Abstract
Distribution of biogenic amines—the diamine putrescine (Put), triamine spermidine (Spd), and tetraamine spermine (Spm)—differs between species with Put and Spd being particularly abundant and Spm the least abundant in plant cells. These amines are important for cell viability and their intracellular levels are tightly regulated, which have made it difficult to characterize individual effects of Put, Spd and Spm on plant growth and developmental processes. The recent transgenic intervention and mutational genetics have made it possible to stably alter levels of naturally occurring polyamines and study their biological effects. We bring together an analysis of certain metabolic changes, particularly in amino acids, to infer the responsive regulation brought about by increased diamine or polyamine levels in actively growing poplar cell cultures (transformed with mouse ornithine decarboxylase gene to accumulate high Put levels) and ripening tomato pericarp (transformed with yeast S-adenosylmethionine decarboxylase gene to accumulate high Spd and Spm levels at the cost of Put). Our analysis indicates that increased Put has little effect on increasing the levels of Spd and Spm, while Spd and Spm levels are inter-dependent. Further, Put levels were positively associated with Ala (α and β), Ile and GABA and negatively correlated with Gln and Glu in both actively growing poplar cell cultures and non-dividing tomato pericarp tissue. Most amino acids showed positive correlations with Spd and Spm levels in actively growing cells. Collectively these results suggest that Put is a negative regulator while Spd–Spm are positive regulators of cellular amino acid metabolism.
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Abbreviations
- DAO:
-
Diamine oxidase
- eIF5A:
-
Eukaryotic initiation factor 5A
- HP:
-
High putrescine
- NAGS:
-
N-acetyl glutamate synthase
- P5CS:
-
Δ1-Pyrroline-5-carboxylate synthase
- PAO:
-
Polyamine oxidase
- Put:
-
Putrescine
- Spd:
-
Spermidine
- Spm:
-
Spermine
- ySAMDC:
-
Yeast S-adenosylmethionine decarboxylase
References
Agostinelli E, Belli F, Molinari A, Condello M, Palmigiani P, Dalla Vedova L, Marra M, Seiler N, Arancia G (2006) Toxicity of enzymatic oxidation products of spermine to human melanoma cells (M14): sensitization by heat and MDL 72527. Biochim Biophys Acta 1763:1040–1050
Aziz A, Larher F (1995) Changes in polyamine titers associated with the proline response and osmotic adjustment of rape leaf discs submitted to osmotic stress. Plant Sci 112:175–186
Aziz A, Martin-Tanguy J, Larher F (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol Plant 104:195–202
Bacchi CJ, Yarlett N (2002) Polyamine metabolism as chemotherapeutic target in protozoan parasites. Mini-Reviews Med Chem 2:553–563
Bachrach U, Wang YC (2002) Cancer therapy and prevention by green tea: role of ornithine decarboxylase. Amino Acids 22:1–13
Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317
Bagni N, Calzoni GL, Speranza A (1978) Polyamines as sole nitrogen sources for Helianthus tuberosus explants in vitro. New Phytol 80:317–323
Bastola DR, Minocha SC (1995) Increased putrescine biosynthesis through transfer of mouse ornithine decarboxylase cDNA in carrot promotes somatic embryogenesis. Plant Physiol 109:63–71
Bauer GA, Bazzaz FA, Minocha R, Long S, Magill A, Aber J, Berntson GM (2004) Effects of chronic N additions on tissue chemistry, photosynthetic capacity and carbon sequestration potential of a red pine (Pinus resinosa Ait.) stand in the NE United States. Forest Ecol Managem 196:173–186
Bhatnagar P, Glasheen B, Bains S, Long S, Minocha R, Walter C, Minocha S (2001) Transgenic manipulation of the metabolism of polyamines in poplar cells. Plant Physiol 125:2139–2153
Bhatnagar P, Minocha R, Minocha S (2002) Genetic manipulation of the metabolism of polyamines in poplar cells: The regulation of putrescine catabolism. Plant Physiol 128:1455–1469
Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115
