Planta

, Volume 231, Issue 6, pp 1237–1249 | Cite as

Polyamines: molecules with regulatory functions in plant abiotic stress tolerance

  • Rubén Alcázar
  • Teresa Altabella
  • Francisco Marco
  • Cristina Bortolotti
  • Matthieu Reymond
  • Csaba Koncz
  • Pedro Carrasco
  • Antonio F. Tiburcio
Review

Abstract

Early studies on plant polyamine research pointed to their involvement in responses to different environmental stresses. During the last few years, genetic, transcriptomic and metabolomic approaches have unravelled key functions of different polyamines in the regulation of abiotic stress tolerance. Nevertheless, the precise molecular mechanism(s) by which polyamines control plant responses to stress stimuli are largely unknown. Recent studies indicate that polyamine signalling is involved in direct interactions with different metabolic routes and intricate hormonal cross-talks. Here we discuss the integration of polyamines with other metabolic pathways by focusing on molecular mechanisms of their action in abiotic stress tolerance. Recent advances in the cross talk between polyamines and abscisic acid are discussed and integrated with processes of reactive oxygen species (ROS) signalling, generation of nitric oxide, modulation of ion channel activities and Ca2+ homeostasis, amongst others.

Keywords

Polyamine metabolism Abiotic stress Plant tolerance Abscisic acid Signalling 

Abbreviations

ABA

Abscisic acid

ACC

Amino cyclopropane carboxylic acid

ACL5

Acaulis5

ADC

Arginine decarboxylase

AIH

Agmatine iminohydrolase

CPA

N-Carbamoyl putrescine amidohydrolase

DAO

Diamine oxidase

Dap

1,3-Diaminopropane

dcSAM

Decarboxylated SAM

FAD

Flavin adenine dinucleotide

GABA

γ-Aminobutyric acid

LSD

Lysine-specific demethylase

NO

Nitric oxide

ODC

Ornithine decarboxylase

PAO

Polyamine oxidase

Pro

Proline

Put

Putrescine

SAM

S-Adenosyl methionine

SAMDC

S-Adenosyl methionine decaboxylase

ROS

Reactive oxygen species

SMO

Spermine oxidase

Spd

Spermidine

SDPS

Spermidine synthase

Spm

Spermine

SPMS

Spermine synthase

TCA

Tricarboxylic acid

tSpm

Thermospermine

References

  1. Alcázar R, García-Martínez JL, Cuevas JC, Tiburcio AF, Altabella T (2005) Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA deficiency. Plant J 43:425–436PubMedCrossRefGoogle Scholar
  2. Alcázar R, Cuevas JC, Patrón M, Altabella T, Tiburcio AF (2006a) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455CrossRefGoogle Scholar
  3. Alcázar R, Marco F, Cuevas JC, Patrón M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006b) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876PubMedCrossRefGoogle Scholar
  4. Alcázar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas JC, Bitrián M, Tiburcio AF, Altabella T (2010) Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants overexpressing the homologous Arginine decarboxylase 2 gene. Plant Physiol Biochem. doi:10.1016/j.plphy.2010.02.002
  5. Alonso-Blanco C, Aarts MGM, Bentsink L, Keurentjes JJB, Reymond M, Vreugdenhil D, Koornneef M (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21:1877–1896PubMedCrossRefGoogle Scholar
  6. Altabella T, Tiburcio AF, Ferrando A (2009) Plant with resistance to low temperature and method of production thereof. Spanish patent application WO2010/004070Google Scholar
  7. An ZF, Jing W, Liu YL, Zhang WH (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825PubMedCrossRefGoogle Scholar
  8. Apelbaum A, Canellakis ZN, Applewhite PB, Kaur-Sawhney R, Galston AW (1988) Binding of spermidine to a unique protein in thin-layer tobacco tissue-culture. Plant Physiol 88:996–998PubMedCrossRefGoogle Scholar
  9. Athwal GS, Huber SC (2002) Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase. Plant J 29:119–129PubMedCrossRefGoogle Scholar
  10. Aziz A, Martin-Tanguy J, 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 104:195–202CrossRefGoogle Scholar
  11. Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317PubMedCrossRefGoogle Scholar
  12. Bethke PC, Jones RL (1997) Reversible protein phosphorylation regulates the activity of the slow-vacuolar ion channel. Plant J 11:1227–1235CrossRefGoogle Scholar
  13. Blatt MR, Thiel G, Trentham DR (1990) Reversible inactivation of K+ channels of Vicia stomatal guard-cells following the photolysis of caged Inositol 1, 4, 5-trisphosphate. Nature 346:766–769PubMedCrossRefGoogle Scholar
  14. Borrell A, Culiañez-Macià FA, Altabella T, Besford RT, Flores D, Tiburcio AF (1995) Arginine decarboxylase is localized in chloroplasts. Plant Physiol 109:771–776PubMedGoogle Scholar
  15. Bortolotti C, Cordeiro A, Alcazar R, Borrell A, Culiañez-Macià FA, Tiburcio AF, Altabella T (2004) Localization of arginine decarboxylase in tobacco plants. Physiol Plant 120:84–92PubMedCrossRefGoogle Scholar
  16. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125CrossRefGoogle Scholar
  17. Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54CrossRefGoogle Scholar
  18. Brieger L (1885) Über Spaltungsprodukte der Bacterien, Zweite Mittheilung. Zeitschr Physiol Chem 9:1–7Google Scholar
  19. Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122PubMedCrossRefGoogle Scholar
  20. Bruggemann LI, Pottosin II, Schonknecht G (1998) Cytoplasmic polyamines block the fast-activating vacuolar cation channel. Plant J 16:101–105CrossRefGoogle Scholar
  21. Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:990–991CrossRefGoogle Scholar
  22. Cheng L, Zou YJ, Ding SL, Zhang JJ, Yu XL, Cao JS, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499PubMedCrossRefGoogle Scholar
  23. Childs AC, Mehta DJ, Gerner EW (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60:1394–1406PubMedCrossRefGoogle Scholar
  24. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88PubMedCrossRefGoogle Scholar
  25. Cuevas JC, Lopez-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105PubMedCrossRefGoogle Scholar
  26. Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2009) Putrescine as a signal to modulate the indispensable ABA increase under cold stress. Plant Signal Behav 4:219–220PubMedCrossRefGoogle Scholar
  27. Datta N, Schell MB, Roux SJ (1987) Spermine stimulation of a nuclear NII kinase from pea plumules and its role in the phosphorylation of a nuclear polypeptide. Plant Physiol 84:1397–1401PubMedCrossRefGoogle Scholar
  28. Delavega AL, Delcour AH (1995) Cadaverine induces closing of Escherichia coli porins. EMBO J 14:6058–6065PubMedGoogle Scholar
  29. Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212PubMedCrossRefGoogle Scholar
  30. Dudley HW, Rosenheim O, Starling WW (1926) The chemical constitution of spermine III. Structure and synthesis. Biochem J 20:1082–1094PubMedGoogle Scholar
  31. Dudley HW, Rosenheim O, Starling WW (1927) The constitution and synthesis of spermidine, a newly discovered base isolated from animal tissues. Biochem J 21:97–103PubMedGoogle Scholar
  32. Fellenberg C, Böttcher C, Vogt T (2009) Phenylpropanoid polyamine conjugate biosynthesis in Arabidopsis thaliana flower buds. Phytochemistry 70:1392–1400PubMedCrossRefGoogle Scholar
  33. Ferrando A, Carrasco P, Cuevas JC, Altabella T, Tiburcio AF (2004) Integrated molecular analysis of the polyamine metabolic pathway in abiotic stress signalling. In: Amâncio S, Stulen I (eds) Nitrogen acquisition and assimilation in higher plants. Kluwer Academic Publishers, The Netherlands, pp 207–230. ISBN:1-4020-2728-1 (e-book)Google Scholar
