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Polyamines and Their Roles in the Alleviation of Ion Toxicities in Plants

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Book cover Ecophysiology and Responses of Plants under Salt Stress

Abstract

Polyamines are ubiquitous polycationic aliphatic compounds known to be essential in physiological responses to different abiotic constraints in plants. Among others, they are involved in ion stress response. It is well known that physiological damages differ as a function of the ion type and the intensity of the stressor. Salinity, heavy metals, iron excess or aluminium are toxicities that were reported to induce modifications in polyamine metabolism. Polyamine metabolism flexibility can be directly linked with ion toxicities or with secondary stresses resulting from tissue injuries.

Advances on polyamines research in relation to environmental constraints considerably benefit from the identification of genes involved in polyamine metabolism and controlling the conversion between free, conjugated and bound forms. Recent transgenic strategies performed with numerous plant species not only allowed gaining better detailed information about the molecular components of signalling pathways leading to modifications in polyamine metabolism but also about the cellular targets interacting with polyamine in ion overloaded tissues.

The state of the art in the modification of polyamines metabolism and putative functions of these molecules in ion- stressed plant tissues will be presented in this review, considering the specificity of each type of mineral toxicity. A special attention will be paid to the interaction between polyamine and ethylene biosynthesis as well as to the interaction between those polycations and other plant growth regulators involved in stress response such as abscisic acid. Interactions between polyamines and ion channels and other transporters influencing mineral status of the stressed plants will be described on the basis of electrophysiological and pharmacological studies. The putative involvement of polyamines in plant water status regulation will be detailed through the analysis of higher plants overexpressing genes involved in putrescine and/or spermidine synthesis. Recent evidence gathered in plants also supports their roles in a wide range of regulatory functions of many basic cellular processes in stressed tissues including DNA replication, transcription, translation, cell division and modulation of enzyme activities. Several evidences demonstrated that polyamines can act as mitigating oxidative damages.

The putative interest of polyamine synthesis as convenient and reliable criteria for selection of cultivated plants exhibiting a higher tolerance to mineral toxicities will be considered.

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References

  • Abdelhady MIS, Beuerle T, Ober D (2009) Homospermidine in transgenic tobacco results in considerably reduced spermidine levels but is not converted to pyrrolizidine alkaloid precursors. Plant Mol Biol 71:145–155

    PubMed  CAS  Google Scholar 

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamagushi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcription activators in abscisic acid signaling. Plant Cell 15:69–78

    Google Scholar 

  • Acosta C, Perez-Amador MA, Carbonell J, Granell A (2005) The two ways to produce putrescine in tomato are cell-specific during normal development. Plant Sci 168:1053–1057

    CAS  Google Scholar 

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    PubMed  CAS  Google Scholar 

  • Ahn SM, Jin CD (2004) Protective role of exogenous spermidine against paraquat toxicity in radish chloroplasts. J Plant Biol 47:338–347

    CAS  Google Scholar 

  • Anjum MA (2010) Response of Cleopatra mandarin seedlings to a polyamine-biosynthesis inhibitor under salt stress. Acta Physiol Plant 32:951–959

    CAS  Google Scholar 

  • Alcazar R, Garcia-Martinez 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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ali RM (2000) Role of putrescine in salt tolerance of Atropa belladonna plant. Plant Science 152:173–179

    CAS  Google Scholar 

  • Ali RM, Abbas HM, Kamal RK (2009) The effects of treatment with polyamines on dry matter and some metabolites in salinity – stressed chamomile and sweet majoram seedlings. Plant Soil Environ 55:477–483

    CAS  Google Scholar 

  • An Z, Jing W, Liu Y, 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

    PubMed  CAS  Google Scholar 

  • Angelini R, Bragaloni M, Federico R, Infantino A, Portapuglia A (1993) Involvement of polyamines, diamine oxidase and peroxidase in resistance of chickpea to Ascochyta rabiei. J Plant Physiol 142:704–709

    CAS  Google Scholar 

  • Antognoni F, Fornalè S, Grimmer C, Komor E, Bagni N (1998) Long-distance translocation of polyamines in phloem and xylem of Ricinus communis L. plants. Planta 204:520–527

    CAS  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubis J (2009) Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. J Plant Growth Regul 28:177–186

    CAS  Google Scholar 

  • Aravind P, Prasad MNV (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: a free floating freshwater macrophyte. Plant Physiol Biochem 41:391–397

    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 signalling. Plant Physiol 136:2556–2576

    PubMed  CAS  Google Scholar 

  • Athwal GS, Huber SC (2002) Divalent cations of polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with posphorylated nitrate reductase. Plant J 29:119–129

    PubMed  CAS  Google Scholar 

  • Aziz A, Martin-Tanguy J, Larher F (1997) Plasticity of polyamine metabolism associated with high osmotic stress in rape leaf discs and with ethylene treatment. Plant Growth Regul 21:153–163

    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 104:195–102

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bais HP, Ravishankar GA (2002) Role of polyamines in the ontogeny of plants and their biotechnological applications. Plant Cell Tissue Organ Cult 69:1–34

    CAS  Google Scholar 

  • Balestrasse KB, Gallego SM, Benavides MP, Tomaro ML (2005) Polyamines and proline are affected by cadmium stress in nodules and roots of soybean plants. Plant Soil 270:343–353

    CAS  Google Scholar 

  • Bar Y, Apelbaum A, Kafkafi U, Goren R (1996) Polyamines in chloride-stressed citrus plants: alleviation of stress by nitrate supplementation via irrigation water. J Am Soc Horticult Sci 121:507–513

    CAS  Google Scholar 

  • Bar Y, Apelbaum A, Kafkafi U, Goren R (1998) Ethylene association with chloride stress in citrus plants. Sci Hortic 73:99–109, Amsterdam

    CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    CAS  Google Scholar 

  • Beauchemin R, Harnois J, Rouillon R, Tajmir-Riahi HA, Carpentier R (2007) Interaction of polyamines with proteins of photosystem II: cation binding and photosynthetic oxygen evolution. J Mol Struct 833:1–3

    Google Scholar 

  • Ben Hassine A, Ghanem ME, Bouzid S, Lutts S (2009) Abscisic acid has contrasting effects on salt excretion and polyamine concentrations of an inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus. Ann Bot 104:925–936

    PubMed  CAS  Google Scholar 

  • Benavides MP, Aizencang G, Tomaro ML (1997) Polyamines in Helianthus annuus L. during germination under salt stress. J Plant Growth Regul 16:205–211

    CAS  Google Scholar 

  • Besford TR, Richardson CM, Campos JL, Tiburcio AF (1993) Effect of polyamines on stabilization of molecular-complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189:201–206

