Increased glutamine in leaves of poplar transgenic with pine GS1a caused greater anthranilate synthetase α-subunit (ASA1) transcript and protein abundances: An auxin-related mechanism for enhanced growth in GS transgenics?

Journal of Experimental Botany

Volumn 62, Issue 13, 2011, Pages 4423-4431

  Man, Huimin ^a   Pollmann, Stephan ^b   Weiler, Elmar W ^b   Kirby, Edward G ^a  

^a RUTGERS UNIVERSITY   (United States)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Anthranilate synthase; glutamine synthetase; indole acetic acid (IAA); nitrogen assimilation; poplar

Indexed keywords

ANTHRANILATE SYNTHASE; CHORISMIC ACID; GLUTAMATE AMMONIA LIGASE; GLUTAMINE; INDOLEACETIC ACID DERIVATIVE; MESSENGER RNA;

ARTICLE; ASPEN; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; METABOLISM; PINE; PLANT LEAF; PROTEIN SUBUNIT; TOBACCO; TRANSGENIC PLANT;

ANTHRANILATE SYNTHASE; CHORISMIC ACID; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLUTAMATE-AMMONIA LIGASE; GLUTAMINE; IMMUNOBLOTTING; INDOLEACETIC ACIDS; PINUS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; POPULUS; PROTEIN SUBUNITS; RNA, MESSENGER; TOBACCO;

NICOTIANA TABACUM; POPULUS;

EID: 80052878050     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err026     Document Type: Article

References (58)

