Skip to main content
Log in

Polyamines: essential factors for growth and survival

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Polyamines are low molecular weight, aliphatic polycations found in the cells of all living organisms. Due to their positive charges, polyamines bind to macromolecules such as DNA, RNA, and proteins. They are involved in diverse processes, including regulation of gene expression, translation, cell proliferation, modulation of cell signalling, and membrane stabilization. They also modulate the activities of certain sets of ion channels. Because of these multifaceted functions, the homeostasis of polyamines is crucial and is ensured through regulation of biosynthesis, catabolism, and transport. Through isolation of the genes involved in plant polyamine biosynthesis and loss-of-function experiments on the corresponding genes, their essentiality for growth is reconfirmed. Polyamines are also involved in stress responses and diseases in plants, indicating their importance for plant survival. This review summarizes the recent advances in polyamine research in the field of plant science compared with the knowledge obtained in microorganisms and animal systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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. Biotechnol Lett 28:1867–1876

    PubMed  Google Scholar 

  • Allen GJ, Sanders D (1996) Control of ionic currents guard cell vacuoles by cytosolic and luminal calcium. Plant J 10:1055–1069

    PubMed  CAS  Google Scholar 

  • Amirsadeghi S, Robson CA, Vanlerberghe GC (2007) The role of the mitochondrion in plant responses to biotic stress. Physiol Plant 129:253–266

    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 

  • 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

    PubMed  CAS  Google Scholar 

  • Belting M, Mani K, Jönsson M, Cheng F, Sandgren S, Jonsson S, Ding K, Delcros J-G, Fransson LÅ (2003) Glypican-1 is a vehicle for polyamine uptake in mammalian cells. J Biol Chem 278:47181–47189

    PubMed  CAS  Google Scholar 

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

    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 

  • Brazeau BJ, Johnson BJ, Wilmot CM (2004) Copper-containing amine oxidases. Biogenesis and catalysis; a structural perspective. Arch Biochem Biophys 428:22–31

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Brüggemann L, Pottosin I, Schönknecht G (1999) Selectivity of the fast activating vacuolar cation channel. J Exp Bot 50:873–876

    Google Scholar 

  • Canellakis ES, Paterakis AA, Huang S-C, Panagiotidis CA, Kyriakidis DA (1993) Identification, cloning, and nucleotide sequencing of the ornithine decarboxylase antizyme gene of Escherichia coli. Proc Natl Acad Sci USA 90:7129–7133

    PubMed  CAS  Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Aca Sci USA 101:9909–9914

    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

    PubMed  CAS  Google Scholar 

  • Casero RA Jr, Pegg AE (1993) Spermidine/spermine N1-acetyltransferase—the turning point in polyamine metabolism. FASEB J 7:653–661

    PubMed  CAS  Google Scholar 

  • Cason AL, Ikeguchi Y, Skinner C, Wood TC, Holden KR, Lubs HA, Martinez F, Simensen RJ, Stevenson RE, Pegg AE, Schwartz CE (2003) X-linked spermine synthase gene (SMS) defect: the first polyamine deficiency syndrome. Eur J Hum Genet 11:937–944

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Cervelli M, Polticelli F, Federico R, Mariottini P (2003) Heterologous expression and characterization of mouse spermine oxidase. J Biol Chem 278:5271–5276

    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

    PubMed  CAS  Google Scholar 

  • Cervelli M, Bianchi M, Cona A, Crosatti C, Stanca M, Angelini R, Federico R, Mariottini P (2006) Barley polyamine oxidase isoforms 1 and 2, a peculiar case of gene duplication. FEBS J 273:3990–4002

    PubMed  CAS  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 

  • Chattopadhyay MK, Tabor CW, Tabor H (2003) Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc Natl Acad Sci USA 100:2261–2265

    PubMed  CAS  Google Scholar 

  • Chattopadhyay MK, Tabor CW, Tabor H (2006) Polyamine deficiency leads to accumulation of reactive oxygen species in a spe2Delta mutant of Saccharomyces cerevisiae. Yeast 23:751–761

    PubMed  CAS  Google Scholar 

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

    PubMed  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 

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

    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

    PubMed  CAS  Google Scholar 

  • Culhane JC, Cole PA (2007) LSD1 and the chemistry of histone demethylation. Curr Opin Chem Biol 11:561–568