    CAS  Google Scholar 

  • Bregier-Jarzebowska R, Gasowska A, Jastrzab R, Lomozik L (2009) Noncovalent interactions and coordination reactions in the systems consisting of copper(II) ions, aspartic acid and diamines. J Inorg Biochem 103:1228–1235

    PubMed  CAS  Google Scholar 

  • Biondi S, Fornale S, Oksman-Caldentey KM, Eeva M, Agostani S, Bagni N (2000) Jasmonates induce over-accumulation of methylputrescine and conjugated polyamines in Hyoscyamus muticus L. root cultures. Plant Cell Rep 19:691–697

    CAS  Google Scholar 

  • Borrell A, Carbonell L, Farras R, Puig-Parellada P, Tiburcio AF (1997) Polyamines inhibit lipid peroxidation in senescing oat leaves. Physiol Plant 99:385–390

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

  • Bryson K, Greenall RJ (2000) Binding sites of the polyamines putrescine, cadaverine, spermidine and spermine on A- and B-DNA located by simulated annealing. J Biomol Struct Dyn 18:393–412

    PubMed  CAS  Google Scholar 

  • Bueno M, Garrido D, Matilla A (1993) Gene-expression induced by spermine in isolated embryonic axes of chickpea seeds. Physiol Plant 87:381–388

    CAS  Google Scholar 

  • Caffaro S, Scaramagli S, Antognoni F, Bagni N (1993) Polyamine content and translocation in soybean plants. J Plant Physiol 141:563–568

    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 157:2108–2117

    PubMed  CAS  Google Scholar 

  • Cavusoglu K, Kilic S, Kabar K (2007) Some morphological and anatomical observations during alleviation of salinity (NaCI) stress on seed germination and seedling growth of barley by polyamines. Acta Physiol Plant 29:551–557

    CAS  Google Scholar 

  • Chai YY, Jiang CD, Shi L, Shi TS, Gu WB (2010) Effects of exogenous spermine on sweet sorghum during germination under salinity. Biol Plant 54:145–148

    Google Scholar 

  • Chang SC, Kang BG (1999) Effects of spermine and plant hormones on nuclear protein phosphorylation in Ranunculus petioles. J Plant Physiol 154:463–470

    CAS  Google Scholar 

  • Charnay D, Nari J, Noat G (1992) Regulation of plant cell-wall pectin methyl esterase by polyamines – interactions with the effect of metal ions. Eur J Biochem 205:711–714

    PubMed  CAS  Google Scholar 

  • Chattopadhayay MK, Gupta S, Sengupta DN, Ghosh B (1997) Expression of arginine decarboxylase in seedlings of indica rice (Oryza sativa L.) cultivars as affected by salinity stress. Plant Mol Biol 34:477–483

    Google Scholar 

  • Chattopadhayay MK, Tiwari BS, Chattopadhayay 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

    PubMed  CAS  Google Scholar 

  • Chen H, Jones AD, Howe GA (2006) Constitutive activation of the jasmonate signalling pathway enhances the production of secondary metabolites in tomato. FEBS Lett 580:2540–2546

    PubMed  CAS  Google Scholar 

  • Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845

    PubMed  CAS  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    PubMed  CAS  Google Scholar 

  • Choudhary SP, Bhardwaj R, Gupta DT, Dutt P, Gupta RK, Biondi S, Kanwar M (2010) Epibrassinolide induces changes in indole-3-acetic acid, abscisic acid and polyamine concentrations and enhances antioxidant potential of radish seedlings under copper stress. Physiol Plant 140:280–296

    PubMed  CAS  Google Scholar 

  • Cicatelli A, Linhua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2010) Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metalothionein and polyamine biosynthetic gene expression. Ann Bot-London 106:791–802

    CAS  Google Scholar 

  • Clay NK, Nelson T (2005) Arabidopsis thickvein 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

    PubMed  CAS  Google Scholar 

  • Cona A, Manetti F, Leone R, Corelli F, Tavladoraki P, Polticelli F, Botta M (2004) Molecular basis for the binding of competitive inhibitors of maize polyamine oxidase. Biochem-US 43:3426–3435

    CAS  Google Scholar 

  • Cvikrova M, Binarova P, Cenklova V, Eder J, Machackova I (1999) Reinitiation of cell division and polyamine and aromatic monoamine levels in alfalfa explants during the induction of somatic embryogenesis. Physiol Plant 105:330–337

    CAS  Google Scholar 

  • D’Agostino L, Di Luccia A (2002) Polyamines interact with DNA as molecular agregates. Eur J Biochem 269:4317–4325

    PubMed  Google Scholar 

  • D’Agostino L, di Pietro M, Di Luccia A (2005) Nuclear aggregates of polyamines are supramolecular structures that play a crucial role in genomic DNA protection and conformation. FEBS J 272:3777–3787

    PubMed  Google Scholar 

  • D’Agostino L, di Pietro M, Di Luccia A (2006) Nuclear agragates of polymaines. IUBMB Life 58:75–82

    PubMed  Google Scholar 

  • Del Duca S, Cai G, Di Sandro A, Serafini-Fracassini D (2010) Compatible and self-incompatible pollination in Pyrus communis displays different polyamine levels and transglutaminase activity. Amino Acids 38:659–667

    PubMed  Google Scholar 

  • Del Duca S, Creus JA, D’Orazi D, Dondini L, Bregoli AM, Serafini-Fracassini D (2000a) Tuber vegetative stages and cell cycle in Helianthus tuberosus: protein pattern and their modification by spermidine. J Plant Physiol 156:17–25

    Google Scholar 

  • Del Duca S, Dondini L, Della Mea M, de Munoz P, Serafini-Fracassini D (2000b) Factors affecting transglutaminase activity catalysing polyamine conjugation to endogenous substrates in the entire chloroplast. Plant Physiol Biochem 38:429–439

    Google Scholar 

  • Della Mea M, Di Sandro A, Dondini L, Del Duca S, Vantini F, Bergamini C, Bassi R, Serafini-Fracassini D (2004) A Zea mays 39-kDa thylakoid transglutaminase catalyses the modification by polyamines of light-harvesting complex II in a light-dependent way. Planta 219:754–764

    PubMed  CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci U S A 98:13454–13459

    PubMed  CAS  Google Scholar 

  • Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplast from Arabidopsis roots. Plant Physiol 128:379–387

    PubMed  CAS  Google Scholar 

  • Desjouis M, LeDily F, Boucaud J (1996) Evidence for a polyamine-mediated control of soluble nitrogen mobilization during post-clipping regrowth of white clover (Trifolium repens L.). J Plant Growth Regul 19:257–264

