Polyamines and stress: Biological role, metabolism, and regulation

  • Vl. V. Kuznetsov
  • N. L. Radyukina
  • N. I. Shevyakova


In this review, we consider recent advances in the study of the multifaceted biological role of polyamines, primarily under stress conditions, discuss molecular mechanisms controlling their anabolism, catabolism, and transport, and also the regulation of gene expression for key enzymes of their biosynthesis and degradation. To understand the place and role of polyamines in plant adaptation, we focus the data concerning gene expression obtained by modern physicochemical methods on mutant and transgenic plants and also on natural stress-tolerant species manifesting a high tolerance to salinity, drought, and other abiotic factors.

Key words

plant putrescine spermidine spermine cadaverine metabolism genes regulation stress 



aminocyclopropan-1-carboxylic acid


arginine decarboxylase




diamine oxidase




γ-aminobutyric acid


heat shock


ornithine decarboxylase




lysine decarboxylase


polyamine oxidase


putrescine aminopropyltransferase (spermidine synthase)






S-adenosylmethionine decarboxylase


spermidine aminopropyltransferase (spermine synthase)


superoxide dismutase






  1. 1.
    Galston, A.W., Kaur-Sawhney, R., Atabella, T., and Tiburcio, A.F., Plant Polyamines in Reproductive Activity and Response to Abiotic Stress, Bot. Acta, 1997, vol. 110, pp. 197–207.Google Scholar
  2. 2.
    Walden, R., Cordeiro, A., and Tiburcio, A.F., Polyamines: Small Molecules Triggering Pathways in Plant Growth and Development, Plant Physiol., 1997, vol. 113, pp. 1009–1013.PubMedCrossRefGoogle Scholar
  3. 3.
    Bouchereau, A., Aziz, A., Larher, F., and Martin-Tanguy, J., Polyamines and Environmental Challenges: Recent Development, Plant Sci., 1999, vol. 140, pp. 103–125.CrossRefGoogle Scholar
  4. 4.
    Kaur-Sawhney, R., Tiburcio, A.F., Atabella, T., and Galston, A.W., Polyamines in Plants: An Overview, J. Cell Mol. Biol., 2003, vol. 2, pp. 1–12.Google Scholar
  5. 5.
    Bhatnagar, P., Glasheen, B.M., Bains, S.K., Long, S.L., Minocha, R., Walter, C., and Minocha, S.C., Transgenic Manipulation of the Metabolism of Polyamines in Poplar Cells, Plant Physiol., 2001, vol. 125, pp. 2139–2153.PubMedCrossRefGoogle Scholar
  6. 6.
    Bagni, N. and Tassoni, A., Biosynthesis, Oxidation and Conjugation of Aliphatic Polyamines in Higher Plants, Amino Acids, 2001, vol. 20, pp. 301–317.PubMedCrossRefGoogle Scholar
  7. 7.
    Kumar, A., Atabella, T., Taylor, M.A., and Tiburcio, A.E., Recent Advances in Polyamine Research, Trends Plant Sci., 1997, vol. 2, pp. 124–130.CrossRefGoogle Scholar
  8. 8.
    Borrel, A., Culianez-Macia, A., Atabella, T., Besford, R.T., Flores, D., and Tiburcio, A.F., Arginine Decarboxylase Is Localized in Chloroplasts, Plant Physiol., 1995, vol. 109, pp. 771–776.Google Scholar
  9. 9.
    Bortolotti, C., Cordeiro, A., Alcázar, R., Borrell, A., Culiañez-Macià, F.A., Tiburcio, A.F., and Atabella, T., Localization of Arginine Decarboxylase in Tobacco Plants, Physiol. Plant., 2004, vol. 120, pp. 84–92.PubMedCrossRefGoogle Scholar
  10. 10.
    Paschalidis, K.A. and Roubelakis-Angelakis, K.A., Spatial and Temporal Distribution of Polyamine Levels and Polyamine Anabolism in Different Organs/Tissues of Tobacco Plants. Correlations with Age, Cell Division/Expansion, and Differentiation, Plant Physiol., 2005, vol. 138, pp. 142–152.PubMedCrossRefGoogle Scholar
  11. 11.
    Erdei, L., Szegletes, Z., Barabas, K., and Pestenacz, A., Responses in Polyamine Titer under Osmotic and Salt Stress in Sorghum and Maize Seedlings, J. Plant Physiol., 1996, vol. 147, pp. 599–603.Google Scholar
  12. 12.
    Basu, R., Maitra, N., and Ghosh, B., Salinity Results in Polyamine Accumulation in Early Rice (Oryza sativa) Seedlings, Aust. J. Plant Physiol., 1998, vol. 15, pp. 777–786.Google Scholar
  13. 13.
    Shevyakova, N.I., Kir’yan, I.G., and Strogonov, B.P., An Increased Rate of Spermidine Synthesis in NaCl-Resistant Cell Culture of Nicotiana sylvestris, Fiziol. Rast. (Moscow), 1984, vol. 31, pp. 810–816 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  14. 14.