  34. Flores HE, Galston AW (1982) Polyamines and plant stress—activation of putrescine biosynthesis by osmotic shock. Science 217:1259–1261PubMedCrossRefGoogle Scholar
  35. Galston AW (1991) On the trail of a new regulatory system in plants. New Biol 3:450–453PubMedGoogle Scholar
  36. Galston AW, Kaur-Sawhney R (1990) Polyamines in plant physiology. Plant Physiol 94:406–410PubMedCrossRefGoogle Scholar
  37. Ghosh B (2000) Polyamines and plant alkaloids. Indian J Exp Biol 38:1086–1091PubMedGoogle Scholar
  38. Gill S, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 7:5(1). PMID: 20023386Google Scholar
  39. Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 346:769–771PubMedCrossRefGoogle Scholar
  40. Grienenberger E, Besseau S, Geoffroy P, Debayle D, Heintz D, Lapierre C, Pollet B, Heitz T, Legrand M (2009) A BAHD acyltransferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoyl spermidines. Plant J 58:246–259PubMedCrossRefGoogle Scholar
  41. Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45PubMedCrossRefGoogle Scholar
  42. Gupta R, Huang YF, Kieber J, Luan S (1998) Identification of a dual-specificity protein phosphatase that inactivates a MAP kinase from Arabidopsis. Plant J 16:581–589PubMedCrossRefGoogle Scholar
  43. Hamasaki-Katagiri N, Katagiri Y, Tabor CW, Tabor H (1998) Spermine is not essential for growth of Saccharomyces cerevisiae: identification of the SPE4 gene (spermine synthase) and characterization of a spe4 deletion mutant. Gene 210:195–201PubMedCrossRefGoogle Scholar
  44. Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J 27:551–560PubMedCrossRefGoogle Scholar
  45. Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256PubMedCrossRefGoogle Scholar
  46. Huang J, Sengupta R, Espejo AB, Lee MG, Dorsey JA, Richter M, Opravil S, Shiekhattar R, Bedford MT, Jenuwein T, Berger SL (2007) p53 is regulated by the lysine demethylase LSD1. Nature 449:105–180PubMedCrossRefGoogle Scholar
  47. Igarashi K, Kashiwagi K (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271:559–564PubMedCrossRefGoogle Scholar
  48. Illingworth C, Mayer MJ, Elliott K, Hanfrey C, Walton NJ, Michael AJ (2003) The diverse bacterial origins of the Arabidopsis polyamine biosynthetic pathway. FEBS Lett 549:26–30PubMedCrossRefGoogle Scholar
  49. Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T (2004a) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152PubMedCrossRefGoogle Scholar
  50. Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004b) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573PubMedCrossRefGoogle Scholar
  51. Imanishi S, Hashizume K, Nakakita M, Kojima H, Matsubayashi Y, Hashimoto T, Sakagami Y, Yamada Y, Nakamura K (1998) Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures. Plant Mol Biol 38:1101–1111PubMedCrossRefGoogle Scholar
  52. Janowitz T, Kneifel H, Piotrowski M (2003) Identification and characterization of plant agmatine iminohydrolase, the last missing link in polyamine biosynthesis of plants. FEBS Lett 544:258–261PubMedCrossRefGoogle Scholar
  53. Jiang D, Yang W, He Y, Amasino RM (2007) Arabidopsis relatives of the human lysine-specific demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19:2975–2987PubMedCrossRefGoogle Scholar
  54. Johnson TD (1996) Modulation of channel function by polyamines. Trends Pharmacol Sci 17:22–27PubMedCrossRefGoogle Scholar
  55. Kakehi JI, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349PubMedCrossRefGoogle Scholar
  56. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282PubMedCrossRefGoogle Scholar
  57. Kasinathan V, Wingler A (2004) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol Plant 121:101–107PubMedCrossRefGoogle Scholar
  58. Kasukabe Y, He LX, Nada K, Misawa S, Ihara I, Tachibana S (2004) 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 Cell Physiol 45:712–722PubMedCrossRefGoogle Scholar
  59. Knott JM, Romer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086PubMedCrossRefGoogle Scholar
  60. Krichevsky A, Gutgarts H, Kozlovsky SV, Tzfira T, Sutton A, Sternglanz R, Mandel G, Citovsky V (2007) C2H2 zinc finger-SET histone methyltransferase is a plant-specific chromatin modifier. Dev Biol 303:259–269PubMedCrossRefGoogle Scholar
  61. Kuehn GD, Affolter HU, Atmar VJ, Seebeck T, Gubler U, Braun R (1979) Polyamine-mediated phosphorylation of a nucleolar protein from Physarum polycephalum that stimulates ribosomal-RNA synthesis. Proc Natl Acad Sci USA 76:2541–2545PubMedCrossRefGoogle Scholar
  62. Kumar A, Altabella T, Taylor MA, Tiburcio AF (1997) Recent advances in polyamine research. Trends Plant Sci 2:124–130CrossRefGoogle Scholar
  63. Kumria R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro morphogenesis and response to salt stress. J Plant Physiol 159:983–990CrossRefGoogle Scholar
  64. Kuppusamy K, Walcher C, Nemhauser J (2009) Cross-regulatory mechanisms in hormone signaling. Plant Mol Biol 69:375–381PubMedCrossRefGoogle Scholar
  65. Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav 2:251–252PubMedGoogle Scholar
  66. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381PubMedCrossRefGoogle Scholar
  67. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633PubMedCrossRefGoogle Scholar
  68. Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1326PubMedCrossRefGoogle Scholar
  69. Luo J, Fuell C, Parr A, Hill L, Bailey P, Elliott K, Fairhurst SA, Martin C, Michael AJ (2009) A novel polyamine acyltransferase responsible for the accumulation of spermidine conjugates in Arabidopsis seed. Plant Cell 21:318–333PubMedCrossRefGoogle Scholar
  70. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefGoogle Scholar
  71. Malmberg RL, Watson MB, Galloway GL, Yu W (1998) Molecular genetic analyses of plant polyamines. Crit Rev Plant Sci 17:199–224CrossRefGoogle Scholar
  72. Martin-Tanguy J (1997) Conjugated polyamines and reproductive development: Biochemical, molecular and physiological approaches. Physiol Plant 100:675–688CrossRefGoogle Scholar
  73. Mehta AM, Saftner RA, Schaeffer GW, Mattoo AK (1991) Translational modification of an 18 Kilodalton polypeptide by spermidine in rice cell-suspension cultures. Plant Physiol 95:1294–1297PubMedCrossRefGoogle Scholar
  74. Michael AJ, Furze JM, Rhodes MJC, Burtin D (1996) Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA. Biochem J 314:241–248PubMedGoogle Scholar
  75. Michard E, Dreyer I, Lacombe B, Sentenac H, Thibaud JB (2005) Inward rectification of the AKT2 channel abolished by voltage-dependent phosphorylation. Plant J 44:783–797PubMedCrossRefGoogle Scholar
  76. Minguet EG, Vera-Sirera F, Marina A, Carbonell J, Blazquez MA (2008) Evolutionary diversification in polyamine biosynthesis. Mol Biol Evol 25:2119–2128PubMedCrossRefGoogle Scholar
  77. Mohapatra S, Minocha R, Long S, Minocha SC (2009) Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids. Amino Acids. doi:10.07/s00726-009-0322-z
  78. Moller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis ATAO1 gene encoding an H2O2-generating diamine oxidase. Plant J 13:781–791PubMedCrossRefGoogle Scholar
  79. Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism: the state of the art. Plant Signal Behav 3:1061–1066PubMedGoogle Scholar
  80. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176PubMedCrossRefGoogle Scholar
  81. Nordborg M, Weigel D (2008) Next-generation genetics in plants. Nature 456:720–723PubMedCrossRefGoogle Scholar
