biol 11: 191–202 (1988).
McNally, SF, Hirel, B, Gadal, P, Mann, AF, Stewart, GR: Glutamine synthetases of higher plants. Plant Physiol 72: 22–25 (1983).
Miflin, BJ, Lea, PJ: Ammonia assimilation. In: Miflin, BJ (ed) The Biochemistry of Plants, pp. 169–202. Academic Press, New York (1980).
Noel, KD, Sanchez, A, Fernandez, L, Leemans, J, Cevallos, MA: Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. J Bact 158: 148–155 (1984).
Ortega, JL, Campos, F, Sanchez, F, Lara, M: Expression of two different glutamine synthetase polypeptides during root development in Phaseolus vulgaris L. Plant Physiol 80: 1051–1054 (1986).
Padilla, JE, Campos, F, Conde, V, Lara, M, Sanchez, F: Nodule-specific glutamine synthetase is expressed before the onset of nitrogen fixation in Phaseolus vulgaris L. Plant Mol Biol 9: 65–74 (1987).
Sato, N: Nucleotide sequence and expression of the phytochrome gene in Pisum satuvim: Differential regulation by light of multiple transcripts. Plant Mol Biol 11: 697–710 (1988).
Swarup, R, Bennett, MJ, Cullimore, JV: Expression of glutamine synthetase genes in cotyledons of germinating Phaseolus vulgaris L. Planta 183: 51–56 (1990).
Tingey, SV, Tsai, F-Y, Edwards, JW, Walker, EL, Coruzzi, GM: Chloroplast and cytosolic glutamine synthetase are encoded by homologous nuclear genes which are differentially expressed in vivo. J Biol Chem 263: 9651–9657 (1988).
Tomizawa, K-I, Sato, N, Furuya, M: Phytochrome control of multiple transcripts of the phytochrome gene in Pisum sativum. Plant Mol Biol 12: 295–299 (1989).
van, Tunen, AJ, Hartman, SA, Mur, LA, Mol, JNM: Regulation of chalcone flavanone isomerase (CHI) gene expression in Petunia hybrida: the use of alternative promoters in corolla, anthers and pollen. Plant Mol Biol 12: 539–551 (1989).
Verbelen, JP, De, Greef, LA: Leaf development of Phaseolus vulgaris L. in light and in darkness. Am J Bot 66: 970–976 (1979).
Wallsgrove, RM, Turner, JC, Hall, NP, Kendall, AC, Bright, SWJ: Barley mutants lacking chloroplastic glutamine synthetase-biochemical and genetic analysis. Plant Physiol 83: 155–158 (1987).
Wilson, GL, Ludlow, MM: Bean leaf expansion in relation to temperature. J Exp Bot 19: 309–321 (1968).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cock, J.M., Brock, I.W., Watson, A.T. et al. Regulation of glutamine synthetase genes in leaves of Phaseolus vulgaris . Plant Mol Biol 17, 761–771 (1991). https://doi.org/10.1007/BF00037059
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00037059