    CAS  Google Scholar 

  • Di Lucia A, Picariello G, Iacomino G, Formisano A, Paduano L, D’Agostino L (2009) The in vitro aggregates of polyamines. FEBS J 276:2324–2335

    Google Scholar 

  • di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Google Scholar 

  • DiTomaso JM, Hart JJ, Kochian LV (1992a) Transport kinetics and metabolism of exogenously applied putrescine in roots of intact maize seedlings. Plant Physiol 98:611–620

    CAS  Google Scholar 

  • Ding C, Shi G, Xu X, Yang H, Xu Y (2010) Effect of exogenous spermidine on polyamine metabolism in water hyacinth leaves under mercury stress. J Plant Growth Regul 60:61–67

    CAS  Google Scholar 

  • Drolet G, Dumbroff EB, Legge RL, Thompson JE (1986) Radical scavenging properties of polyamines. Phytochemistry 25:367–371

    CAS  Google Scholar 

  • El-Shintinawy F (2000) Photosynthesis in two wheat cultivars differing in salt susceptibility. Photosynthetica 38:615–620

    CAS  Google Scholar 

  • Erdei L, Szegletes Z, Barabas K, Pestenacz A (1996) Responses in polyamine titer under osmotic and salt stress in sorghum and maize seedlings. J Plant Physiol 147:599–603

    CAS  Google Scholar 

  • Falasca G, Franceschetti M, Bagni N, Altamura MM, Biasi R (2010) Polyamine biosynthesis and control of the development of functional pollen in kiwifruit. Plant Physiol Biochem 48:565–573

    PubMed  CAS  Google Scholar 

  • Friedman R, Levin N, Altman A (1986) Presence and identification of polyamines in xylem and phloem exudates of plants. Plant Physiol 82:1154–1157

    CAS  Google Scholar 

  • Figueras X, Gendy CA, Pinol MT, Van KTT, Tiburcio AF (1990) Polyamine content in relation to ploidy level and to different organs of Nicotiana plumbaginifolia. Plant Cell Physiol 31:823–828

    CAS  Google Scholar 

  • Fincato P, Moschou PN, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis-Angelakis KA, Tavladoraki P (2011) Functional diversity inside the Arabidopsis polyamine oxidase gene family. J Exp Bot 62:1155–1168

    PubMed  CAS  Google Scholar 

  • Fowler MR, Kirby MJ, Scott NW, Slater A, Eliott MC (1996) Polyamine metabolism and gene regulation during the transition of autonomous sugar beet cells in suspension culture from quiescence to division. Physiol Plant 98:439–446

    CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    PubMed  CAS  Google Scholar 

  • Franchin C, Fossati T, Pasquini E, Lingua G, Castiglione S, Torrigiani P, Biondi S (2007) High concentrations of zinc and copper induce differential polyamine responses in micropropagated white poplar (Populus alba). Physiol Plant 130:77–90

    CAS  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Gao HJ, Yang HQ, Wang JX (2009) Arginine metabolism in roots and leaves of apple (Malus domestica Borkh.): the tissue-specific formation of both nitric oxide and polyamines. Sci Hortic 119:147–152, Amsterdam

    CAS  Google Scholar 

  • Garufi A, Visconti S, Camoni L, Aducci P (2007) Polyamines as physiological regulators of 14-3-3 içnteraction with the plasma memebrane H+-ATPase. Plant Cell Physiol 48:434–440

    PubMed  CAS  Google Scholar 

  • Geny L, Broquedis M, MartinTanguy J, Soyer JP, Bouard J (1997) Effects of potassium nutrition on polyamine content of various organs of fruiting cuttings of Vitis vinifera L cv Cabernet Sauvignon. Am J Enol Viticult 48:85–92

    CAS  Google Scholar 

  • Geuns JMC, Cuypers AJF, Michiels T, Colpaert JV, VanLaere A, VandenBroeck KAO, Vandecasteele CHA (1997) Mung bean seedlings as bio-indicators for soil and water contamination by cadmium. Sci Total Environ 203:183–197

    CAS  Google Scholar 

  • Ghanem ME, van Elteren J, Albacete A, Quinet M, Martinez-Andujar C, Kinet JM, Perez-Alfocea F, Lutts S (2009) Impact of salinity on early reproductive physiology of tomato (Solanum lycopersicum) in relation to a heterogeneous distribution of toxic ions in flower organs. Funct Plant Biol 36:125–136

    CAS  Google Scholar 

  • Girard MC, Walter C, Rémy JC, Berthelin J, Morel JL (2005). Présence et impact des elements en trace dans les sols. In Sols et environnement: cours, exercices et études de cas. Dunod, Paris

    Google Scholar 

  • Gomez-Jimenez MC, Paredes MA, Gallardo M, Fernandez-Garcia N, Olmos E, Sanchez-Calle IM (2010) Tissue-specific expression of olive S-adenosyl methionine decarboxylase and spermidine systhase genes and polyamine metabolism during flower opening and early fruit development. Planta 232:629–647

    PubMed  CAS  Google Scholar 

  • Goossens A, Hakkinen ST, Laakso I, Seppanen-Laakso T, Biondi S, De Sutter V, Lammertyn F, Nuutila AM, Soderlund H, Zabeau M, Inzé D, Oksman-Caldentey KM (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci U S A 100:8595–8600

    PubMed  CAS  Google Scholar 

  • Gorecka K, Cvikrova M, Kowalska U, Eder J, Szafranska K, Gorecki R, Janas KM (2007) The impact of Cu treatment on phenolic and polyamine levels in plant material regenerated from embryos obtained in anther culture of carrot. Plant Physiol Biochem 45:54–61

    PubMed  CAS  Google Scholar 

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

    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

    CAS  Google Scholar 

  • Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615

    PubMed  CAS  Google Scholar 

  • Groppa MD, Tomaro ML, Benavides MP (2001) Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci 161:481–488

    CAS  Google Scholar 

  • Guo YL, Roux SJ (1995) Partial-purification and characterization of an enzyme from pea nuclei with protein-tyrosine-phosphatase activity. Plant Physiol 107:167–175

    PubMed  CAS  Google Scholar 

  • Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM, Casero RA (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 95:11140–11145

    PubMed  CAS  Google Scholar 

  • Häkkinen ST, Tilleman S, Šwiątek A, De Sutter V, Rischer H, Vanhoutte I, Van Onckelen H, Hilson P, Inzé D, Oksman-Caldentey KM, Goossens A (2007) Functional characterisation of genes involved in pyridine alkaloid biosynthesis in tobacco. Phytochemistry 68:2778–2785