Capell T, Escobar C, Liu H, Burtin D, Lepri O, Christou P (1998) Over-expression of the oat arginine decraboxylase cDNA in transgenic rice (Oryza sativa L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theor Appl Genet 97:246–254
Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914
Casero RA Jr, Marton LJ (2007) Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 6:373–390
Cassol T, Mattoo AK (2003) Do polyamines and ethylene interact to regulate plant growth, development and senescence? In: Nath P, Mattoo AK, Ranade SA, Weil JH (eds) Molecular insight in plant biology. Science, Enfield, pp 121–132
Chou WC, Huang YW, Tsay WS, Chiang TY, Huang DD, Huang HJ (2004) Expression of genes encoding the rice translation initiation factor, eIF5A, is involved in developmental and environmental responses. Physiol Plant 121:50–57
Cohen SS (1998) A guide to the polyamines. Oxford University Press, New York
Corruzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4:247–253
Coruzzi G, Last R (2000) In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, MD, pp 358–410
Del Duca S, Bregoli AM, Bergamini C, Serafini-Fracassini D (1997) Transglutaminase-catalyzed modification of cytoskeletal proteins by polyamines during the germination of Malus domestica pollen. Sex Plant Reprod 10:89–95
DeScenzo RA, Minocha SC (1993) Modulation of cellular polyamines in tobacco by transfer and expression of mouse ornithine decarboxylase cDNA. Plant Mol Biol 22:113–127
Fluhr R, Mattoo AK (1996) Ethylene—biosynthesis and perception. Crit Rev Plant Sci 15:479–523
Foyer CH, Noctor G (2002) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Kluwer, Boston
Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864
Houdusse F, Zamarreño A, Garnica M, García-Mina J (2005) The importance of nitrate in ameliorating the effects of ammonium and urea nutrition on plant development: the relationships with free polyamines and plant proline contents. Funct Plant Biol 32:1057–1067
Ioannidis NE, Kotzabasis K (2007) Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta 1767:1372–1382
Jänne J, Alhonen L, Pietila M, Keinanen TA (2004) Genetic approaches to the cellular functions of polyamines in mammals. Eur J Biochem 271:877–894
Jao DL, Chen KY (2005) Tandem affinity purification revealed the hypusine-dependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. J Cell Biochem 97:583–598
Jell J, Merali S, Hensen ML, Mazurchuk R, Spernyak JA, Diegelman P, Kisiel ND, Barrero C, Deeb KK, Alhonen L, Patel MS, Porter CW (2007) Genetically altered expression of spermidine/spermine N 1-acetyltransferase affects fat metabolism in mice via acetyl-CoA. J Biol Chem 282:8404–8413
Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282
Kaur-Sawhney R, Tiburcio AF, Altabella T, Galston AW (2003) Polyamines in plants: an overview. J Cell Mol Biol 2:1–12
Krishnamurthy R, Bhagwat KA (1989) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol 91:500–504
Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research. Curr Topics Plant Res 120:345–350
Lee J, Sperandio V, Frantz DE, Longgood J, Camilli A, Phillipis MA, Michael AJ (2009a) An alternative polyamine biosynthetic pathway is widespread in bacteria and essential for biofilm formation in Vibrio cholerae. J Biol Chem 284:9899–9907
Lee SB, Park JH, Kaeval J, Sramkova M, Weigert R, Park MH (2009b) The effect of hypusine modification on the intracellular localization of eIF5A. Biochem Biophys Res Commun 383:497–502
Li AL, Li HY, Jin BF, Ye QN, Zhou T, Yu XD, Pan X, Man JH, He K, Yu M et al (2004) A novel eIF5A complex functions as a regulator of p53 and p53-dependent apoptosis. J Biol Chem 279:49251–49258
Mattoo AK, Handa AK (2008) Higher polyamines restore and enhance metabolic memory in ripening fruit. Plant Sci 174:386–393
Mattoo AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy based metabolite profiles of transgenic tomato fruit engineered to accumulate polyamines spermidine and spermine reveal enhanced anabolic nitrogen-carbon interactions. Plant Physiol 142:1759–1770
Mattoo AK, Chung S-H, Goyal RK, Fatima T, Srivastava A, Solomos T, Handa AK (2007) Over-accumulation of higher polyamines in ripening transgenic tomato fruit revives metabolic memory, upregulates anabolism-related genes, and positively impacts nutritional quality. J AOAC Intl 90:1456–1464
Mehta AM, Saftner RA, Schaeffer GW, Mattoo AK (1991) Translational modification of an 18 kilodalton polypeptide by spermidine in rice cell suspension cultures. Plant Physiol 95:1294–1297
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
Mengoli M, Chriqui D, Bagni N (1992) Putrescine biosynthesis and oxidation in normal and hairy root tobacco plants. J Plant Physiol 140:153–155
Minocha R, Minocha SC (2005) Effects of soil pH and aluminum on plant respiration. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem advances in photosynthesis and respiration. Springer, Dordrecht, pp 159–176
Minocha R, Lee JS, Long S, Bhatnagar P, Minocha SC (2004a) Physiological responses of wild type and putrescine-overproducing transgenic cells of poplar to variations in the form and concentration of nitrogen in the medium. Tree Physiol 24:551–560
Minocha R, Minocha SC, Long S (2004b) Polyamines and their biosynthetic enzymes during somatic embryo development in red spruce (Picea rubens Sarg.). In vitro Cell Dev Biol 40:572–580
Mohapatra S, Minocha R, Long S, Minocha SC (2009a) Putrescine overproduction negatively impacts the oxidative state of poplar cells in culture. Plant Physiol Biochem 47:262–271
Mohapatra S, Minocha R, Long S, Minocha S (2009b) Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids. Amino Acids doi:10.1007/s00726-009-0322-z
Morris S (2007) Arginine metabolism: boundaries of our knowledge. J Nutr 137:1602S–1609S
Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism. The state of the art. Plant Signal Behav 3:1061–1066
Neelam A, Cassol T, Mehta RA, Abdul-Baki AA, Sobolev A, Goyal RK, Abbott J, Segre AL, Handa AK, Mattoo AK (2008) A field-grown transgenic tomato line expressing higher levels of polyamines reveals legume cover crop mulch-specific perturbations in fruit phenotype at the levels of metabolite profiles, gene expression and agronomic characteristics. J Exp Bot 59:2337–2346
Page A, Mohapatra S, Minocha R, Minocha SC (2007) The effects of genetic manipulation of putrescine biosynthesis on transcription and activities of the polyamine biosynthetic enzymes. Physiol Plant 129:707–724
Park MH, Cooper HL, Folk JE (1981) Identification of hypusine, an unusual amino acid, in a protein from human lymphocytes and of spermidine as its biosynthetic precursor. Proc Natl Acad Sci USA 78:2869–2873
Park JH, Aravind L, Wolff EC, Kaevel J, Kim YS, Park MH (2006) Molecular cloning, expression, and structural prediction of deoxyhypusine hydroxylase: a HEAT-repeat-containing metalloenxyme. Proc Natl Acad Sci USA 103:51–56
Paschalidis K, Roubelakis-Angelakis KA (2005) Sites and regulation of polyamine catabolism in the tobacco plant Correlations with cell division/expansion, cell cycle progression, and vascular development. Plant Physiol 138:2174–2184
Pfeffer LM, Yang CH, Murti A, McCormack SA, Viar MJ, Ray RM, Johnson LR (2001) Polyamine depletion induces rapid NF-κB activation in IEC-6 cells. J Biol Chem 276:45909–45913
Pignatti C, Tantini B, Stefanelli C, Flamigni F (2004) Signal transduction pathways linking polyamines to apoptosis. Amino Acids 27:359–365
Quan Y, Minocha R, Minocha SC (2002) Genetic manipulation of polyamine metabolism in poplar II: effects on ethylene biosynthesis. Plant Physiol Biochem 40:929–937
Rennenberg H, Kreutzer K, Papen H, Weber P (1998) Consequences of high loads of nitrogen for spruce (Picea abies) and beech (Fagus sylvatica) forests. New Phytol 139:71–86
Roosens N, Bitar F, Loenders K, Angenon G, Jacobs M (2002) Overexpression of ornithine-δ-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Mol Breed 9:73–80
Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302
Sharma S, Dietz K (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726
Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde J (2005) Genetic manipulation of proline accumulation influences the concentrations of other amino acids in soybean subjected to simultaneous drought and heat stress. J Agric Food Chem 53:7512–7517
Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde JA (2006) Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Plant Biol 50:793–796
Slocum R (2005) Genes, enzymes and regulation of arginine biosynthesis in plants. Plant Physiol Biochem 43:729–745
Slocum RD, Flores HE (1991) Biochemistry and physiology of polyamines in plants. CRC Press, Boca Raton
Srivastava A, Chung SH, Fatima T, Datsenka T, Handa AK, Mattoo AK (2007) Polyamines as anabolic growth regulators revealed by transcriptome analysis and metabolite profiles of tomato fruits engineered to accumulate spermidine and spermine. Plant Biotechnol 24:57–70
Stitt M, Muller C, Matt P, Gibon Y, Carillo P, Morcuendo R, Scheible WR, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53:959–970
Székely G, Ábrahám E, Cséplö A, Rigó G, Zsgimond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28
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
Taylor CA, Sun Z, Cliche DO, Ming H, Eshaque B, Jin S, Hopkins MT, Thai B, Thompson JE (2007) Eukaryotic translation initiation factor 5A induces apoptosis in colon cancer cells and associates with the nucleus in response to tumour necrosis factor alpha signaling. Exp Cell Res 313:437–449
Tome ME, Gerner EW (1997) Cellular eukaryotic initiation factor 5A content as a mediator of polyamine effects on growth and apoptosis. Biol Signals 6:150–156
Tomitori H, Usui T, Saeki N, Ueda S, Kase H, Nishimura K, Kashiwagi K, Igarashi K (2005) Polyamine oxidase and acrolein as novel biochemical markers for diagnosis of cerebral stroke. Stroke 36:2609–2613
Urbanczyk E, Fernie AR (2005) Metabolic profiling reveals altered nitrogen nutrient regimes have diverse effects on the metabolism of hydroponically-grown tomato (Solanum lycopersicum) plants. J Exp Bot 56:309–321
Wang TW, Lu L, Zhang CG, Taylor CA, Thompson JE (2003) Pleiotropic effects of suppressing deoxyhypusine synthase expression in Arabidopsis thaliana. Plant Mol Biol 52:1223–1235
Wolff EC, Folk JE, Park MH (1997) Enzyme-substrate intermediate formation at lysine 329 of human deoxyhypusine synthase. J Biol Chem 272:15865–15871
Wolff EC, Kang KR, Kim YS, Park MH (2007) Posttranslational synthesis of hypusine: evolutionary progression and specificity of the hypusine modification. Amino Acids 33:341–350
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788
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 352:486–490
Zanelli CF, Valentini SR (2007) Is there a role for eIF5A in translation? Amino Acids 33:351–358
Zhu X, Galili G (2003) Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulates the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15:845–853
Acknowledgments
We acknowledge the contributions of our collaborators listed in the cited references. The research presented here was funded by USDA-NRI award No. 2002-35318-12674 to SCM); the NH Agricultural Experiment Station (to SCM and RKM); the US Forest Service, Northern Research Station; US–Israel BARD grant (to AKH and AKM; Grant N0. IS-3441-03), a grant from the U.S. Department of Agriculture, IFAFS program (to AKH; Award No. 741740), and U.S. Department of Agriculture, Agricultural Research Service. This is scientific contribution number 2407 from the NH Agricultural Experiment Station. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.
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Mattoo, A.K., Minocha, S.C., Minocha, R. et al. Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38, 405–413 (2010). https://doi.org/10.1007/s00726-009-0399-4
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DOI: https://doi.org/10.1007/s00726-009-0399-4