Biochemical mechanism on GABA accumulation during fruit development in tomato

Plant and Cell Physiology

Volumn 49, Issue 9, 2008, Pages 1378-1389

  Akihiro, Takashi ^a   Koike, Satoshi ^a   Tani, Ryoji ^a   Tominaga, Takehiro ^a   Watanabe, Shin ^a   Iijima, Yoko ^b   Aoki, Koh ^b   Shibata, Daisuke ^b   Ashihara, Hiroshi ^d   Matsukura, Chiaki ^a   Akama, Kazuhito ^c   Fujimura, Tatsuhito ^a   Ezura, Hiroshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^c SHIMANE UNIVERSITY   (Japan)

^d OCHANOMIZU UNIVERSITY   (Japan)

Author keywords

GABA; GABA TK; Glutamate; Micro Tom

Indexed keywords

4 AMINOBUTYRATE AMINOTRANSFERASE; 4 AMINOBUTYRIC ACID; COMPLEMENTARY DNA; GLUTAMATE DECARBOXYLASE; MESSENGER RNA; PLANT DNA;

ARTICLE; COMPARATIVE STUDY; FRUIT; GENE EXPRESSION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; MASS FRAGMENTOGRAPHY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; TOMATO;

4-AMINOBUTYRATE TRANSAMINASE; DNA, COMPLEMENTARY; DNA, PLANT; FRUIT; GAMMA-AMINOBUTYRIC ACID; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION; GENOME, PLANT; GLUTAMATE DECARBOXYLASE; LYCOPERSICON ESCULENTUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TIME FACTORS;

ANIMALIA; LYCOPERSICON ESCULENTUM; SOLANUM;

EID: 51749124699     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcn113     Document Type: Article

References (49)