    Tiburcio, A.F., Besford, R.T., Capell, T., Borell, A., Testillano, P.S., and Risueño, M.C., Mechanisms of Polyamine Action during Senescence Responses Induced by Osmotic Stress, J. Exp. Bot., 1994, vol. 45, pp. 1789–1800.Google Scholar
  15. 15.
    Bertoldi, D., Tassoni, A., Martinelli, L., and Bagni, N., Polyamine and Somatic Embryogenesis in Two Vitis vinifera Cultivars, Physiol. Plant., 2004, vol. 120, pp. 657–666.PubMedCrossRefGoogle Scholar
  16. 16.
    Yoo, T.H., Park, C.-J., Ham, B.-K., Kim, K.-J., and Paek, K.-H., Ornithine Decarboxylase Gene (CaODC1) Is Specifically Induced during TMV-Mediated but Salicylate-Independent Resistant Response in Hot Pepper, Plant Cell Physiol., 2004, vol. 45, pp. 1537–1542.PubMedCrossRefGoogle Scholar
  17. 17.
    Kakkar, R.K. and Sawney, V.K., Polyamine Research in Plants — a Changing Perspective, Physiol. Plant., 2002, vol. 116, pp. 281–292.CrossRefGoogle Scholar
  18. 18.
    Slocum, R.D., Tissue and Subcellular Localization of Polyamines and Enzymes of Polyamine Metabolism, Biochemistry and Physiology of Polyamines in Plants, Slocum, R.D. and Flores, H.E., Eds., Boca Raton (FL): CRC, 1991, pp. 93–103.Google Scholar
  19. 19.
    Tiburcio, A.F., Atabella, T., Borell, A., and Masgrau, C., Polyamine Metabolism and Its Regulation, Physiol. Plant., 1997, vol. 100, pp. 664–674.CrossRefGoogle Scholar
  20. 20.
    Legocka, J. and Zaichert, J., Role of Spermidine in the Stabilization of Apoprotein of the Light-Harvesting Chlorophyll a/b-Protein Complex of Photosystem II during Leaf Senescence Process, Acta Physiol. Plant., 1999, vol. 21, pp. 127–137.Google Scholar
  21. 21.
    Besford, R.T., Richardson, C.M., Campos, J.L., and Tiburcio, A.F., Effect of Polyamines on Stabilization of Molecular Complexes of Thylakoid Membranes of Osmotically Stressed Oat Leaves, Planta, 1993, vol. 189, pp. 201–206.CrossRefGoogle Scholar
  22. 22.
    Bagni, N., Torrigiani, P.A., and Barbieri, P., Effect of Various Inhibitors of Polyamine Synthesis on the Growth of Helianthus tuberosus, Med. Biol., 1981, vol. 59, pp. 403–406.PubMedGoogle Scholar
  23. 23.
    Espartero, J., Pintor-Toro, J.A., and Pardo, J.N., Differential Accumulation of S-Adenosylmethionine Synthase Transcripts in Response to Salt Stress, Plant Mol. Biol., 1994, vol. 25, pp. 217–227.PubMedCrossRefGoogle Scholar
  24. 24.
    Hirasawa, E. and Suzuki, Y., Biosynthesis of Spermidine in Maize Seedlings, Phytochemistry, 1983, vol. 22, pp. 103–106.CrossRefGoogle Scholar
  25. 25.
    Yamanoha, B. and Cohen, S.S., S-Adenosylmethionine Decarboxylase and Spermidine Synthase from Chinese Cabbage, Plant Physiol., 1985, vol. 78, pp. 784–790.PubMedGoogle Scholar
  26. 26.
    Terui, Y., Osnuma, M., Hiraga, K., Kawashima, E., and Oshima, T., Stabilization of Nucleic Acids by Unusual Polyamines Produced by an Extreme Thermophile, Thermus thermophilus, Biochem. J. Immediate Publ., 2005, Doi.V.10.1042/BJ20041778.Google Scholar
  27. 27.
    Matsazaki, S., Hamana, K., and Isobe, K., Occurrence of N6-Methylagmatine in Seeds of Leguminosae Plants, Phytochemistry, 1990, vol. 29, pp. 1313–1315.CrossRefGoogle Scholar
  28. 28.
    Roy, M. and Ghosh, B., Polyamines, Both Common and Uncommon, under Heat Stress in Rice (Oryza sativa) Callus, Physiol. Plant., 1996, vol. 98, pp. 196–200.CrossRefGoogle Scholar
  29. 29.
    Kuehn, G.D., Bagga, S., and Rodriguez-Garay, A.C., Biosynthesis of Uncommon Polyamines in Higher Plants and Their Relation to Abiotic Stress Responses, Polyamines and Ethylene: Biosynthesis, Physiology and Interactions, Flores, H.E., Arteca, R.N., and Shannon, J.C., Eds., Rockville: American Society of Plant Physiologists, 1990, pp. 190–202.Google Scholar
  30. 30.
    Bagga, S., Rochford, J., Klaene, Z., Kuehn, C.D., and Phillips, G.C., Putrescine Aminopropyltransferase Is Responsible for Biosynthesis of Spermidine, Spermine and Multiple Uncommon Polyamines in Osmotic Stress-Tolerant Alfalfa, Plant Physiol., 1997, vol. 114, pp. 445–454.PubMedGoogle Scholar
  31. 31.
    Kuehn, G.D., Rodriquez-Garay, B., Bagga, S., and Phillips, G.C., Novel Occurrence of Uncommon Polyamines in Higher Plants, Plant Physiol., 1990, vol. 92, pp. 88–96.PubMedGoogle Scholar
