1. bookVolume 55 (2006): Issue 1-6 (December 2006)
Journal Details
First Published
22 Feb 2016
Publication timeframe
1 time per year
access type Open Access

The Overexpression of Glutamine Synthetase in Transgenic Poplar: A Review

Published Online: 19 Oct 2017
Volume & Issue: Volume 55 (2006) - Issue 1-6 (December 2006)
Page range: 278 - 284
Received: 22 Sep 2006
Accepted: 30 Oct 2006
Journal Details
First Published
22 Feb 2016
Publication timeframe
1 time per year

In investigating the pivotal role of glutamine synthetase in woody plant development, we have strived to develop an understanding of the biochemical and physiological mechanisms whereby enhanced expression of glutamine synthetase (GS) in poplar contributes to vegetative growth through enhanced nitrogen use efficiency. Considerable effort has also centered on characterization of enhanced resistance of transgenic GS overexpressor lines to abiotic stresses and proposed mechanisms. This summary of our work also focuses on future applications in forest tree improvement.


ANDERSON, J. M., Y. I. PARK and W. S. CHOW (1997): Photoinactivation and photoprotection of photosystem II in nature. Physiologia Plantarum 100: 214-233.10.1111/j.1399-3054.1997.tb04777.xOpen DOISearch in Google Scholar

ÁVILA, C., M. F. SUÁREZ, J. GÓMEZ-MALDONADO and F. M. CÁNOVAS (2001): Spatial and temporal expression of two cytosolic glutamine synthetase genes in Scots pine: functional implications on nitrogen metabolism during early stages of conifer development. The Plant Journal 25: 93-102.10.1046/j.1365-313x.2001.00938.xOpen DOISearch in Google Scholar

BARKER, D. H. and W. W. ADAMS (1997): The xanthophyll cycle and energy dissipation in differently oriented faces of the cactus Opuntia macrorhiza. Oecologia 109: 353-361.10.1007/s004420050093Search in Google Scholar

BAUER, D., K. BIEHLER, H. FOCK, E. CARRAYOL, B. HIREL, A. MIGGE and T.W. BECKER (1997): A role for cytosolic glutamine synthetase in the remobilization of leaf nitrogen during water stress in tomato. Physiologia Plantarum 99: 241-248.10.1111/j.1399-3054.1997.tb05408.xSearch in Google Scholar

BOHLMANN, J., T. LINS, W. MARTIN and U. EILERT (1996): Anthranilate synthase from Ruta graveolens: duplicated ASα genes encode tryptophan-sensitive and tryptophaninsensitive isoenzymes specific to amino acid and alkaloid biosynthesis. Plant Physiology 111: 507-514.10.1104/pp.111.2.507Search in Google Scholar

BRUGIÈRE, N., F. DUBOIS, C. MASCLAUX, R. S. SANGWAN and B. HIREL (2000): Immunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tabacum L.) leaves suggests that ammonia assimilation is progressively shifted to the mesophyll cytosol. Planta 211: 519-527.10.1007/s004250000309Search in Google Scholar

CARVALHO, H., S. PEREIRA, C. SUNKEL and R. SALEMA (1992): Detection of cytosolic glutamine synthetase in leaves of Nicotiana tabacum L. by immunocytochemical methods. Plant Physiology 100: 1591-1594.10.1104/pp.100.3.1591Open DOISearch in Google Scholar

CHO, H. J., J. E. BROTHERTON, H. S. SONG and J. M. WIDHOLM (2000): Increasing tryptophan synthesis in a forage legume Astragalus sinicus by expressing the tobacco feedback-insensitive anthranilate synthase (ASA2) gene. Plant Physiology 123: 1069-1076.10.1104/pp.123.3.1069Search in Google Scholar

CORUZZI, G. and L. ZHOU (2001): Carbon and nitrogen sensing and signaling in plants: emerging “matrix effects”. Current Opinion in Plant Biology 4: 247-253.10.1016/S1369-5266(00)00168-0Open DOISearch in Google Scholar

CRAWFORD, I. P. (1989): Evolution of a biosynthetic pathway: the tryptophan paradigm. Annual Review of Microbiology 43: 567-600.10.1146/annurev.mi.43.100189.0030312679363Open DOISearch in Google Scholar

CROZIER, A., Y. KAMIYA, G. BISHOP and T. YOKOTA (2000): Biosynthesis of hormones and elicitor molecules, pp. 888-896 in Biochemistry & Molecular Biology of Plants, edited by B. B. BUCHANAN, E. GRUISSEM and R. L. JONES, Courier Companies, Inc., USA.Search in Google Scholar

