Accumulated expression level of cytosolic glutamine synthetase 1gene (OsGS1;1or OsGS1;2) alter plant development and the carbon-nitrogen metabolic status in rice

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Bao, Aili ^a   Zhao, Zhuqing ^a   Ding, Guangda ^a   Shi, Lei ^a   Xu, Fangsen ^a   Cai, Hongmei ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; CARBOXYLIC ACID; PROTEIN; SUGAR; CARBON; GLUTAMATE AMMONIA LIGASE; NITROGEN;

ARTICLE; CARBON METABOLISM; CARBON NITROGEN RATIO; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENETIC ANALYSIS; GS1 GENE; NITROGEN METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOTOSYNTHETIC RATE; PLANT DEVELOPMENT; PLANT GENETICS; PLANT GROWTH; PLANT LEAF; PLANT STEM; RICE; GENE EXPRESSION REGULATION; METABOLISM;

CARBON; GENE EXPRESSION REGULATION, PLANT; GLUTAMATE-AMMONIA LIGASE; NITROGEN; ORYZA SATIVA;

EID: 84899709506     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095581     Document Type: Article

References (65)

1. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Ann Rev of Plant Physiol and Plant Mol Bio 47: 569-593.
2. Tabuchi M, Abiko T, Yamaya T (2007) Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). J Exp Bot 58: 2319-2327. (Pubitemid 47216540)
3. Frink CR, Waggoner PE, Ausubel JH (1999) Nitrogen fertilizer: retrospect and prospect. Proc Natl Acad Sci USA 96: 1175-1180. (Pubitemid 29098424)
4. Crawford NM, Forde BG (2002) Molecular and developmental biology of inorganic nitrogen nutrition. In Meyerowitz E, Somerville C, eds, The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD.
5. Zheng Z (2009) Carbon and nitrogen nutrient balance signaling in plants. Plant Signal Behav 4(7): 584-591.
6. Krapp A, Ferrario-Méry S, Touraine B (2002) Nitrogen and signalling. In Foyer C, Noctor G, eds, Advances in Photosynthesis.
7. Krapp A, Truong HN (2005) Regulation of C/N interaction in model plant species. In Goyal S, Tischner R, Basra A, eds, Enhancing the Efficiency of Nitrogen Utilization in Plants. Haworth Press, New York, 127-173.
8. Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging 'matrix effects'. Curr Opin Plant Biol 4: 247-253. (Pubitemid 32406372)
9. Martin T, Oswald O, Graham IA (2002) Arabidopsis seedling growth, storage lipid mobilization and photosynthetic gene expression are regulated by carbon: nitrogen availability. Plant Physiol 128(2): 472-481. (Pubitemid 34190862)
10. Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3(6): 973-996.
11. Miflin BJ, Lea PJ (1980) Ammonia assimilation. In Miflin BJ ed, The Biochemistry of Plants, Vol 5, Academic Press, New York, 169-202.
12. Hirel B, Lea PJ (2001) Ammonium Assimilation. In: Lea PJ, Morof Gaudry JF, eds. Plant Nitrogen. Berlin: Springer-Verlag, 79-99.
13. Tobin AK, Yamaya T (2001) Cellular compartmentation of ammonium assimilation in rice and barley. J Exp Bot 53: 591-604. (Pubitemid 32533259)
14. Ireland RJ, Lea PJ (1999) The enzymes of glutamine, glutamate, asparagines and aspirate metabolism. In: Singh B K, ed. Plant Amino Acids: Biochemistry And Biotechnology. New York: Marcel Dekker, 49-109.
15. Mann AF, Fenten PA, Stewart GR (1979) Identification of two forms of glutamine synthetase in barley (Hordeum vulgare, L.). Biochem and Biophy Res Comm 88: 515-521.
16. Hirel B, Gadal P (1980) Glutamine synthetase in rice: a comparative study of the enzymes from roots and leaves. Plant Physiol 66: 619-623.
17. Hayakawa T, Kamachi K, Oikawa M, Ojima K, Yamaya T (1990) Response of glutamine synthetase and glutamate synthase isoforms to nitrogen sources in rice cell cultures. Plant Cell Physiol 31: 1071-1077.
18. Kamachi K, Yamaya T, Maie T, Ojima K (1991) A role for glutamine synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiol 96: 411-417. (Pubitemid 21914028)
19. Zozaya-Garza M, Sengupta-Gopalan C (1999) Glutamine synthetase gene isolation from an alfalfa leaf cDNA library. Plant Physiol 119(4): 1568.
20. Ishiyama K, Inoue E, Tabuchi M, Yamaya T, Takahashi H (2004) Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol 45: 1640-1647. (Pubitemid 40033472)