    PubMed  CAS  Google Scholar 

  • Davenport R (2002) Glutamate receptors in plants. Ann Bot 90:549–557

    PubMed  CAS  Google Scholar 

  • Del Duca S, Betti L, Trebbi G, Serafini-Fracassini D, Torrigiani P (2007) Transglutaminase activity changes during the hypersensitive reaction, a typical defense response of tobacco NN plants to TMV. Physiol Plant 131:241–250

    PubMed  CAS  Google Scholar 

  • Della Mea M, Caparro`s-Ruiz D, Claparols I, Serafini-Fracassini D, Rigau J (2004) AtPng1p. The first plant transglutaminase. Plant Physiol 135:2046–2054

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dobrovinskaya OR, Muñiz J, Pottosin I (1999a) Inhibition of vacuolar ion channels by polyamines. J Membr Biol 167:127–140

    PubMed  CAS  Google Scholar 

  • Dobrovinskaya OR, Muñiz J, Pottosin I (1999b) Asymmetric block of the plant vacuolar Ca2+-permeable channel by organic cations. Eur Biophys J 28:552–563

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Federico R, Cona A, Angelini R, Schininà ME, Giartosio A (1990) Characterization of maize polyamine oxidase. Phytochemistry 29:2411–2414

    PubMed  CAS  Google Scholar 

  • Ficker E, Taglialatela M, Wible BA, Henly CM, Brown AM (1994) Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science 266:1068–1072

    PubMed  CAS  Google Scholar 

  • Folk JE, Park MH, Chung SI, Schrode J, Lester EP, Cooper HL (1980) Polyamines as physiological substrates for transglutaminases. J Biol Chem 255:3695–3700

    PubMed  CAS  Google Scholar 

  • Franceschetti M, Hanfrey C, Scaramagli S, Torrigiani P, Bagni N, Burtin D, Michael AJ (2001) Characterization of monocot and dicot plant S-adenosyl-l-methionine decarboxylase gene families including identification in the mRNA of a highly conserved pair of upstream overlapping open reading frames. Biochem J 353:403–409

    PubMed  CAS  Google Scholar 

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

    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

    PubMed  CAS  Google Scholar 

  • Griffin M, Casadio R, Bergamini CM (2002) Transglutaminases: nature’s biological glues. Biochem J 368:377–396

    PubMed  CAS  Google Scholar 

  • Groppa MD, Benavides MP (2007) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    PubMed  Google Scholar 

  • Ha HC, Sirosoma NS, Kuppusamy P, Zweiler 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 

  • Hamana K, Niitsu M, Samejima K, Itoh T, Hamana H, Shinozawa T (1998) Polyamines of thermophilic eubacteria belonging to the genera Thermotoga, Thermodesulfovibrio, Thermoleophilum, Thermus, Rhodothermus and Meiothermus, and the thermophilic archaebacteria belonging to the genera Aeropyrum, Picrophilus, Methanobacterium and Methanococcus. Microbios 94:7–21

    Google Scholar 

  • Hamasaki-Katagiri N, Katagiri Y, Tabor CW, Tabor H (1998) Spermine is not essential for growth of Saccharomyces cerevisiae: identification of the SPE4 gene (spermine synthase) and characterization of a spe4 deletion mutant. Gene 210:195–201

    PubMed  CAS  Google Scholar 

  • Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J 27:551–560

    PubMed  CAS  Google Scholar 

  • Hanfrey C, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ (2002) Abrogation of upstream open reading frame-mediated translational control of a plant S-adenosylmethionine decarboxylase results in polyamine disruption and growth perturbations. J Biol Chem 277:44131–44139

    PubMed  CAS  Google Scholar 

  • Hanfrey C, Franceschetti M, Mayer MJ, Illingworth C, Elliot K, Collier M, Thompson B, Perry B, Michael AJ (2003) Translational regulation of the plant S-adenosylmethionine decarboxylase. Biochem Soc Trans 31:424–427

    PubMed  CAS  Google Scholar 

  • Hanfrey C, Elliot KA, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ (2005) A dual upstream open reading frame-based autoregulatory circuit controlling polyamine-responsive translation. J Biol Chem 280:39229–39237