DE LA TORRE, F., A. GARCÍA-GUTIÉRREZ, C. CRESPILLO, F. R. CANTÓN, C. AVILA and F. M. CÁNOVAS (2002): Functional expression of two pine glutamine synthetase genes in bacteria reveals that they encode cytosolic isoenzymes with different molecular and catalytic properties. Plant and Cell Physiology 43: 802-809.10.1093/pcp/pcf094Open DOISearch in Google Scholar

EL-KHATIB, R. T., E. HAMERLYNCK, F. GALLARDO and E. G. KIRBY (2004): Transgenic poplar characterized by ectopic expression of a pine cytosolic glutamine synthetase gene exhibits enhanced tolerance to water stress. Tree Physiology 24: 729-736.10.1093/treephys/24.7.729Open DOISearch in Google Scholar

FOYER, C. H. and C. BOWSHER (2004): Plant carbon-nitrogen interactions from rhizosphere to planet. Journal of Experimental Botany 55: 394.Search in Google Scholar

FU, J., R. SAMPALO, F. GALLARDO, F. M. CÁNOVAS and E. G. KIRBY (2003): Assembly of a cytosolic pine glutamine synthetase holoenzyme in leaves of transgenic poplar leads to enhanced vegetative growth in young plants. Plant, Cell and Environment 26: 411-418.10.1046/j.1365-3040.2003.00972.xOpen DOISearch in Google Scholar

FUENTES, S. I., D. J. ALLEN, A. ORTIZ-LOPEZ and G. HERNANDEZ (2001): Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. Journal of Experimental Botany 52: 1071-1081.10.1093/jexbot/52.358.1071Open DOISearch in Google Scholar

GALLARDO, F., J. FU, Z. P. JING, E. G. KIRBY and F. M. CÁNOVAS (2003): Genetic modification of amino acid metabolism in woody plants, Metabolic Networks in Plants (Special issue). Plant Physiology and Biochemistry 41: 587-594.10.1016/S0981-9428(03)00081-0Open DOISearch in Google Scholar

GALLARDO, F., J. FU, F. R. CANTON, A. GARCIA-GUTIERREZ , F. M. CÁNOVAS and E. G. KIRBY (1999): Expression of a conifer glutamine synthetase gene in transgenic poplar. Planta 210: 19-26.10.1007/s004250050649Search in Google Scholar

GALLARDO, F., S. GÁLVEZ, M. A. QUESEDA, F. M. CÁNOVAS and I. NÚÑEZ DE CASTRO (1988): Glutamine synthetase activity during the ripening of tomato fruit. Plant Physiology and Biochemistry 26: 747-752.Search in Google Scholar

GÁLVEZ, S., F. GALLARDO and F. M. CÁNOVAS (1990): The occurrence of glutamine synthetase isoenzymes in tomato plants is correlated to plastid differentiation. Journal of Plant Physiology 137: 1-4.10.1016/S0176-1617(11)80002-7Search in Google Scholar

GARCÍA-GUTIÉRREZ, A., F. DUBOIS, F. R. CANTÓN, F. GALLARDO, R. S. SANGWAN and F. M. CÁNOVAS (1998): Two different modes of early development and nitrogen assimilation in gymnosperm seedlings. The Plant Journal 13: 187-199.10.1046/j.1365-313X.1998.00018.xOpen DOISearch in Google Scholar

GESSLER, A., S. KOPRIVA and H. RENNENBERG (2004): Regulation of nitrate uptake at the whole-tree level: interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiology 24: 1313-1321.10.1093/treephys/24.12.131315465694Open DOISearch in Google Scholar

GLASS, A. D. M., D. T. BRITO, B. N. KAISER, J. R. KINGHORN, H. J. KRONZUCKER, A. KUMAR, M. OKAMOTO, S. RAWAT, M.Y. SIDDIQI, S. E. UNKLES and J. J. VIDMAR (2002): The regulation of nitrate and ammonium transport systems in plants, Inorganic Nitrogen Assimilation Special issue. Journal of Experimental Botany 53: 855-864.10.1093/jexbot/53.370.85511912228Search in Google Scholar

HIREL, B., M. MARSOLIER, A. HOARAU, J. HOARAU, J. BRANGEON, R. SCHAFER and D. P. S. VERMA (1992): Forcing expression of a soybean root glutamine synthetase gene in tobacco leaves induces a native gene encoding the cytosolic enzyme. Plant Molecular Biology 20: 207-218.10.1007/BF000144891356501Open DOISearch in Google Scholar