    Google Scholar 

  • Hamdani S, Tajmir-Riahi HA, Carpentier R (2009) Methylamine interaction with proteins of photosystem II: a comparison with biogenic polyamines. J Photochem Photobiol B 96:201–206

    PubMed  CAS  Google Scholar 

  • Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Biochem 48:540–546

    PubMed  CAS  Google Scholar 

  • Hao YJ, Kitashiba H, Honda C, Nada K, Moriguchi T (2005) Expression of arginine decarboxylase genes in apple cells and stressed shoots. J Exp Bot 56:1105–1115

    PubMed  CAS  Google Scholar 

  • Hao GP, Xing Y, Zhang JH (2008) Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signaling of maize seedling. J Integr Plant Biol 50:435–442

    PubMed  CAS  Google Scholar 

  • Hashimoto T, Yukimune Y, Yamada Y (1989) Putrescine and putrescine N-methyltransferase in the biosynthesis of tropane alkaloids in cultured roots of Hyoscyamus albus.2. incorporation of labeled precursors. Planta 178:131–137

    CAS  Google Scholar 

  • Hiraga S, Ito Y, Yamakawa H, Ohtsubo N, Seo S, Mitsuhara I, Matsui H, Honma M, Ohashi Y (2000) An HR-induced tobacco peroxidase gene is responsive to spermine, but not to salicylate, methyl jasmonate, and etephon. Mol Plant Microbe Interact 13:210–216

    PubMed  CAS  Google Scholar 

  • Hobbs CA, Paul BA, Glimour SK (2002) Deregulation of polyamine biosynthesis alters intrinsic histone acetyltransferase and deacetylase activities in murine skin and tumors. Cancer Res 62:67–74

    PubMed  CAS  Google Scholar 

  • Hong-Bo S, Li-Ye C, Ming-An S (2008a) Calcium as a versatile plant signal transducer under soil water stress. Bioessays 30:634–641

    PubMed  Google Scholar 

  • Hong-Bo S, Li-Ye C, Ming-An S, Shi-Qing L, Ji-Cheng Y (2008b) Bioengineering plant resistance to abiotic stresses by the global calcium signal system. Biotechnol Adv 26:503–510

    PubMed  Google Scholar 

  • Hsu YT, Kao CH (2007) Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant Soil 291:27–37

    CAS  Google Scholar 

  • Hummel I, Gouesbet G, El Amrani A, Ainouche A, Couée 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Igarashi K, Ueda S, Yoshida K, Kashiwagi K (2006) Polyamines in renal failure. Amino Acids 31:477–483

    PubMed  CAS  Google Scholar 

  • Jiménez-Bremont JF, Becerra-Flora A, Hernández-Lucero E, Rodríguez-Kessler M, Acosta-Gallegos JA, Ramírez-Pimentel JG (2006) Proline accumulation in two bean cultivars under salt stress and the effect of polyamines and ornithine. Biologia Plant 50:763–766

    Google Scholar 

  • Jiménez-Bremont JF, Ruiz OA, Rodríguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821

    PubMed  Google Scholar 

  • Jokela A, Sarjala T, Kaunisto S, Huttunen S (1997) Effects of foliar potassium concentration on morphology, ultrastructure and polyamine concentrations of Scot pine needles. Tree Physiol 17:677–685

    PubMed  CAS  Google Scholar 

  • Kacperska A (2004) Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol Plant 122:159–168

    CAS  Google Scholar 

  • Kakkar RK, Sawhney VK (2002) Polyamine research in plants – a changing perspective. Physiol Plant 116:281–292

    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

    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

    PubMed  CAS  Google Scholar 

  • Keypour H, Azadbakht R, Salehzadeh S, Khanmohammadi H, Khavasi H, Adams H (2008) Synthesis, crystal structure and spectroscopic properties of some cadmium(II) complexes with three polyamine and corresponding macroacyclic Schiff base ligands. J Organomet Chem 693:2237–2243

    CAS  Google Scholar 

  • Kim SY (2006) The role of ABF family bZIP class transcription factors in stress response. Physiol Plant 126:519–527

    CAS  Google Scholar 

  • Kishor PBK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438, India

    CAS  Google Scholar 

  • Kolodynska D, Hubicki Z, Geca M (2008) Application of a new-generation complexing agent in removal of heavy metal ions from aqueous solutions. Ind Eng Chem Res 47:3192–3199

    CAS  Google Scholar 

  • Kotzabasis K, Navakoudis E, Tsolakis G, Senger H, Dornemann D (1999) Characterization of thye photoreceptors responsible for the regulation of the intracellular polyamine level and the putative participation of heterotrimeric G-proteins in the signal transduction chain. J Photochem Photobiol B 50:38–44

    CAS  Google Scholar 

  • Krishnamurthy K (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 

  • Kuehn GD, Atmar VJ, Daniels GR (1983) Polyamine-dependent protein-kinase from the slime-mold Physarum polycephalum. Methods Enzymol 94:147–154

    PubMed  CAS  Google Scholar 

  • Kubis J (2005) The effect of exogenous spermidine on superoxide dismutase activity, H2O2 and superoxide radical level in barley leaves under water deficit conditions. Acta Physiol Plant 27:289–295

    Google Scholar 

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

    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

    CAS  Google Scholar 

  • Kurepa J, Smalle J, Van Montagu M, Inzé D (1998) Polyamines and paraquat toxicity in Arabidopsis thaliana. Plant Cell Physiol 39:987–992

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. J Plant Res 120:345–350

    PubMed  CAS  Google Scholar 

  • Kuznetsov VV, Radyukina NL, Shevyakova NI (2006) Polyamines and stress: biological role, metabolism, and regulation. Russ J Plant Physiol 53:583–604

    CAS  Google Scholar 

  • Kuznetsov VV, Shevyakova NI (1997) Stress responses of tobacco cells to high temperature and salinity. Proline accumulation and phosphorylation of polypeptides. Physiol Plant 100:320–326

    CAS  Google Scholar 

  • Langebartels C, Kerner K, Leonardi S, Schraudner M, Trost M, Heller W, Sandermann H (1991) Biochemical-plant responses to ozone.1. differential induction of polyamine and ethylene biosynthesis in tobacco. Plant Physiol 95:882–889

    PubMed  CAS  Google Scholar 

  • Larher F, Aziz A, Deleu C, Lemesle P, Ghaffar A, Bouchard F, Plasman M (1998) Suppression of the osmoinduced proline response of rapeseed leaf discs by polyamines. Physiol Plant 102:139–147

    CAS  Google Scholar 

  • Laurenzi M, Tipping AJ, Marcus SE, Knox JP, Federico R, Angelini R, McPherson MJ (2001) Analysis of the distribution of copper amine oxidase in cell walls of legume seedlings. Planta 214:37–45

    PubMed  CAS  Google Scholar 

  • Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269

    PubMed  CAS  Google Scholar 

  • Lefèvre I, Correal E, Faz-Cano A, Zanuzzi A, Lutts S (2009a) Structural development, water status, pigment concentrations, and oxidative stress of Zygophyllum fabago seedlings in relation to cadmium distribution in the shoot organs. Int J Plant Sci 170:226–236

    Google Scholar 

  • Lefèvre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci 161:943–952

    Google Scholar 

  • Lefèvre I, Marchal G, Meerts P, Corréal E, Lutts S (2009b) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65:142–152

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Legocka J, Zajchert I (1999) Role of spermidine in the stabilization of the apoprotein of the light-harvesting chlorophyll a/b-protein complex of photosystem II during leaf senescence process. Acta Physiol Plant 21:127–132

    CAS  Google Scholar 

  • Li M, Hong Y, Wang X (2009) Phospholopase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta 1791:927–935

    PubMed  CAS  Google Scholar 

  • Lin CC, Kao CH (1999) Excess copper induces an accumulation of putrescine in rice leaves. Bot Bull Acad Sinica 40:213–218

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta G (2008) Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 153:137–147

    PubMed  CAS  Google Scholar 

  • Liu HP, Dong BH, Zhang YY, Liu ZP, Liu YL (2004) Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings. Plant Sci 166:1261–1267

    CAS  Google Scholar 

  • Liu K, Fu HH, Bei QX, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1325

    PubMed  CAS  Google Scholar 

  • Liu J, Jiang MY, Zhou YF, Liu YL (2005) Production of polyamines is enhanced by endogenous abscisic acid in maize seedlings subjected to salt stress. J Integr Plant Biol 47:1326–1334

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Liu J, Yu BJ, Liu YL (2006b) Effects of spermidine and spermine levels on salt tolerance associated with tonoplast H+-ATPase and H+-PPase activities in barley roots. Plant Growth Regul 49:119–126

    CAS  Google Scholar 

  • Liu H, Ji X, Yu B, Liu Y (2006c) Relationship between osmotic stress and polyamines conjugated to the deoxyribonucleic acid-protein in wheat seedling roots. Science in China: Series C Life Sciences 49:12–17

    CAS  Google Scholar 

  • Locke JM, Bryce JH, Morris PC (2000) Contrasting effects of ethylene perception and biosynthesis inhibitors on germination and seedling growth of barley (Hordeum vulgare L.). J Exp Bot 51:1843–1849

    PubMed  CAS  Google Scholar 

  • Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochimica et Biophysica Acta - Biomembranes 1666:142–157

    CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot-London 78:389–398

    CAS  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: An overview. Archives of Biochemistry and Biophysics 444:139–158

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mahajan A, Sharma S (2009) Antagonistic effect of polyamines on ABA-induced suppression of mitosis in Allium cepa L. Indian J Exp Biol 47:136–139

    CAS  Google Scholar 

  • Maiale SJ, Marina M, Sánchez DH, Pieckenstain FL, Ruiz OA (2008) In vitro and in vivo inhibition of plant polyamine oxidase activity by polyamine analogues. Phytochemistry 69:2552–2558

    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

    PubMed  CAS  Google Scholar 

  • Majerus V, Bertin P, Lutts S (2007) Effects of iron toxicity on osmotic potential, osmolytes and polyamines concentrations in the African rice (Oryza glaberrima Steud.). Plant Sci 173:96–105

    CAS  Google Scholar 

  • Majewska-Sawka A, Butowt R, Niklas A (1998) Do polyamines release membrane-bound calcium in sugar beet protoplasts? J Plant Physiol 153:247–250

    CAS  Google Scholar 

  • Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiol Plant 29:177–187

    CAS  Google Scholar 

  • Malik AU, Singh Z (2005) Pre-storage application of polyamines improves shelf-life and fruit quality of mango. J Hortic Sci Biotech 80:363–369

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Martin-Tanguy J, Carré M (1993) Polyamines in grapevine microcuttings cultivated in-vitro - effects of amines and inhibitors of polyamine biosynthesis on polyamine levels and microcutting growth and development. Plant Growth Regul 13:269–280

    CAS  Google Scholar 

  • Mascher R, Lippmann B, Holzinger S, Bergmann H (2002) Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Sci 163:961–969

    CAS  Google Scholar 

  • Masgrau C, Altabella T, Farras R, Flores D, Thompson AJ, Besford RT, Tiburcio AF (1997) Inducible overexpression of oat arginine decarboxylase in transgenic tobacco plants. Plant J 11:465–473

    PubMed  CAS  Google Scholar 

  • Mattoo K, Chung SH, Goyal RK, Fatima T, Solomos T, Srivastava A, Handa AK (2007) Overaccumulation of higher polyamines in ripening transgenic tomato fruits revives metabolic memory, upregulates anabolism-related genes, and positively impacts nutritional quality. J AOAC Int 90:1456–1464

    PubMed  CAS  Google Scholar 

  • Mayer MJ, Michael AJ (2003) Polyamine homeostasis in transgenic plants overexpressing ornithine decarboxylase includes ornithine limitation. J Biochem 134:765–772

    PubMed  CAS  Google Scholar 

  • Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nat Biotechnol 20:613–618

    PubMed  CAS  Google Scholar 

  • Messiaen J, Cambier P, Van Cutsem P (1997) Polyamines and pectins: I. Ion exchange and ­selectivity. Plant Physiol 113:387–395

    PubMed  CAS  Google Scholar 

  • Messiaen J, Van Cutsem P (1999) Polyamines and pectins. II. Modulation of pectic-signal transduction. Planta 208:247–256

    PubMed  CAS  Google Scholar 

  • Minocha R, Long S (2004) Effects of aluminum on organic acid metabolism and secretion by red spruce cell suspension cultures and the reversal of A1 effects on growth and polyamine metabolism by exogenous organic acids. Tree 24:55–64

    CAS  Google Scholar 

  • Minocha R, Shortle WC, Coughlin DJ, Minocha SC (1996) Effects of aluminum on growth, polyamine metabolism, and inorganic ions in suspension cultures of red spruce (Picea rubens). Can J Forest Res 26:550–559

    CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    PubMed  CAS  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. Physiol Plant 114:439–449