    PubMed  CAS  Google Scholar 

  • Hanzawa Y, Takahashi T, Komeda Y (1997) ACL5: an Arabidopsis gene required for internodal elongation after flowering. Plant J 12:863–874

    PubMed  CAS  Google Scholar 

  • Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256

    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

    PubMed  CAS  Google Scholar 

  • Hayashi S, Murakami Y, Matsufuji S (1996) Ornithine decarboxylase antizyme: a novel type of regulatory protein. Trends Biochem Sci 21:27–30

    PubMed  CAS  Google Scholar 

  • He Y, Suzuki T, Kashiwagi K, Igarashi K (1994) Antizyme delays the restoration by spermine of growth of polyamine-deficient cells through its negative regulation of polyamine transport. Biochem Biophys Res Commun 203:608–614

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hibi N, Higashiguchi S, Hashimoto T, Yamada Y (1994) Gene expression in tobacco low-nicotine mutants. Plant Cell 6:723–735

    PubMed  CAS  Google Scholar 

  • Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122

    PubMed  CAS  Google Scholar 

  • Igarashi K (2006) Physiological functions of polyamines and regulation of polyamine contents in cells. Yakugaku Zasshi 126:455–471 in Japanese

    PubMed  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (1999) Polyamine transport in bacteria and yeast. Biochem J 344:633–642

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (2006) Polyamine modulon in Escherichia coli: genes involved in the stimulation of cell growth by polyamines. J Biochem (Tokyo) 139:11–16

    CAS  Google Scholar 

  • Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T (2004a) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152

    PubMed  CAS  Google Scholar 

  • Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004b) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573

    PubMed  CAS  Google Scholar 

  • Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T (2006) The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133:3575–3585

    PubMed  CAS  Google Scholar 

  • Ivanov IP, Matsufuji S, Murakami Y, Gesteland RF, Atkins JF (2000) Conservation of polyamine regulation by translational frameshifting from yeast to mammals. EMBO J 19:1907–1917

    PubMed  CAS  Google Scholar 

  • Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285

    PubMed  CAS  Google Scholar 

  • Janowitz T, Kneifel H, Piotrowski M (2003) Identification and characterization of plant agmatine iminohydrolase, the last missing link in polyamine biosynthesis of plants. FEBS Lett 544:258–261

    PubMed  CAS  Google Scholar 

  • Jiang D, Yang W, He Y, Amasino RA (2007) Arabidopsis relatives of the human lysine-specific demethylase1 repress the expression of FWA and Flowering Locus C and thus promote the floral transition. Plant Cell 19:2975–2987

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jung IL, Oh TJ, Kim IG (2003) Abnormal growth of polyamine-deficient Escherichia coli mutant is partially caused by oxidative stress-induced damage. Arch Biochem Biophys 418:125–132

    PubMed  CAS  Google Scholar 

  • Kamauchi S, Nakatani H, Nakano C, Urade R (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J 272:3461–3476

    PubMed  CAS  Google Scholar 

  • Kameji T, Pegg AE (1987) Effect of putrescine on the synthesis of S-adenosylmethionine decarboxylase. Biochem J 243:285–288

    PubMed  CAS  Google Scholar 

  • Kamio Y, Itoh Y, Terawaki Y, Kusano T (1981) Cadaverine is covalently linked to peptidoglycan in Selenomonas ruminantium. J Bacteriol 145:122–128

    PubMed  CAS  Google Scholar 

  • Kashiwagi K, Taneja SK, Liu TY, Tabor CW, Tabor H (1990) Spermidine biosynthesis in Saccharomyces cerevisiae. J Biol Chem 265:22321–22328

    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 

  • Kasukabe Y, He L, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol 23:75–83

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG (2001) Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol 42:74–84

    PubMed  CAS  Google Scholar 

  • Kitashiba H, Hao Y-J, Honda C, Moriguchi T (2005) Two types of spermine synthase gene: MdACL5 and MdSPMS are differentially involved in apple fruit development and cell growth. Gene 361:101–111

    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

    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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Kurihara S, Oda S, Kato K, Kim HG, Koyanagi T, Kumagai H, Suzuki H (2005) A novel putrescine utilization pathway involves γ-glutamylated intermediates of Escherichia coli K-12. J Biol Chem 280:4602–4608