HOERLEIN, G. (1994): Glufosinate (phosphinothricin), a natural amino acid with unexpected herbicidal properties. Review of Environmental Contamination and Toxicology 138: 73-145.10.1007/978-1-4612-2672-7_47938785Search in Google Scholar

HOSHIDA, H., Y. TANAKA, T. HIBINO, Y. HAYAZHI, A. TANAKA, T. TAKABE and T. TAKABE (2000): Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Molecular Biology 43: 103-111.10.1023/A:1006408712416Open DOISearch in Google Scholar

HYMUS, G. J., D. D. ELLSWORTH, N. R. BAKER and S. P. LONG (1999): Does free-air carbon dioxide enrichment affect photochemical energy use by evergreen trees in different seasons? A chlorophyll fluorescence study of mature loblolly pine. Plant Physiology 120: 1183-1191.10.1104/pp.120.4.11835935210444102Search in Google Scholar

IRELAND, R. J. and P. J. LEA (1999) The enzymes of glutamine, glutamate, asparagine, and aspartate metabolism, pp. 49-109 in Plant amino acids: biochemistry and biotechnology edited by B. K. SINGH, Marcel Dekker Inc., New York.Search in Google Scholar

JING, Z. P., F. GALLARDO, M. B. PASCUAL, R. SAMPALO, J. ROMERO, A. TORRES DE NAVARRA and F. M. CÁNOVAS (2004): Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytologiost 164: 137-145.10.1111/j.1469-8137.2004.01173.x33873472Search in Google Scholar

KOZAKI, A. and G. TAKEBA (1996): Photorespiration protects C3 plants from photooxidation. Nature 384: 557-560. 10.1038/384557a0Search in Google Scholar

KRAPP, A., V. SALIBA-COLOMBANI and F. DANIEL-VEDELE (2005): Analysis of C and N metabolisms and of C/N interactions using quantitative genetice. Photosynthesis Research 83: 251-263.10.1007/s11120-004-3196-716143855Open DOISearch in Google Scholar

LA CUESTA, M., A. MUÑOZ-RUEDA, C. GONZÁLEZ-MURUA and M. N. SIVAK (1992): Effect of phosphinothricin (glufosinate) on photosynthesis and chloropyll fluorescence emission by barley leaves illuminated under photorespiratory and non-photorespiratory conditions. Journal of Experimental Botany 43: 246-251.Search in Google Scholar

LAM, H. M., K. T. COSCHIGANO, I. C. OLVEIRA, R. MELOOLIVEIRA and G. M. CORUZZI (1996): The molecular genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 569-593.10.1146/annurev.arplant.47.1.56915012301Open DOISearch in Google Scholar

LEAKEY, A. D. B., M. C. PRESS, J. D. SCHOLES and J. R. WATLING (2002): Relative enhancement of photosynthesis and growth at elevated CO2 is greater under sunflecks than uniform irradiance in a tropical rain forest seedling. Plant, Cell and Environment 25: 1701-1714.10.1046/j.1365-3040.2002.00944.xSearch in Google Scholar

LEAKEY, A. D. B., J. D. SCHOLES and M. C. PRESS (2005): Physiological and ecological significance of sunflecks for dipterocarp seedlings. Journal of Experimental Botany 56: 469-482.10.1093/jxb/eri05515596478Search in Google Scholar

MAN, H. M., R. BORIEL, R. EL-KHATIB and E. G. KIRBY (2005): Characterization of transgenic poplar with ectopic expression of pine cytosolic glutamine synthetase under conditions of varying nitrogen availability. New Phytologist 167: 31-39.10.1111/j.1469-8137.2005.01461.xSearch in Google Scholar

MAXWELL, K. and G. N. JOHNSON (2000): Chlorophyll fluorescence- a practical guide. Journal of Experimental Botany 51: 659-668.10.1093/jexbot/51.345.659Open DOISearch in Google Scholar

MIFLIN, B. and D. Z. HABASH (2002): The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. Journal of Experimental Botany 53: 979-987.10.1093/jexbot/53.370.979Search in Google Scholar

NIYOGI, K. K and G. R. FINK (1992): Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. The Plant Cell 4: 721-733.10.1105/tpc.4.6.721Open DOISearch in Google Scholar