    PubMed  CAS  Google Scholar 

  • Mohapatra S, Cherry S, Minocha R, Majumdar R, Thangavel P, Long S, Minocha SC (2010) The response of high and low polyamine-producing cell lines to aluminum and calcium stress. Plant Physiol Biochem 48:612–620

    PubMed  CAS  Google Scholar 

  • Mohapatra S, Minocha R, Long S, Minocha SC (2009) Putrescine overproduction negatively impacts on the oxidative state of poplar cells in culture. Plant Physiol Biochem 47:262–271

    PubMed  CAS  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann Rev Plant Physiol 52:561–591

    Google Scholar 

  • Moschou PN, Delis ID, Paschalidis KA, Roubelakis-Angelakis KA (2008a) Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiol Plant 133:140–156

    PubMed  CAS  Google Scholar 

  • Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumatis DI, Roubelakis-Angelakis KA (2008b) 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

    PubMed  CAS  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 147:1845–1857

    PubMed  CAS  Google Scholar 

  • Mulo P, Eloranta T, Aro EM, Maenpaa P (1998) Disruption of a spe-like open reading frame alters polyamine content and psbA-2 mRNA stability in the cyanobacterium Synechocystis sp. PCC 6803. Botanica Acta 111:71–76

    CAS  Google Scholar 

  • Munnik T, Meijer HJC (2001) Osmotic stress activates distinct lipid and MAPK signalling pathways in plants. FEBS Lett 498:172–178

    PubMed  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Physiol 59:651–681

    CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71

    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 190:355–365

    CAS  Google Scholar 

  • Ndayiragije A, Lutts S (2006a) Exogenous putrescine reduces sodium and chloride accumulation in NaCl-treated calli of the salt-sensitive rice cultivar I Kong Pao. Plant Growth Regul 48:51–63

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ndayirajige A, Lutts S (2007) Long term exogenous putrescine applicatrion improves grain yield of a salt-sensitive rice cultivar exposed to NaCl. Plant Soil 291:225–238

    Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    PubMed  CAS  Google Scholar 

  • Ober D, Hartmann T (1999) Homospermidine synthase, the first pathway-specific enzyme of pyrrolizidine alkaloid biosynthesis, evolved from deoxyhypusine synthase. Proc Natl Acad Sci USA 96:14777–14782

    PubMed  CAS  Google Scholar 

  • Oliver D, Baukrowitz T, Fakler B (2000) Polyamines as gating molecules of inward-rectifier K+ channels. Eur J Biochem 267:5824–5829

    PubMed  CAS  Google Scholar 

  • Pagoria DA, Maravolo NC (2005) DNA fragmentation in Marchantia polymorpha Thalli in response to spermine treatment. Int J Plant Sci 166:589–594

    CAS  Google Scholar 

  • Papadakis AK, Roubelakis-Angelakis KA (2005) Polyamines inhibit NADPH oxidase-mediated superoxide generation and putrescine prevents programmed cell death induced by polyamine oxidase-generated hydrogen peroxide. Planta 220:826–837

    PubMed  CAS  Google Scholar 

  • Paschalidis KA, Roubelakis-Angelakis KA (2005) Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant. Correlations with age, cell division/expansion, and differentiation. Plant Physiol 138:142–152

    PubMed  CAS  Google Scholar 

  • Pedreno E, Lopez-Contreras AJ, Cremades A, Penafiel R (2005) Protecting or promoting effects of spermine on DNA strand breakage induced by iron or copper ions as a function of metal concentration. J Inorg Biochem 99:2074–2080

    PubMed  CAS  Google Scholar 

  • Peremarti A, Bassie L, Christou P, Capell T (2009) Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Mol Biol 70:253–264

    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 Physiology 130:1454–1463

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pistocchi R, Kashiwagi K, Miyamoto S, Nukui E, Sadakata Y, Kobayashi H, Igarashi K (1993) Characteristics of the operon for a putrescine transport-system that maps at 19 minutes on the Escherichia-coli chromosome. J Biol Chem 268:146–152

    PubMed  CAS  Google Scholar 

  • Poduslo JF, Curran GL (1996) Increased permeability of superoxide dismutase at the blood-nerve and blood–brain barriers with retained enzymatic activity after covalent modification with the naturally occurring polyamine, putrescine. J Neurochem 67:734–741

    PubMed  CAS  Google Scholar 

  • Poschenrieder C, Barceló J (1999) Water relations in heavy metal stressed plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants, from molecules to ecosystems. Springer Verlag, Berlin, pp 207–229

    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

    PubMed  CAS  Google Scholar 

  • Rabiti A, Pistocchi R, Bagni N (1989) Putrescine uptake and translocation in higher plants. Physiol Plant 77:225–230

    CAS  Google Scholar 

  • Rea G, de Pinto MC, Tavazza R, Biondi S, Gobbi V, Ferrante P, De Gara L, Federico R, Angelini R, Tavladoraki P (2004) Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants. Plant Physiol 134:1414–1426

    PubMed  CAS  Google Scholar 

  • Rea G, Laurenzi M, Tranquilli E, D’Ovidio R, Federico R, Angelini R (1998) Developmentally and wound-regulated expression of the gene encoding a cell wall copper amine oxidase in chickpea seedlings. FEBS Lett 437:177–182

    PubMed  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

    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

    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 toleranbce. J Plant Physiol 68:317–328

    Google Scholar 

  • Saibo NJM, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Annals of Botany 103:609–623

    CAS  Google Scholar 

  • Santa-Cruz A, Perez-Alfocea F, Caro M, Acosta M (1998) Polyamines as short-term salt tolerance traits in tomato. Plant Sci 138:9–16

    CAS  Google Scholar 

  • Sarjala T, Haggman H, Aronen T (1997) Effect of exogenous polyamines and inhibitors of polyamine biosynthesis on growth and free polyamine contents of embryogenic Scots pine ­callus. J Plant Physiol 150:597–602

    CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    PubMed  CAS  Google Scholar 

  • Scaramagli S, Biondi S, Torrigiani P (1999) Methyl(bis-guanylhydrazone) inhibition of organogenesis is not due to S-adenosylmethionine decarboxylase inhibition/polyamine depletion in tobacco thin layers. Physiol Plant 107:353–360

    CAS  Google Scholar 

  • Serafini-Fracassini D, Delduca S, Beninati S (1995) Plant transglutaminases. Phytochemistry 40:355–365

    PubMed  CAS  Google Scholar 

  • Serafini-Fracassini D, Di Sandro A, Del Duca S (2010) Spermine delays leaf senescence in Lactuca sativa and prevents the decay of chloroplast photosystems. Plant Physiol Biochem 48:602–611

