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Polyamines: molecules with regulatory functions in plant abiotic stress tolerance

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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.

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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

  • 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 43:425–436

    Article  PubMed  CAS  Google Scholar 

  • Alcázar R, Cuevas JC, Patrón M, Altabella T, Tiburcio AF (2006a) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455

    Article  CAS  Google Scholar 

  • 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 28:1867–1876

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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 21:1877–1896

    Article  PubMed  CAS  Google Scholar 

  • Altabella T, Tiburcio AF, Ferrando A (2009) Plant with resistance to low temperature and method of production thereof. Spanish patent application WO2010/004070

  • 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 59:815–825

    Article  PubMed  CAS  Google Scholar 

  • 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 88:996–998

    Article  PubMed  CAS  Google Scholar 

  • 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 29:119–129

    Article  PubMed  CAS  Google Scholar 

  • 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 104:195–202

    Article  CAS  Google Scholar 

  • Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Jones RL (1997) Reversible protein phosphorylation regulates the activity of the slow-vacuolar ion channel. Plant J 11:1227–1235

    Article  CAS  Google Scholar 

  • 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 346:766–769

    Article  PubMed  CAS  Google Scholar 

  • Borrell A, Culiañez-Macià FA, Altabella T, Besford RT, Flores D, Tiburcio AF (1995) Arginine decarboxylase is localized in chloroplasts. Plant Physiol 109:771–776

    PubMed  CAS  Google Scholar 

  • 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 120:84–92

    Article  PubMed  CAS  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Brieger L (1885) Über Spaltungsprodukte der Bacterien, Zweite Mittheilung. Zeitschr Physiol Chem 9:1–7

    Google Scholar 

  • 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 45:113–122

    Article  PubMed  CAS  Google Scholar 

  • Bruggemann LI, Pottosin II, Schonknecht G (1998) Cytoplasmic polyamines block the fast-activating vacuolar cation channel. Plant J 16:101–105

    Article  CAS  Google Scholar 

  • 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 101:990–991

    Article  Google Scholar 

  • 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 51:489–499

    Article  PubMed  CAS  Google Scholar 

  • Childs AC, Mehta DJ, Gerner EW (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60:1394–1406

    Article  PubMed  CAS  Google Scholar 

  • Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88

    Article  PubMed  CAS  Google Scholar 

  • 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 148:1094–1105

    Article  PubMed  Google Scholar 

  • 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 4:219–220

    Article  PubMed  CAS  Google Scholar 

  • 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 84:1397–1401

    Article  PubMed  CAS  Google Scholar 

  • Delavega AL, Delcour AH (1995) Cadaverine induces closing of Escherichia coli porins. EMBO J 14:6058–6065

    PubMed  CAS  Google Scholar 

  • 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 55:205–212

    Article  PubMed  CAS  Google Scholar 

  • Dudley HW, Rosenheim O, Starling WW (1926) The chemical constitution of spermine III. Structure and synthesis. Biochem J 20:1082–1094

    PubMed  CAS  Google Scholar 

  • Dudley HW, Rosenheim O, Starling WW (1927) The constitution and synthesis of spermidine, a newly discovered base isolated from animal tissues. Biochem J 21:97–103

    PubMed  CAS  Google Scholar 

  • Fellenberg C, Böttcher C, Vogt T (2009) Phenylpropanoid polyamine conjugate biosynthesis in Arabidopsis thaliana flower buds. Phytochemistry 70:1392–1400

    Article  PubMed  CAS  Google Scholar 

  • 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)

  • Flores HE, Galston AW (1982) Polyamines and plant stress—activation of putrescine biosynthesis by osmotic shock. Science 217:1259–1261

    Article  PubMed  CAS  Google Scholar 

  • Galston AW (1991) On the trail of a new regulatory system in plants. New Biol 3:450–453

    PubMed  CAS  Google Scholar 

  • Galston AW, Kaur-Sawhney R (1990) Polyamines in plant physiology. Plant Physiol 94:406–410

    Article  PubMed  CAS  Google Scholar 

  • Ghosh B (2000) Polyamines and plant alkaloids. Indian J Exp Biol 38:1086–1091

    PubMed  CAS  Google Scholar 

  • Gill S, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 7:5(1). PMID: 20023386

    Google Scholar 

  • Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 346:769–771

    Article  PubMed  CAS  Google Scholar 

  • 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 58:246–259

    Article  PubMed  CAS  Google Scholar 

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    Article  PubMed  CAS  Google Scholar 

  • 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 16:581–589

    Article  PubMed  CAS  Google Scholar 

  • 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 210:195–201

    Article  PubMed  CAS  Google Scholar 

  • 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 27:551–560

    Article  PubMed  CAS  Google Scholar 

  • 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 19:4248–4256

    Article  PubMed  CAS  Google Scholar 

  • 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 449:105–180

    Article  PubMed  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271:559–564