OBARA, M., T. SATO and T. YAMAYA (2001): Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.) Journal of Experimental Botany 52: 1209-1217.Search in Google Scholar

OLIVEIRA, I. C., T. BREARS, T. J. KNIGHT, A. CLARK and G. M. CORUZZI (2002): Overexpression of cytosolic glutamine synthetase. Relation to nitrogen, light and photorespiration. Plant Physiology 129: 1170-1180.10.1104/pp.020013Search in Google Scholar

OSMOND, C. B. (1994): What is photoinhibition? Some insights from comparison of shade and sun plants, pp. 1-24. In: Photoinhibition: Molecular Mechanisms to the Field, edited by N. R. BAKER and J. R. BOYER, Bios Scientific Publishers, Oxford, UK.Search in Google Scholar

POULSEN, C., R. J. M. BONGAERTS and R. VERPOORTE (1993): Purification and characterization of anthranilate synthase from Catharanthus roseus. European Journal of Biochemistry 212: 431-440.10.1111/j.1432-1033.1993.tb17679.xSearch in Google Scholar

PEREIRA, S., H. CARVALHO, C. SUNKEL and R. SALEMA (1992): Immunocytolocalization of GS in mesophyll and phloem of leaves of Solanum tuberosum L. Protoplasma 167: 66-73.10.1007/BF01353582Search in Google Scholar

PÉREZ-GARCÍA, A., S. PEREIRA, J. PISARRA, A. GARCÍAGUTIÉRREZ, F. CAZORLA, R. SALEMA, A. DE VICENTE and F. M. CÁNOVAS (1998): Cytosolic localization in tomato mesophyll cells of a novel glutamine synthetase induced in response to bacterial infection or phosphinothricin treatment. Planta 206: 426-434.10.1007/s004250050418Search in Google Scholar

RADWANSKI, E. R, and R. L. LAST (1995): Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. The Plant Cell 7: 921-934.Search in Google Scholar

ROMERO, R. M. and M. F. ROBERTS (1996): Anthranilate synthase from Ailanthus altissima cell suspension cultures. Phytochemistry 41: 395-402.10.1016/0031-9422(95)00617-6Open DOISearch in Google Scholar

SAUTER, J. J. and B. VANCLEVE (1994): Storage, mobilization and interrelations of starch, sugars, protein and fat in the ray storage tissue of poplar trees. Trees 8: 297-304.10.1007/BF00202674Search in Google Scholar

SCHWANZ, P. and A. POLLE (2001): Differential stress responses of oxidative systems to drought in pendunculate oak (Quercus robur) and maritime pine (Pinus pinaster) grown under high CO2 concentrations. Journal of Experimental Botany 52: 133-143.Search in Google Scholar

SMITH, P. M. C. and C. A. ATKINS (2002): Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiology 128: 793-802.10.1104/pp.010912154021611891236Search in Google Scholar

TOZAWA, Y., H. HASEGAWA, T. TERAKAWA and K. WAKASA (2001): Characterization of rice anthranilate synthase α-subunit genes OASA1 and OASA2. Tryptophan accumulation in transgenic rice expressing a feedbackinsensitive mutant of OASA1. Plant Physiology 126: 1493-1506.10.1104/pp.126.4.149311714911500548Search in Google Scholar

VINES, H., M. SENYIMBA, S. IMBAMBA and J. TROUGHTON (1983): Environmental responses of the post-lower illumination CO2 burst as related to leaf photorespiration. Plant Physiology 73: 25-30.10.1104/pp.73.1.25106640016663179Open DOISearch in Google Scholar

WETZEL, S., C. DEMMERS and J. GREENWOOD (2001): Seasonally fluctuating bark proteins are a potential form of nitrogen storage in three temperate hardwoods. Planta 178: 275-281.10.1007/BF0039185424212893Search in Google Scholar

WOLT, J. D. and J. WOLT (1994): Soil Solution Chemistry: Applications to Environmental Science and Agriculture. John Wiley & Sons, New York.Search in Google Scholar

ZHANG, X., L. ZHANG, F. DONG, J. GAO, D.W. GALBRAITH and C. P. SONG (2001): Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology 126: 1438-1448.10.1104/pp.126.4.143811714411500543Search in Google Scholar

ZHU, B. and G. COLEMAN (2001): Phytochrome-mediated photoperiod perception, shoot growth, glutamine, calcium and protein phosphorylation influence the activity of the poplar bark storage protein gene promoter (bspA). Plant Physiology 126: 342-351.10.1104/pp.126.1.34210230811351097Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo