Overexpression of Spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana

Plant and Cell Physiology

Volumn 45, Issue 6, 2004, Pages 712-722

  Kasukabe, Yoshihisa ^a   He, Lixiong ^a   Nada, Kazuyoshi ^b   Misawa, Shuhei ^a   Ihara, Izumi ^a   Tachibana, Shoji ^b  

^a Toyobo Research Center Co Ltd   (Japan)

^b MIE UNIVERSITY   (Japan)

Author keywords

Arabidopsis thaliana; Gene expression; Gene technology; Polyamine; Spermidine synthase; Stress tolerance

Indexed keywords

ARABIDOPSIS PROTEIN; ARGININE DECARBOXYLASE; CARBOXYLYASE; COMPLEMENTARY DNA; DREB1A PROTEIN, ARABIDOPSIS; SPERMIDINE; SPERMIDINE SYNTHASE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; COLD; ENVIRONMENTAL EXPOSURE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC PLANT; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBOXY-LYASES; COLD; DNA, COMPLEMENTARY; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION REGULATION, PLANT; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; SPERMIDINE; SPERMIDINE SYNTHASE; TRANSCRIPTION FACTORS; TRANSFECTION; TRANSGENES; UP-REGULATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA OLERACEA VAR. BOTRYTIS; CAULIFLOWER MOSAIC VIRUS; CUCURBITA; CUCURBITA FICIFOLIA; EMBRYOPHYTA;

EID: 3142567130     PISSN: 00320781     EISSN: None     Source Type: Journal    
DOI: 10.1093/pcp/pch083     Document Type: Article

References (62)