  32. 32.
    Srere, P.A., Complexes of Sequential Metabolic Enzymes, Annu. Rev. Biochem., 1987, vol. 56, pp. 89–124.PubMedCrossRefGoogle Scholar
  33. 33.
    Abadjieva, A., Pauwels, K., Hilven, P.A., and Crabeel, M.A., A New Yeast Metabolon Involving at Least the Two First Enzymes of Arginine Biosynthesis, J. Biol. Chem., 2001, vol. 276, pp. 42 869–42 880.CrossRefGoogle Scholar
  34. 34.
    Shevyakova, N.I. and Kir’yan, I.G., Regulation of Methionine Biosynthesis in Salt-Resistant Cells of Nicotiana sylvestris L., Fiziol. Rast. (Moscow), 1995, vol. 42, pp. 94–99 (Russ. J. Plant Physiol., Engl. Transl., pp. 82–87).Google Scholar
  35. 35.
    Smith, T.A. and Wilshire, G., Distribution of Cadaverine and Other Amines in Higher Plants, Phytochemistry, 1975, vol. 14, pp. 2341–2346.CrossRefGoogle Scholar
  36. 36.
    Aziz, A., Martintanguy, J., and Larher, F., Plasticity of Polyamine Metabolism Associated with High Osmotic-Stress in Rape Leaf Discs and with Ethylene Treatment, Plant Growth Regul., 1997, vol. 21, pp. 153–163.CrossRefGoogle Scholar
  37. 37.
    Shevyakova, N.I., Rakitin, V.Yu., Duong, D.B., Sadomov, N.G., and Kuznetsov, V.V., Heat Shock-Induced Cadaverine Accumulation and Translocation throughout the Plant, Plant Sci., 2001, vol. 161, pp. 1125–1133.CrossRefGoogle Scholar
  38. 38.
    Kuznetsov, Vl.V., Rakitin, V.Yu., Sadomov, N.G., Dam, D.V., Stetsenko, L.A., and Shevyakova, N.I., Do Polyamines Participate in the Long-Distance Translocation of Stress Signals in Plants? Fiziol. Rast. (Moscow), 2002, vol. 49, pp. 136–147 (Russ. J. Plant Physiol., Engl. Transl., pp. 120–130).Google Scholar
  39. 39.
    Borrell, A., Carbonell, L., Farrás, R., Puig-Parellada, P., and Tiburcio, A.F., Polyamines Inhibit Lipid Peroxidation in Senescing Oat Leaves, Physiol. Plant., 1997, vol. 99, pp. 385–390.CrossRefGoogle Scholar
  40. 40.
    Herminghaus, S., Schreier, P.H., McCarthy, J.E.G., Landsmann, J., Botterma, J., and Berlin, J., Expression of Bacterial Lysine Decarboxylase Gene and Transport of the Protein into Chloroplasts of Transgenic Tobacco, Plant Mol. Biol., 1991, vol. 17, pp. 475–486.PubMedCrossRefGoogle Scholar
  41. 41.
    Friedman, R., Altman, A., and Levin, N., The Effect of Salt Stress on Polyamine Biosynthesis and Content in Mung Bean Plants and in Halophytes, Physiol. Plant., 1989, vol. 76, pp. 295–302.Google Scholar
  42. 42.
    Fecker, L.F., Hillebrandt, S., Rügenhagen, C., Hermingaus, S., Landsmann, J., and Berlin, J., Metabolic Effect of a Bacterial Lysine Decarboxylase Gene Expressed in Hairy Root Culture of Nicotiana glauca, Biotech. Lett., 1992, vol. 14, pp. 1035–1040.CrossRefGoogle Scholar
  43. 43.
    Xiong, H., Stanley, B.A., Tekwani, B.L., and Pegg, A.E., Processing of Mammalian and Plant S-Adenosylmethionine Decarboxylase Proenzymes, J. Biol. Chem., 1997, vol. 272, pp. 28 342–28 348.Google Scholar
  44. 44.
    Watson, M.B. and Malmberg, R.L., Post-Translational Regulation of Arabidopsis Arginine Decarboxylase in Response to Potassium-Deficiency Stress, Plant Physiol., 1996, vol. 111, pp. 1077–1083.PubMedCrossRefGoogle Scholar
  45. 45.
    Borrell, A., Besford, R.T., Altabella, T., Masgrau, C., and Tiburcio, A.F., Regulation of Arginine Decarboxylase by Spermine in Osmotically-Stressed Oat Leaves, Physiol. Plant., 1996, vol. 98, pp. 105–110.CrossRefGoogle Scholar
  46. 46.
    Nam, K.H., Lee, S.H., and Lee, J.H., The Purification and Characterization of Arginine Decarboxylase from Soybean (Glycine max) Hypocotyls, Plant Cell Physiol., 1997, vol. 38, pp. 1150–1155.PubMedGoogle Scholar
  47. 47.
    Hanfrey, C., Sommer, S., Mayer, M.J., Burtin, D., and Michael, A.J., Arabidopsis Polyamine Biosynthesis: Absence of Ornithine Decarboxylase and the Mechanism of Arginine Decarboxylase Activity, Plant J., 2001, vol. 27, pp. 551–560.PubMedCrossRefGoogle Scholar
  48. 48.
    Galloway, G.L., Malmberg, R.L., and Price, R.A., Phylogenetic Utility of the Nuclear Gene of the Arginine Decarboxylase: An Example from Brassicaceae, Mol. Biol. Evol., 1998, vol. 15, pp. 1312–1320.PubMedGoogle Scholar
  49. 49.
