Redundancy and metabolic function of the glutamine synthetase gene family in poplar

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Castro Rodríguez, Vanessa ^a   García Gutiérrez, Angel ^a   Cañas, Rafael A ^a   Pascual, Ma Belén ^a   Avila, Concepción ^a   Cánovas, Francisco M ^a  

^a Fac C   (Spain)

Author keywords

Ammonium assimilation; Gene duplication; Gene family; Glutamine; Populus

Indexed keywords

GLUTAMATE AMMONIA LIGASE; ISOENZYME; MESSENGER RNA; NITROGEN; PEPTIDE; RECOMBINANT PROTEIN;

BIOCATALYSIS; BIOSYNTHESIS; ENZYME STABILITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; KINETICS; LASER; METABOLISM; MICRODISSECTION; MOLECULAR WEIGHT; MULTIGENE FAMILY; PH; POPULUS; TEMPERATURE;

BIOCATALYSIS; ENZYME STABILITY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLUTAMATE-AMMONIA LIGASE; HYDROGEN-ION CONCENTRATION; ISOENZYMES; KINETICS; LASERS; MICRODISSECTION; MOLECULAR WEIGHT; MULTIGENE FAMILY; NITROGEN; PEPTIDES; POPULUS; RECOMBINANT PROTEINS; RNA, MESSENGER; TEMPERATURE;

EID: 84923860944     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0365-5     Document Type: Article

References (41)

