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Plant polyamines in abiotic stress responses

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Abstract

Significance of naturally occurring intracellular polyamines (PAs), such as spermine, spermidine, and putrescine, in relation to the mechanism and adaptation to combat abiotic stress has been well established in plants. Because of their polycationic nature at physiological pH, PAs bind strongly to negative charges in cellular components such as nucleic acids, proteins, and phospholipids. Accumulation of the three main PAs occurs under many types of abiotic stress, and modulation of their biosynthetic pathway confers tolerance to drought or salt stress. Maintaining crop yield under adverse environmental conditions is probably the major challenge faced by modern agriculture, where PAs can play important role. Over the last two decades, genetic, transcriptomic, proteomic, metabolomic, and phenomic approaches have unraveled many significant functions of different PAs in the regulation of plant abiotic stress tolerance. In recent years, much attention has also been devoted to the involvement of PAs in ameliorating different environmental stresses such as osmotic stress, drought, heat, chilling, high light intensity, heavy metals, mineral nutrient deficiency, pH variation, and UV irradiation. The present review discusses the various reports on the role of PAs in the abiotic stress of plants with a note on current research tendencies and future perspectives. Co-relating all these data into a signal network model will be an uphill task, and solving this will give a clearer picture of the intricate abiotic stress signalling network in the plant kingdom.

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Abbreviations

ABA:

Abscisic acid

ADC:

Arginine decarboxylase

AIH:

Agmatine iminohydrolase

AOs:

Amine oxidases

CPA:

N‐Carbamoylputrescine amidohydrolase

CuAO:

Copper binding diamine oxidases

DAO:

Diamine oxidases

DAP:

Diaminopropane

DFMO:

α‐dl‐Difluoromethylornithine

GA:

Gibberelic acid

MGBG:

Methylglyoxal bis‐(guanylhydrazone)

MIPKs:

Mitogen‐activated protein kinases

NO:

Nitric oxide

ODC:

Ornithine decarboxylase

PA:

Polyamine

PAL:

Phenylalalnine ammonia lyase

PAO:

Polyamine oxidases

PCD:

Programmed cell death

PDH:

Pyrroline dehydrogenase

Put:

Putrescine

ROS:

Reactive oxygen species

SAM:

S‐Adenosylmethionine

SAMDC:

SAM decarboxylase

Spd:

Spermidine

Spm:

Spermine

SPDS:

Spermidine synthase

SPMS:

Spermine synthase

References

  • Alcázar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J, Bitrian M, Tiburcio AF, Altabella T (2010a) Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants overexpressing the homologous arginine decarboxylase 2 gene. Plant Physiol Biochem 48:547–552

    Article  PubMed  CAS  Google Scholar 

  • Alcázar R, Marco F, Cuevas JC, Patrón M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876

    Article  PubMed  CAS  Google Scholar 

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio A (2010b) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  PubMed  CAS  Google Scholar 

  • Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Salinas J, Tiburcio AF, Altabella T (2011) Integration of polyamines in the cold acclimation response. Plant Sci 180(1):31–38

    Article  PubMed  CAS  Google Scholar 

  • Alet AI, Sánchez DH, Cuevas JC, Marina M, Carrasco P, Altabella T, Tiburcio AF, Ruiz OA (2012) New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci 182:94–100

    Article  PubMed  CAS  Google Scholar 

  • An Z, Jing W, Zhang W (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 

  • Angelini R, Tisi A, Rea G, Chen MM, Botta M, Federico R, Cona A (2008) Involvement of polyamine oxidase in wound healing. Plant Physiol 146:162–177

    Article  PubMed  CAS  Google Scholar 

  • Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases “on the move”: an update. Plant Physiol Biochem 48:560–564

    Article  PubMed  CAS  Google Scholar 

  • Apel H, Kirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–379

    Article  PubMed  CAS  Google Scholar 

  • Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576

    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 

  • Bachrach U (2010) The early history of polyamine research. Plant Physiol Biochem 48(7):490–495

    Article  PubMed  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 

  • Bajguz A (2011) Suppression of Chlorella vulgaris growth by cadmium, lead, and copper stress and its restoration by endogenous brassinolide. Arch Environ Contam Toxicol 60:406–416

    Article  PubMed  CAS  Google Scholar 

  • Bassard JE, Ullmann P, Bernier F, Werck-Reichhart D (2010) Phenolamides: bridging polyamines to the phenolic metabolism. Phytochemistry 71:1808–1824

    Article  PubMed  CAS  Google Scholar 

  • Becker JV, Mtwisha L, Crampton BG, Stoychev S, van Brummelen AC et al (2010) Plasmodium falciparum spermidine synthase inhibition results in unique perturbation-specific effects observed on transcript, protein and metabolite levels. BMC Genomics 11:235

    Article  PubMed  CAS  Google Scholar 

  • Bell E, Malmberg RL (1990) Analysis of a cDNA encoding arginine decarboxylase from oat reveals similarity to the Escherichia coli arginine decarboxylase and evidence of protein processing. Mol Gen Genet 224:431–436

    Article  PubMed  CAS  Google Scholar 

  • Bhatnagar P, Glasheen BM, Bains SK, Long SL, Minocha R, Walter C, Minocha SC (2001) Transgenic manipulation of the metabolism of polyamines in poplar cells. Plant Physiol 125:2139–2153

    Article  PubMed  CAS  Google Scholar 

  • Bitrián M, Zarza X, Altabella T, Tiburcio AF, Alcázar R (2012) Polyamines under abiotic stress: metabolic crossroads and hormonal crosstalks in plants. Metabolites 2(3):516–528