1. Allen, R.D. (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol. 107: 1049-1054.
2. Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol. 24: 1-15.
3. Aziz, A., Martin-Tanguy, J. and Larher, F. (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol. Plant. 104: 195-202.
4. Bagni, N. and Tassoni, A. (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20: 301-317.
5. Berger, S. (2002) Jasmonate-related mutants of Arabidopsis as tools for studying stress signaling. Planta 214: 497-504.
6. Besford, R.T., Richardson, C.M., Campos, J.L. and Tiburcio, A.F. (1993) Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189: 201-206.
7. Biondi, S., Scoccianti, V., Scaramagli, S., Ziosi, V. and Torrigiani, P. (2003) Auxin and cytokinin modify methyl jasmonate effects on polyamine metabolism and ethylene biosynthesis in tobacco leaf discs. Plant Sci. 165: 95-101.
8. Bouchereau, A., Aziz, A., Larher, F. and Martin-Tanguy, J. (1999) Polyamines and environmental challenges: recent development. Plant Sci. 140: 103-125.
9. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
10. Bundock, P.C., Christopher, J.T., Eggler, P., Ablett, G., Henry, R.J. and Holton, T.A. (2003) Single nucleotide polymorphisms in cytochrome P450 genes from barley. Theor. Appl. Genet. 106: 676-682.
11. Calderbank, A. (1968) The bipyridylium herbicides. Adv. Pest Cont. Res. 8: 127-235.
12. Childs, A.C., Mehta, D.J. and Gerner, E.W. (2003) Polyamine-dependent gene expression. Cell. Mol. Life Sci. 60: 1394-1406.
13. De Agazio, M., Zacchini, M., Federico, R. and Grego, S. (1995) Putrescine accumulation in maize roots treated with spermidine: evidence for spermidine to putrescine conversion. Plant Sci. 111: 181-185.
14. Groppa, M.D., Tomaro, M.L. and Benavides, M.P. (2001) Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci. 161: 481-488.
15. Gupta, S., Chattopadhyay, M.K., Chatterjee, P., Ghosh, B. and SenGupta, D.N. (1998) Expression of abscisic acid-responsive element-binding protein in salt-tolerant indica rice (Oryza sativa L. cv. Pokkali). Plant Mol. Biol. 37: 629-637.
16. Hanfrey, C., Sommer, S., Mayer, M.J., Burtin, M.D. and Michael, A.J. (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J. 27: 551-560.
17. Hashimoto, T., Tamaki, K., Suzuki, K. and Yamada, Y. (1998) Molecular cloning of plant spermidine synthase. Plant Cell Physiol. 39: 73-79.
18. He, L., Nada, K., Kasukabe, Y. and Tachibana, S. (2002) Enhanced susceptibility of photosynthesis to low-temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxylase activity in leaves of spinach (Spinacia oleracea L.). Plant Cell Physiol. 43: 196-206.
19. Holmberg, N. and Bülow, L. (1998) Improving stress tolerance in plants by gene transfer. Trends Plant Sci. 3: 61-66.
20. Hughes, T.R., Mao, M., Jones, A.R., Burchard, J. Linsley, P.S., et al. (2001) Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat. Biolechnol. 19: 342-347.
21. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O. and Thomashow, M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280: 104-106.
22. Kakkar, R.K., Nagar, P.K., Ahuja, P.S. and Rai, V.K. (2000) Polyamines and plant morphogenesis. Biol. Plant. 43: 1-11.
23. Kalde, M., Barth, M., Somssich, I.E. and Lippok, B. (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol. Plant-Microbe Interact. 16: 295-305.
24. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17: 287-291.
25. Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T., Wang, X. and Harper, J.F. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130: 2129-2141.
26. Krishnamurthy, R. and Bhagwat, K.A. (1989) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol. 91: 500-504.
27. Kumar, A., Altabella, T., Taylor, M.A. and Tiburcio, A.F. (1997) Recent advances in polyamine research. Trends Plant Sci. 2: 124-130.
28. Kumria, R. and Rajam, M.V. (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro-morphogenesis and response to salt stress. J. Plant Physiol. 159: 983-990.
29. Kurepa, J., Smalle, J., Montagu, M.V. and Inzé. D. (1998) Polyamines and paraquat toxicity in Arabidopsis thaliana. Plant Cell Physiol. 39: 987-992.
30. Laemmli, N.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
31. Langebartels, C., Kerner, K., Leonardi, S., Schraudner, M., Trost, M., Heller, W. and Sandermann, H. Jr, (1991) Biochemical plant responses to ozone. 1. Differential induction of polyamine and ethylene biosynthesis in tobacco. Plum Physiol. 95: 882-889.
32. Lee, T.M., Lur, H.S. and Chu, C. (1997) Role of abscisic acid in chilling tolerance of rice (Oryza sativa L.) seedlings. 2. Modulation of free polyamine levels. Plant Sci. 126: 1-10.
33. Li, Z.Y. and Chen, S.Y. (2000) Differential accumulation of the S-adenosylmethionine decarboxylase transcript in rice seedlings in response to salt and drought stress. Theor. Appl. Genet. 100: 782-788.