1. Neale D, Kremer A: Forest tree genomics: growing resources and applications. Nat Review Genet 2011, 12:111-122.
2. Xu G, Fan X, Miller AJ: Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 2012, 63:153-182.
3. Yamaya T, Kasano M: Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases in rice. J Exp Bot 2014, 65:5519-5525.
4. Unno H, Uchida T, Sugawara H, Kurisu G, Sugiyama T, Yamaya T, Sakakibara H, Hase T, Kusunoki M: Atomic structure of plant glutamine synthetase: a key enzyme for plant productivity. J Biol Chem 2006, 281:29287-29296.
5. Seabra AR, Carvalho H, Pereira PJB: Crystallization and preliminary crystallographic characterization of glutamine synthetase from Medicago truncatula. Acta Crystallogr Sect F 2009, 65:1309-1312.
6. Lea PJ, Blackwell RD, Chen FL, Hetch U: Enzymes of ammonia assimilation. In Methods in Plant Biochemistry. Volume 3. Edited by Lea PJ. London: Academic Press; 1990:257-276.
7. Givan CV, Joy KW, Kleczkowski LA: A decade of photorespiratory nitrogen cycling. Trends Biochem Sci 1988, 13:433-437.
8. Singh S, Lewis NG, Towers GH: Nitrogen recycling during phenylpropanoid metabolism in sweet potato tubers. J Plant Physiol 1998, 153:316-323.
9. Cantón FR, Suárez MF, Cánovas FM: Molecular aspects of nitrogen mobilization and recycling in trees. Photosynth Res 2005, 83:265-278.
10. Pérez-García A, De Vicente A, Cantón FR, Cazorla FM, Codina JC, García-Gutiérrez A, Cánovas FM: Light-dependent changes of tomato glutamine synthetase in response to Pseudomonas syringae infection or phosphinothricin treatment. Physiol Plant 1998, 102:377-384.
11. Pérez-García A, Pereira S, Pissarra J, García-Gutiérrez A, Cazorla FM, Salema R, De Vicente A, Cánovas FM: Cytosolic localization in tomato mesophyll cells of a novel glutamine synthetase induced in response to bacterial infection or phosphinothricin treatment. Planta 1998, 206:426-434.
12. Buchanan-Wollaston V, Ainsworth C: Leaf senescence in Brassica napus: cloning of senescence related genes by subtractive hybridisation. Plant Mol Biol 1997, 33:821-834.
13. Betti B, García-Calderón M, Pérez-Delgado CM, Credali A, Pal'ove-Balang P, Estivill G, Miroslav R, Vega JM, Galván F, Márquez AJ: Reassimilation of ammonium in Lotus japonicus. J Exp Bot 2014, 65:5557-5566.
14. Bernard SM, Habash DZ: The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 2009, 182:608-620.
15. Lea PJ: Primary nitrogen metabolism. In Plant Biochemistry. Edited by Dey PM, Harborne JB. San Diego: Academic Press; 1997:273-313.
16. Castro-Rodríguez V, García-Gutiérrez A, Canales J, Avila C, Kirby EG, Cánovas FM: The glutamine synthetase gene family in Populus. BMC Plant Biol 2011, 11:119.
17. Mathews CK, Van Holde KE, Appling DR, Anthony-Cahill SJ: Biochemistry. 4th edition. NJ, USA: Prentice Hall; 2013.
18. Stadtman E, Oliver CN: Metal-catalyzed oxidation of proteins: Physiological consequences. J Biol Chem 1991, 266:2005-2200.
19. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, et al: The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313:1596-1604.
20. Bennett M, Cullimore J: Expression of three plant glutamine synthetase cDNA in Escherichia coli. Eur J Biochem 1990, 193:319-324.
21. de la Torre F, García-Gutiérrez A, Crespillo C, Cantón FR, Avila C, Cánovas FM: Functional expression of two pine glutamine synthetase genes in bacteria reveals that they encode cytosolic isoenzymes with different molecular and catalytic properties. Plant Cell Physiol 2002, 43:802-809.
22. Seabra AR, Silva LS, Carvalho HG: Novel aspects of glutamine synthetase (GS) regulation revealed by a detailed expression analysis of the entire GS gene family of Medicago truncatula under different physiological conditions. BMC Plant Biol 2013, 13:137.
23. McNally SF, Hirel B, Gadal P, Mann AF, Stewart GR: Glutamine synthetases of higher plants evidence for a specific isoform content related to their possible physiological role and their compartmentation within the leaf. Plant Physiol 1983, 72:22-25.
24. Levitzki A, Koshland DE Jr: The role of negative cooperativity and half-of-the-sites reactivity in enzyme regulation. In Current topics in cellular regulation, Vol 10. Edited by Horecker BL, Stadman ER. New York: Academic Press; 1976:1-40.
25. Ishiyama K, Inoue E, Yamaya T, Takahashi H: Gln49 and Ser174 residues play critical roles in determining the catalytic efficiencies of plant glutamine synthetase. Plant Cell Physiol 2006, 47:299-303.
26. Goodall AJ, Kumar P, Tobin AK: Identification and expression analyses of cytosolic glutamine synthetase genes in barley ( Hordeum vulgare L.). Plant Cell Physiol 2013, 54:492-505.
27. Orsel M, Moison M, Clouet V, Thomas J, Leprince F, Canoy S, Just J, Chalhoub B, Masclaux-Daubresse C: Sixteen cytosolic glutamine synthetase genes identified in the Brassica napus L. genome are differentially regulated depending on nitrogen regimes and leaf senescence. J Exp Bot 2014, 65:3927-3947.
28. El Omari R, Rueda-López M, Avila C, Nhiri M, Cánovas FM: Ammonium tolerance and the regulation of two cytosolic glutamine synthetases in the roots of Sorghum. Funct Plant Biol 2010, 37:55-63.
29. Tabuchi M, Abiko T, Yamaya T: Assimilation of ammonium ions and reutilization of nitrogen in rice ( Oryza sativa L.). J Exp Bot 2007, 58:2319-2327.
30. Cánovas FM, Avila C, Cantón FR, Cañas RA, de la Torre F: Ammonium assimilation and amino acid metabolism in conifers. J Exp Bot 2007, 58:2307-2318.
31. Gómez-Maldonado J, Avila C, Torre F, Cañas R, Cánovas FM, Campbell MM: Functional interactions between a glutamine synthetase promoter and MYB proteins. Plant J 2004, 39:513-526.
32. Craven-Bartle B, Pascual MB, Cánovas FM, Avila C: A Myb transcription factor regulates genes of the phenylalanine pathway in maritime pine. Plant J 2013, 74:755-766.
33. Bekaert M, Edger PP, Pires JC, Conant GC: Two-phase resolution of polyploidy in the Arabidopsis metabolic network gives rise to relative and absolute dosage constraints. Plant Cell 2011, 23:1719-1728.
34. De Smet R, Van de Peer Y: Redundancy and rewiring of genetic networks following genome-wide duplication events. Curr Opin Plant Biol 2012, 15:168-176.
35. Jing ZP, Gallardo F, Pascual MB, Sampalo R, Romero J, Torres De Navarra A, Cánovas FM: Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytol 2004, 164:137-145.
36. Man H, Boriel R, El-Khatib R, Kirby EG: Characterization of transgenic poplar with ectopic expression of pine cytosolic glutamine synthetase under conditions of varying nitrogen availability. New Phytol 2005, 167:31-39.
37. Cánovas FM, Gallardo F, Jing ZP, Pascual B: Transgenic approaches to engineer nitrogen metabolism. In Tree Transgenesis. Recent Developments. Edited by M Fladung M, Ewald S. Heildelberg, Germany: Springer Verlag; 2006:157-178.
38. Bradford M: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
39. Cánovas FM, Cantón FR, Gallardo F, García-Gutiérrez A, De Vicente A: Accumulation of glutamine synthetase during early development of maritime pine ( Pinus pinaster ) seedlings. Planta 1991, 185:372-378.
40. Cánovas F, Valpuesta V, Núñez de Castro I: Characterization of glutamine synthetase from tomato leaves. Plant Sci Lett 1984, 37:79-85.
41. Cantón FR, Suárez MF, Josè-Estanyol M, Cánovas FM: Expression analysis of a cytosolic glutamine synthetase gene in cotyledons of Scots pine seedlings: developmental, light regulation and spatial distribution of specific transcripts. Plant Mol Biol 1999, 40:623-634.