1. Altschul SF, Madden TL, Schaeffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389-3402. (Pubitemid 27359211)
2. Amezaine R, Bernhard K, Lightfoot D. 2000. Expression of the bacterial gdhA gene encoding a NDAPH glutamate dehydrogenase in tobacco affects plant growth and development. Plant and Soil 221, 47-57. (Pubitemid 30597575)
3. Benjamins R, Scheres B. 2008. Auxin: the looping star in plant development. Annual Review of Plant Biology 59, 443-465. (Pubitemid 351813038)
4. Bernasconi P, Walters EW, Woodworth AR, Siehl DL, Stone TE, Subramanian MV. 1994. Functional expression of Arabidopsis thaliana anthranilate synthase subunit I in Escherichia coli. Plant Physiology 106, 353-358.
5. Bohlmann J, Deluca V, Eilert U, Martin W. 1995. Purification and cDNA cloning of anthranilate synthase from Ruta graveolens: modes of expression and properties of native and recombinant enzymes. The Plant Journal 7, 491-501.
6. Bohlmann J, Lins T, Martin W, Eilert U. 1996. Anthranilate synthase from Ruta graveolens: duplicated ASa genes encode tryptophan-sensitive and tryptophan-insensitive isoenzymes specific to amino acid and alkaloid biosynthesis. Plant Physiology 111, 507-514. (Pubitemid 126640495)
7. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
8. Brunner AM, Yakovlev IA, Strauss SH. 2004. Validating internal controls for quantitative plant gene expression studies. BMC Plant Biology 4, 14.
9. Chandler JW. 2009. Local auxin production: a small contribution to a big field. BioEssays 31, 60-70.
10. Chang S, Puryear J, Caimey J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113-116.
11. Cho HJ, Brotherton JE, Song HS, Widholm JM. 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. (Pubitemid 30466859)
12. Crawford IP. 1989. Evolution of a biosynthetic pathway: the tryptophan paradigm. Annual Review of Microbiology 43, 567-600. (Pubitemid 19250058)
13. Crozier A, Kamiya Y, Bishop G, Yokota T. 2000. Biosynthesis of hormones and elicitor molecules. In: Buchanan BB, Gruissem W, Jones RL, eds. Biochemistry and molecular biology of plants. Rockville, MD: American Society of Plant Biologists, 850-928.
14. Eckes P, Schmitt P, Daub W, Wengenmayer F. 1989. Overproduction of alfalfa glutamine synthetase in transgenic tobacco plants. Molecular and General Genetics 217, 263-268.
15. El-Khatib R, Hamerlynck EP, Gallardo F, Kirby EG. 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. (Pubitemid 39538782)
16. Fu JM, Gallardo F, Kirby EG. 2003. Assembly of a cytosolic pine glutamine synthetase holoenzyme in leaves of transgenic poplar leads to enhanced vegetative growth. Plant, Cell and Environment 26, 411-418. (Pubitemid 36380510)
17. Gallardo F, Fu J, Canton FR, Garcia-Gutierrez A, Cá novas FM, Kirby EG. 1999. Expression of a conifer glutamine synthetase gene in transgenic poplar. Planta 210, 19-26. (Pubitemid 30000911)
18. Hemon P, Robbins M, Cullimore J. 1990. Targeting of glutamine synthetase to the mitochondrioa of transgenic tobacco. Plant Molecular Biology 15, 895-904.
19. Hirel B, Marsolier M, Hoarau A, Hoarau J, Brangeon J, Schafer R, Verma DPS. 1992. Forcing expression of a soybean root glutamine synthetase gene in tobacco leaves induces a native gene encoding cytosolic enzyme. Plant Molecular Biology 20, 207-218.
20. Inaba Y, Zhong WQ, Zhang XH, Widholm JM. 2007. Specificity of expression of the GUS reporter gene (uidA) driven by the tobacco ASA2 promoter in soybean plants and tissue cultures. Journal of Plant Physiology 164, 824-834.
21. Jing ZP, Gallardo F, Pascual MB, Sampalo R, Romero J, Torres de Navarra A, Cá novas FM. 2004. Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytologist 164, 37-145.
22. Johnson C, Stout P, Broyer T, Carlton A. 1957. Comparative chlorine requirements of different plant species. Plant and Soil 8, 337-353.
23. Kirby EG, Gallardo F, Man HM, Rl-Khatib R. 2006. The overexpression of glutamine synthetase in transgenic poplar: a review. Silvae Genetica 55, 278-284. (Pubitemid 46141452)
24. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
25. Lam HM, Coschigano K, Schultz C, Oliveira RM, Tjaden G, Oliveira I, Ngai N, Hsieh MH, Coruzzi G. 1995. Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. The Plant Cell 7, 887-898.
26. Lam HM, Coschigano K, Olivera IC, Melo-Olivera R, Coruzzi G. 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.
27. Leplé JC, Brasileiro ACM, Michel MF, Delmotte F, Jouanine L. 1992. Transgenic poplars: expression of chimeric genes using four different constructs. Plant Cell Reports 11, 137-141.
28. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G. 2002. Biosynthesis, conjugation, catabolism and homeostasis of indol-3-acetic acid in Arabidopsis thaliana. Plant Molecular Biology 50, 309-332. (Pubitemid 38458823)
29. 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)
30. Matsuda F, Yamada T. 2005. Characterization of tryptophan-overproducing potato transgenic for a mutant rice anthranilate synthase a-subunit gene (OASA1D). Planta 222, 535-545. (Pubitemid 41443653)
31. Minocha R, Long S. 2004. Simultaneous separation and quantitation of amino acids and polyamines of forest tree tissues and cell cultures within a single high-performance liquid chromatography run using dansyl derivatization. Journal of Chromatography A 1035, 63-73. (Pubitemid 38446797)