1. Abe, Y., Umemura, S., Sugimoto, K., Hirawa, N., Kato, Y., Yokoyama, N., Yokoyama, T., Iwai, J. and Ishii, M. (1995) Effect of green tea rich in γ-aminobutyric acid on blood pressure of Dahl salt sensitive rats. Am. J. Hypertens. 92: 411-417.
2. Abdou, A.M., Higashiguchi, S., Horie, K., Kim, M., Hatta, H. and Yokogoshi, H. (2006) Relaxation and immunity enhancement effects of γ-aminobutyric acid (GABA) administration in humans. BioFactors 26: 201-208.
3. Akama, K. and Takaiwa, F. (2007) C-terminal extension of rice glutamate decarboxylase (OsGAD2) functions as an autoinhibitory domain and overexpression of a truncated mutant results in the accumulation of extremely high levels of GABA in plant cells. J. Exp. Bot. 58: 2699-2707.
4. Akihiro, T., Mizuno, K. and Fujimura, T. (2005) Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA. Plant Cell Physiol. 46: 937-946.
5. Akihiro, T., Umezawa, T., Ueki, C., Lobna, B.M., Mizuno, K., Ohta, M. and Fujimura, T. (2006) Genome wide cDNA-AFLP analysis of genes rapidly induced by combined sucrose and ABA treatment in rice cultured cells. FEBS Lett. 580: 5947-5952.
6. Aoki, H., Furuya, Y., Endo, Y. and Fujimoto, K. (2003) Effect of γ-aminobutyric acid-enriched tempeh-like fermented soybean (GABA-Tempeh) on the blood pressure of spontaneously hypertensive rats. Biosci. Biotechnol. Biochem. 67: 1806-1808.
7. Arazi, T., Baum, G., Snedden, W.A., Shelp, B.J. and Fromm, H. (1995) Molecular and biochemical analysis of calmodulin interactions with the calmodulin-binding domain of plant glutamate decarboxylase. Plant Physiol. 108: 551-561.
8. Baum, G., Chen, Y., Arazi, T., Takatsuji, H. and Fromm, H. (1993) A plant glutamate decarboxylase containing a calmodulin binding domain. Cloning, sequence, and functional analysis. J. Biol. Chem. 268: 19610-19617.
9. Beutler, H.O. (1989) Succinate. In Methods of Enzymatic Analysis, 3rd edn, Vol. VII. Edited by Bergmeyer, H.U. pp. 25-33. VCH publishers, Cambridge.
10. Bouchè, N., Fait, A., Bouchez, D., Møller, S.G. and Fromm, H. (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the γ-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc. Natl Acad. Sci. USA 100: 6843-6848.
11. Bouchè, N. and Fromm, H. (2004) GABA in plants; just a metabolite? Trends Plant Sci. 9: 110-115.
12. Breitkreuz, K.E., Shelp, B.J., Fischer, W.N., Schwacke, R. and Rentsch, D. (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Lett. 450: 280-284.
13. Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E., Zanor, M., et al. (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol. 142: 1380-1396.
14. Carrari, F. and Fernie, A.R. (2006) Metabolic regulation underlying tomato fruit development. J. Exp. Bot. 57: 1883-1897.
15. Cauwenberghe, O.R.V., Makhmoudova, A., McLean, M.D., Clark, S.M. and Shelp, B.J. (2002) Plant pyruvate-dependent gamma-aminobutyrate transaminase: identification of an Arabidopsis cDNA and its expression in Escherichia coli. Can. J. Bot. 80: 933-941.
16. Elliott, C.A.K. and Hobbiger, F. (1959) Gamma aminobutyric acid: circulatory and respiratory effects in different species: re-investigation of the anti-strychine action in mice. J. Physiol. 146: 70-84.
17. Fait, A., Fromm, H., Walter, D., Galili, G. and Fernie, A.R. (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 13: 14-19.
18. Gallego, P.P., Whotton, L., Picton, S., Grierson, D. and Gray, J.E. (1995) A role for glutamate decarboxylase during tomato ripening: the characterization of a cDNA encoding a putative glutamate decarboxylase with a calmodulin-binding site. Plant. Mol. Biol. 27: 1143-1151.
19. Hayakawa, K., Kimura, M., Kasaha, K., Matsumoto, K., Sansawa, H. and Yamori, Y. (2004) Effect of γ-aminobutyric acid-enriched dairy production on the blood pressure of spontaneously hypertensive and normotensice Wistar-Kyoto rats. Br. J. Nutr. 92: 411-417.
20. Inaba, A., Yamamoto, T., Ito, T. and Nakamura, R. (1980) Changes in the concentrations of free amino acids and soluble nucleotide in attached and detached tomato fruits during ripening. J. Jpn. Soc. Hort. Sci. 49: 435-441.
21. Inoue, K., Shirai, T., Ochiai, H., Kasao, M., Hayakawa, K., Kimura, M. and Sansawa, H. (2003) Blood-pressure-lowering effect of a novel fermented milk containing gamma-aminobutyric acid (GABA) in mild hypertensives. Eur. J. Clin. Nutr. 57: 490-495.
22. Jaarma, M. (1969) Comparison of chemical changes in potato tubers induced by γ-irradiation and by chemical treatment. Acta Chim. Scand. 23: 3435-3442.
23. Jakoby, W.B. (1962) Enzymes of gamma-aminobutyrate metabolism (bacterial). Methods Enzymol. 5: 765-778.
24. Kajimoto, O., Hirata, H., Nakagawa, S., Kajimoto, Y., Hayakawa, K. and Kimura, M. (2004) Hypotensive effect of fermented milk containing γ-aminobutyric acid (GABA) in subjects with high normal blood pressure (in Japanese). Nippon Shokuhin Kagaku Kogaku Kaishi 51: 79-86.
