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Stimulation of γ-Aminobutyric Acid Synthesis Activity in Brown Rice by a Chitosan/Glutamic Acid Germination Solution and Calcium/Calmodulin

  • Received : 2002.12.24
  • Accepted : 2003.02.10
  • Published : 2003.05.31

Abstract

Changes in the concentrations of $\gamma$-aminobutyric acid (GABA), soluble calcium ions, glutamic acid, and the activity of glutamate decarboxylase (GAD) were investigated in non-germinated vs. germinated brown rice. Brown rice was germinated for 72 h by applying each of the following solutions: (1) distilled water, (2) 5 mM lactic acid, (3) 50 ppm chitosan in 5 mM lactic acid, (4) 5 mM glutamic acid, and (5) 50 ppm chitosan in 5 mM glutamic acid. GABA concentrations were enhanced in all of the germinated brown rice when compared to the non-germinated brown rice. The GABA concentration was highest in the chitosan/glutamic acid that germinated brown rice at 2,011 nmol/g fresh weight, which was 13 times higher than the GABA concentration in the non-germinated brown rice at 154 nmol/g fresh weight. The concentrations of glutamic acid were significantly decreased in all of the germinated rice, regardless of the germination solution. Soluble calcium and GAD were higher in the germinated brown rice with the chitosan/glutamic acid solution when compared to the rice that was germinated in the other solutions. GAD that was partially purified from germinated brown rice was stimulated about 3.6-fold by the addition of calmodulin in the presence of calcium. These data show that the germination of brown rice in a chitosan/glutamic acid solution can significantly increase GABA synthesis activity and the concentration of GABA.

