Abstract
Arabidopsis thaliana was transformed previously with thecodA gene from the soil bacteriumArthrobacter globiformis. This gene encodes choline oxidase, the enzyme that converts choline to glycinebetaine. Transformation with thecodA gene significantly enhanced the tolerance of transgenic plants to low temperature and high-salt stress. We report here that seeds of transgenic plants that expressed thecodA gene were also more tolerant to salt stress during germination than seeds of non-transformed wild-type plants. Seedlings of transgenic plants grew more rapidly than those of wild-type plants under salt-stress conditions. Furthermore, exogenously applied glycinebetaine was effective in alleviating the harmful effects of salt stress during germination of seeds and growth of young seedlings, a result that suggests that it was glycinebetaine that had enhanced the tolerance of the transgenic plants. These observations indicate that synthesis of glycinebetaine in transgenic plantsin vivo, as a result of the expression of thecodA gene, might be veryuseful in improving the ability of crop plants to tolerate salt stress.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
alia, Hayashi, H., Chen, T.H.H. and Murata, N. 1998. Transformation with a gene for choline oxidase enhanced the cold tolerance ofArabidopsis during germination and early growth. Plant Cell Environ. in press.
Bernard, T., Ayache, M. andRudulier, D.L. 1988. Restoration of growth and enzymic activities ofEscherichia coli Lac− mutants by glycine betaine. C.R. Acad. Sci. III.307: 99–104.
Boyer, J.S. 1982. Plant productivity and environment. Science218: 443–448.
Coughlan, S.J. andHeber, U. 1982. The role of glycinebetaine in the protection of spinach thylakoids against freezing stress. Planta156: 62–69.
Csonka, L.N. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev.53: 121–147.
Deshnium, P., Gombos, Z., Nishiyama, Y. andMurata, N. 1997. The actionin vivo of glycine betaine in enhancement of tolerance ofSynechococcus sp. strain PCC 7942 to low temperature. J. Bacteriol.179: 339–344.
Deshnium, P., Los, D.A., Hayashi, H., Mustardy, L. andMurata, N. 1995. Transformation ofSynechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol. Biol.29: 897–907.
Epstein, E., Norlyn, J.D., Rush, D.W., Kingsbury, R.W., Kelley, D.B., Cunningham, G.A. andWrona, A.F. 1980. Saline culture of crops: A genetic approach. Science210: 399–404.
Garcia-Perez, A. andBurg, M.B. 1991. Renal medullary organic osmolytes. Physiol. Rev.71: 1081–1115.
Hayashi, H., Alia, Mustardy, L., Deshnium, P., Ida, M. andMurata, N. 1997. Transformation ofArabidopsis thaliana with thecodA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J.12: 133–142.
Ikuta, S., Imamura, S., Misaki, H. andHoriuchi, Y. 1977. Purification and characterization of choline oxidase fromArthrobacter globiformis. J. Biochem.82: 1741–1749.
Incharoenskdi, A., Takabe, T. andAkazawa, T. 1986. Effect of betaine on enzyme activity and subunit interaction of ribulose-1,5-bisphosphate carboxylase/oxygenase fromAphanothece halophytica. Plant Physiol.81: 1044–1049.
Kavi Kishor, P.B., Hong, Z., Miao, G.-H., Hu, C.-A. A. andVerma, D.P.S. 1995. Overexpression of Δ1 synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol.108: 1387–1394.
Kishitani, S., Watanabe, K., Yasuda, S., Arakawa, K. andTakabe, T. 1994. Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant Cell Environ.17: 89–95.
Ko, R., Tombras, L., andSmith, G.M. 1994. Glycine betaine confers enhanced osmotolerance and cryotolerance onListeria monocytogenes. J. Bacteriol.176: 426–431.
Lever, M., Sizeland, P.C., Bason, L.M., Hayman, C.M. andChambers, S.T. 1994. Glycine betaine and proline betaine in human blood and urine. Biochim. Biophys. Acta1200: 259–264.
Makela, P., Mantila, J., Hinkkanen, R., Pehu, E. andPeltonen-Sainio, P. 1996. Effect of foliar applications of glycinebetaine on stress tolerance, growth, and yield of spring cereals and summer turnip rape in Finland. J. Agron. Crop. Sci.176: 223–234.
McKersie, B.D. andLeshem, Y.Y. 1994. Stress and Stress Coping in Cultivated Plants. Kluwer Academic Publishers, Dordrecht/Boston/London.
Murashige, T. andSkoog, F. 1962. A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol. Plant15: 473–497.
Murata, N., Ishizaki-Nishizawa, O., Higashi, S., Hayashi, H., Tasaka, Y. andNishida, I. 1992a. Genetically engineered alteration in the chilling sensitivity of plants. Nature356: 710–713.
Murata, N., Mohanty, P.S., Hayashi, H. andPapageorgiou, G.C. 1992b. Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygenevolving complex. FEBS Lett.296: 187–189.
Nomura, M., Muramoto, Y., Yasuda, S., Takabe, T. andKishitani, S. 1995. The accumulation of glycine betaine during cold acclimation in early and late cultivars of barley. Euphytica83: 247–250.
Papageorgiou, G.C., Fujimura, Y. andMurata, N. 1991. Protection of the oxygen-evolving photosystem II complex by glycinebetaine. Biochim. Biophys. Acta1057: 361–366.
Papageorgiou, G.C. andMurata, N. 1995. The unusually strong stabilizing effects of glycinebetaine on the structure and function in the oxygen-evolving photosystem II complex. Photosynth. Res.44: 243–252.
Robinson, S.P. andJones, G.P. 1986. Accumulation of glycinebetaine in chloroplasts provides osmotic adjustment during salt stress. Aust. J. Plant Physiol.13: 659–668.
Santoro, M.M., Liu, Y., Khan, S.M., Hou, L.X. andBolen, D.W. 1992. Increased thermal stability of proteins in the presence of naturally occurring osmolytes. Biochemistry31: 5278–5283.
Tarczynski, M.C., Jensen, R.G. andBohnert, H.J. 1993. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science259: 508–510.
Wall, J.S., Christianson, D.D., Dimler, R.J. andSenti, F.R. 1960. Spectrophotometric determination of betaines and other quaternary nitrogen compounds as their periodides. Analyt. Chem.32: 870–874.
Winzor, C.L., Winzor, D.J., Paleg, L.G., Jones, G.P. andNaidu, B.P. 1992. Rationalization of the effects of compatible solutes on protein stability in terms of thermodynamic nonideality. Arch. Biochem. Biophys.296: 102–107.
Wyn Jones, R.G. andStorey, R. 1981. Betaines.In L.G. Paleg and D. Aspinal, eds., The Physiology and Biochemistry of Drought Resistance in Plants, Academic Press, New York, pp. 171–204.
Xu, D., Duan, X., Wang, B., Hong, B., Ho, T.-H. andWu, R. 1996. Expression of a late embryogenesis abundant protein geneHVA1 from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol.110: 249–257.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hayashi, H., Alia, Sakamoto, A. et al. Enhanced germination under high-salt conditions of seeds of transgenicArabidopsis with a bacterial gene (codA) for choline oxidase. J. Plant Res. 111, 357–362 (1998). https://doi.org/10.1007/BF02512197
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02512197