    Perez-Amador, M.A., Leon, J., Greem, P.J., and Carbonell, J., Induction of the Arginine Decarboxylase ADC2 Gene Provides Evidence for the Involvement of Polyamines in the Wound Response in Arabidopsis, Plant Physiol., 2002, vol. 130, pp. 1454–1463.PubMedCrossRefGoogle Scholar
  50. 50.
    Smith, T.A., Polyamines, Annu. Rev. Plant Physiol., 1985, vol. 36, pp. 117–143.CrossRefGoogle Scholar
  51. 51.
    Angelini, R. and Federico, R., Histochemical Evidence of Polyamine Oxidation and Generation of Hydrogen Peroxide in Cell Wall, J. Plant Physiol., 1990, vol. 135, pp. 212–217.Google Scholar
  52. 52.
    Scoccianti, V., Torrigiani, P., and Bagni, N., Occurrence of Diamine Oxidase Activity in Protoplasts and Isolated Mitochondria of Helianthus tuberosus Tuber, J. Plant Physiol., 1991, vol. 138, pp. 752–756.Google Scholar
  53. 53.
    McGuirl, M.A., McCahon, C.D., McKeown, K.A., and Dooley, D.M., Purification and Characterization of Pea Seedling Amino Oxidase for Crystallization Studies, Plant Physiol., 1994, vol. 106, pp. 1205–1211.PubMedCrossRefGoogle Scholar
  54. 54.
    Tipping, A.J. and McPherson, M.J., Cloning and Molecular Analysis of the Pea Seedling Copper Amine Oxidase, J. Biol. Chem., 1995, vol. 270, pp. 16939–16946.PubMedCrossRefGoogle Scholar
  55. 55.
    Turano, F.J. and Kramer, G.F., Effect of Metabolic Intermediates on the Accumulation of Polyamines in Detached Soybean Leaves, Phytochemistry, 1993, vol. 34, pp. 959–968.CrossRefGoogle Scholar
  56. 56.
    Duhazé, C., Gouzerh, G., Gagneul, D., Larher, F., and Bouchereau, A., The Conversion of Spermidine to Putrescine and 1,3-Diaminopropane in the Roots of Limonium tataricum, Plant Sci., 2002, vol. 163, pp. 639–646.CrossRefGoogle Scholar
  57. 57.
    Pistocchi, R., Keller, F., Bagni, N., and Matile, P., Transport and Subcellular Localization of Polyamines in Carrot Protoplasts and Vacuoles, Plant Physiol., 1988, vol. 87, pp. 514–518.PubMedGoogle Scholar
  58. 58.
    Friedman, R., Levin, N., and Altman, A., Presence and Identification of Polyamines in Xylem and Phloem Exudates of Plants, Plant Physiol., 1986, vol. 86, pp. 1154–1157.Google Scholar
  59. 59.
    Yokota, T., Nakayama, M., Harasawa, J., Sato, M., Katsuhara, M., and Kawabe, S., Polyamines, Indole-3-Acetic Acid and Abscisic Acid in Rice Phloem Sap, Plant Growth Regul., 1994, vol. 15, pp. 125–128.CrossRefGoogle Scholar
  60. 60.
    Escribano, M.J., Aguado, P., Reguera, R.M., and Merido, C., Conjugated Polyamine Levels and Putrescine Synthesis in Cherimoya Fruits during Storage at Different Temperatures, J. Plant Physiol., 1996, vol. 147, pp. 736–742.Google Scholar
  61. 61.
    Pistocchi, R., Kashiwagi, K., Miyamoto, S., Nukii, E., Sadakata, Y., Kobayashi, H., and Igarashi, K., Characteristics of the Operon for a Putrescine Transport System That Maps at 19 Minutes on the Esherichia coli Chromosome, J. Biol. Chem., 1993, vol. 268, pp. 146–152.PubMedGoogle Scholar
  62. 62.
    Kashiwagi, K., Kiraishi, A., Tomitory, H., Igarashi, A., Nishimura, K., Shirahata, A., and Igarashi, K., Identification of the Putrescine Recognition Site on Polyamine Transport Protein PotE, J. Biol. Chem., 2000, vol. 275, pp. 36 007–36 012.CrossRefGoogle Scholar
  63. 63.
    Uemura, T., Tachihara, K., Tomitori, H., Kashiwagi, K., and Igarashi, K., Characteristics of the Polyamine Transporter TRO1 and Regulation of Its Activity and Cellular Localization by Phosphorylation, J. Biol. Chem., 2005, vol. 280, pp. 9646–9652.PubMedCrossRefGoogle Scholar
  64. 64.
    Tachihara, K., Uemura, T., Kashiwagi, K., and Igarashi, K., Excretion of Putrescine and Spermidine by the Protein Encoded by YKL174c (TPO5) in Saccharomyces cerevisiae, J. Biol. Chem., 2005, vol. 280, pp. 12637–12642.PubMedCrossRefGoogle Scholar
  65. 65.
    Aouida, M., Leduc, A., Poulin, R., and Ramotar, D., AGR2 Encodes the Major Permease for High Affinity Polyamine Import in Saccharomyces cerevisiae, J. Biol. Chem., 2005, vol. 280, abst.Google Scholar
  66. 66.
    Tomitori, H., Kashiwagi, K., Sakata, K., Kakinuma, Y., and Igarashi, K., Identification of a Gene for Polyamine Transport Protein in Yeast, J. Biol. Chem., 1999, vol. 274, pp. 3265–3267.PubMedCrossRefGoogle Scholar
  67. 67.