    Article  PubMed  CAS  Google Scholar 

  • 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 549:26–30

    Article  PubMed  CAS  Google Scholar 

  • 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 556:148–152

    Article  PubMed  CAS  Google Scholar 

  • 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 135:1565–1573

    Article  PubMed  CAS  Google Scholar 

  • 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 38:1101–1111

    Article  PubMed  CAS  Google Scholar 

  • 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 544:258–261

    Article  PubMed  CAS  Google Scholar 

  • 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 19:2975–2987

    Article  PubMed  CAS  Google Scholar 

  • Johnson TD (1996) Modulation of channel function by polyamines. Trends Pharmacol Sci 17:22–27

    Article  PubMed  CAS  Google Scholar 

  • Kakehi JI, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349

    Article  PubMed  CAS  Google Scholar 

  • 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 49:1272–1282

    Article  PubMed  CAS  Google Scholar 

  • 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 121:101–107

    Article  PubMed  CAS  Google Scholar 

  • 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 45:712–722

    Article  PubMed  CAS  Google Scholar 

  • Knott JM, Romer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086

    Article  PubMed  CAS  Google Scholar 

  • 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 303:259–269

    Article  PubMed  CAS  Google Scholar 

  • 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 76:2541–2545

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Altabella T, Taylor MA, Tiburcio AF (1997) Recent advances in polyamine research. Trends Plant Sci 2:124–130

    Article  Google Scholar 

  • Kumria R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro morphogenesis and response to salt stress. J Plant Physiol 159:983–990

    Article  CAS  Google Scholar 

  • Kuppusamy K, Walcher C, Nemhauser J (2009) Cross-regulatory mechanisms in hormone signaling. Plant Mol Biol 69:375–381

    Article  PubMed  CAS  Google Scholar 

  • Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav 2:251–252

    PubMed  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  PubMed  CAS  Google Scholar 

  • 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 22:2623–2633

    Article  PubMed  CAS  Google Scholar 

  • 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 124:1315–1326

    Article  PubMed  CAS  Google Scholar 

  • 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 21:318–333

    Article  PubMed  CAS  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  PubMed  CAS  Google Scholar 

  • Malmberg RL, Watson MB, Galloway GL, Yu W (1998) Molecular genetic analyses of plant polyamines. Crit Rev Plant Sci 17:199–224

    Article  CAS  Google Scholar 

  • Martin-Tanguy J (1997) Conjugated polyamines and reproductive development: Biochemical, molecular and physiological approaches. Physiol Plant 100:675–688

    Article  CAS  Google Scholar 

  • 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 95:1294–1297

    Article  PubMed  CAS  Google Scholar 

  • Michael AJ, Furze JM, Rhodes MJC, Burtin D (1996) Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA. Biochem J 314:241–248

    PubMed  CAS  Google Scholar 

  • Michard E, Dreyer I, Lacombe B, Sentenac H, Thibaud JB (2005) Inward rectification of the AKT2 channel abolished by voltage-dependent phosphorylation. Plant J 44:783–797

    Article  PubMed  CAS  Google Scholar 

  • Minguet EG, Vera-Sirera F, Marina A, Carbonell J, Blazquez MA (2008) Evolutionary diversification in polyamine biosynthesis. Mol Biol Evol 25:2119–2128

    Article  PubMed  CAS  Google Scholar 

  • 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

  • Moller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis ATAO1 gene encoding an H2O2-generating diamine oxidase. Plant J 13:781–791

    Article  PubMed  CAS  Google Scholar 

  • Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism: the state of the art. Plant Signal Behav 3:1061–1066

    PubMed  Google Scholar 

  • 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 59:165–176

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Weigel D (2008) Next-generation genetics in plants. Nature 456:720–723

    Article  PubMed  CAS  Google Scholar 

  • Pandey S, Ranade SA, Nagar PK, Kumar N (2000) Role of polyamines and ethylene as modulators of plant senescence. J Biosci 25:291–299

    Article  PubMed  CAS  Google Scholar 

  • 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 14:2539–2551

    Article  PubMed  CAS  Google Scholar 

  • Pegg AE, Michael A (2009) Spermine synthase. Cell Mol Life Sci 67:113–121

    Article  PubMed  CAS  Google Scholar 

  • 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 130:1454–1463

    Article  PubMed  CAS  Google Scholar 

  • 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 278:1708–1712

    Article  PubMed  CAS  Google Scholar 

  • Rambla JL, Vera-Sirera F, Blázquez MA, Carbonell J, Granell A (2010) Quantitation of biogenic tetramines in Arabidopsis thaliana. Anal Biochem 397:208–211

    Article  PubMed  CAS  Google Scholar 

  • Richards FJ, Coleman RG (1952) Occurrence of putrescine in potassium-deficient barley. Nature 170:460

    Article  PubMed  CAS  Google Scholar 

  • Roberts SC, Jiang YQ, Jardim A, Carter NS, Heby O, Ullman B (2001) Genetic analysis of spermidine synthase from Leishmania donovani. Mol Biochem Parasitol 115:217–226