Keywords

References

  1. Akama, K., Akihiro, T., Kitagawa, M. and Takaiwa, F. (2001) Rice (Oryza sativa) contains a novel isoform of glutamate decarboxylase that lacks an authentic calmodulin-binding domain at the C-terminus. Biochim. Biophys. Acta 1522, 143-150. https://doi.org/10.1016/S0167-4781(01)00324-4
  2. 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. https://doi.org/10.1104/pp.108.2.551
  3. Bach, M., Schnitzler, J. P. and Seitz. H. U. (1993) Elicitor-induced changes in $Ca^{2+}$ influx, $K^{+}$ eftlux, and 4-hydroxybenzoic acid synthesis in protoplasts of Daucus carota L. Plant Physiol. 103, 407-412.
  4. Baek. N. I., Ahn, E. M., Han, J. T., Park, J. K., Cho, S. W, Jeon, S. G., Bahn, J. H., Sun, H. J. and Choi, S. Y. (2000) Effects of several medicinal plants on the activity of GABA-metabolizing enzymes. Kor. J. Pharmacogn. 31, 23-27.
  5. Bartnick, M. and Szafranska, J. (1987) Change in phytate content and phytase during the germination of some cereals. J. Cereal Sci. 5, 23-28. https://doi.org/10.1016/S0733-5210(87)80005-X
  6. 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. BioI. Chem. 268, 19610-19617.
  7. Baum, G., Lev-Yadun, S., Fridmann, Y., Arazi, T., Katsnelson, H., Zik, M. and Fromm, H. (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J. 15. 2988-2996.
  8. Bown, A. W. and Shelp, B. J. (1997) The metabolism and functions of $\Upsilon$-aminobutyric acid. Plant Physiol. 115, 1-5.
  9. Bradford. M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein dye binding. Anal. Biochem. 72, 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  10. Chen, y, Baum, G. and Fromm, H. (1994) The 58-kilodalton calmodulin-binding glutamate decarboxylase is a ubiquitous protein in petunia organs and its expression is developmentally regulated. Plant Physiol. 106, 1381-1387.
  11. Choi, S. Y., Bahn, J. H., Jeon, S. G., Chung, Y. M., Hong, J. W., Ahn, J. Y., Hwang, E. J., Cho, S. W., Park, J. K. and Baek, N. I. (1998) Stimulatory effects of ginsenoside on bovine brain glutamate decarboxylase. J. Biochem. Mol. Biol. 31, 233-239.
  12. Cohen, Y., Niderman, T., Mosinger, E. and Fluhr, R. (1994) $\beta$-Aminobutyric acid induces the accumulation of pathogenesis-related proteins in tomato Lycopersicum esculentum plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiol. 104, 59-66.
  13. Collinge, M. and Trewavas, A. J. (1989) The location of calmodulin in the pea plasma membrane. J. Biol. Chem. 262, 8865-8872.
  14. Erlander, M. G. and Tobin, A. J. (1991) The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem. Res. 16, 215-226. https://doi.org/10.1007/BF00966084
  15. Graf, E. (1983) Calcium binding to phytic acid. J. Agric. Food Chem. 31, 851-855. https://doi.org/10.1021/jf00118a045
  16. Hepler, P. K. and Wayne, R. O. (1985) Calcium and plant development. Ann. Rev. Plant Physiol. 36, 397-439. https://doi.org/10.1146/annurev.pp.36.060185.002145
  17. Jung, B. O., Lee, Y. M., Kim, J. J., Choi. Y. J., Jung. K. J., Kim, J. J. and Chung, S. J. (1999) The antimicrobial effect of water soluble chitosan. J. Korean Ind. Eng. Chem. 10, 660-665.
  18. Knight, M. R., Campbell, A. K., Smith, S. M. and Trewavas, A. J. (1991) Transgenic plant aequorin reports the effect of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352, 524-526. https://doi.org/10.1038/352524a0
  19. Laboure, A. M., Gangnon, J. and Lescure, A. M. (1993) Purification and characterization of a phytase (myo-inositol-hexakisphosphate phospho-hydrolase) accumulated in maize (Zea mays) seedlings during germination. Biochem. J. 295, 413-419.
  20. Lee, S. H., Seo, H. Y., Kim, J. C., Lee, M. S., Heo, W. D., Chung, W. S., Lee, K. J., Kim, M. C., Cheong, Y. H., Choi, J. Y. and Cho, M. J. (1997) Differential activation of NAD kinase by plant calmodulin isoforms: The critical role of domain I. J. Biol. Chem. 272, 9252-9259. https://doi.org/10.1074/jbc.272.14.9252
  21. Lee, S. H., Kim, C. Y., Lim, C. O., Lee, S. I., Gal, S. W. and Choi, Y. J. (2000) Molecular characterization of three cDNA clones encoding calmodulin isoforms of rice. Agric. Chem. Biotechnol. 43, 5-11.
  22. Lee, E. Y., Yoon, H. Y., Kim, T. U., Choi. S. Y., Won, M. H. and Cho, S. W. (2001) Inactivation of brain glutamate dehydrogenase isoproteins by MDL 29951. J. Biochem. Mol. BioI. 34, 268-271.
  23. Ling, V., Snedden, W. A., Shelp, B. J. and Assmann, S. M. (1994) Analysis of a soluble calmodulin binding protein from fava bean roots: Identification of glutamate decarboxylase as a calmodulin-activated enzyme. Plant Cell 6, 1135-1143. https://doi.org/10.1105/tpc.6.8.1135
  24. Mody, I., Dekoninck, Y., Otis, T. S. and Soltesz. I. (1994) Bringing the cleft at GABA synapses in the brain. Trends Neurosci. 17, 517-525. https://doi.org/10.1016/0166-2236(94)90155-4
  25. Nakagawa, K. and Onota, A. (1996) Accumulation of $\Upsilon$-aminobutyric acid (GABA) in the rice germ. Shokuhin Kaihatsu 31, 43-46.
  26. Notsu, S., Saito, N., Kosaki, H., Inui, H. and Hirano, S. (1994) Stimulation of phenylalanine ammonia-lysate activity and lignification in rice callus treated with chitin, chitosan, and their derivatives. Biosci. Biotech. Biochem. 58, 552-553. https://doi.org/10.1271/bbb.58.552
  27. Novak, W. K. and Haslberger, A. G. (2000) Substantial equivalence of antinutrients and inherent plant toxins in genetically modified novel foods. Food Chem. Toxicol. 38, 473-483. https://doi.org/10.1016/S0278-6915(00)00040-5
  28. Oh, S. H. and Yun, S. J. (1999) Effects of various calmodulins on the activation of glutamate decarboxylase and nicotinamide adenine dinucleotide kinase isolated from tobacco plants. Agric. Chem. Biotechnol. 42, 19-24.
  29. Oh, S. H. and Choi, W. G. (2000) Production of the quality germinated brown rice containing high $\Upsilon$-aminobutyric acid by chitosan application. Korean J. Biotechnol. Bioeng. 15, 615-620.
  30. Oh, S. H. and Choi, W. G. (2001) Changes in the levels of $\Upsilon$-aminobutyric acid and glutamate decarboxylase in developing soybean seedlings. J. Plant Res. 114, 309-313. https://doi.org/10.1007/PL00013992
  31. Oh, S. H. and Cha, Y. S. (2001) Effects of diets supplemented with pharhitis seed powder on serum and hepatic lipid levels and enzyme activities of rats administered with ethanol chronically. J. Biochem. Mol. Biol. 34, 166-171.
  32. Oh, S, H., Kim, S. H., Moon, Y. J. and Choi, W. G. (2002) Changes in the levels of $\Upsilon$-aminobutyric acid and some amino acids by application of glutamic acid solution for the germination of brown rice. Korean J. Biotechnol. Bioeng. 17, 49-53.
  33. Omori, M., Yano, T., Okamoto, T., Tsushida, T., Murai, T. and Higuchi, M. (1987) Effect of anaerobically treated tea (Gaharon tea) on blood pressure of spontaneously hypertensive rats. Nippon Nogilwgaku Kaishi 61, 1449-1451. https://doi.org/10.1271/nogeikagaku1924.61.1449
  34. Park, J. K., Jin, S. H., Choi, K. H., Ko, J. H., Baek, N. I., Choi, S. Y., Cho, S. W., Choi, K. J. and Nam, K. Y. (1999) Influence of ginsenosides on the kainic acid-induced seizure activity in immature rats. J. Biochem. Mol. Biol. 32, 339-344.
  35. Pearce. R. B. and Ride, J. P. (1982) Chitin and related compounds as elicitors of the lignification response in wounded wheat leaves. Physiol. Plant Pathol. 20, 119-123. https://doi.org/10.1016/0048-4059(82)90030-3
  36. Ramputh, A. and Bown, A. W. (1996) Rapid $\Upsilon$-aminobutyric acid synthesis and inhibition of the growth and development of oblique-banded leaf-roller larvae. Plant Physiol. 111, 1349-1353.
  37. Rasi-Caldogno, F., Camelli, A. and De Michelis, M. J. (1993) Controlled proteolysis activates the plasma membrane $Ca^{2+}$ pump of higher plants. Plant Physiol. 103, 385-390.
  38. Selman, I. W. and Cooper, P. (1978) Changes in free amino compounds in young tomato plants in light and darkness with particular references to $\Upsilon$-aminobutyric acid. Ann. Bot. 42, 627-636. https://doi.org/10.1093/oxfordjournals.aob.a085497
  39. Serraj, R., Shelp, B. J. and Sinclair, T. R. (1998) Accumulation of $\Upsilon$-aminobutyric acid in nodulated soybean in response to drought stress. Physiol. Plantarum 102, 79-86. https://doi.org/10.1034/j.1399-3054.1998.1020111.x
  40. Shelp, B. J., Walton, C. S., Snedden, W. A., Tuin, L. G., Oresnik, J. J. and LayzeIl, D. B. (1995) GABA shunt in developing soybean seeds is associated with hypoxia. Physiol. Plant. 94, 219-228. https://doi.org/10.1111/j.1399-3054.1995.tb05304.x
  41. Shelp, B. J., Bown, A. W. and McLean, M. D. (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci. 4, 446-452. https://doi.org/10.1016/S1360-1385(99)01486-7
  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. Snedden, W. A. and Fromm, H. (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci. 3, 299-304. https://doi.org/10.1016/S1360-1385(98)01284-9
  44. Stayanarayan, V. and Nair, P. M. (1990) Metabolism, enzymology and possible roles of 4-aminobutyrate in higher plants. Phytochem. 29, 367-375. https://doi.org/10.1016/0031-9422(90)85081-P
  45. Vandewalle, I. and Olsson, R. (1983) The $\Upsilon$-aminobutyric acid shunt in gemrinating Sinapis alba seeds. Plant Sci. Lett. 31, 269-273. https://doi.org/10.1016/0304-4211(83)90065-2
  46. Yun, S. J., Choi, K. G. and Kim, J. K. (1998) Effect of anaerobic treatment on carbohydrate-hydrolytic enzyme activities and free amino acid contents in barley malt. Kor. J. Crop Sci. 43, 19-22.

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