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144

    CAS  Google Scholar 

  • Shao HB, Guo QJ, Chu LY, Zhao XN, Su ZL, Hu YC, Cheng JF (2007) Understanding molecular mechanism of higher plant plasticity under abiotic stress. Colloids Surf B 54:37–45

    CAS  Google Scholar 

  • Shevyakova NIO, Il’Ina EN, Stetsenko LA, Kuznetsov VV (2011) Nickel accumulation in rape shoots (Brassica napus L.) increased by putrescine. Int J Phytoremediat 13:345–356

    CAS  Google Scholar 

  • Shih CY, Kao CH (1996) Growth inhibition in suspension-cultured rice cells under phosphate deprivation is mediated through putrescine accumulation. Plant Physiol 111:721–724

    PubMed  CAS  Google Scholar 

  • Sitrit Y, Bennett AB (1998) Regulation of tomato fruit polygalacturonase mRNA accumulation by ethylene: a re-examination. Plant Physiol 116:1145–1150

    PubMed  CAS  Google Scholar 

  • Smith MA, Maravolo NC (2004) The influence of spermine on the in situ expression of a protein kinase associated with senescence in Marchantia polymorpha thalli. Int J Plant Sci 165:745–751

    CAS  Google Scholar 

  • Srivastava HS, Ormrod DP, Hale BA (1995) Polyamine mediated modifications of bean leaf response to nitrogen-dioxide. J Plant Physiol 146:313–317

    CAS  Google Scholar 

  • Su GX, An ZF, Zhang WH, Liu YL (2005) Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls. J Plant Physiol 162:1297–1303

    PubMed  CAS  Google Scholar 

  • Su GX, Bai X (2008) Contribution of putrescine degradation to proline accumulation in soybean leaves under salinity. Biol Plantarum 52:796–799

    CAS  Google Scholar 

  • Sudha G, Ravishankar GA (2002) Involvement and interaction of various signaling compounds on the plant metabolic events during the defense response, resistance to stress factors, formation of secondary metabolites and their molecular aspects. Plant Cell Tiss Org 71:181–212

    CAS  Google Scholar 

  • Sung HI, Liu LF, Kao CH (1994) Putrescine accumulation is associated with growth-inhibition in suspension-cultured rice cells under potassium-deficiency. Plant Cell Physiol 35:313–316

    CAS  Google Scholar 

  • Suzuki Y (1996) Purification and characterization of diamine oxidase from Triticum aestivum shoots. Phytochemistry 42:291–293

    CAS  Google Scholar 

  • Szalai G, Janda T, Bartok T, Paldi E (1997) Role of light in changes in free amino acid and polyamine contents at chilling temperature in maize (Zea mays). Physiol Plantarum 101:434–438

    CAS  Google Scholar 

  • Tabur S, Demir K (2010) Protective roles of exogenous polyamines on chromosomal aberrations in Hordeum vulgare exposed to salinity. Biologia 65:947–953

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Tamai T, Inoué M, Sugimoto T, Sueyoshi K, Shiraishi N, Oji Y (1999) Ethylene-induced putrescine accumulation modulates K+ partitioning between roots and shoots in barley seedlings. Physiol Plantarum 106:296–301

    CAS  Google Scholar 

  • Tang W, Newton RJ, Outhavong V (2004) Exogenously added polyamines recover browning tissues into normal callus cultures and improve plant regeneration in pine. Physiol Plant 122:386–395

    CAS  Google Scholar 

  • Tari I, Csiszar J, Gemes K, Szepesi A (2006) Modulation of Cu2+ accumulation by (aminoethoxyvinyl)glycine and methyloxal bis(guanylhydrazone), the inhibitors of stress ethylene and polyamine synthesis in wheat genotypes. Cereal Res Commun 34:989–996

    CAS  Google Scholar 

  • Tassoni A, Accettulli P, Bagni N (2006) Exogenous spermidine delays senescence of Dianthus caryophyllus flowers. Plant Biosyst 140:107–114

    Google Scholar 

  • Tassoni A, Antognoni F, Bagni N (1996) Polyamine binding to plasma membrane vesicles isolated from zucchini hypocotyms. Plant Physiol 110:817–824

    PubMed  CAS  Google Scholar 

  • Tassoni A, Antognoni F, Battostini ML, Sanvido O, Bagni N (1998) Characterization of spermidine binding to solubilized plasma membrane proteins from succhini hypocotyls. Plant Physiol 117:971–977

    PubMed  CAS  Google Scholar 

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

    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

    PubMed  CAS  Google Scholar 

  • Terui Y, Ohnuma M, Hiraga K, Kawashima E, Oshima T (2005) Stabilization of nucleic acids by unusual polyamines produced by an extreme thermophile, Thermus thermophilus. Biochem J 388:427–433

    PubMed  CAS  Google Scholar 

  • Thu-Hang P, Bassie L, Safwat G, Trung-Nghia P, Christou P, Capell T (2002) Expression of heterologous S-adenosylmethionine decarboxylase cDNA in plants demonstrates that changes in S-adenosyl-L-methionine decarboxylase activity determine levels of the higher polyamines spermidine and spermine. Plant Physiol 129:1744–1754

    PubMed  Google Scholar 

  • Todeschini V, Franchin C, Castiglione S, Burlando B, Biondi S, Torrigiani P, Berta G, Lingua G (2007) Responses to copper of two registered poplar clones inoculated or not with arbuscular mycorrhizal fungi. Caryologia 60:146–155

    Google Scholar 

  • Torrigiani P, Scaramagli S, Castiglione S, Maddalena A, Biondi S (2003) Downregulation of ethylene production and biosynthetic gene expression is associated to changes in putrescine metabolism in shoot-forming tobacco thin layers. Plant Sci 164:1087–1094

    CAS  Google Scholar 

  • Torrigiani P, Serafini-Fracassini D, Biondi S, Bagni N (1986) Evidence for the subcellular-localization of polyamines and their biosynthetic-enzymes in plant cells. J Plant Physiol 124:23–29

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Upreti KK, Murti GSR (2010) Response of grape rootstocks to salinity: changes in root growth, polyamines and abscisic acid. Biologia Plant 54:730–734

    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

    PubMed  CAS  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekigushi F, Yamagushi-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

    CAS  Google Scholar 

  • Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754

    PubMed  CAS  Google Scholar 

  • Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984

    PubMed  Google Scholar 

  • Vandenroeck D, Vanderstraeten D, Vanmontagu M, Caplan A (1994) A group of chromosomal-proteins is specifically released by spermine and loses DNA-binding activity upon phosphorylation. Plant Physiol 106:559–566