  82. Pandey S, Ranade SA, Nagar PK, Kumar N (2000) Role of polyamines and ethylene as modulators of plant senescence. J Biosci 25:291–299PubMedCrossRefGoogle Scholar
  83. Panicot M, Minguet EG, Ferrando A, Alcázar R, Blazquez MA, Carbonell J, Altabella T, Koncz C, Tiburcio AF (2002) A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14:2539–2551PubMedCrossRefGoogle Scholar
  84. Pegg AE, Michael A (2009) Spermine synthase. Cell Mol Life Sci 67:113–121PubMedCrossRefGoogle Scholar
  85. Perez-Amador MA, Leon J, Green PJ, Carbonell J (2002) Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol 130:1454–1463PubMedCrossRefGoogle Scholar
  86. Piotrowski M, Janowitz T, Kneifel H (2003) Plant C-N hydrolases and the identification of a plant N-carbamoylputrescine amidohydrolase involved in polyamine biosynthesis. J Biol Chem 278:1708–1712PubMedCrossRefGoogle Scholar
  87. Rambla JL, Vera-Sirera F, Blázquez MA, Carbonell J, Granell A (2010) Quantitation of biogenic tetramines in Arabidopsis thaliana. Anal Biochem 397:208–211PubMedCrossRefGoogle Scholar
  88. Richards FJ, Coleman RG (1952) Occurrence of putrescine in potassium-deficient barley. Nature 170:460PubMedCrossRefGoogle Scholar
  89. Roberts SC, Jiang YQ, Jardim A, Carter NS, Heby O, Ullman B (2001) Genetic analysis of spermidine synthase from Leishmania donovani. Mol Biochem Parasitol 115:217–226PubMedCrossRefGoogle Scholar
  90. Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875PubMedCrossRefGoogle Scholar
  91. Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987–992CrossRefGoogle Scholar
  92. Sebela M, Radova A, Angelini R, Tavladoraki P, Frebort I, Pec P (2001) FAD-containing polyamine oxidases: a timely challenge for researchers in biochemistry and physiology of plants. Plant Sci 160:197–207PubMedCrossRefGoogle Scholar
  93. Seiler N, Raul F (2005) Polyamines and apoptosis. J Cell Mol Med 9:623–642PubMedCrossRefGoogle Scholar
  94. Seyfred MA, Farrell LE, Wells WW (1984) Characterization of D-myo-Inositol 1, 4, 5-trisphosphate phosphatase in rat-liver plasma-membranes. J Biol Chem 259:3204–3208Google Scholar
  95. Shabala S, Cuin TA, Pottosin I (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999PubMedCrossRefGoogle Scholar
  96. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726PubMedCrossRefGoogle Scholar
  97. She XP, Song XG, He JM (2004) Role and relationship of nitric oxide and hydrogen peroxide in light/dark-regulated stomatal movement in Vicia faba. Acta Bot Sin 46:1292–1300Google Scholar
  98. Shi YJ, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953PubMedCrossRefGoogle Scholar
  99. Singh SS, Chauhan A, Brockerhoff H, Chauhan VPS (1995) Differential-effects of spermine on phosphatidylinositol 3-kinase and phosphatidylinositol phosphate 5-kinase. Life Sci 57:685–694PubMedCrossRefGoogle Scholar
  100. Slocum RD, Kaur-Sawhney R, Galston AW (1984) The physiology and biochemistry of polyamines in plants. Arch Biochem Biophys 235:283–303PubMedCrossRefGoogle Scholar
  101. Smith TA, Richards FJ (1964) The biosynthesis of putrescine in higher plants and its relation to potassium nutrition. Biochem J 84:292–294Google Scholar
  102. Soyka S, Heyer AG (1999) Arabidopsis knockout mutation of ADC2 gene reveals inducibility by osmotic stress. Febs Lett 458:219–223PubMedCrossRefGoogle Scholar
  103. Takahashi T, Kakehi J-I (2009) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6CrossRefGoogle Scholar
  104. Tassoni A, Antognoni F, Battistini ML, Sanvido O, Bagni N (1998) Characterization of spermidine binding to solubilized plasma membrane proteins from zucchini hypocotyls. Plant Physiol 117:971–977PubMedCrossRefGoogle Scholar
  105. Tassoni A, Napier RM, Franceschetti M, Venis MA, Bagni N (2002) Spermidine-binding proteins. Purification and expression analysis in maize. Plant Physiol 128:1303–1312PubMedCrossRefGoogle Scholar