    Article  PubMed  CAS  Google Scholar 

  • Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875

    Article  PubMed  CAS  Google Scholar 

  • Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987–992

    Article  CAS  Google Scholar 

  • 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 160:197–207

    Article  PubMed  CAS  Google Scholar 

  • Seiler N, Raul F (2005) Polyamines and apoptosis. J Cell Mol Med 9:623–642

    Article  PubMed  CAS  Google Scholar 

  • 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 259:3204–3208

    Google Scholar 

  • Shabala S, Cuin TA, Pottosin I (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999

    Article  PubMed  CAS  Google Scholar 

  • 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 57:711–726

    Article  PubMed  CAS  Google Scholar 

  • 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 46:1292–1300

    CAS  Google Scholar 

  • 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 119:941–953

    Article  PubMed  CAS  Google Scholar 

  • Singh SS, Chauhan A, Brockerhoff H, Chauhan VPS (1995) Differential-effects of spermine on phosphatidylinositol 3-kinase and phosphatidylinositol phosphate 5-kinase. Life Sci 57:685–694

    Article  PubMed  CAS  Google Scholar 

  • Slocum RD, Kaur-Sawhney R, Galston AW (1984) The physiology and biochemistry of polyamines in plants. Arch Biochem Biophys 235:283–303

    Article  PubMed  CAS  Google Scholar 

  • Smith TA, Richards FJ (1964) The biosynthesis of putrescine in higher plants and its relation to potassium nutrition. Biochem J 84:292–294

    Google Scholar 

  • Soyka S, Heyer AG (1999) Arabidopsis knockout mutation of ADC2 gene reveals inducibility by osmotic stress. Febs Lett 458:219–223

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Kakehi J-I (2009) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6

    Article  CAS  Google Scholar 

  • 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 117:971–977

    Article  PubMed  CAS  Google Scholar 

  • Tassoni A, Napier RM, Franceschetti M, Venis MA, Bagni N (2002) Spermidine-binding proteins. Purification and expression analysis in maize. Plant Physiol 128:1303–1312

    Article  PubMed  CAS  Google Scholar 

  • 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 141:1519–1532

    Article  PubMed  CAS  Google Scholar 

  • 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 63:787–801

    Article  PubMed  CAS  Google Scholar 

  • 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 16-0

  • 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 47:346–354

    Article  PubMed  CAS  Google Scholar 

  • 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 26:1917–1926

    Article  CAS  Google Scholar 

  • 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 313:369–375

    Article  PubMed  CAS  Google Scholar 

  • Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–1564

    Article  PubMed  CAS  Google Scholar 

  • 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 57:1065–1078

    Article  PubMed  CAS  Google Scholar 

  • van Leeuwenhoek A (1678) Observationes D. Anthonii Leeuwenhoek, de natis e semine genitali animalculis. Philos Trans R Soc Lond 12:1040–1043

    Google Scholar 

  • 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 164:727–734

    Article  CAS  Google Scholar 

  • Walden R, Cordeiro A, Tiburcio AF (1997) Polyamines: Small molecules triggering pathways in plant growth and development. Plant Physiol 113:1009–1013

    Article  PubMed  CAS  Google Scholar 

  • 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 279:51370–51375

    Article  PubMed  CAS  Google Scholar 

  • 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 66:471–478

    Article  CAS  Google Scholar 

  • 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 13:209–220

    PubMed  CAS  Google Scholar 

  • 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 25:1111–1121

    Article  PubMed  CAS  Google Scholar 

  • 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 58:299–317

    Article  PubMed  CAS  Google Scholar 

  • 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 580:6783–6788

    Article  PubMed  CAS  Google Scholar 

  • 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 352:486–490

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki H, Cohen MF (2006) NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci 11:522–524

    Article  PubMed  CAS  Google Scholar 

  • 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 145:1061–1072

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We apologize to the researchers, whose works are not cited in this review due to space limitation. We are grateful to our past and present colleagues. Our research was supported by grants from the Ministerio de Educación y Ciencia, Spain (BIO2005-09252-C02-01 and BIO2008-05493-C02-01) and the Comissionat per Universitats i Recerca (Generalitat de Catalunya, SGR2009-1060). AFT, CK, MR, RA and PC also acknowledge grants-in-aid from COST-Action FA0605.

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Correspondence to Antonio F. Tiburcio.

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This review is dedicated to the memory of Prof. Arthur W. Galston (Yale University, New Haven, CT, USA) for his pioneering work and important contribution to the plant polyamine field.

R. Alcázar and T. Altabella contributed equally to this work.

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Alcázar, R., Altabella, T., Marco, F. et al. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237–1249 (2010). https://doi.org/10.1007/s00425-010-1130-0

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  • DOI: https://doi.org/10.1007/s00425-010-1130-0

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