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007b) The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav 2:250–251

    Google Scholar 

  • Kusunoki S, Yasumasu I (1978) Inhibitory effect of α-hydrazinoornithine on egg cleavage in sea urchin eggs. Dev Biol 67:336–345

    PubMed  CAS  Google Scholar 

  • Ladenburg A (1886) Über die Identität des Cadaverin mit dem Pentamethyldiamin. Ber Dtsch Chem Ges 19:2585–2586

    Google Scholar 

  • Ladenburg A, Abel J (1888) Über das Aethylenimin (Spermin?). Ber Dtsch Chem Ges 21:758–766

    Google Scholar 

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

    PubMed  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

    Google Scholar 

  • Li Y-F, Hess S, Pannell LK, Tabor CW, Tabor H (2001) In vivo mechanism-based inactivation of S-adenosylmethionine decarboxylases from Escherichia coli, Salmonella typhimurium, and Saccharomyces cerevisiae. Proc Natl Acad Sci USA 98:10578–10583

    PubMed  CAS  Google Scholar 

  • Li J, Doyle KM, Tatlisumak T (2007) Polyamines in the brain: distribution, biological interactions, and their potential therapeutic role in brain ischaemia. Curr Med Chem 14:1804–1813

    Google Scholar 

  • Lioliou EE, Kyriakidis DA (2004) The role of bacterial antizyme: from an inhibitory protein to AtoC transcriptional regulator. Microb Cell Fact 3:8–16

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372:366–369

    PubMed  CAS  Google Scholar 

  • Lorenz B, Francis F, Gempel K, Boddrich A, Josten M, Schmahl W, Schmidt J, Lehrach H, Meitinger T, Strom TM (1998) Spermine deficiency in Gy mice caused by deletion of the spermine synthase gene. Hum Mol Genet 7:541–547

    PubMed  CAS  Google Scholar 

  • Lu Z, Ding L (1999) Blockage of a retinal cGMP-gated channel by polyamines. J Gen Physiol 113:35–43

    PubMed  CAS  Google Scholar 

  • Mackintosh CA, Pegg AE (2000) Effect of spermine synthase deficiency on polyamine biosynthesis and content in mice and embryonic fibroblasts, and the sensitivity of fibroblasts to 1,3-bis-(2-chloroethyl)-N-nitrosourea. Biochem J 351:439–447

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Mangold U (2005) The antizyme family: polyamines and beyond. IUBMB Life 57:671–676

    PubMed  CAS  Google Scholar 

  • Marini F, Betti L, Scaramagli S, Biodi S, Torrigiani P (2001) Polyamine metabolism is upregulated in response to tobacco mosaic virus in hypersensitive, but not in susceptible, tobacco. New Phytol 149:301–309

    CAS  Google Scholar 

  • Matsufuji S, Matsufuji T, Miyazaki Y, Murakami Y, Atkins JF, Gesteland RF, Hayashi S (1995) Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell 80:51–60

    PubMed  CAS  Google Scholar 

  • Matto AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen–carbon interactions. Plant Physiol 142:1759–1770

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    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. Biochem J 299:19–22

    PubMed  CAS  Google Scholar 

  • Mitsuya Y, Takahashi Y, Uehara Y, Berberich T, Miyazaki A, Takahashi H, Kusano T (2007) Identification of a novel Cys2/His2-type zinc finger protein as a component of a spermine-signaling pathway in tobacco. J Plant Physiol 164:785–793

    PubMed  CAS  Google Scholar 

  • Møller 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

    PubMed  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 

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

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Park MH (2006) The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J Biochem (Tokyo) 139:161–169

    CAS  Google Scholar 

  • Pegg AE (1986) Recent advances in the biochemistry of polyamines in eukaryotes. Biochem J 234:249–262

    PubMed  CAS  Google Scholar 

  • Pegg AE (2006) Regulation of ornithine decarboxylase. J Biol Chem 281:14529–14532

    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

    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 

  • Rhee HJ, Kim E-J, Lee JK (2007) Physiological polyamines: simple primordial stress molecules. J Cell Mol Med 11:685–703

    PubMed  CAS  Google Scholar 

  • Rider JE, Hacker A, Mackintosh CA, Pegg AE, Woster PM, Casero RA Jr (2007) Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33:231–240

    PubMed  CAS  Google Scholar 

  • Rob M, Roelfsema G, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol 167:665–691

    Google Scholar 

  • Romero-Puertas MC, Perazzolli M, Zago ED, Delledonne M (2004) Nitric oxide signalling functions in plant–pathogen interactions. Cell Microbiol 6:795–803

    PubMed  CAS  Google Scholar 

  • Ruan H, Shantz LM, Pegg AE, Morris DR (1996) The upstream open reading frame of the mRNA encoding S-adenosylmethionine decarboxylase is a polyamine-responsive translational control element. J Biol Chem 271:29576–29582

    PubMed  CAS  Google Scholar 

  • Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14:20–28

    PubMed  CAS  Google Scholar 

  • Saunder FR, Wallace HM (2007) Polyamine metabolism and cancer prevention. Biochem Soc Trans 35:364–368

    Google Scholar 

  • Šebela M, Radová A, Angelini R, Tavladoraki P, Frébort I, Peč P (2001) FAD-containing polyamine oxidases: a timely challenge for researchers in biochemistry and physiology of plants. Plant Sci 160:197–207

    PubMed  Google Scholar 

  • Seiler N (2004) Catabolism of polyamines. Amino Acids 26:217–233

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Seiler N, Raul F (2007) Polyamines and the intestinal tract. Crit Rev Clin Lab Sci 44:365–411

    PubMed  CAS  Google Scholar 

  • Seiler N, Duranton B, Raul F (2002) The polyamine oxidase inactivator MDL 72527. Prog Drug Res 59:1–40

    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 

  • Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylase mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Takahashi Y, Berberich T, Miyazaki A, Seo S, Ohashi Y, Kusano T (2003) Spermine signalling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J 36:820–829

    PubMed  CAS  Google Scholar 

  • Takahashi Y, Berberich T, Yamashita K, Uehara Y, Miyazaki A, Kusano T (2004a) Identification of tobacco HIN1 and two closely related genes as spermine-responsive genes and their differential expression during the Tobacco mosaic virus-induced hypersensitive response and during leaf- and flower-senescence. Plant Mol Biol 54:613–622

    PubMed  CAS  Google Scholar 

  • Takahashi Y, Uehara Y, Berberich T, Ito A, Saitoh H, Miyazaki A, Terauchi R, Kusano T (2004b) A subset of the hypersensitive response marker genes including HSR203J is downstream target of a spermine-signal transduction pathway in tobacco. Plant J 40:586–595

    PubMed  CAS  Google Scholar 

  • Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617

    PubMed  CAS  Google Scholar 

  • Tang W, Newton RJ, Li C, Charles TM (2007) Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis. Plant Cell Rep 26:115–124

    PubMed  CAS  Google Scholar 

  • Tateda C, Ozaki R, Onodera Y, Takahashi Y, Yamaguchi K, Berberich T, Koizumi N, Kusano T (2008) NtbZIP60, an endoplasmic reticulum-localized transcription factor, plays a role in defense response against bacterial pathogen in tobacco. J Plant Res (in press)

  • 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

    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

    PubMed  CAS  Google Scholar 

  • Terui Y, Higashi K, Taniguchi S, Shigemasa A, Nishimura K, Yamamoto K, Kashiwagi K, Ishihama A, Igarashi K (2004) Enhancement of the synthesis of RpoN, Cra, and H-NS by polyamines at the level of translation in Escherichia coli cultured with glucose and glutamate. J Bacteriol 189:2359–2368

    Google Scholar 

  • Thomas T, Thomas TJ (2001) Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell Mol Life Sci 58:244–258

    PubMed  CAS  Google Scholar 

  • Thomas T, Thomas TJ (2003) Polyamine metabolism and cancer. J Cell Mol Med 7:113–126

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Torrigiani P, Rabiti AL, Bortolotti C, Betti L, Marani F, Canova A, Bagni N (1997) Polyamine synthesis and accumulation in the hypersensitive response to TMV in Nicotiana tabacum. New Phytol 135:467–473

    CAS  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354

    PubMed  CAS  Google Scholar 

  • Uehara Y, Takahashi Y, Berberich T, Miyazak A, Takahashi H, Matsui K, Ohme-Takagi M, Saitoh H, Terauchi R, Kusano T (2005) Tobacco ZFT1, a transcriptional repressor with a Cys2/His2 type zinc finger motif that functions in spermine-signaling pathway. Plant Mol Biol 59:435–448