32. Mousli M, Hopfner R, Abbady AQ, Monte D, Jeanblanc M, Oudet P, Louis B, Bronner C. 2003. CBP90 belongs to a new family of proteins with an expression that is deregulated in cancer cells. British Journal of Cancer 89, 120-127. (Pubitemid 36897947)
33. Mueller A, Weiler EW. 2000. IAA-synthase, an enzyme complex from Arabidopsis thaliana catalyzing the formation of indole-3-acetic acid from (S)-tryptophan. Biological Chemistry 381, 679-686.
34. Mungur R, Glass ADM, Goodenow DB, Lightfoot DA. 2005. Metabolite fingerprinting in transgenic Nicotiana tabacum altered by the Escherichia coli glutamate dehydrogenease gene. Journal of Biomedicine and Biotechnology 2, 198-214. (Pubitemid 41627877)
35. Niyogi KK, Fink GR. 1992. Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. The Plant Cell 4, 721-733.
36. Normanly J. 1997. Auxin metabolism. Physiologia Plantarum 100, 431-442. (Pubitemid 27340683)
37. Normanly J. 2010. Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harbor Perspectives in Biology 2, a001594.
38. Olivera IC, Brears T, Knight TJ, Clark A, Coruzzi G. 2002. Overexpression of cytosolic glutamine synthetase. Relation to nitrogen, light, and photorespiration. Plant Physiology 129, 1170-1180. (Pubitemid 34801087)
39. Paul MJ, Primavesin LF, Jhurreea D, Zhang Y. 2008. Trehalose metabolism and signaling. Annual Review of Plant Biology 59, 417-441. (Pubitemid 351813037)
40. Park WJ, Schafer A, Prinsen E, van Onckelen H, Kang BG, Hertel R. 2001. Auxin-induced elongation of short maize coleoptile segments is supported by 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one. Planta 213, 92-100. (Pubitemid 32507455)
41. Pollmann S, Duechting P, Weiler EW 2009. Tryptophan-dependent indole-3-acetic biosynthesis by 'IAA-synthase' proceeds via indole-3-acetamide. Phytochemistry 70, 523-531.
42. Pollman S, Mü ller A, Piotrowski M, Weiler EW. 2002. Occurrence and formation of indole-3-acetamide in Arabidopsis thaliana. Planta 216, 155-161. (Pubitemid 36761559)
43. Poulsen C, Bongaerts RJM, Verpoorte R. 1993. Purification and characterization of anthranilate synthase from Catharanthus roseus. European Journal of Biochemistry 212, 431-440. (Pubitemid 23076111)
44. Radwanski ER, Last RL. 1995. Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. The Plant Cell 7, 921-934.
45. Romero RM, Roberts MF. 1996. Anthranilate synthase from Ailanthus altissima cell suspension cultures. Phytochemistry 41, 395-402.
46. Rutherford R, Gallois P, Masson PH. 1998. Mutations in Arabidopsis thaliana genes involved in the tryptophan biosynthesis pathway affect root waving on tilted agar surface. The Plant Journal 16, 145-154.
47. Sazuka T, Kamiya N, Nishimura T, et al. 2009. A rice tryptophan deficient dwarf mutant, tdd1, contains a reduced level of indole acetic acid and develops abnormal flowers and organless embryos. The Plant Journal 60, 227-241.
48. Smith PMC, Atkins CA. 2002. Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiology 128, 793-802. (Pubitemid 34243817)
49. Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM. 2005. A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. The Plant Cell 17, 2230-2242. (Pubitemid 41672943)
50. Stepanova AN, Robinson-Hoytt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jü rgens G, Alanso JM. 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177-191. (Pubitemid 351442990)
51. Tarlton JF, Knight PJ. 1996. Comparison of reflectance and transmission densitometry, using document and laser scanners, for quantitation of stained western blots. Analytical Biochemistry 237, 123-128. (Pubitemid 26155639)
52. Temple S, Knight T, Unkefer P, Sengupta-Gopalan C. 1993. Modulation of glutamine synthetase gene expression in tobacco by introduction of an alfalfa glutamine synthetase gene in a sense and antisense orientation: molecular and biochemical analysis. Molecular and General Genetics 236, 315-325. (Pubitemid 23055571)
53. Tozawa Y, Hasegawa H, Terakawa T, Wakasa K. 2001. Characterization of rice anthranilate synthase a-subunit genes OASA1 and OASA2. Tryptophan accumulation in transgenic rice expressing a feedback-insensitive mutant of OASA1. Plant Physiology 126, 1493-1506. (Pubitemid 32752378)
54. Tsuno Y, Taniyama T, Suprpto H. 1983. The photosynthesis and estimation of productivity in cassava. Japanese Journal of Crop Science 52, 484-492.
55. Vierck JJ, Byrne KM, Dodson MV, Krabbenhoft L, Chen Y. 2001. Evaluating dot and western blots using image analysis and pixel quantification of electronic images. Methods in Cell Science 22, 313-318. (Pubitemid 32926957)
56. Zalkin H, Paluh JL, van Cleemput M, Moye WS, Yanofsky C. 1984. Nucleotide sequence of Saccharomyces cerevisiae genes TRP2 and TRP3 encoding bifunctional anthranilate synthase: indole-3-glycerol phosphate synthase. Journal of Biological Chemistry 259, 3985-3992. (Pubitemid 14170116)
57. Zhang XH, Brotherton JE, Widholm JM, Portis Jr. AR. 2001. Targeting a nuclear anthranilate synthase a-subunit gene to the tobacco plastid genome results in enhanced tryptophan biosynthesis. Return of a gene to its pre-endosymbiotic origin. Plant Physiology 127, 131-141. (Pubitemid 32925543)
58. Zhao Y. 2010. Auxin biosynthesis and its role in plant development. Annual Review of Plant Biology 61, 49-64.