25. Kusakabe, H., Midorikawa, Y., Fujishima, T., Kuninaka, A. and Yoshino, H. (1983) Purification and properties of a new enzyme, L-glutamate oxidase, from Streptomyces sp. X-119-6 grown on wheat bran. Agric. Biol. Chem. 47: 1323-1328.
26. Lane, T.R. and Stiller, M. (1970) Glutamic acid decarboxylation in Chlorella. Plant Physiol. 45: 558-562.
27. MacGregor, K.B., Shelp, B.J., Peiris, S.E. and Bown, A.W. (2003) Overexpression of glutamate decarboxylase in transgenic tobacco deters feeding by phytophagous insect larvae. J. Chem. Ecol. 29: 2177-2182.
28. Mattoo, K., Sobolve, A.P., Neelam, A., Goyal, R.K., Handa, A.K. and Segre, L. (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen-carbon interactions. Plant Physiol. 142: 1759-1770.
29. Matumoto, Y., Ohno, K. and Hiraoka, Y. (1997) Studies on the utilization of functional food materials containing high levels of gamma-aminobutyric acid (Part 1). Ehime Kougi Kenkyu Houkoku 35: 97-100 (in Japanese).
30. McLean, M.D., Yevtushenko, D.P., Deschene, D., Van, Cauwenberghe. O. R., Makhmoudova, A, Potter, J.W., Bown, A.W. and Shelp, B.J. (2003) Overexpression of glutamate decarboxylase in transgenic tobacco plants confers resistance to the northern root-knot nematode. Mol. Breed. 11: 277-285.
31. Mounet, F., Lemaire-Chamley, M., Maucourt, M., Cabasson, C., Giraude, J.L., et al. (2007) Quantitative metabolic profiles of tomato flesh and seeds during fruit development: complementary analysis with ANN and PCA. Metabolomics 3: 273-288.
32. Müeller, L.A., Tanksley, S.D., Giovannoni, J.J., Eck, J.V., Stack, S., et al. (2005) The tomato sequencing project, the first cornerstone of the international Solanaceae project (SOL). Comp. Funct. Genom. 6: 153-158.
33. Noguchi, T., Nakamura, K., Nagai, T., Katsuda, S. and Koga, H. (2007) Antihypertensive effects of GABA-enriched potato snacks in spontaneously hypertensive rats. Nippon Shokuhin Kagaku Kogaku Kaishi 54: 75-81.
34. Palanivelu, R., Brass, L., Edlund, A.F. and Preuss, D. (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell. 114: 47-59.
35. Reggiani, R., Cantú, C.A., Brambilla, I. and Betani, A. (1988) Accumulation and interconversion of amino acids in rice roots under anoxia. Plant Cell Physiol. 29: 981-987.
36. Rolin, D., Baldet, P., Just, D., Chevalier, C., Biran, M. and Raymond, P. (2000) NMR study of low subcellular pH during the development of cherry tomato fruit. Aust. J. Plant Physiol. 27: 61-69.
37. Roessner-Tunali, U., Hegemann, B., Lytovchenko, A., Carrari, F., Bruedigam, C., Granot, D. and Fernie, A.R. (2003) Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol. 133: 84-99.
38. Ronen, G., Carmel-Goren, L., Zamir, D. and Hirschberg, J. (2000) An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc. Natl Acad. Sci. USA 97: 11102-11107.
39. Saito, T., Matsukura, C., Sugiyama, M., Watahiki, A., Ohshima, I., et al. (2008) Screening for γ-aminobutyric acid (GABA)-rich tomato varieties. J. Jpn. Soc. Hort. Sci. 77: 242-250.
40. Schroeder, A, Müeller, O., Stocker, S., Salowsky, R., Leiber, M., Gassmann, M., Lightfoot, S., Menzel, W., Granzow, M. and Ragg, T. (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC. Mol. Biol. 7: 3.
41. Shelp, B.J., Walton, C.S., Snedden, W.A., Tuin, L.G., Oresnik, I.J. and Layzell, D.B. (1995) Gaba shunt in developing soybean seed is associated with hypoxia. Physiol. Plant. 94: 219-228.
42. Snedden, W.A., Arazi, T., Fromm, H. and Shelp, B.J. (1995) Calcium/calmodulin activation of soybean glutamate decarboxylase. Plant Physiol. 108: 543-549.
43. Steward, F.C., Thompson, J.F. and Dent, C.E. (1949) γ-Aminobutyric acid: a constituent of potato tubers? Science 110: 439-440.
44. Streeter, J.G. and Thompson, J.F. (1972) In vivo and in vitro studies on γ-aminobutyric acid metabolism with the radish plant (Raphanus sativus L.). Plant Physiol. 49: 579-584.
45. Studart-Guimarães, C., Fait, A., Nunes-Nesi, A., Carrari, F., Usadel, B. and Fernie, A.R. (2007) Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiol. 145: 626-639.
46. Takahashi, H., Sumi, M. and Koshino, F. (1961) Effect of gamma-aminobutyric acid (GABA) on normotensive or hypertensive rats and men. Jpn. J. Physiol. 11: 89-95.
47. Tanase, S., Kojima, H. and Morino, Y. (1979) Pyridoxal 5′-phosphate binding site of pig heart alanine aminotransferase. Biochemistry 18: 3002-3007.
48. Torre, F.D.L., Santis, L.D., Suarez, M.F., Crespillo, R. and Canovas, F.M. (2006) Identification and functional analysis of a prokaryotic-type aspartate aminotransferase: implications for plant amino acid metabolism. Plant J. 46: 414-425.
49. Wallace, W., Secor, J. and Schrader, L.E. (1984) Rapid accumulation of γ-aminobutyric acid and alanine in soybean leaves in response to an abrupt transfer to lower temperature, darkness, or meachnical manipulation. Plant Physiol. 75: 170-175.