    PubMed  CAS  Google Scholar 

  • Umekage S, Ueda T (2006) Spermidine inhibits transient and stable ribosome subunit dissociation. FEBS Lett 580:1222–1226

    PubMed  CAS  Google Scholar 

  • Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J 274:1152–1171

    PubMed  CAS  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926

    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

    PubMed  CAS  Google Scholar 

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

    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 

  • von Udransky L, Baumann E (1888) Über die Identität des Putrescins und des Tetramethylendiamins. Ber Dtsch Chem Ges 21:2938–2941

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Walters DR (2003a) Resistance to plant pathogens: possible roles for free polyamines and polyamine catabolism. New Phytol 159:109–115

    CAS  Google Scholar 

  • Walters DR (2003b) Polyamines and plant disease. Phytochemistry 64:97–107

    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 X, Ikeguchi Y, McCloskey DE, Nelson P, Pegg AE (2004) Spermine synthesis is required for normal viability, growth, and fertility in the mouse. J Biol Chem 279:51370–51375

    PubMed  CAS  Google Scholar 

  • Ward JM, Schroeder JI (1994) Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6:669–683

    PubMed  CAS  Google Scholar 

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

    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, Pang XM, Matsuda N, Kita M, Inoue H, Hao Y-J, Honda C, Moriguchi T (2007) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17:251–263

    PubMed  Google Scholar 

  • William K (1997a) Interactions of polyamines with ion channels. Biochem J 325:289–297

    Google Scholar 

  • Williams K (1997b) Modulation and block of ion channels: a new biology of polyamines. Cell Signal 9:1–13

    PubMed  CAS  Google Scholar 

  • Wortham BW, Patel CN, Oliveira MA (2007) Polyamines in bacteria: pleiotropic effects yet specific mechanisms. Adv Exp Med Biol 603:106–115

    PubMed  Google Scholar 

  • Wrede F (1925) Über die aus menschlichem Sperma isolierte Base Spermin. Dtsch Med Wochenschr 51:24

    Article  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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yamaguchi Y, Takatsuka Y, Kamio Y (2002) Identification of a 22-kDa protein required for the degradation of Selenomonas ruminantium lysine decarboxylase by ATP-dependent protease. Biosci Biotechnol Biochem 66:1431–1434

    PubMed  CAS  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:783–6788

    Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael A, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:86–490

    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

    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 

  • Yamasaki H, Shimoji H, Ohshiro Y, Sakihama Y (2001) Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide 5:261–270

    PubMed  CAS  Google Scholar 

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

    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

    PubMed  CAS  Google Scholar 

  • Yoshida M, Kashiwagi K, Shigemasa A, Taniguchi S, Yamamoto K, Makinoshima H, Ishihama A, Igarashi K (2004) A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J Biol Chem 279:46008–46013

    PubMed  CAS  Google Scholar 

  • Zeller EA (1938) Zur Kenntnis der Diamin-oxydase. 3. Mitteilung über den enzymatischen Abbau von Poly-aminen. Helv Chim Acta 21:1645–1665

    CAS  Google Scholar 

  • Zhao F, Song C-P, He J, 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 

Download references

Acknowledgments

We apologize to the researchers whose works are not cited in this review due to space limitation. We are grateful to our past and present colleagues, especially Y. Uehara, Y. Mitsuya and K. Yamaguchi. Drs. A. Mator and T. Moriguchi are appreciated for providing their preprints. Dr. Matthew R. Shenton is acknowledged for critically reading the manuscript. Our research was partly supported by Grants-in-Aid from the Japan Society for the Promotion of Science to TK (19658039) and to YT (19780002), and grants from Saito Gratitude Foundation to CT and the Sumitomo Foundation to YT. We deeply acknowledge the remarks of Dr. D. Scheel and the anonymous reviewers who contributed to improving this review.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Kusano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kusano, T., Berberich, T., Tateda, C. et al. Polyamines: essential factors for growth and survival. Planta 228, 367–381 (2008). https://doi.org/10.1007/s00425-008-0772-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0772-7

Keywords

Navigation