  106. Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Federico R (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141:1519–1532PubMedCrossRefGoogle Scholar
  107. Teuber M, Azemi ME, Namjoyan F, Meier AC, Wodak A, Brandt W, Drager B (2007) Putrescine N-methyltransferases—a structure–function analysis. Plant Mol Biol 63:787–801PubMedCrossRefGoogle Scholar
  108. Tiburcio AF, Kaur-Sawhney R, Galston AW (1990) Polyamine metabolism. In: Stumpf PK, Conn EE (eds) The Biochemistry of plants. Academic Press, New York, USA, pp 283–235. ISBN:0-12-6754 16-0Google Scholar
  109. Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354PubMedCrossRefGoogle Scholar
  110. Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926CrossRefGoogle Scholar
  111. Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313:369–375PubMedCrossRefGoogle Scholar
  112. Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–1564PubMedCrossRefGoogle Scholar
  113. Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078PubMedCrossRefGoogle Scholar
  114. van Leeuwenhoek A (1678) Observationes D. Anthonii Leeuwenhoek, de natis e semine genitali animalculis. Philos Trans R Soc Lond 12:1040–1043Google Scholar
  115. Waie B, Rajam MV (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727–734CrossRefGoogle Scholar
  116. Walden R, Cordeiro A, Tiburcio AF (1997) Polyamines: Small molecules triggering pathways in plant growth and development. Plant Physiol 113:1009–1013PubMedCrossRefGoogle Scholar
  117. Wang XJ, Ikeguchi Y, McCloskey DE, Nelson P, Pegg AE (2004) Spermine synthesis is required for normal viability, growth, and fertility in the mouse. J Biol Chem 279:51370–51375PubMedCrossRefGoogle Scholar
  118. Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T (2009) Aluminum tolerance in a spermidine synthase-overexpressing transgenic European pear is correlated with the enhanced level of spermidine via alleviating oxidative status. Environ Exp Bot 66:471–478CrossRefGoogle Scholar
  119. Wi SJ, Park KY (2002) Antisense expression of carnation cDNA encoding ACC synthase or ACC oxidase enhances polyamine content and abiotic stress tolerance in transgenic tobacco plants. Mol Cells 13:209–220PubMedGoogle Scholar
  120. Wi SJ, Kim WT, Park KY (2006) Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Rep 25:1111–1121PubMedCrossRefGoogle Scholar
  121. Wilson PB, Estavillo GM, Field KJ, Pornsiriwong W, Carroll AJ, Howell KA, Woo NS, Lake JA, Smith SM, Millar AH, von Caemmerer S, Pogson BJ (2009) The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J 58:299–317PubMedCrossRefGoogle Scholar
  122. Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788PubMedCrossRefGoogle Scholar
  123. Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490PubMedCrossRefGoogle Scholar
  124. Yamasaki H, Cohen MF (2006) NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci 11:522–524PubMedCrossRefGoogle Scholar
  125. Zhao FG, Song CP, He JQ, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Rubén Alcázar
    • 2
  • Teresa Altabella
    • 1
  • Francisco Marco
    • 3
  • Cristina Bortolotti
    • 1
  • Matthieu Reymond
    • 2
  • Csaba Koncz
    • 2
  • Pedro Carrasco
    • 4
  • Antonio F. Tiburcio
    • 1
  1. 1.Departament de Productes Naturals, Biologia Vegetal i Edafologia, Facultat de FarmàciaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Max-Planck Institut für ZüchtungsforschungCologneGermany
  3. 3.Fundacion CEAMValenciaSpain
  4. 4.Departament de Bioquímica i Biologia Molecular, Facultat de Ciències BiològiquesUniversitat de ValènciaValenciaSpain

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