21. Bernard SM, Moller AL, Dionisio G, Kichey T, Jahn TP, et al. (2008) Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Mol Biol 67: 89-105.
22. Deng Y-W, Zhang Y-D, Chen Y, Wang S, Tang D-M, et al. (2010) Isolation and characterization of a GS2 gene in melon (Cucumis melo L.) and its expression patterns under the fertilization of different forms of N. Mol Biotechnol 44: 51-60.
23. Gadaleta A, Nigro D, Giancaspro A, Blanco A (2011) The glutamine synthetase (GS2) genes in relation to grain protein content of durum wheat. Funct Integr Genomics 11: 665-670.
24. Tabuchi M, Sugiyama K, Ishiyama K, Inoue E, Sato T, et al. (2005) Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. Plant J 42: 641-651. (Pubitemid 40809883)
25. Vincent R, Fraisier V, Chaillou S, Limani AM, Deleens E, et al. (1997) Overexpression of a soybean gene encoding cytosolic glutamine synthetase in shoots of transgenic Lotus corniculatus L. plants triggers changes in ammonium assimilation and plant development. Planta 201: 424-433. (Pubitemid 27186060)
26. Gallardo F, Fu J, Canton FR, Garcia-Gutierez A, Canovas FM, et al. (1999) Expression of a conifer glutamine synthetase gene in transgenic poplar. Planta 210: 19-26. (Pubitemid 30000911)
27. Migge A, Carrayol E, Hirel B, Becker TW (2000) Leaf-specific overexpression of plastidic glutamine synthetase stimulates growth of transgenic tobacco seedlings. Planta 210: 252-260. (Pubitemid 30067889)
28. Jing ZP, Gallardo F, Pascual MB, Sampalo R, Romero J, et al. (2004) Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytologist 164: 137-145. (Pubitemid 39260336)
29. Pascual MB, Jing ZP, Kirby EG, Conovas FM, Gallardo F (2008) Response of transgenic poplar overexpressing cytosolic glutamine synthetase to phosphino-thricin. Phytochemistry 69: 382-389.
30. Fuentes SI, Allen DJ, Ortiz-Lopez A, Herhandez G (2001) Overexpression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J Exp Bot 52: 1071-1081. (Pubitemid 32623697)
31. Oliveira IC, Brears T, Knight TJ, Clark A, Coruzzi GM (2002) Overexpression of cytosolic glutamine synthetase: relation to nitrogen, light and photorespiration. Plant Physiol 129: 1170-1180. (Pubitemid 34801087)
32. Man HM, Boriel R, El-Khatib R, Kirby EG (2005) Characterization of transgenic poplar with ectopic expression of pine cytosolic glutamine synthetase under conditions of varying nitrogen availability. New Phytologist 167: 31-39. (Pubitemid 40885826)
33. Ortega JL, Temple SJ, Bagga S, Ghoshroy S, Sengupta-Gopalan C (2004) Biochemical and molecular characterization of transgenic Lotus japonicas plants constitutively over-expressing a cytosolic glutamine synthetase gene. Planta 219: 807-818. (Pubitemid 39282945)
34. Habash DZ, Massiah AJ, Rong HL, Wallsgrove RM, Leigh RA (2001) The role of cytosolic glutamine synthetase in wheat. Ann Appl Biol 138: 83-89. (Pubitemid 32623672)
35. Limami A, Phillipson B, Ameziane R, Pernollet N, Jiang QJ, et al. (1999) Does root glutamine synthetase control plant biomass production in Lotus japonicus L.? Planta 209: 495-502.
36. Fei H, Chaillou S, Hirel B, Mahon JD, Vessey JK (2003) Overexpression of a soybean cytosolic glutamine synthetase gene linked to organ-specific promoters in pea plants grown in different concentrations of nitrate. Planta 216: 467-474. (Pubitemid 36761769)
37. Kusano M, Tabuchi M, Fukushima A, Funayama K, Diaz C, et al. (2011) Metabolomics data reveal a crucial role of cytosolic glutamine synthetase 1;1 in coordinating metabolic balance in rice. Plant J 66: 456-466.
38. Martin A, Lee J, Kichey T, Gerentes D, Zivy M, et al. (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18: 3252-3274. (Pubitemid 46013289)
39. Cañas RA, Quilleré I, Lea PJ, Hirel B (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotech J 8: 966-978.
40. Lothier J, Gaufichon L, Sormani R, Lemâitre T, Azzppardi M, et al. (2011) The cytosolic glutamine synthetase GLN1;2 plays a role in the control of plant growth and ammonium homeostasis in Arabidopsis rosettes when nitrate supply is not limiting. J Exp Bot 62: 1375-1390.
41. Socolow R (1999) Nitrogen management and the future of food: Lessons from the management of energy and carbon. Proc Natl Acad Sci USA 96: 6001-6008. (Pubitemid 29256609)
42. Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, et al. (2010) Significant acidification in major Chinese croplands. Science 327: 1008-1010.
43. Cai H, Zhou Y, Xiao J, Li X, Zhang Q, et al. (2009) Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant Cell Rep 28: 527-537.
44. Cai H, Xiao J, Zhang Q, Lian X (2010) Co-suppressed glutamine synthetase 2 gene modifies nitrogen metabolism and plant growth in rice. Chinese Science Bulletin 55: 823-833.
45. Yoshida S, Forno DA, Cook JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd eds. International Rice Research Institute, Manila.
46. Melo PM, Lima LM, Santos IM, Carvalho HG, Cullimore JV (2003) Expression of the plastid-located glutamine synthetase of Medicago truncatula: accumulation of the precursor in root nodules reveals an in vivo control at the level of protein import into plastids. Plant Physiol 132: 390-399. (Pubitemid 36590428)
47. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein binding. Anal Biochem 72: 248-254.
48. Morris DL (1948) Quantitative determination of carbohydrates with Dreywood's anthrone reagent. Science 107: 254-255.
49. Maness N (2010) Extraction and analysis of soluble carbohydrates. Methods Mol Biol 639: 341-370.
50. Kusano M, Fukushima A, Kobayashi M, Hayashi N, Jonsson P, et al. (2007b) Application of a metabolomic method combining one-dimensional and two-dimensional gas chromatographytime-of-flight/mass spectrometry to metabolic phenotyping of natural variants in rice. J Chromatogr B Analyt Technol Biomed Life Sci 855: 71-79. (Pubitemid 47077730)
51. Redestig H, Fukushima A, Stenlund H, Moritz T, Arita M, et al. (2009) Compensation for systematic cross-contribution improves normalization of mass spectrometry based metabolomics data. Anal Chem 81: 7974-7980.
52. Yamaya T, Obara M, Nakajima H, Sasaki S, Hayakawa T, et al. (2002) Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. J Exp Bot 53: 917-925. (Pubitemid 34287175)
53. Obara M, Sato T, Sasaki S, Kashiba K, Nagano A, et al. (2004) Identification and characterization of a QTL on chromosome 2 for cytosolic glutamine synthetase content and panicle number in rice. Theo App Gen 110: 1-11. (Pubitemid 40240633)
54. Gallais A, Hirel B (2004) An approach to the genetics of nitrogen use efficiency in maize. J Exp Bot 55: 295-306. (Pubitemid 38204112)
55. Gutiérrez RA, Lejay L, Dean A, Chiaromonte F, Shasha DE, et al. (2007) Qualitative network models and genome wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8: R7.
56. Vidal EA, Gutiérrez RA (2008) A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol 11: 521-529.
57. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, et al. (2009) Identification of nutrient responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time PCR profiling and small RNA sequencing. Plant Physiol 150: 1541-1555.
58. Vidal EA, Araus V, Lu C, Parry G, Green PJ, et al. (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107: 4477-4482.
59. Schlüter U, Colmsee C, Scholz U, Bräutigam A, Weber AP, et al. (2013) Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balance. BMC Genomics 14(1): 442.
60. Tingey SV, Corruzi GM (1987) Glutamine synthetase of Nicotiana plumbaginifolia: cloning and in vivo expression. Plant Physiol 84: 366-373.
61. Li MG, Villemur R, Hussey PJ, Silflow CD, Gantt JS, et al. (1993) Differential expression of six glutamine synthetase genes in Zea mays. Plant Mol Biol 23: 401-440.
62. Oliveira IC, Coruzzi G (1999) Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in Arabidopsis thaliana. Plant Physiol 121: 301-309. (Pubitemid 29452017)
63. Yamaya T, Oaks A (2004) Metabolic regulation of ammonium uptake and assimilation. In: Amancio S, Stulen I (eds) Nitrogen acquisition and assimilation in higher plants. Kluwer Academic Publishers, Dordrecht, 35-63.
64. Canovas FM, Avila C, Canton FR, Canas R, de la Torre F (2007) Ammonium assimilation and amino acid metabolism in conifers. J Exp Bot 58: 2307-2318. (Pubitemid 47216542)
65. Hirel B, Legovis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58: 2369-2387. (Pubitemid 47216545)