    Bagni, N. and Pistocchi, R., Binding, Transport, and Subcellular Compartmentation of Polyamines, Polyamines and Ethylene Biochemistry, Physiology, and Interactions, Flores, H.E., Arteca, R.N., and Shannon, J.C., Eds., Rockville: American Society of Plant Physiologists, 1990, pp. 62–72.Google Scholar
  68. 68.
    Di Tomaso, J.M., Hart, J.J., and Kochian, L.V., Transport Kinetics and Metabolism of Exogenously Applied Putrescine in Roots of Intact Maize Seedlings, Plant Physiol., 1992, vol. 98, pp. 611–620.Google Scholar
  69. 69.
    Tassoni, A., Antognoni, F., Battistini, M.L., Sanvido, O.A., and Bagni, N., Characterization of Spermidine Binding to Solubilized Plasma Membrane Proteins from Zucchini Hypocotyls, Plant Physiol., 1998, vol. 117, pp. 971–977.PubMedCrossRefGoogle Scholar
  70. 70.
    Tassoni, A., Napier, R.M., Francescheti, M., Venis, M.A., and Bagni, N., Spermidine-Binding Proteins, Purification and Expression Analysis in Maize, Plant Physiol., 2002, vol. 128, pp. 1303–1312.PubMedCrossRefGoogle Scholar
  71. 71.
    Minocha, R., Minocha, S.C., and Long, S., Polyamines and Their Biosynthetic Enzymes during Somatic Embryo Development in Red Spruce (Picea rubens Sarg.), In Vitro Cellular Dev. Biol., 2004, vol. 40, pp. 572–580.CrossRefGoogle Scholar
  72. 72.
    Martin-Tanguy, J., Metabolism and Function of Polyamines in Plants: Recent Development (New Approaches), Plant Growth Regul., 2001, vol. 34, pp. 135–148.CrossRefGoogle Scholar
  73. 73.
    Trull, M.C., Holaway, B.L., and Malmberg, R.L., Development of Stigmatoid Anthers in a Tobacco Mutant-Implications for Regulation of Stigma Differentiation, Can. J. Bot., 1992, vol. 70, pp. 2339–2346.Google Scholar
  74. 74.
    De Scenzo, R.A. and Minochas, C., Modulation of Cellular Polyamines in Tobacco by Transfer and Expression of Mouse Ornithine Decarboxylase cDNA, Plant. Mol. Biol., 1993, vol. 22, pp. 113–127.CrossRefGoogle Scholar
  75. 75.
    Hamill, J.D., Robins, R.J., Parr, A.J., Evans, D.M., Furze, J.M., and Rhodes, M.J.C., Over-Expressing a Yeast Ornithine Decarboxylase Gene in Transgenic Roots of Nicotiana rustica Can Lead to Enhanced Nicotine Accumulation, Plant Mol. Biol., 1990, vol. 15, pp. 27–38.PubMedCrossRefGoogle Scholar
  76. 76.
    Imai, A., Matsuyama, T., Hanzawa, Y., Akiyama, T., Tamaoki, M., Saji, H., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., Tabata, S., Komeda, Y., and Takahashi, T., Spermidine Synthase Genes Are Essential for Survival of Arabidopsis, Plant Physiol., 2004, vol. 135, pp. 1565–1573.PubMedCrossRefGoogle Scholar
  77. 77.
    Bastola, D.R. and Minocha, S.C., Increased Putrescine Biosynthesis through Transfer of Mouse Ornithine Decarboxylase cDNA in Carrot Promotes Somatic Embryogenesis, Plant Physiol., 1995, vol. 109, pp. 63–71.PubMedGoogle Scholar
  78. 78.
    Roy, M. and Wu, R., Arginine Decarboxylase Transgene Expression and Analysis of Environmental Stress Tolerance in Transgenic Rice, Plant Sci., 2001, vol. 160, pp. 869–875.PubMedCrossRefGoogle Scholar
  79. 79.
    Masgrau, C., Altabella, T., Farras, R., Flores, D., Thompson, A.J., Besford, R.T., and Tiburcio, A.F., Inducible Overexpression of Oat Arginine Decarboxylase in Transgenic Tobacco Plants, Plant J., 1997, vol. 11, pp. 465–473.PubMedCrossRefGoogle Scholar
  80. 80.
    Seiler, N., Delcros, J.G., and Moulinoux, J.P., Polyamine Transport in Mammalian Cells: An Update, Int. J. Biochem. Cell Biol., 1996, vol. 28, pp. 843–861.PubMedCrossRefGoogle Scholar
  81. 81.
    Mehta, R.A., Cassol, T., Li, N., Ali, N., Handa, A.K., and Mattoo, A.K., Engineered Polyamine Accumulation in Tomato Enhances Phytonutrient Content, Juice Quality and Vine Life, Nat. Biotech., 2002, vol. 20, pp. 613–618.CrossRefGoogle Scholar
  82. 82.
    Bracale, M., Levi, M., Savini, C., Dicarato, N., and Galli, M.G., Water Deficit in Pea Root Tips: Effects on the Cell Cycle and on Production of Dehydrin-Like Proteins, Ann. Bot., 1997, vol. 79, pp. 593–600.CrossRefGoogle Scholar
  83. 83.
    Strogonov, B.P., Kabanov, V.V., Shevyakova, N.I., Lapina, L.P., Komizerko, E.I., Popov, V.A., Dostanova, R.Kh., and Prikhod’ko, L.S., Struktura i funktsii kletok rastenii pri zasolenii (Structure and Functions of Plant Cells under Salt Stress), Moscow: Nauka, 1970.Google Scholar