34. Løvaas, E. (1991) Antioxidative effects of polyamines. J. Amer. Oil Chem. Soc. 68: 353-358.
35. Mader, J.C. (1997) Effects of jasmonic acid, silver nitrate and L-AOPP on the distribution of free and conjugated polyamines in roots and shoots of S. tuberosus in vitro. J. Plant Physiol. 154: 79-88.
36. Malan, C., Greyling, M.M. and Gressel, J. (1990) Correlation between CuZn superoxide dismutase and glutathione reductase, and environmental and xenobiotic stress tolerance in maize inbreds. Plant Sci. 69: 157-166.
37. Malmberg, R.L., Watson, M.B., Galloway, G.L. and Yu, W. (1998) Molecular genetic analyses of plant polyamines. Crit. Rev. Plant Sci. 17: 199-224.
38. Martin-Tanguy, J. (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul. 100: 675-688.
39. Martínez-Téllez, M.A., Ramos-Clamont, M.G., Gardea A.A. and Vargas-Arispuro, I. (2002) Effect of infiltrated polyamines on polygalacturonase activity and injury responses in zucchini squash (Cucurbita pepo L.). Biochim. Biophys. Res. Commun. 295: 98-101.
40. Masgrau, C., Altabella, T., Farrás, R., Flores, D., Thompson, A.J., Besford, R.T. and Tiburcio, A.F. (1997) Inducible overexpression of oat arginine decarboxylase in transgenic tobacco plants. Plant J. 11: 465-473.
41. Mehta, R.A., Cassol, T., Li, N., Ali, N., Handa, A.K. and Mattoo, A.K. (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nat. Biotechnol. 20: 613-618.
42. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
43. Murata, N., Ishizaki-Nishizawa, O., Higashi, S., Hayashi, H., Takase, Y. and Nishida, I. (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356: 710-713.
44. Nada, K., Iwatani, E., Doi, T. and Tachibana, S. (2004) Effect of putrescine pretreatment to roots on growth and lactate metabolism in the roots of tomato (Lycopersicon esculentum Mill.) under root-zone hypoxia. J. Japan. Soc. Hort. Sci. 74: (In press)
45. Panagiotidis, C.A., Artandi, S., Calame, K. and Silverstein, S.J. (1995) Polyamines alter sequence-specific DNA-protein interaction. Nucleic Acids Res. 23: 1800-1809.
46. Rizhsky, L., Liang, H. and Mittler, R. (2002) The combined effect of drought and heat shock on gene expression in tobacco. Plant Physiol. 130: 1143-1151.
47. Roberts, D.R., Dumbroff, E.B. and Thompson, J.E. (1986) Exogenous polyamines alter membrane fluidity in bean leaves - a basis for potential misinterpretation of their true physiological role. Planta 167: 395-401.
48. Roy, M. and Ghosh, B. (1996) Polyamines, both common and uncommon, under heat stress in rice (Oryza sativa) callus. Physiol. Plant. 98: 196-200.
49. Roy, M. and Wu, R. (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci. 160: 869-875.
50. Roy, M. and Wu, R. (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci. 163: 987-992.
51. 2+-dependent protein kinase confers both cold and salt/ drought tolerance on rice plants. Plant J. 23: 319-327.
52. Shen, W., Nada, K. and Tachibana, S. (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol. 124: 431-439.
53. Shinozaki, K. and Yamaguchi-Shinozaki, K. (2000) Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3: 217-223.
54. Song, J., Nada, K. and Tachibana, S. (2002) Suppression of S-adenosylmethionine decarboxylase activity is a major cause for high-temperature inhibition of pollen germination and tube growth in tomato (Lycopersicon esculentum Mill.). Plant Cell Physiol. 43: 619-627.
55. Sudha, G. and Ravishankar, G.A. (2002) Involvement and interaction of various signaling compounds on the plant metabolic events during defense responses, resistance to stress factors, formation of secondary metabolites and their molecular aspects. Plant Cell Tiss. Org. Cult. 71: 181-212.
56. Thomashow, M.F., Gilmour, S.J., Stockinger, E.J., Jaglo-Ottosen, K.R. and Zarka, D.G. (2001) Role of the Arabidopsis CBF transcriptional activators in cold acclimation. Pliysiol. Plant. 112: 171-175.
57. Waie, B. and Rajam, M.V. (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci. 164: 727-734.
58. Yamaguchi-Shinozaki, K. and Shinozaki, K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 252-264.
59. Ye, G.N., Stone, D., Pang, S.Z., Creely, W., Gonzalez, K. and Hinchee, M. (1999) Arabidopsis ovule is the target for Agrobacterium in plant vacuum infiltration transformation. Plant J. 19: 249-257.
60. Yoon, S.O., Lee, Y.S., Lee, S.H. and Cho, Y.D. (2000) Polyamine synthesis in plants: isolation and characterization of spermidine synthase from soybean (Glycine max) axes. Biochim. Biophys. Acta 1475: 17-26.
61. Yoshida, R., Hobo, T., Ichimura, K., Mizoguchi, T., Takahashi, F., Aronso, J., Ecker, J.R. and Shinozaki, K. (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 43: 1473-1483.
62. Yoshida, I., Yamagata, H. and Hirasawa, E. (1999) Blue- and red-light regulation and circadian control of gene expression of S-adenosylmethionine decarboxylase in Pharbitis nil. J. Exp. Bot. 50: 319-326.