    Article  CAS  Google Scholar 

  • Bolenius FN, Seiler N (1981) Acetylderivatives as intermediates in polyamine catabolism. Int J Biochem 13:287–292

    Article  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 

  • 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 

  • Camacho-Cristobal JJ, Maldonado JM, Gonza′lez-Fontes A (2005) Boron deficiency increases putrescine levels in tobacco plants. J Plant Physiol 162:921–928

    Article  PubMed  CAS  Google Scholar 

  • Camacho-Cristóbal JJ, Lunar L, Lafont F, Baumert A, González-Fontes A (2004) Boron deficiency causes accumulation of chlorogenic acid and caffeoyl polyamine conjugates in tobacco leaves. J Plant Physiol 161:879–881

    Article  PubMed  CAS  Google Scholar 

  • Campestre MP, Bordenave CD, Origone AC, Mene′ndez AB, Ruiz OA, Rodríguez AA, Maiale SJ (2011) Polyamine catabolism is involved in response to salt stress in soybean hypocotyls. J Plant Physiol. doi:10.1016/j.jplph.2011.01.007

    PubMed  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 101:9909–9914

    Article  PubMed  CAS  Google Scholar 

  • Casero RA Jr, Marton LJ (2007) Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 6:373–390

    Article  PubMed  CAS  Google Scholar 

  • Castiglione S, Todeschini V, Franchin C, Torrigiani P, Gastaldi D, Cicatelli A, Rinaudo C, Berta G, Biondi S, Lingua G (2009) Clonal differences in survival capacity, copper and zinc accumulation, and correlation with leaf polyamine levels in poplar: a large-scale field trial on heavily polluted soil. Environ Pollut 157(7):2108–2117

    Google Scholar 

  • Cervelli M, Cona A, Angelini R, Polticelli F, Federico R, Mariottini P (2001) A barley polyamine oxidase isoform with distinct structural features and subcellular localization. Eur J Biochem 268:3816–3830

    Article  PubMed  CAS  Google Scholar 

  • Cervelli M, Caro OD, Penta AD, Angelini R, Federico R, Vitale A, Mariottini P (2004) A novel C-terminal sequence from barley polyamine oxidase is a vacuolar sorting signal. Plant J 40:410–418

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199

    Article  PubMed  CAS  Google Scholar 

  • Cheng L, Zou Y, Ding S, Zhang J, Yu X, Cao J, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integrative Plant Biol 51:489–499

    Article  CAS  Google Scholar 

  • Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LS (2012a) Chromium stress mitigation by polyamine–brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS One 7:e33210

    Article  PubMed  CAS  Google Scholar 

  • Choudhary SP, Oral HV, Bhardwaj R, Yu JQ, Tran LSP (2012b) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63(15):5659–5675

    Article  PubMed  CAS  Google Scholar 

  • Ciamician G, Ravenna C (1911) cited by Smith TA, Historical perspective on research in plant polyamine biology. In: Slocum RD, Flores HE (eds) Biochemistry and Physiology of Polyamines in Plants. CRC Press, Boca Raton, p 2

    Google Scholar 

  • Clay NK, Nelson T (2005) Arabidopsis thick vein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol 138:767–777

    Article  PubMed  CAS  Google Scholar 

  • Cohen SS (1998) A guide to the polyamines. Oxford University Press, New York

    Google Scholar 

  • Cohen AS, Popovic RB, Zalik S (1979) Effects of polyamines on chlorophyll and protein content, photochemical activity, and chloroplast ultrastructure of barley leaf discs during senescence. Plant Physiol 64:717–720

    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 

  • Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci 101:15243–15248

    Article  PubMed  CAS  Google Scholar 

  • Cowley T, Walters DR (2005) Local and systemic changes in arginine decarboxylase activity, putrescine levels and putrescine catabolism in wounded oilseed rape. New Phytol 156:807–811

    Google Scholar 

  • Cuevas JC, Lopez-Cobollo R, Alcazar 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  CAS  Google Scholar 

  • Cuevas JC, Lopez-Cobollo R, Alcázar 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 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  PubMed  CAS  Google Scholar 

  • Cvikrová M, Gemperlová L, Dobrá J, Martincová O, Prásil IT, Gubis J, Vanková R (2012) Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Sci 182:49–58

    Article  PubMed  CAS  Google Scholar 

  • Danon A, Botari VI, Gordon A, Mailhac N, Gallois P (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35, and defender against apoptotic death. J Biol Chem 279:779–787

    Article  PubMed  CAS  Google Scholar 

  • de Agazio M, Federico R, Angelini R, De Cesare F, Grego S (1992) Spermidine pretreatment or root tip removal in maize seedlings: effects on K+ uptake and tissue modifications. J Plant Physiol 140:741–746

    Article  Google Scholar 

  • Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus: the protective role of polyamines. Biochim Biophys Acta 1767:272–280

    Article  PubMed  CAS  Google Scholar 

  • Di Tomaso JM, Hart JJ, Kochian LV (1992) Transport kinetics and metabolism of exogenously applied putrescine in roots of intact maize seedlings. Plant Physiol 98:611–662

    Article  Google Scholar 

  • Dickinson BC, Chang CJ (2011) Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 7(8):504–511

    Article  PubMed  CAS  Google Scholar 

  • Dittami SM, Gravot A, Renault D, Goulitquer S, Eggert A, Bouchereau A, Boyen C, Tonon T (2011) Integrative analysis of metabolite and transcript abundance during the short-term response to saline and oxidative stress in the brown alga Ectocarpus siliculosus. Plant Cell Environ 34(4):629–642. doi:10.1111/j.1365-3040.2010.02268.x

    Article  PubMed  CAS  Google Scholar 

  • Dufe VT, Lürsen K, Eschbach ML, Haider N, Karlberg T, Walter RD, Al-Karadaghi S (2005) Cloning, expression, characterization and three-dimensional structure determination of Caenorhabditis elegans spermidine synthase. FEBS Lett 579:6037–6043

    Article  PubMed  CAS  Google Scholar 

  • Dutra NT, Silveira V, de Azevedo IG, Gomes-Neto LR, Façanha AR, Steiner N, Guerra MP, Floh EIS, Santa-Catarina C (2012) Polyamines affect the cellular growth and structure of pro-embryogenic masses in Araucaria angustifolia embryogenic cultures through the modulation of proton pump activities and endogenous levels of polyamines. Physiol Plant. doi:10.1111/j.1399-3054.2012.01695.x

    PubMed  Google Scholar 

  • Edreva AM, Velikova VB, Tsonov TD (2007) Phenylamides in plants. Russ J Plant Physiol 54:289–302

    Article  CAS  Google Scholar 

  • Evans PT, Malmberg RL (1989) Do polyamines have roles in plant development? Annu Rev Plant Physiol Plant Mol Biol 40:235–269

    Article  CAS  Google Scholar 

  • Facchini PJ, Hagel J, Zulak KG (2002) Hydroxycinnamic acid amide metabolism: physiology and biochemistry. Can J Bot 80:577–589

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Lee DJ (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiologiae Plantarum 31(5):937–945

    Article  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 

  • Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radical Biol Med 56:172–183. doi:10.1016/j.freeradbiomed.2012.09.037

  • Fincato P, Moschou PN, Ahou A, Angelini R, Roubelakis-Angelakis KA, Federico R, Tavladoraki P (2012) The members of Arabidopsis thaliana PAO gene family exhibit distinct tissue- and organ-specific expression pattern during seedling growth and flower development. Amino Acids 42:831–841

    Article  PubMed  CAS  Google Scholar 

  • Finkel E (2009) With ‘phenomics’, plant scientists hope to shift breeding into overdrive. Science 325:380–381

    Article  PubMed  CAS  Google Scholar 

  • Flores HE (1991) Changes in polyamine metabolism in response to abiotic stress. In: Slocum RD, Flores HE (eds) The biochemistry and physiology of polyamines in plants. CRC Press, Boca Raton, pp 214–255

    Google Scholar 

  • Flores HE, Filner P (1985) Polyamine catabolism in higher plants: characterization of pyrroline dehydrogenase. Plant Growth Reg 3:277–291

    Article  CAS  Google Scholar 

  • Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48(7):513–520

    Article  PubMed  CAS  Google Scholar 

  • Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio AF (1997) Plant polyamines in reproductive activity and response to abiotic stress. Bot Acta 110:197–207

    CAS  Google Scholar 

  • Garcıa-Jimenez P, Just PM, Delgado AM, Robaina RR (2007) Transglutaminase activity decrease during acclimation to hyposaline conditions in marine seaweed Grateloupia doryphora (Rhodophyta, Halymeniaceae). J Plant Physiol 164:367–370

    Article  PubMed  CAS  Google Scholar 

  • Ge C, Cui X, Wang Y, Hu Y, Fu Z, Zhang D, Cheng Z, Li J (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456

    Article  PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33

    Article  PubMed  CAS  Google Scholar 

  • Grienenberger E, Besseau S, GeoVroy 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 

  • Groppa MD, Benavides MP, Tomaro ML (2003) Polyamine metabolism in sunflower and wheat leaf discs under cadmium or copper stress. Plant Sci 164:293–299

    Article  CAS  Google Scholar 

  • Grün S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516

    Article  PubMed  CAS  Google Scholar 

  • Gupta B, Gupta K, Sengupta DN (2012a) Spermidine-mediated in vitro phosphorylation of transcriptional regulator OSBZ8 by SNF1-type serine/threonine protein kinase SAPK4 homolog in indica rice. Acta Physiol Plant 34(4):1321–1336

    Article  Google Scholar 

  • Gupta K, Gupta B, Ghosh B, Sengupta DN (2012b) Spermidine and abscisic acid-mediated phosphorylation of a cytoplasmic protein from rice root in response to salinity stress. Acta Physiol Plant 34(1):29–40. doi:10.1007/s11738-011-0802-0

    Article  CAS  Google Scholar 

  • Guye MG, Vigh L, Wilson JM (1986) Polyamine titer in relation to chill-sensitivity in Phaseolus sp. J Exp Bot 37:1036–1043

    Article  CAS  Google Scholar 

  • Hamana K, Matsuzaki S (1985) Distinct difference in the polyamine compositions of bryophyta and pteridophyta. J Biochem 97:1595–1601

    PubMed  CAS  Google Scholar 

  • Hancock JT (2012) NO synthase? Generation of nitric oxide in plants. Periodicum Biologorum 114(1):19–24

    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 

  • Hanzawa Y, Imai A, Michael AJ, Komeda Y, Takahashi T (2002) Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana. FEBS Lett 527:176–180

    Article  PubMed  CAS  Google Scholar 

  • He LX, Nada K, Kasukabe Y, Tachibana S (2002a) Enhanced susceptibility of photosynthesis to low-temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxylase activity in leaves of spinach (Spinacia oleracea L.). Plant Cell Physiol 43:196–206

    Article  PubMed  CAS  Google Scholar 

  • He LX, Nada K, Tachibana S (2002b) Effects of spermidine pretreatment through the roots on growth and photosynthesis of chilled cucumber plants (Cucumis sativus L.). J Jpn Soc Hortic Sci 71:490–498

    Article  CAS  Google Scholar 

  • Heim WG, Sykes KA, Hildreth SB, Sun J, Lu RH, Jelesko JG (2007) Cloning and characterization of a Nicotiana tabacum methylputrescine oxidase transcript. Phytochemistry 68:454–463

    Article  PubMed  CAS  Google Scholar 

  • Hewezi T, Howe PJ, Maier TR, Hessey RS, Mitchum MG, Davis EL, Baum TJ (2010) Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol 152:968–984

    Article  PubMed  CAS  Google Scholar 

  • Houdusse F, Zamarreno AM, Garnica M, Garcia-Mina J (2005) The importance of nitrate in ameliorating the effects of ammonium and urea nutrition on plant development: the relationships with free polyamines and plant proline contents. Func Plant Biol 32:1057–1067

    Article  CAS  Google Scholar 

  • Hu WW, Gong H, Pua EC (2005) Molecular cloning and characterization of S-adenosyl methionine decarboxylase genes from mustard (Brassica juncea). Plant Physiol 124:25–40

    Article  CAS  Google Scholar 

  • Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708

    Article  PubMed  CAS  Google Scholar 

  • Hummel I, Gouesbet G, El Amrani A, Ainouche A, Couee I (2004) Characterization of the two arginine decarboxylase (polyamine biosynthesis) paralogues of the endemic subantarctic cruciferous species Pringlea antiscorbutica and analysis of their differential expression during development and response to environmental stress. Gene 342:199–209

    Article  PubMed  CAS  Google Scholar 

  • Hussain SS, Ali M, Ahmad M, Siddique KH (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29(3):300–311

    Article  PubMed  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (2006) Bacterial and eukaryotic transport systems. In: Wang J-Y, Casero RA Jr (eds) Polyamine Cell Signaling. Human Press, New Jersey, pp 433–448

    Chapter  Google Scholar 

  • Igarashi K, Kashiwagi K (2010) Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 48:506–512

    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 

  • Jantaro S, Mäenpää P, Mulo P, Incharoensakdi A (2003) Content and biosynthesis of polyamines in salt and osmotically stressed cells of Synechocystis sp. PCC 680. FEMS Microbiol Lett 228:129–135

    Article  PubMed  CAS  Google Scholar 

  • Kakinuma Y, Maruyama T, Nozaki T, Wada Y, Ohsumi Y, Igarashi K (1994) Cloning of the gene encoding a putative serine/threonine protein kinase which enhances spermine uptake in Saccharomyces cerevisiae. Biochim Biophys Acta 1194:289–295

    Article  PubMed  Google Scholar 

  • Kaouass M, Audette M, Ramotar D, Verma S, DeMontigny D, Gamache I, Torossian K, Poulin R (1997) The STK2 gene, which encodes a putative Ser/Thr protein kinase, is required for high-affinity spermidine transport in Saccharomyces cerevisiae. Mol Cell Biol 17:2994–3004

    PubMed  CAS  Google Scholar 

  • Kaouass M, Gamache I, Ramotar D, Audette M, Poulin R (1998) The spermidine transport system is regulated by ligandi nactivation endocytosis, and by the Npr1p Ser/Thr protein kinase in Saccharomyces cerevisiae. J Biol Chem 273:2109–2117

    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 L, 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 

  • Katoh A, Shoji T, Hashimoto T (2007) Molecular cloning of N-methylputrescine oxidase from tobacco. Plant Cell Physiol 48:550–554

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Kaur-Sawhney R, Tiburcio AF, Atabella T, Galston AW (2003) Polyamines in plants: an overview. J Cell Mol Biol 2:1–12

    Google Scholar 

  • Kim TE, Kim SK, Han TJ, Lee JS, Chang SC (2002) ABA and polyamines act independently in primary leaves of cold-stressed tomato (Lycopersicon esculentum). Physiol Plant 115:370–376

    Article  PubMed  CAS  Google Scholar 

  • Kitashiba H, Hao YJ, Honda C, Moriguchi T (2005) Two types of spermine synthase gene: mdACL5 and MdSPMS are diVerentially involved in apple fruit development and cell growth. Gene 361:101–111

    Article  PubMed  CAS  Google Scholar 

  • Knott JM, Römer 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 

  • Korolev S, Ikeguchi Y, Skarina T, Beasley S, Arrowsmith C, Edwards A, Joachimiak A, Pegg AE, Savchenko A (2002) The crystal structure of spermidine synthase with a multisubstrate adduct inhibitor. Nat Struct Biol 9:27–31

    Article  PubMed  CAS  Google Scholar 

  • Kramer GF, Wang CY (1989) Correlation of reduced chilling injury with increased spermine and spermidine levels in zucchini squash. Physiol Plant 76:479–484

    Article  CAS  Google Scholar 

  • Krishnamurthy R (1991) Amelioration of salinity effect in salt tolerant rice (Oryza sativa L.) by foliar application of putrescine. Plant Cell Physiol 32:699–703

    CAS  Google Scholar 

  • Krishnamurthy R, Bhagwat KA (1989) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol 91:500–504

    Article  PubMed  CAS  Google Scholar 

  • Kubis J (2003) Polyamines and “scavenging system”: influence of exogenous spermidine on catalase and guaiacol peroxidise activities and free polyamine level in barley leaves under water deficit. Acta Physiol Plant 25:337–343

    Article  CAS  Google Scholar 

  • Kubiś J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. J Plant Physiol 165:397–406

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

    Article  PubMed  CAS  Google Scholar 

  • Kuthanová A, Gemperlová L, Zelenková S, Eder J, Macháčková I, Opatrńy Z, Cvikrová M (2004) Cytological changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells. Plant Physiol Biochem 42:149–156

    Article  PubMed  CAS  Google Scholar 

  • Ladenburg A, Abel J (1888) Überdasaethylenimin (spermine). Ber Dtsch Chem Ges 21:758–766

    Article  Google Scholar 

  • Landry J, Sternglanz R (2003) Yeast Fms1 is a FAD-utilizing polyamine oxidase. Biochem Biophys Res Commun 303:771–776

    Article  PubMed  CAS  Google Scholar 

  • Lee TM, Lur HS, Chu C (1997) Role of abscisic acid in chilling tolerance of rice (Oryza sativa L.) seedlings. 2. Modulation of free polyamine levels. Plant Sci 126:1–10

    Article  CAS  Google Scholar 

  • Leete E (1980) The alkaloids. In: Bell EA, Charwood BV (eds) Encyclopedia of plant physiology. New series, vol 8. Springer, Berlin, pp 65–91

  • Legocka J, Kluk A (2005) Effect of salt and osmotic stress on changes in polyamine content and arginine decarboxylase activity in Lupinus luteus seedlings. J Plant Physiol 162:662–668

    Article  PubMed  CAS  Google Scholar 

  • Lie K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1326

    Article  Google Scholar 

  • Lin CC, Kao CH (2002) NaCl-induced changes in putrescine content and diamine oxidase activity in roots of rice seedlings. Biol Plant 45:633–636

    Article  CAS  Google Scholar 

  • Liu JH, Nada K, Honda C, Kitashiba H, Wen XP, Pang XM, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot 57:2589–2599

    Article  PubMed  CAS  Google Scholar 

  • Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotech 24:117–126

    Article  CAS  Google Scholar 

  • Liu JH, Nakajima I, Moriguchi T (2011) Effects of salt and osmotic stresses on free polyamine content and expression of polyamine biosynthetic genes in Vitis vinifera. Biol Plant 55:340–344

    Article  CAS  Google Scholar 

  • Logothetis K, Dakanali S, Ioannidis N, Kotzabasis K (2004) The impact of high CO2 concentrations on the structure and function of the photosynthetic apparatus and the role of polyamines. J Plant Physiol 161:715–724

    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, Pandey GK, Tuteja N (2008) Calcium-and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471(2):146–158

    Article  PubMed  CAS  Google Scholar 

  • Maiale S, Sanchez DH, Guirado A, Vidal A, Ruiz OA (2004) Spermine accumulation under salt stress. J Plant Physiol 161:35–42

    Article  PubMed  CAS  Google Scholar 

  • Mapelli S, Brambilla IM, Radyukina NL, Yu V, Ivanov AV, Kartashov R, Reggiani Vl, Kuznetsov V (2008) Free and bound polyamines changes in different plants as a consequence of UV-B light irradiation. Gen Appl Plant Physiol 34(1–2):55–66

    CAS  Google Scholar 

  • Marina M, Maiale SJ, Rossi FR, Romero MF, Rivas EI, Ga′rriz A, Ruiz OA, Pieckenstain FL (2008) Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava. Plant Physiol 147:2164–2178

    Article  PubMed  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 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Plant Physiol 133:481–489

    Article  CAS  Google Scholar 

  • Minguet EG, Vera-Sirera F, Marina A, Carbonell J, Blázquez MA (2008) Evolutionary diversification in polyamine biosynthesis. Mol Biol Evol 25(10):2119–2128

    Article  PubMed  CAS  Google Scholar 

  • Mitchell JL, Judd GG, Bareyal-Leyser A, Ling SY (1994) Feedback repression of polyamine transport is mediated by antizyme in mammalian tissue-culture cells. Biochemical Journal 299:19–22

    Google Scholar 

  • Mo H, Pua EC (2002) Up-regulation of arginine decarboxylase gene expression and accumulation of polyamines in mustard (Brassica juncea) in response to stress. Plant Physiol 114:439–449

    Article  CAS  Google Scholar 

  • 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, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008a) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008c) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147(4):1845–1857

    Article  PubMed  CAS  Google Scholar 

  • Moschou PN, Sarris PF, Skandalis N, Andriopoulou AH, Paschalidis KA, Panopoulos NJ, Roubelakis-Angelakis KA (2009) Engineered polyamine catabolism preinduces tolerance of tobacco to bacteria and oomycetes. Plant Physiol 149:1970–1981

    Article  PubMed  CAS  Google Scholar 

  • Moschou PN, Wu J, Cona A, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63(14):5003–5015

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee K, Roy Choudhury A, Gupta B, Gupta S, Sengupta DN (2006) An ABRE-binding factor, OSBZ8, is highly expressed in salt tolerant cultivars than in salt sensitive cultivars of indica rice. BMC Plant Biol 6:18

    Article  PubMed  CAS  Google Scholar 

  • Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blázquez MA, Tuominen H (2008) ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2573–2582

    Article  PubMed  CAS  Google Scholar 

  • Nadeau P, Delaney S, Chouinard L (1987) Effects of cold hardening on the regulation of polyamine levels in wheat (Triticum aestivum L.) and alfalfa (Medicago sativa L.). Plant Physiol 84:73–77

    Article  PubMed  CAS  Google Scholar 

  • Navakoudis E, Lütz C, Langebartels C, Lütz-Meindl U, Kotzabasis K (2003) Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochim Biophys Acta 1621:160–169

    Article  PubMed  CAS  Google Scholar 

  • Navakoudis E, Vrentzou K, Kotzabasis K (2007) A polyamine- and LHCII protease activity-based mechanism regulates the plasticity and adaptation status of the photosynthetic apparatus. Biochim Biophys Acta 1767:261–271