  84. 84.
    Shevyakova, N.I., Strogonov, B.P., Kiryan, I.G., and Vasilyev, S.V., Polyamines and the Adaptation of Plants to Salt Stress, Recent Progress in Polyamine Research, Selmeci, L., Brosnan, M.E., and Seiler, N., Eds., Budapest, 1985, pp. 537–544.Google Scholar
  85. 85.
    Tofilon, P.J., Oredsson, S.M., Deen, D.F., and Marton, L.J., Polyamine Depletion Influences Drug-Induced Chromosomal Damage, Science, 1982, vol. 217, pp. 1044–1046.PubMedGoogle Scholar
  86. 86.
    Thomas, T. and Thomas, T.J., Polyamine Metabolism and Cancer, J. Cell Mol. Med., 2003, vol. 7, pp. 113–126.PubMedGoogle Scholar
  87. 87.
    Lindemose, S., Nielson, P.E., and Møllegaard, N.E., Polyamines Preferentially Interact with Bent Adenine Tracts in Double-Stranded DNA, Nucleic Acids Res., 2005, vol. 33, pp. 1790–1803.PubMedCrossRefGoogle Scholar
  88. 88.
    Cohen, S., The Enlarging Interest to Polyamine Studies, Abst. Int. Symp. Polyamines in Molecular and Medical Biology, Kyoto (Japan), 1990, p. 18.Google Scholar
  89. 89.
    Speranza, A. and Bagni, N., Putrescine Biosynthesis in Agrobacterium tumefaciens and in Normal and Crown Gall Tissues of Scorzonera hispanica L., Z. Pflanzenphysiol., 1976, vol. 81, pp. 226–233.Google Scholar
  90. 90.
    Hemerly, A., Eugler, J.A., Bergounioux, C., van Montagu, M., Engler, G., Inze, D., and Ferriera, P., Dominant Negative Mutants of the cdc2 Kinase Uncouple Cell Division from Iterative Plant Development, EMBO J., 1995, vol. 14, pp. 3925–3936.PubMedGoogle Scholar
  91. 91.
    Schuppler, U., Pe, P.H., John, P.C.C., and Munns, P., Effect of Water-Stress on Cell Division and Cell-Division Cycle 2-Like Cell-Cycle Kinase Activity in Wheat Leaves, Plant Physiol., 1998, vol. 117, pp. 667–678.PubMedCrossRefGoogle Scholar
  92. 92.
    Fowler, M.R., Kirby, M.J., Scott, N.W., Slater, A., and Elliott, M.C., Polyamine Metabolism and Gene Regulation during the Transition of Autonomous Sugar Beet Cell in Suspension Culture from Quiescence to Division, Physiol. Plant., 1996, vol. 98, pp. 439–446.CrossRefGoogle Scholar
  93. 93.
    Koenig, H., Goldstone, A., and Lu, C.Y., Polyamines Regulate Calcium Fluxes in a Rapid Plasma Membrane Occurrence, Nature, 1983, vol. 305, pp. 530–534.PubMedCrossRefGoogle Scholar
  94. 94.
    Bueb, L., Silva, A., Mousli, M., and Landry, Y., Natural Polyamines Stimulate G-Proteins, Biochem. J., 1992, vol. 282, pp. 545–550.PubMedGoogle Scholar
  95. 95.
    Ficker, E., Taglialatella, M., Wible, B.A., Henley, Ch.M., and Brown, A.M., Spermine and Spermidine as Gating Molecules for Inward Rectifier K+ Channels, Science, 1994, vol. 266, pp. 1068–1071.PubMedGoogle Scholar
  96. 96.
    Dobrovinskaya, O.R., Muniz, J., and Pottosin, I., Inhibition of Vacuolar Ion Channels by Polyamines, J. Membr. Biol., 1999, vol. 162, pp. 127–140.CrossRefGoogle Scholar
  97. 97.
    Messiaen, J. and van Custem, P., Polyamines and Pectins: 2. Modulation of Pectic-Signal Transduction, Planta, 1999, vol. 208, pp. 247–250.PubMedCrossRefGoogle Scholar
  98. 98.
    Bellincampi, D., Cardarelli, M., Zaghi, D., Serino, G., Gatz, C., Cervone, F., Altamura, M.M., Costantino, P., and de Lorenzo, G., Oligogalacturonides Prevent Rhizogenesis in RolB-Transformed Tobacco Explants by Inhibiting Auxin-Induced Expression of the RolB Gene, Plant Cell, 1995, vol. 8, pp. 477–478.CrossRefGoogle Scholar
  99. 99.
    Takahashi, Y., Berberich, T., Yamamashita, K., Uehara, Y., Miyazaki, A., and Kusano, T., Identification of Tobacco HINI and Two Closely Related Genes as Spermine-Responsive Genes and Their Differential Expression during the Tobacco Mosaic Virus-Induced Hypersensitive Response and during Leaf and Flower Senescence, Plant Mol. Biol., 2004, vol. 54, pp. 613–622.PubMedCrossRefGoogle Scholar
  100. 100.
    Hanzawa, Y., Takahashi, T., Michael, J., Burtin, D., Long, D., Pineiro, M., Coupland, G., and Komeda, Y., ACAULIS5, an Arabidopsis Gene Required for Stem Elongation, Encodes a Spermine Synthase, EMBO J., 2000, vol. 19, pp. 4248–4256.PubMedCrossRefGoogle Scholar
  101. 101.