    Google Scholar 

  • Velikova VB, Yordanov IT, Georgieva KM, Tsonev TD, Goltsev V (1998) Effects of exogenous polyamines applied separately and in combination with simulated acid rain on functional activity of photosynthetic apparatus. J Plant Physiol 153:299–307

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Vusoku J, Jokela A, Laara E, Saaskilathi M, Muilu R, Sutela S, Altabella T, Sarjala T, Hagglman H (2006) Consistency of polyamines profiles and expression of arginine decarboxylase in mitosis during zygotic embryogenesis of Scot pine. Plant Physiol 142:1027–1038

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Wang JW, Kao CH (2006) Aluminium-inhibited root growth of rice seedlings is mediated through putrescine accumulation. Plant Soil 288:373–381

    CAS  Google Scholar 

  • Wang X, Shi G, Xu Q, Hu J (2007) Exogenous polyamines enhance copper tolerance of Nymphoides peltatum. J Plant Physiol 164:1062–1070

    PubMed  CAS  Google Scholar 

  • Wasilewska A, Vald F, Sirichandra C, Redko Y, Jammes F, Valon C, Frey N, Leung J (2008) An update on abscissic acid signaling in plants and more…. Mol Plant 1:198–217

    PubMed  CAS  Google Scholar 

  • Watson MB, Emory KK, Piatak RM, Malmberg RL (1998) Arginine decarboxylase (polyamine synthesis) mutants of Arabidopsis thaliana exhibit altered root growth. Plant J 13:231–239

    PubMed  CAS  Google Scholar 

  • Watson MB, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L) Heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111:1077–1084

    PubMed  CAS  Google Scholar 

  • Wen XP, Ban Y, Inoué H, Matsuda N, Moriguchi T (2009) Aluminium 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

    CAS  Google Scholar 

  • Wen XP, Ban Y, Inoué 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

    PubMed  CAS  Google Scholar 

  • Wilson PB, Estavillo GM, Field KJ, Pornsiriwong W, Carroll AJ, Hiowell 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

    PubMed  CAS  Google Scholar 

  • Wen XP, Pang XM, Matsuda N, Kita M, Inoué H, Hao YJ, Honda C, Moriguchi C (2008) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamines titers. Transgenic Res 17:251–263

    PubMed  CAS  Google Scholar 

  • Wisniewski JP, Rathbun EA, Knox JP, Brewin NJ (2000) Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implication for pea nodule initiation by Rhizobium leguminosarum. Mol Plant Microbe Interact 13:413–420

    PubMed  CAS  Google Scholar 

  • Xing SG, Jun BY, Hau ZW, Liang LY (2007) Higher accumulation of γ-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

    PubMed  CAS  Google Scholar 

  • Xiong L, Schumacher KS, Zhu JK (2002) Cell signaling during cold, drought and salt stress. Plant Cell 14:S165–S285

    PubMed  CAS  Google Scholar 

  • Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139

    PubMed  CAS  Google Scholar 

  • Xu BF, Sheehan MJ, Timko MP (2004) Differential induction of ornithine decarboxylase (ODC) gene family members in transgenic tobacco (Nicotiana tabacum L. cv. Bright Yellow 2) cell suspensions by methyl-jasmonate treatment. Plant Growth Regul 44:101–116

    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 Comm 352:486–490

    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

    PubMed  CAS  Google Scholar 

  • Ye XS, Avidiushko SA, Kuc J (1994) Effects of polyamines on in-vitro phoshorylation of soluble and plasma-membrane proteins in tobacco, cucumber and Arabidopsis thaliana. Plant Sci 97:109–118

    CAS  Google Scholar 

  • Ye B, Muller HH, Zhang J, Gressel J (1997) Constitutively elevated levels of putrescine and putrescine-generating enzymes correlated with oxidant stress resistance in Conyza bobariensis and wheat. Plant Physiol 115:1443–1451

    PubMed  CAS  Google Scholar 

  • Zacchini M, Rea E, Tullio M, de Agazio M (2003) Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol Biochem 41:49–54

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Zhao FG, Qin P (2005) Protective effects of exogenously fatty acids on root tonoplast function against salt stress in barley seedlings. Environ Exp Bot 53:215–223

    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

    PubMed  CAS  Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Google Scholar 

  • Zhang WP, Jiang BA, Li WG, Song H, Yu YS, Chen JF (2009) Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulatinfg antioxidative system. Sci Hortic 122:200–208, Amsterdam

    CAS  Google Scholar 

  • Zheleva D, Tsonev V, Sergiev I, Karanov E (1994) Protective effects of exogenous polyamines against atrazine in pea plants. Plant Growth Regul 13:203–211

    CAS  Google Scholar 

  • Zhu JK (2001) Cell signalling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    PubMed  CAS  Google Scholar 

  • Zhu H, Ding GH, Fang K, Zhao FG, Qin P (2006) New perspective on the mechanism of alleviating salt stress by spermidine in barley seedlings. Plant Growth Regul 49:147–156

    CAS  Google Scholar 

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Acknowledgements

This work was partly supported by the National Research Fund, Luxembourg, and the Ministry of Finances, Luxembourg.

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Authors and Affiliations

  1. Groupe de Recherche en Physiologie végétale (GRPV), Earth and Life Institute – Agronomy, Université catholique de Louvain, Croix du Sud 4-5 bte L7.07.13, Louvain-la-Neuve, 1348, Belgium

    Stanley Lutts, Muriel Quinet & Isabelle Lefèvre

  2. Department EVA, Centre de Recherche Public – Gabriel Lippmann, 41, rue du Brill, Belvaux, L-4422, Luxembourg

    Jean-François Hausman & Isabelle Lefèvre

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  1. Stanley Lutts
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  2. Jean-François Hausman
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  3. Muriel Quinet
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  4. Isabelle Lefèvre
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Correspondence to Stanley Lutts .

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Editors and Affiliations

  1. A.S. College, Department of Botany, University of Kashmir, Srinagar, 190008, India

    Parvaiz Ahmad

  2. , Department of Botany, South Valley University, Qena, 83523, Egypt

    M.M. Azooz

  3. , Department of Plant Sciences, University of Hydrabad, n/a, Hydrabad, 500046, India

    M.N.V. Prasad

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Lutts, S., Hausman, JF., Quinet, M., Lefèvre, I. (2013). Polyamines and Their Roles in the Alleviation of Ion Toxicities in Plants. In: Ahmad, P., Azooz, M., Prasad, M. (eds) Ecophysiology and Responses of Plants under Salt Stress. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4747-4_12

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