    Article  PubMed  CAS  Google Scholar 

  • Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci 190(5):355–365

    Article  CAS  Google Scholar 

  • Ndayiragije A, Lutts S (2006) Do exogenous polyamines have an impact on the response of a salt-sensitive rice cultivar to NaCl? J Plant Physiol 163:506–516

    Article  PubMed  CAS  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35

    Article  CAS  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 

  • Nozaki T, Nishimura K, Michael AJ, Maruyama T, Kakinuma Y, Igarashi K (1995) A second gene encoding a putative serine/threonine protein kinase which enhances spermine uptake in Saccharomyces cerevisiae. Biochem Biophys Res Commun 216:985–992

    Article  PubMed  Google Scholar 

  • Ogawa S, Mitsuya S (2012) S-methylmethionine is involved in the salinity tolerance of Arabidopsis thaliana plants at germination and early growth stages. Physiol Plant 144:13–19

    Article  PubMed  CAS  Google Scholar 

  • Ono Y, Kim DW, Watanabe K, Sasaki A, Niitsu M, Berberich T, Kusano T, Takahashi Y (2012) Constitutively and highly expressed Oryza sativa polyamine oxidases localize in peroxisomes and catalyze polyamine back conversion. Amino Acids 42(2):867–876

    Article  PubMed  CAS  Google Scholar 

  • Oshima T (2007) Unique polyamines produced by an extreme thermophile, Thermus thermophilus. Amino Acids 33:367–372

    Article  PubMed  CAS  Google Scholar 

  • Palavan-Unsal N, Arisan D (2009) Nitric oxide signalling in plants. Bot Rev 75:203–229

    Article  Google Scholar 

  • Panicot M, Minguet EG, Ferrando A, Alcazar 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 

  • Paschalidis KA, Toumi I, Moschou PN, Roubelakis-Angelakis KA (2010) ABA-dependent amine oxidases-derived H2O2 affects stomata conductance. Plant Signal Behav 5(9):1153–1156

    Article  CAS  Google Scholar 

  • Pegg AE (2009) Mammalian polyamine metabolism and function. IUBMB Life 61(9):880–894

    Article  PubMed  CAS  Google Scholar 

  • Peleg Z, Blumwald E (2010) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295

    Article  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 hydrolase and the identification of plant N-carbamoylputrescine amidohydrolase involved in polyamine biosynthesis. J Biol Chem 278:1708–1712

    Article  PubMed  CAS  Google Scholar 

  • Pistocchi R, Bagni N, Creus JA (1987) Polyamine uptake in carrot cell cultures. Plant Physiol 84:374–380

    Article  PubMed  CAS  Google Scholar 

  • Popovic RB, Kyle DJ, Cohen AS, Zalik S (1979) Stabilization of thylakoid membranes by spermine during stress induced senescence of barley leaf discs. Plant Physiol 64:721–726

    Article  PubMed  CAS  Google Scholar 

  • Prabhavathi VR, Rajam MV (2007) Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol 24:273–282

    Article  CAS  Google Scholar 

  • Quinet M, Ndayiragije A, Lefèvre I, Lambillotte B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733

    Article  PubMed  CAS  Google Scholar 

  • Radhakrishnan R, Lee IJ (2013) Ameliorative effects of spermine against osmotic stress through antioxidants and abscisic acid changes in soybean pods and seeds. Acta Physiol Plant 35:263–269

    Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  PubMed  CAS  Google Scholar 

  • Rea G, Metoui O, Infantino A, Federico R, Angelini R (2002) Copper amine oxidase expression in defence responses to wounding and Ascochyta rabiei invasion. Plant Physiol 128:865–875

    Article  PubMed  CAS  Google Scholar 

  • Reape TJ, McCabe PF (2008) Apoptotic-like programmed cell death in plants. New Phytol 180:13–26

    Article  PubMed  CAS  Google Scholar 

  • Rhee SG (2006) H2O2, a necessary evil for cell signaling. Science 312(5782):1882–1883

    Article  PubMed  Google Scholar 

  • Rodríguez AA, Maiale SJ, Mene′ndez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongationn under saline stress. J Exp Bot 60:4249–4262

    Article  PubMed  CAS  Google Scholar 

  • Rosales EP, Iannone MF, Groppa MD, Benavides MP (2012) Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide. Amino Acids 42(2):857–865

    Article  PubMed  CAS  Google Scholar 

  • Rosenheim O (1924) The isolation of spermine phosphate from semen and testis. Biochem J 18:1253–1263

    PubMed  CAS  Google Scholar 

  • Roy M, Ghosh B (1996) Polyamines, both common and uncommon, under heat stress in rice (Oryza sativa) callus. Physiol Plant 98:196–200

    Article  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 

  • Roy P, Niyogi K, Sengupta DN, Ghosh B (2005) Spermidine treatment to rice seedlings recovers salinity stress induced damage of Plasma membrane and PM-bound H+-ATPase in salt-tolerant and salt sensitive rice cultivars. Plant Sci 168:583–591

    Article  CAS  Google Scholar 

  • RoyChoudhury A, Gupta B, Sengupta DN (2008) Trans-acting factor designated OSBZ8 interacts with both typical abscisic acid responsive elements as well as abscisic acid responsive element like sequences in the vegetative tissues of indica rice cultivars. Plant Cell Rep 27:779–794

    Article  PubMed  CAS  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168(4):317–328

    Article  PubMed  CAS  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2012) Antioxidants and stress-related metabolites in the seedlings of two indica rice varieties exposed to cadmium chloride toxicity. Acta Physiol Plant 34(3):835–847

    Google Scholar 

  • Sagor GH, Berberich T, Takahashi Y, Niitsu M, Kusano T (2012) The polyamine spermine protects Arabidopsis from heat stress induced damage by increasing expression of heat shock-related genes. Transgenic Res. doi:10.1007/s11248-012-9666-3

  • Schreiner P (1878) Über eine neue organische basis inthierischen organismen. Liebigs Ann 194:68–84

    Article  Google Scholar 

  • Sfichi L, Ioannidis N, Kotzabasis K (2004) Thylakoid-associated polyamines adjust the UV-B sensitivity of the photosynthetic apparatus by means of light-harvesting complex II changes. Photochem Photobiol 80:499–506

    PubMed  CAS  Google Scholar 

  • Shen WY, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439

    Article  PubMed  CAS  Google Scholar 

  • Shevyakova NI, Cheremisina AI, Kuznetsov VV (2011) Phytoremediation potential of amaranthus hybrids: antagonism between nickel and iron and chelating role of polyamines. Russ J Plant Physiol 58(4):634–642

    Article  CAS  Google Scholar 

  • Slocum RD (1991) Polyamine biosynthesis in plants. In: Slocum RD, Flores HE (eds) The biochemistry and physiology of polyamines in plants. CRC Press, Boca Raton, pp 23–40

    Google Scholar 

  • Soulet D, Gagnon B, Rivest S, Audette M, Poulin R (2004) A Xuorescent probe of polyamine transport accumulates into intracellular acidic vesicles via a two-step mechanism. J Biol Chem 279:49355–49366

    Article  PubMed  CAS  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 

  • Sung MS, Chow TJ, Lee TM (2011) Polyamine acclimation alleviates hypersalinity-induced oxidative stress in a marine green macroalga, Ulva fasciata, by modulation of antioxidative enzyme gene expression. J Phycol 47(3):538–547

    Article  CAS  Google Scholar 

  • Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749–790

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105(1):1–6

    Article  PubMed  CAS  Google Scholar 

  • Tassoni A, Franceschetti M, Bagni N (2008) Polyamines and salt stress response and tolerance in Arabidopsis thaliana flowers. Plant Physiol Biochem 46(5):607–613

    Article  PubMed  CAS  Google Scholar 

  • Tassoni A, Bagni N, Ferri M, Franceschetti M, Khomutov A, Marques MP, Serafini-Fracassini D (2010) Helianthus tuberosus and polyamine research: past and recent applications of a classical growth model. Plant Physiol Biochem 48(7):496–505

    Article  PubMed  CAS  Google Scholar 

  • Tavladoraki P, Schininà ME, Cecconi F, Di Agostino S, Manera F, Rea G, Mariottini P, Federico R, Angelini R (1998) Maize polyamine oxidase: primary structure from protein and cDNA sequencing. FEBS Lett 426:62–66

    Article  PubMed  CAS  Google Scholar 

  • Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Ferderico 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 

  • Tavladoraki P, Alessandra Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Toninello A, Agostinelli E (2012) Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids 42:411–426

    Article  PubMed  CAS  Google Scholar 

  • Theocharis A, Cle′ment EA, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    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, pp 283–325. ISBN 0-12-675416-0

    Google Scholar 

  • Tipping AJ, McPherson MJ (1995) Cloning and molecular analysis of the pea seedling copper amine oxidase. J Biol Chem 270:16939–16946

    Article  PubMed  CAS  Google Scholar 

  • Tisi A, Angelini R, Cona A (2011a) Does polyamine catabolism influence root development and xylem differentiation under stress conditions? Plant Signal Behav 6:1–4

    Article  CAS  Google Scholar 

  • Tisi A, Federico R, Moreno S, Lucretti S, Moschou PN, Roubelakis-Angelakis KA, Angelini R, Cona A (2011b) Perturbation of polyamine catabolism can strongly affect root development and xylem differentiation. Plant Physiol 157:200–215

    Article  PubMed  CAS  Google Scholar 

  • Tossi V, Lamattina L, Cassia R (2009) An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive response to UV-B irradiation. New Phytol 181:871–879

    Article  PubMed  CAS  Google Scholar 

  • Toumi I, Moschou PN, Paschalidis KA, Bouamama B, Salem-fnayou AB, Ghorbel AW, Mliki A, Roubelakis-Angelakis KA (2010) Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine. J Plant Physiol 167:519–525

    Article  PubMed  CAS  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveria 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 

  • Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Signal Behav 3(8):525–536

    Article  PubMed  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, 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 

  • Usadel B, Blasing OE, Gibon Y, Poree F, Hohne M, Gunter M, Trethewey R, Kamlage B, Poorter H, Stitt M (2008) Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ 31:518–547

    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 

  • Velarde-Buendía AM, Shabala S, Cvikrova M, Dobrovinskaya O, Pottosin I (2012) Salt sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines. Plant Physiol Biochem 61:18–23

    Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151(1):59–66

    Article  CAS  Google Scholar 

  • Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blázquez MA, Carbonell J (2010) Role of polyamines in plant vascular development. Plant Physiol Biochem 48:534–539

    Article  PubMed  CAS  Google Scholar 

  • Vergnolle C, Vaultier MN, Taconnat L, Renou JP, Kader JC, Zachowski A, Ruelland E (2005) The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions. Plant Physiol 139:1217–1233

    Article  PubMed  CAS  Google Scholar 

  • Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669–677

    Article  PubMed  CAS  Google Scholar 

  • Vl Kuznetsov, Shevyakova NI (2007) Polyamines and stress tolerance of plants. Plant Stress 1:50–71

    Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Article  PubMed  CAS  Google Scholar 

  • Vujcic S, Diegelmann P, Bacchi CJ, Kramer DL, Porter CW (2002) Identification and characterization of a novel Xavin-containing spermine oxidase of mammalian cell origin. Biochem J 367:665–675

    Article  PubMed  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 

  • Wallace HM, Duthie J, Evans DM, Lamond S, Nicoll KM, Heys SD (2000) Alterations in polyamine catabolic enzymes in human breast cancer tissue. Clin Cancer Res 6:3657–3661

    PubMed  CAS  Google Scholar 

  • Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Devereux W, Woster PM, Stewart TM, Hacker A, Casero RA Jr (2001) Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 61:5370–5373

    PubMed  CAS  Google Scholar 

  • Wang H, Huang J, Liang W, Liang X, Bi Y (2012) Involvement of putrescine and nitric oxide in aluminum tolerance by modulating citrate secretion from roots of red kidney bean. Plant Soil. doi:10.1007/s11104-012-1447-5

  • Watson MB, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L.) Heynh arginine decarboxilase by potassium deficiency stress. Plant Physiol 111:1077–1083

    Article  PubMed  CAS  Google Scholar 

  • Watson MW, Yu W, Galloway GL, Malmberg RL (1997) Isolation and characterization of a second arginine decarboxylase cDNA from Arabidopsis (PGR97–114). Plant Physiol 114:1569

    Google Scholar 

  • Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T (2010) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res 19:91–103

    Article  PubMed  CAS  Google Scholar 

  • White JW, Andrade-Sanchez P, Gore MA, Bronson KF, Coffelt TA, Conley MM et al (2012) Field-based phenomics for plant genetics research. Field Crop Res 133:101–112

    Article  Google Scholar 

  • Wimalasekara R, Tebartz F, Scherer GFE (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Science 181:593–603

    Google Scholar 

  • Wu G, Bazer FW, Hu J, Hohnson GA, Spencer TE (2005) Polyamine synthesis from proline in the developing porcine placenta. Biol Reprod 72:842–850

    Article  PubMed  CAS  Google Scholar 

  • Xing SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of c-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45:560–566

    Article  PubMed  CAS  Google Scholar 

  • Xiong H, Stanly BA, Tekwani BL, Pegg AE (1997) Processing of mammalian and plant Sadenosylmethionine decarboxylase proenzymes. J Biol Chem 272:28342–28348

    Article  PubMed  CAS  Google Scholar 

  • Xue B, Zhang A, Jiang M (2009) Involvement of polyamine oxidase in abscisic acid-induced cytosolic antioxidant defense in leaves of maize. J Integr Plant Biol 51:225–234

    Article  PubMed  CAS  Google Scholar 

  • Radhakrishnan R, Lee IJ (2012) Ameliorative effects of spermine against osmotic stress through antioxidants and abscisic acid changes in soybean pods and seeds. Acta Physiologiae Plantarum 1–7. doi:10.1007/s11738-012-1072-1

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael AJ, Kusano T (2006) The polyamine spermine protects against high salinity stress in Arabidopsis. FEBS Lett 580:67783–76788

    Article  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 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature, or high salt stress. Plant Cell 6:251–264

    PubMed  CAS  Google Scholar 

  • Yamakawa H, Kamada H, Satoh M, Ohashi Y (1998) Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus infection. Plant Physiol 118:213–1222

    Article  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 

  • Yoda H, Hamaguchi R, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol 132:1973–1981

    Article  PubMed  CAS  Google Scholar 

  • Yoda H, Hiroi Y, Sano H (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142:193–206

    Article  PubMed  CAS  Google Scholar 

  • Zapata PJ, Serrano M, Pretel MT, Amoros A, Botella MA (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788

    Article  CAS  Google Scholar 

  • Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, Jayakumar B, Shabala S, Muñiz J, Pottosin I (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Phys 157:1–14

    Article  CAS  Google Scholar 

  • Zhang RH, Li J, Guo SR, Tezuka T (2009) Effects of exogenous putrescine on gas exchange characteristics and chlorophyll fluorescence of NaCl-stressed cucumber seedlings. Photosynth Res 100:155–162

    Article  PubMed  CAS  Google Scholar 

  • Zhou Q, Yu B (2010) Changes in content of free, conjugated and bound polyamines and osmotic adjustment in adaptation of vetiver grass to water deficit. Plant Physiol Biochem 48(6):417–425

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Authors acknowledge the support of technical facilities available at Presidency University (Government of West Bengal, India). Financial assistance (RGYI Grant) from the Department of Biotechnology (Government of India) to BG (PI) and KG (Co-PI) and DST-SERB project from the Department of Science and Technology (Government of India) to KG (PI) are also gratefully acknowledged. We thank the anonymous referees for helpful comments on our manuscript.

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Authors and Affiliations

  1. Department of Botany, Presidency University, 86/1 College Street, Kolkata, West Bengal, 700073, India

    Kamala Gupta & Abhijit Dey

  2. Molecular Biology Laboratory, Department of Biotechnology, Presidency University, 86/1 College Street, Kolkata, West Bengal, 700073, India

    Bhaskar Gupta

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  1. Kamala Gupta
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  2. Abhijit Dey
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  3. Bhaskar Gupta
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Correspondence to Bhaskar Gupta.

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Communicated by A. K. Kononowicz.

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Gupta, K., Dey, A. & Gupta, B. Plant polyamines in abiotic stress responses. Acta Physiol Plant 35, 2015–2036 (2013). https://doi.org/10.1007/s11738-013-1239-4

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