    Rakova, N.Yu. and Romanov, G.A., Polyamines Suppress Manifestation of Cytokinin Primary Effects, Fiziol. Rast. (Moscow), 2005, vol. 52, pp. 59–67 (Russ. J. Plant Physiol., Engl. Transl., pp. 50–57).Google Scholar
  102. 102.
    Rastogi, R. and Davies, P.J., Effects of Light and Plant Growth Regulators on Polyamine Metabolism in Higher Plants, Biochemistry and Physiology of Polyamines in Plants, Slocum, R.D. and Flores, H.E., Eds., Boca Raton (FL): CRC, 1991, pp. 187–199.Google Scholar
  103. 103.
    Altman, A., Polyamines and Plant Hormones, The Physiology of Polyamines, Bachrach, U. and Heimer, Y.M., Eds., Boca Raton (FL): CRC, 1989, pp. 121–145.Google Scholar
  104. 104.
    Frydman, R.B. and Gamarnik, A., Cadaverine, an Essential Diamine for Normal Root Development of Germinating Soybean (Glycine max) Seeds, Plant Physiol., 1991, vol. 97, pp. 778–785.PubMedGoogle Scholar
  105. 105.
    Bueno, M. and Matilla, A.J., Gene Expression Induced by Spermine in Isolated Embryonic Axes of Chick-Pea Seeds, Physiol. Plant., 1993, vol. 87, pp. 381–383.CrossRefGoogle Scholar
  106. 106.
    Basu, R., Maitra, N., and Ghosh, B., Salinity Results in Polyamine Accumulation in Early Rice (Oryza sativa L.) Seedlings, Aust. J. Plant Physiol., 1998, vol. 15, pp. 777–786.CrossRefGoogle Scholar
  107. 107.
    Ha, H.L., Sirisoma, N.S., Kuppusamy, P., Zweller, J.L., Woster, P.M., and Casero, R.A., Jr., The Natural Polyamine Spermine Functions as a Free Radical Scavenger, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 11140–11145.PubMedCrossRefGoogle Scholar
  108. 108.
    Neill, S., Desikan, R., and Hancock, J., Hydrogen Peroxide Signalling, Curr. Vererbungslehre, 2002, vol. 96, pp. 93–104.Google Scholar
  109. 109.
    Bors, W., Langebartels, C., Michel, C., and Sandermann, H., Polyamines as Radical Scavengers and Protectants against Ozone Damage, Phytochemistry, 1989, vol. 28, pp. 1589–1595.CrossRefGoogle Scholar
  110. 110.
    Ye, B., Müller, H., Zhang, J., and Gressel, J., Constitutively Elevated Levels of Putrescine and Putrescine-Generating Enzymes Correlated with Oxidant Stress Resistance in Coniza bonariensis and Wheat, Plant Physiol., 1997, vol. 115, pp. 1443–1451.PubMedCrossRefGoogle Scholar
  111. 111.
    Shevyakova, N.I., Shorina, M.V., Rakitin, V.Yu., Stetsenko, L.A., and Kuznetsov, Vl.V., Ethylene-Induced Cadaverine Generation Mediated by Processes of Protein Phosphorylation/Dephosphorylation, Dokl. Akad. Nauk, 2004, vol. 395, pp. 283–285.Google Scholar
  112. 112.
    Paramonova, N.V., Shevyakova, N.I., Shorina, M.V., Stetsenko, L.A., Rakitin, V.Yu., and Kuznetsov, Vl.V., The Effect of Putrescine on the Apoplast Ultrastructure in the Leaf Mesophyll of Mesembryanthemum crystallinum under Salinity Stress, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 661–674 (Russ. J. Plant Physiol., Engl. Transl., pp. 587–598).Google Scholar
  113. 113.
    Aronova, E.E., Shevyakova, N.I., Stetsenko, L.A., and Kuznetsov, Vl.V., Cadaverine-Induced Superoxide Dismutase Gene Expression in Mesembryanthemum crystallinum L., Dokl. Akad. Nauk, 2005, vol. 403, pp. 1–3.Google Scholar
  114. 114.
    Ślesak, J., Karpinska, B., Surówka, E., Miszalski, Z., and Karpinski, S., Redox Changes in the Chloroplast and Hydrogen Peroxide Are Essential for Regulation of C3-CAM Transition and Photooxidative Stress Responses in the Facultative CAM Plant Mesembryanthemum crystallinum L., Plant Cell Physiol., 2003, vol. 44, pp. 573–581.PubMedCrossRefGoogle Scholar
  115. 115.
    Rea, G., Concetta de Pinto, M., Tavazza, R., Biondi, S., Gobbi, V., Ferrante, P., de Gara, L., Federico, R., Angelini, R., and Tavladoraki, P., Ectopic Expression of Maize Polyamine Oxidase and Pea Copper Amine Oxidase in the Cell Wall of Tobacco Plants, Plant Physiol., 2004, vol. 134, pp. 1414–1426.PubMedCrossRefGoogle Scholar
  116. 116.
    Hiraga, S., Ito, H., Yamakawa, H., Ohtsubo, N., Seo, S., Mitsuhara, I., Matsui, H., Honma, M., and Ohashi, Y., An HR-Induced Tobacco Peroxidase Gene Is Responsive to Spermine, but Not to Salicylate, Methyljasmonate, and Ethephon, Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 210–216.PubMedGoogle Scholar
  117. 117.
    Serafini-Fracassini, D., del Duca, S., and Beninati, S., Plant Transglutaminases, Phytochemistry, 1995, vol. 40, pp. 355–365.PubMedCrossRefGoogle Scholar
  118. 118.
    Dondini, L., Serafini-Fracassini, D., del Duca, S., Bregoli, A.M., and Tsolova, M., Plant Transglutaminases, Polyamines: Biological and Clinical Aspects, Caldarere, C.M., Clo, C., and Morruzzi, M.S., Eds., Bologna: CLUEB, 1994, pp. 183–194.Google Scholar
  119. 119.
    Slocum, R.D. and Galston, A.W., Change in Polyamine Biosynthesis Associated with Post-Fertilization Growth and Development in Tobacco Ovary Tissue, Plant Physiol., 1985, vol. 39, pp. 223–230.Google Scholar
  120. 120.
    Biondi, S., Scaramagli, S., Capitani, F., Altamura, M.M., and Torrigiani, P., Methyljasmonate Upregulates Biosynthetic Gene Expression, Oxidation and Conjugation of Polyamines and Inhibits Shoot Formation in Tobacco Thin Layers, J. Exp. Bot., 2001, vol. 52, pp. 231–242.PubMedCrossRefGoogle Scholar
  121. 121.
    Kushad, M.M., Richardson, D.G., and Ferro, A.J., Intermediates in the Recycling of 5-Methylthioribose to Methionine in Fruits, Plant Physiol., 1983, vol. 73, pp. 257–261.PubMedCrossRefGoogle Scholar
  122. 122.
    Isekson, I., Bakhanashvili, M., and Apelboum, A., Inhibition by Ethylene of Polyamine Biosynthetic Enzymes Enhanced Lysine Decarboxylase Activity and Cadaverine Localized in Pea Seedlings, Plant Physiol., 1986, vol. 82, pp. 607–609.Google Scholar
  123. 123.
    Novikova, G.V., Moshkov, I.E., Smith, A.R., and Hall, M.A., Ethylene and Phosphorylation of Pea Epicotyl Proteins, Cellular and Molecular Aspects of the Plant Hormone Ethylene, Pech, J.C., Latché, A., and Balagué, C., Eds., Dordrecht: Kluwer, 1993, pp. 371–372.Google Scholar
  124. 124.
    Shorina, M.V., Ragulin, V.V., Kuznetsov, Vl.V., and Shevyakova, N.I., Do Cadaverine and Ethylene Participate in Induction of CAM-Type Photosynthesis in Mesembryanthemum crystallinum? Dokl. Akad. Nauk, 2005, vol. 400, pp. 115–120.Google Scholar
  125. 125.
    Bryson, K. and Greenall, R.J., Binding Sites of the Polyamines Putrescine, Cadaverine, Spermidine and Spermine on A-and B-DNA Located by Stimulated Annealing, J. Biomol. Struct. Dyn., 2000, vol. 18, pp. 393–412.PubMedGoogle Scholar
  126. 126.
    Wada, Y., Miyamoto, T., Kusano, T., and Sano, H., Association between Up-Regulation of Stress-Responsive Genes and Hypomethylation of Genomic DNA in Tobacco Plants, Mol. Gen. Genomics, 2004, vol. 271, pp. 658–666.CrossRefGoogle Scholar
  127. 127.
    Feuerstein, B.G., Pattabiraman, N., and Marton, L.J., Molecular Mechanisms of the Interactions of Spermine with DNA:DNA Bending as a Result of Ligand Bending, Nucleic Acids Res., 1990, vol. 18, pp. 1271–1282.PubMedGoogle Scholar
  128. 128.
    Hasegawa, P.M., Bressan, R.A., Zhu, J.-K., and Bohnert, H.J., Plant Cellular and Molecular Responses to High Salinity, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2000, vol. 51, pp. 463–497.PubMedCrossRefGoogle Scholar
  129. 129.
    Liu, K., Fu, H., Bei, Q., and Luan, S., Inward Potassium Channel in Guard Cells as a Target for Polyamine Regulation of Stomatal Movements, Plant Physiol., 2000, vol. 124, pp. 1315–1325.PubMedCrossRefGoogle Scholar
  130. 130.
    Ozaki, S., de Wald, D.B., Shope, J.C., Chen, J., and Prestwich, G.D., Intracellular Delivery of Phosphoinositides and Inositol Phosphates Using Polyamine Carriers, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 11286–11291.PubMedCrossRefGoogle Scholar
  131. 131.
    Zhu, J.-K., Plant Salt Tolerance, Trends Plant Sci., 2001, vol. 6, pp. 65–71.Google Scholar
  132. 132.
    Cushman, J.C. and Bonnert, H.J., Genomic Approaches to Plant Stress Tolerance, Curr. Opin. Plant Biol., 2000, vol. 3, pp. 117–124.PubMedCrossRefGoogle Scholar
  133. 133.
    Gong, Q., Li, P., Ma, S., Rupassara, S.I., and Bohnert, H.J., Salinity Stress Adaptation Competence in the Extremophile Thellungiella halophila in Comparison with Its Relative Arabidopsis thaliana, Plant J., 2005, vol. 41, pp. 1–14.CrossRefGoogle Scholar

Copyright information

© MAIK “Nauka/Interperiodica” 2006

Authors and Affiliations

  • Vl. V. Kuznetsov
    • 1
  • N. L. Radyukina
    • 1
  • N. I. Shevyakova
    • 1
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations