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The role of polyamines during in vivo and in vitro development

  • Kevin Baron
  • Claudio StasollaEmail author
Article

Abstract

Polyamines are ubiquitous polycationic compounds that mediate fundamental aspects of cell growth, differentiation, and cell death in eukaryotic and prokaryotic organisms. In plants, polyamines are implicated in a variety of growth and developmental processes, in addition to abiotic and biotic stress responses. In the last decade, mutant studies conducted predominantly in Arabidopsis thaliana revealed an obligatory requirement for polyamines in zygotic and somatic embryogenesis. Moreover, our appreciation for the intricate spatial and temporal regulation of intracellular polyamine levels has advanced considerably. The exact molecular mechanism(s) through which polyamines exert their physiological response remains somewhat enigmatic and likely serves as a major area for future research efforts. In the following review, we discuss recent advances in the plant polyamine field, which range from metabolism and mutant characterization to molecular genetics and potential mode(s) of polyamine action during growth and development in vitro and in vivo. This review will also focus on the specific role of polyamines during embryogenesis and organogenesis.

Keywords

Polyamine Embryogenesis Organogenesis Arabidopsis Abscisic acid Ethylene Putrescine Spermine Spermidine Ornithine Arginine Adenosylmethionine Nitric oxide Calcium Potassium Ion channel Angiosperm Gymnosperm Biotechnology Tissue culture 

Notes

Acknowledgment

The authors wish to thank Bert Luit for critically reviewing the manuscript.

References

  1. Acosta, C.; Pérez-Amador, M. A.; Carbonell, J.; Granell, A. The two ways to produce putrescine in tomato are cell-specific during normal development. Plant Sci. 168: 1053–1057; 2005 doi: 10.1016/j.plantsci.2004.12.006.Google Scholar
  2. Alcázar, R.; Cuevas, J. C.; Patron, M.; Altabella, T.; Tiburcio, A. F. Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol. Plant 128: 448–455; 2006b doi: 10.1111/j.1399-3054.2006.00780.x.Google Scholar
  3. Alcázar, R.; Garcia-Martinez, J. L.; Cuevas, J. C.; Tiburcio, A. F.; Altabella, T. Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA-deficiency. Plant J. 43: 425–436; 2005 doi: 10.1111/j.1365-313X.2005.02465.x.PubMedGoogle Scholar
  4. Alcázar, R.; Marco, F.; Cuevas, J. C.; Patron, M.; Ferrando, A.; Carrasco, P.; Tiburcio, A. F.; Altabella, T. Involvement of polyamines in plant response to abiotic stress. Biotechnol. Lett. 28: 1867–1876; 2006a doi: 10.1007/s10529-006-9179-3.PubMedGoogle Scholar
  5. Altamura, M. M.; Capitani, F.; Falasca, G.; Gallelli, A.; Scaramagli, S.; Bagni, N. De novo root-formation in tobacco thin-layers is affected by inhibition of polyamine biosynthesis. J. Exp. Bot. 42: 1575–1582; 1991 doi: 10.1093/jxb/42.12.1575.Google Scholar
  6. Altamura, M. M.; Capitani, F.; Falasca, G.; Gallelli, A.; Scaramagli, S.; Bueno, M.; Torrigiani, P.; Bagni, N. Morphogenesis in cultured thin-layers and pith explants of tobacco.1. effect of putrescine on cell-size, xylogenesis and meristemoid organization. J. Plant Physiol. 147: 101–106; 1995.Google Scholar
  7. An, Z.; Jing, W.; Liu, Y.; Zhang, W. Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J. Exp. Bot. 59: 815–825; 2008 doi: 10.1093/jxb/erm370.PubMedGoogle Scholar
  8. Antognoni, F.; Fornale, S.; Grimmer, C.; Komor, E.; Bagni, N. Long-distance translocation of polyamines in phloem and xylem of Ricinus communis L. plants. Planta 204: 520–527; 1998 doi: 10.1007/s004250050287.Google Scholar
  9. Aouida, M.; Leduc, A.; Poulin, R.; Ramator, D. AGP2 Encodes the major permease for high affinity polyamine import in Saccharomyces cerevisiae. J. Biol. Chem. 280: 24267–24276; 2005 doi: 10.1074/jbc.M503071200.PubMedGoogle Scholar
  10. Applewhite, P. B.; Kaur-Sawhney, R.; Galston, A. W. A role for spermidine in the bolting and flowering of Arabidopsis. Physiol. Plant. 108: 314–320; 2000 doi: 10.1034/j.1399-3054.2000.108003314.x.Google Scholar
  11. Athwal, G. S.; Huber, S. C. Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase. Plant J. 29: 119–129; 2002 doi: 10.1046/j.0960-7412.2001.01200.x.PubMedGoogle Scholar
  12. Bagga, S.; Rochford, J.; Klaene, Z.; Kuehn, G. D.; Phillips, G. C. Putrescine aminopropyl transferase is responsible for biosynthesis of spermidine, spermine, and multiple uncommon polyamines in osmotic stress-tolerant alfalfa. Plant Physiol. 114: 445–454; 1997.PubMedGoogle Scholar
  13. Bagni, N.; Tassoni, A. Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20: 301–317; 2001 doi: 10.1007/s007260170046.PubMedGoogle Scholar
  14. Bais, P. H.; Ravishankar, G. A. Role of polyamines in the ontogeny of plants and their biotechnological applications. Plant Cell Tissue Org. Cult. 69: 1–34; 2002.Google Scholar
  15. Bastola, D. R.; Minocha, S. C. Increased putrescine biosynthesis through transfer of mouse ornithine decarboxylase cDNA in carrot promotes somatic embryogenesis. Plant Physiol. 109: 63–71; 1995.PubMedGoogle Scholar
  16. Besson-Bard, A.; Courtois, C.; Gauthier, A.; Dahan, J.; Dobrowolska, G.; Jeandroz, S.; Pugin, A.; Wendehenne, D. Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Molecular Plant 1: 218–228; 2008 doi: 10.1093/mp/ssm016.PubMedGoogle Scholar
  17. Biondi, S.; Scaramagli, S.; Capatini, F.; Maddalena, Altamura, M.; Torrigiani, P. Methyl jasmonate upregulates biosynthesis gene expression, oxidation and conjugation of polyamines, and inhibits shoot formation in tobacco thin layers. J. Exp. Bot. 52: 231–242; 2001 doi: 10.1093/jexbot/52.355.231.PubMedGoogle Scholar
  18. Bortolotti, C.; Cordeiro, A.; Alcàzar, R.; Borrell, A.; Culiañez-Macià, F. A.; Tiburcio, A. F.; Altabella, T. Localization of arginine decarboxylase in tobacco plants. Physiol. Plant 120: 84–92; 2004 doi: 10.1111/j.0031-9317.2004.0216.x.PubMedGoogle Scholar
  19. Bozhkov, P. V.; Filonova, L. H.; Suarez, M. F. Programmed cell death in plant embryogenesis. Curr. Top. Dev. Biol. 67: 135–179; 2005 doi: 10.1016/S0070-2153(05)67004-4.PubMedGoogle Scholar
  20. Bregante, M.; Yang, Y.; Formentin, E.; Carpaneto, A.; Schroeder, J. I.; Gambale, F.; Schiavo, F. L.; Costa, A. KDC1, a carrot Shaker-like potassium channel, reveals its role as a silent regulatory subunit when expressed in plant cells. Plant Mol. Biol. 66: 61–72; 2008 doi: 10.1007/s11103-007-9252-x.PubMedGoogle Scholar
  21. Caffaro, S. V.; Antognoni, F.; Scaramagli, S.; Bagni, N. Polyamine translocation following photoperiodic flowering induction in soybean. Physiol. Plant 91: 251–256; 1994 doi: 10.1111/j.1399-3054.1994.tb00426.x.Google Scholar
  22. Capell, T.; Bassie, L.; Christou, P. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Natl. Acad. Sci. U. S. A. 101: 9909–9914; 2004 doi: 10.1073/pnas.0306974101.PubMedGoogle Scholar
  23. Clay, N. K.; Nelson, T. 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; 2005 doi: 10.1104/pp.104.055756.PubMedGoogle Scholar
  24. Cona, A.; Rea, G.; Angelina, R.; Federico, R.; Tavladoraki, P. Functions of amine oxidases in plant development and defence. Trend Plant Sci. 11: 80–88; 2006 doi: 10.1016/j.tplants.2005.12.009.Google Scholar
  25. Costa, A.; Carpaneto, A.; Varotto, S.; Formentin, E.; Marin, O.; Barizza, E.; Terzi, M.; Gambale, F.; Schiavo, F. L. Potassium and carrot embryogenesis: Are K+ channels necessary for development. Plant Mol. Biol. 54: 837–852; 2004 doi: 10.1007/s11103-004-0236-9.PubMedGoogle Scholar
  26. Coueé, I.; Hummel, I.; Sulmon, C.; Gouesbet, G.; El Amrani, A. Involvement of polyamines in root development. Plant Cell Tissue Org. Cult. 76: 1–10; 2004.Google Scholar
  27. Della Mea, M.; De Filippis, F.; Genovesi, V.; Serafini-Fracassini, D.; Del Duca, S. The acropetal wave of developmental cell death of tobacco corolla is preceded by activation of transglutaminase in different cell compartments. Plant Physiol. 144: 1211–1222; 2007b doi: 10.1104/pp.106.092072.PubMedGoogle Scholar
  28. Della Mea, M.; Serafini-Fracassini, D.; Del Duca, S. Programmed cell death: similarities and differences in animals and plants. A flower paradigm. Amino Acids 33: 395–404; 2007a doi: 10.1007/s00726-007-0530-3.PubMedGoogle Scholar
  29. Del Duca, S.; Beninati, S.; Serafini-Fracassini, D. Polyamines in chloroplasts: identification of their glutamyl and acetyl derivatives. Biochem. J. 305: 233–237; 1995.PubMedGoogle Scholar
  30. Delis, C.; Dimou, M.; Efrose, R. C.; Flemetakis, E.; Aivalakis, G.; Katinakis, P. Ornithine decarboxylase and arginine decarboxylase gene transcripts are co-localized in developing tissues of Glycine max etiolated seedlings. Plant Physiol. Biochem. 43: 19–25; 2005 doi: 10.1016/j.plaphy.2004.11.006.PubMedGoogle Scholar
  31. Diepold, A.; Li, G.; Lennarz, W. J.; Nürnburger, T.; Brunner, F. The Arabidopsis AtPNG1 gene encodes a peptide: N-glycanase. Plant J. 52: 94–104; 2007 doi: 10.1111/j.1365-313X.2007.03215.x.PubMedGoogle Scholar
  32. Dobrovinskaya, O. R.; Müntz, J.; Pottosin, I. I. Asymmetric block of the plant vacuolar Ca2+ -permeable channel by organic cations. Eur. Biophys. J. 28: 552–563; 1999 doi: 10.1007/s002490050237.PubMedGoogle Scholar
  33. Evans, P. T.; Malmberg, R. L. Do polyamines have roles in plant development? Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 235–269; 1989.Google Scholar
  34. Feinberg, A. A.; Choi, J. H.; Lubich, W. P.; Sung, Z. R. Developmental regulation of polyamine metabolism in growth and differentiation of carrot culture. Planta 162: 532–539; 1984 doi: 10.1007/BF00399919.Google Scholar
  35. Feirer, R. P.; Mignon, G.; Litvay, J. D. Arginine decarboxylase and polyamines required for embryogenesis in the wild carrot. Science 223: 1433–1435; 1984 doi: 10.1126/science.223.4643.1433.PubMedGoogle Scholar
  36. Formentin, E.; Naso, A.; Varotto, S.; Picco, C.; Gambale, F.; Schiavo, F. L. KDC2, a functional homomeric potassium channel expressed during carrot embryogenesis. FEBS Lett. 580: 5009–5015; 2006 doi: 10.1016/j.febslet.2006.08.017.PubMedGoogle Scholar
  37. Galston, A. W.; Sawhey, R. K. Polyamines and plant physiology. Plant Physiol. 94: 406–410; 1990.PubMedCrossRefGoogle Scholar
  38. Ge, C.; Cui, X.; Wang, Y.; Hu, Y.; Fu, Z.; Zhang, D.; Cheng, Z.; Li, J. BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res. 16: 446–456; 2006 doi: 10.1038/sj.cr.7310056.PubMedGoogle Scholar
  39. Gemperlová, L.; Eder, J.; Cvikrová, M. Polyamine metabolism during the growth cycle of tobacco BY-2 cells. Plant Physiol. Biochem. 43: 375–381; 2005.PubMedGoogle Scholar
  40. Gemperlová, L.; Novàková, M.; Vanková, R.; Eder, J.; Cvikrová, M. Diurnal changes in polyamine content, arginine and ornithine decarboxylase, and diamine oxidase in tobacco leaves. J. Exp. Bot. 57: 1413–1421; 2006 doi: 10.1093/jxb/erj121.PubMedGoogle Scholar
  41. Goldberg, R. B.; de Paiva, G.; Yadegari, R. Plant embryogenesis: zygote to seed. Science 266: 605–614; 1994 doi: 10.1126/science.266.5185.605.PubMedGoogle Scholar
  42. Hagenbeek, D.; Quatrano, R. S.; Rock, C. D. Trivalent ions activate abscisic acid-inducible promoters through an ABI1-dependent pathway in rice protoplasts. Plant Physiol. 123: 1553–1560; 2000 doi: 10.1104/pp.123.4.1553.PubMedGoogle Scholar
  43. Hanfrey, C.; Elliott, K. A.; Franceschetti, M.; Mayer, M. J.; Illingworth, C.; Michael, A. J. A dual upstream open reading frame-based autoregulatory circuit controlling polyamine-responsive translation. J. Biol. Chem. 47: 39229–39237; 2005 doi: 10.1074/jbc.M509340200.Google Scholar
  44. Hanfrey, C.; Franceschetti, M.; Mayer, M. J.; Illingworth, C.; Elliott, K.; Collier, M.; Thompson, B.; Perry, B.; Michael, A. J. Translational regulation of the plant S-adenosylmethionine decarboxylase. Biochem. Soc. Trans. 31: 424–427; 2003 doi: 10.1042/BST0310424.PubMedGoogle Scholar
  45. Hanfrey, C.; Sommer, S.; Mayer, M. J.; Burtin, D.; Michael, A. J. Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J. 27: 551–560; 2001 doi: 10.1046/j.1365-313X.2001.01100.x.PubMedGoogle Scholar
  46. Hanzawa, Y.; Takahashi, T.; Michael, A. J.; Burtin, D.; Long, D.; Pineiro, M.; Coupland, G.; Komeda, Y. ACAULIS5, and Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J. 19: 4248–4256; 2000 doi: 10.1093/emboj/19.16.4248.PubMedGoogle Scholar
  47. Heby, O. DNA methylation and polyamines in embryonic development and cancer. Int. J. Dev. Biol. 39: 737–757; 1995.PubMedGoogle Scholar
  48. Hu, W. -W.; Gong, H.; Pua, E.-C. Modulation of SAMDC expression in Arabidopsis thaliana alters in vitro shoot organogenesis. Physiol. Plant 128: 740–750; 2006 doi: 10.1111/j.1399-3054.2006.00799.x.Google Scholar
  49. Hummel, I.; Bourdais, G.; Gousbet, G.; Coueé, I.; Malmberg, R. L.; El Amrani, A. Differential gene expression of arginine decarboxylase ADC1 and ADC2 in Arabidopsis thaliana: characterization of transcriptional regulation during seed germination and seedling development. New Phytol. 163: 519–531; 2004 doi: 10.1111/j.1469-8137.2004.01128.x.Google Scholar
  50. Ibaraki, Y.; Kurata, K. Automation of somatic embryo production. Plant Cell Tissue Org. Cult. 65: 179–199; 2001.Google Scholar
  51. Illingworth, C.; Mayer, M. J.; Elliott, K.; Hanfrey, C.; Walton, N. J.; Michael, A. J. The diverse bacterial origins of the Arabidopsis polyamine biosynthetic pathway. FEBS Lett. 549: 26–30; 2003 doi: 10.1016/S0014-5793(03)00756-7.PubMedGoogle Scholar
  52. Imai, A.; Akiyama, T.; Kato, T.; Sato, S.; Tabata, S.; Yamamoto, K. T.; Takahashi, T. Spermine is not essential for survival of Arabidopsis. FEBS Lett. 556: 148–152; 2004b doi: 10.1016/S0014-5793(03)01395-4.PubMedGoogle Scholar
  53. Imai, A.; Hanzawa, Y.; Komura, M.; Yamamoto, K. T.; Komeda, Y.; Takahashi, T. 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; 2006 doi: 10.1242/dev.02535.PubMedGoogle Scholar
  54. 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. Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol. 135: 1565–1573; 2004a doi: 10.1104/pp.104.041699.PubMedGoogle Scholar
  55. Janowitz, T.; Kneifel, H.; Piotrowski, M. Identification and characterization of plant agmatine iminohydrolase, the last missing link in polyamine biosynthesis of plants. FEBS Lett. 544: 258–261; 2003 doi: 10.1016/S0014-5793(03)00515-5.PubMedGoogle Scholar
  56. Kakkar, R. K.; Sawhey, V. P. Polyamine research in plants—a changing perspective. Physiol. Plant. 116: 281–292; 2002 doi: 10.1034/j.1399-3054.2002.1160302.x.Google Scholar
  57. Kaplan, B.; Davydov, O.; Knight, H.; Galon, Y.; Knight, K. R.; Fluhr, R.; Fromm, H. Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell. 18: 2733–2748; 2006 doi: 10.1105/tpc.106.042713.PubMedGoogle Scholar
  58. Knott, J. M.; Römer, P.; Sumper, M. Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett. 581: 3081–3086; 2007 doi: 10.1016/j.febslet.2007.05.074.PubMedGoogle Scholar
  59. Kumria, R.; Rajam, M. V. Alteration in polyamine titres during Agrobacterium-mediated transformation of indica rice with ornithine decarboxylase gene affects plant regeneration potential. Plant Sci. 162: 769–777; 2002 doi: 10.1016/S0168-9452(02)00020-1.Google Scholar
  60. Kusano, T.; Yamaguchi, K.; Berberich, T.; Takahashi, Y. Advances in polyamine research in 2007. J. Plant Res. 120: 345–350; 2007 doi: 10.1007/s10265-007-0074-3.PubMedGoogle Scholar
  61. Kwak, S.-H.; Lee, S. H. The transcript-level-independent activation of ornithine decarboxylase in suspension-cultured BY2 cells entering the cell cycle. Plant Cell Physiol. 43: 1165–1170; 2002 doi: 10.1093/pcp/pcf132.PubMedGoogle Scholar
  62. Lambe, P.; Mutambel, H. S. N.; Fouche, J. G.; Deltour, R.; Foidart, J. M. DNA methylation as a key process in regulation of organogenic totipotency and plant neoplastic progression. In Vitro Cell Dev. Biol. Plant 33: 155–162; 1997 doi: 10.1007/s11627-997-0015-9.Google Scholar
  63. Liu, K. L.; Fu, H.; Bei, Q.; Luan, S. Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol. 124: 1315–1325; 2000 doi: 10.1104/pp.124.3.1315.PubMedGoogle Scholar
  64. Loenen, W. A. M. S-Adenosylmethionine: jack of all trades and master of everything? Biochem. Soc. Trans. 34: 330–333; 2006 doi: 10.1042/BST20060330.PubMedGoogle Scholar
  65. Loukanina, N.; Thorpe, T. A. Arginine and ornithine decarboxylases in embryonic and non-embryonic carrot cell suspensions. In Vitro Cell. Dev. Biol. Plant 44: 59–64; 2008 doi: 10.1007/s11627-007-9080-3.Google Scholar
  66. Martin-Tanguay, J. Conjugated polyamines and reproductive development: biochemical, molecular and physiological approaches. Physiol. Plant. 100: 675–688; 1997 doi: 10.1111/j.1399-3054.1997.tb03074.x.Google Scholar
  67. McDaniel, C. N.; Sangrey, K. A.; Jegla, D. E. Cryptic floral determination: stem explants from vegetative tobacco plants have the capacity to regenerate floral shoots. Dev. Biol. 134: 473–478; 1989 doi: 10.1016/0012-1606(89)90120-6.PubMedGoogle Scholar
  68. Mehta, R. A.; Cassol, T.; Li, N.; Ali, N.; Handa, A. K.; Mattoo, A. K. Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nature Biotechnol. 20: 613–618; 2002 doi: 10.1038/nbt0602-613.Google Scholar
  69. Minocha, R.; Minocha, S. C.; Long, S. Polyamines and their biosynthetic enzymes during somatic embryo development in red spruce (Picea rubens Sarg.). In Vitro Cell Dev. Biol. Plant 40: 572–580; 2004 doi: 10.1079/IVP2004569.Google Scholar
  70. Minocha, R.; Smith, D. R.; Reeves, C.; Steele, K. D.; Minocha, S. C. Polyamine levels during the development of zygotic and somatic embryos of Pinus radiate. Physiol. Plant 105: 155–164; 1999 doi: 10.1034/j.1399-3054.1999.105123.x.Google Scholar
  71. Møller, S. G.; McPherson, M. J. Developmental expression and biochemical analysis of the Arabidopsis atao1 gene encoding an H2O2-generating diamine oxidase. Plant J 13: 781–791; 1998.PubMedGoogle Scholar
  72. Munksgaard, D.; Mattsson, O.; Okkels, F. T. Somatic embryo development in carrot is associated with an increase in levels of S-adenosylmethionine, S-adenosylhomocysteine and DNA methylation. Physiol. Plant. 93: 5–10; 1995 doi: 10.1034/j.1399-3054.1995.930102.x.Google Scholar
  73. Neill, S. Interactions between abscisic acid, hydrogen peroxide and nitric oxide mediate survival response during water stress. New Phytol. 175: 4–6; 2007 doi: 10.1111/j.1469-8137.2007.02112.x.PubMedGoogle Scholar
  74. Oliver, D.; Baukrowitz, T.; Fakler, B. Polyamines as gating molecules of inward-rectifier K+ channels. Eur. J. Biochem. 267: 5824–5829; 2000 doi: 10.1046/j.1432-1327.2000.01669.x.PubMedGoogle Scholar
  75. Oredsson, S. M. Polyamine dependence of normal cell-cycle progression. Biochem. Soc. Trans. 31: 366–370; 2003 doi: 10.1042/BST0310366.PubMedGoogle Scholar
  76. Orzaéz, D.; Granell, A. The plant homologue of the defender against apoptotic death gene is down-regulated during senescence of flower petals. FEBS Lett. 404: 275–278; 1997 doi: 10.1016/S0014-5793(97)00133-6.PubMedGoogle Scholar
  77. Palmieri, L.; Arrigoni, R.; Blanco, E.; Carrari, F.; Zanor, M. I.; Studart-Guimaraes, C.; Fernie, A. R.; Palmieri, F. Molecular identification of an Arabidopsis S-adenosylmethionine transporter. Analysis of organ distribution, bacterial expression, reconstitution into liposomes, and functional characterization. Plant Physiol. 142: 855–865; 2006 doi: 10.1104/pp.106.086975.PubMedGoogle Scholar
  78. Panicot, M.; Minguet, E. G.; Ferrando, A.; Alcázar, R.; Blázquez, M. A.; Carbonell, J.; Altabella, T.; Koncz, C.; Tiburcio, A. F. A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14: 2539–2551; 2002 doi: 10.1105/tpc.004077.PubMedGoogle Scholar
  79. Papadakis, A. K.; Roubelakis-Angelakis, K. A. Polyamines inhibit NADPH oxidase-mediated superoxide generation and putrescine prevents programmed cell death induced by polyamine oxidase-generated hydrogen peroxide. Planta 220: 826–837; 2005 doi: 10.1007/s00425-004-1400-9.PubMedGoogle Scholar
  80. Paschalidis, K. A.; Roubelakis-Angelakis, K. A. 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; 2005 doi: 10.1104/pp.104.055483.PubMedGoogle Scholar
  81. Phillips, R.; Press, M. C.; Bingham, L.; Grimmer, C. Polyamines in cultured artichoke explants—effects are primarily on xylogenesis rather that cell-division. J. Exp. Bot. 39: 473–480; 1988 doi: 10.1093/jxb/39.4.473.Google Scholar
  82. Piotrowski, M.; Kneifer, H. Plant C–N hydrolases and the identification of a plant N-carbamoylputrescine amidohydrolase involved in polyamine biosynthesis. J Biol. Chem. 278: 1708–1712; 2003 doi: 10.1074/jbc.M205699200.PubMedGoogle Scholar
  83. Puga-Hermida, M. I.; Gallardo, M.; Matilla, A. J. The zygotic embryogenesis and ripening of Brassica rapa seeds provokes important alterations in the levels of free and conjugated abscisic acid and polyamines. Physiol. Plant 117: 279–288; 2003 doi: 10.1034/j.1399-3054.2003.00033.x.Google Scholar
  84. Rocha, P. S. C. F.; Sheikh, M.; Melchiorre, R.; Fagard, M.; Boutet, S.; Loach, R.; Moffatt, B.; Wagner, C.; Vaucheret, H.; Furner, I. The Arabidopsis homology-dependent gene silencing gene codes for an S-adenosyl-l-homocysteine hydrolase required for DNA methylation-dependent gene silencing. Plant Cell 17: 404–417; 2005 doi: 10.1105/tpc.104.028332.PubMedGoogle Scholar
  85. Santa-Catarina, C.; Silveira, V.; Balbuena, T. S.; Viana, A. M.; Estelita, M. E. M.; Handro, W.; Floh, E. I. S. IAA, ABA, polyamines and free amino acids associated with zygotic embryo development of Ocotea catharinensis. Plant Growth Regul. 49: 237–247; 2006 doi: 10.1007/s10725-006-9129-z.Google Scholar
  86. Scaramagli, S.; Biondi, S.; Capitani, F.; Gerola, P.; Altamura, M. M.; Torrigiani, P. Polyamine conjugate levels and ethylene biosynthesis: inverse relationship with the vegetative bud formation in tobacco thin layers. Physiol. Plant 105: 367–376; 1999 doi: 10.1034/j.1399-3054.1999.105223.x.Google Scholar
  87. Serafini-Fracassini, D.; Del Duca, S. Transglutaminases: widespread cross-linking enzymes in plants. Ann. Bot. 102: 145–452; 2008, May 20.PubMedGoogle Scholar
  88. Shoeb, F.; Yadav, J. S.; Bajaj, S.; Rajam, M. V. Polyamines as biomarkers for plant regeneration capacity: improvement of regeneration by modulation of polyamine metabolism in different genotypes of indica rice. Plant Sci. 160: 1229–1235; 2001 doi: 10.1016/S0168-9452(01)00375-2.PubMedGoogle Scholar
  89. Silveira, V.; Balbuena, T. S.; Santa-Catarina, C.; Floh, E. I. S.; Guerra, M. P.; Handro, W. Biochemical changes during seed development in Pinus taeda L. Plant Growth Regul. 44: 147–156; 2004.CrossRefGoogle Scholar
  90. Stasolla, C.; van Zyl, L.; Egertsdotter, U.; Craig, D.; Liu, W.; Sederoff, R. R. The effects of polyethylene glycol on gene expression of developing white spruce somatic embryos. Plant Physiol. 131: 49–60; 2003 doi: 10.1104/pp.015214.PubMedGoogle Scholar
  91. Stasolla, C.; Yeung, E. C. Recent advances in conifer somatic embryogenesis: improving somatic embryo quality. Plant Cell Tissue Org. Cult. 74: 15–35; 2003.Google Scholar
  92. Tassoni, A.; Fornalé, S.; Bagni, N. Putative ornithine decarboxylase activity in Arabidopsis thaliana: inhibition and intracellular localization. Plant Physiol. Biochem. 41: 871–875; 2003 doi: 10.1016/S0981-9428(03)00141-4.Google Scholar
  93. Tavladoraki, P.; Rossi, M. N.; Saccuti, G.; Perez-Amador, M. A.; Polticelli, F.; Angelini, R.; Federico, R. Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol. 141: 1519–1532; 2006 doi: 10.1104/pp.106.080911.PubMedGoogle Scholar
  94. Thorpe, T. A.; Stasolla, C. Somatic embryogenesis. In: S. S. Bhojwani, W. Y. Soh (Eds.), Current trends in the embryology of angiosperms. Kluwer, Dordrecht; 2001: pp. 279–336.Google Scholar
  95. Tiburcio, A. F.; Kaur-Sawhney, R.; Galston, A. W. Effect of polyamine biosynthetic inhibitors on alkaloids and organogenesis in tobacco callus culture. Plant Cell Tissue Org. Cult. 9: 111–120; 1987.Google Scholar
  96. Torrigiani, P.; Scaramagli, S.; Castiglione, S.; Altamura, M.; Biondi, S. 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; 2003 doi: 10.1016/S0168-9452(03)00115-8.Google Scholar
  97. Tun, N. N.; Santa-Catarina, C.; Begum, T.; Silveira, V.; Handro, W.; Floh, E. I. S.; Scherer, G. F. E. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol. 47: 346–354; 2006 doi: 10.1093/pcp/pci252.PubMedGoogle Scholar
  98. Uemura, T.; Kashiwagi, K.; Igarashi, K. Polyamine uptake by DUR3 and SAM3 in Saccharomyces cerevisiae. J. Biol. Chem. 282: 7733–7741; 2007 doi: 10.1074/jbc.M611105200.PubMedGoogle Scholar
  99. Urano, K.; Hobo, T.; Shinozaki, K. Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett. 579: 1557–1564; 2005 doi: 10.1016/j.febslet.2005.01.048.PubMedGoogle Scholar
  100. Urano, K.; Yoshiba, Y.; Nanjo, T.; Igarashi, Y.; Seki, M.; Sekiguchi, F.; Yamagushi-Shinozaki, K.; Shinozaki, K. Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ. 26: 1917–1926; 2003 doi: 10.1046/j.1365-3040.2003.01108.x.Google Scholar
  101. Vandenberg, C. A. Integrins step up the pace of cell migration through polyamines and potassium channels. Proc. Natl. Acad. Sci. U. S. A. 105: 7109–7110; 2008 doi: 10.1073/pnas.0803231105.PubMedGoogle Scholar
  102. Venkatachalam, L.; Bhagyalakshmi, N. Spermine-induced morphogenesis and effect of partial immersion system on the shoot cultures of banana. Appl. Biochem. Biotechnol. 2008 doi: 10.1007/s12010-008-8226-z.
  103. Vuosku, J.; Jokela, A.; Läärä, E.; Sääskilahti, M.; Muili, R.; Sutela, S.; Altabella, T.; Sarjala, T.; Häggman, H. Consistency of polyamine profiles and expression of arginine decarboxylase in mitosis during zygotic embryogenesis of Scots pine. Plant Physiol. 142: 1027–1038; 2006 doi: 10.1104/pp.106.083030.PubMedGoogle Scholar
  104. Wachter, A.; Tunc-Ozdemir, M.; Grove, B. C.; Green, P. J.; Shintani, D. K.; Breaker, R. R. Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19: 3437–3450; 2007 doi: 10.1105/tpc.107.053645.PubMedGoogle Scholar
  105. Walden, R.; Cordeiro, A.; Tiburcio, A. F. Polyamines: small molecules triggering pathways in plant growth and development. Plant Physiol. 113: 1009–1013; 1997 doi: 10.1104/pp.113.4.1009.PubMedGoogle Scholar
  106. Wallace, H. M.; Fraser, A. V.; Hughes, A. A perspective of polyamine metabolism. Biochem. J. 376: 1–14; 2003 doi: 10.1042/BJ20031327.PubMedGoogle Scholar
  107. Wang, J. X.; Breaker, R. R. Riboswitches that sense S-adenosylmethionine and S-adenosylhomocysteine. Biochem. Cell. Biol. 86: 157–168; 2008 doi: 10.1139/O08-008.PubMedGoogle Scholar
  108. Wang, Y.; Xiao, L.; Thiagalingam, A.; Nelkin, B. D.; Casero, R. A. The identification of a Cis-element and a trans-acting factor involved in the response to polyamines and polyamine analogues in the regulation of the human spermidine/spermine N 1-acetyltransferase gene transcription. J. Biol. Chem. 51: 34623–34630; 1998 doi: 10.1074/jbc.273.51.34623.Google Scholar
  109. Watson, M. B.; Emory, K. K.; Platak, R. M.; Malmberg, R. L. Arginine decarboxylase (polyamine synthesis) mutants of Arabidopsis thaliana exhibit altered root growth. Plant J. 13: 231–239; 1998 doi: 10.1046/j.1365-313X.1998.00027.x.PubMedGoogle Scholar
  110. Xiao, W.; Custard, K. D.; Brown, R. C.; Lemmon, B. E.; Harada, J. J.; Goldberg, R. B.; Fischer, R. L. DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18: 805–814; 2006 doi: 10.1105/tpc.105.038836.PubMedGoogle Scholar
  111. Yadav, J. S.; Rajam, M. V. Temporal regulation of somatic embryogenesis by adjusting cellular polyamine content in eggplant. Plant Physiol. 116: 617–625; 1998 doi: 10.1104/pp.116.2.617.Google Scholar
  112. Yamaguchi, K.; Takahashi, Y.; Berberich, T.; Imai, A.; Miyazaki, A.; Takahashi, T.; Michael, A.; Kusano, T. The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett. 580: 6783–6788; 2006 doi: 10.1016/j.febslet.2006.10.078.PubMedGoogle Scholar
  113. Yamaguchi, K.; Takahashi, Y.; Berberich, T.; Imai, A.; Takahashi, T.; Michael, A. J.; Kusano, T. A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem. Biophys. Res. Commun. 352: 486–490; 2007 doi: 10.1016/j.bbrc.2006.11.041.PubMedGoogle Scholar
  114. Yamasaki, H.; Cohen, M. F. NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants. Trend Plant Sci. 11: 522–524; 2006.Google Scholar
  115. Zhao, F.; Song, C. -P.; He, J.; Zhu, H. Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol. 145: 1061–1072; 2007 doi: 10.1104/pp.107.105882.PubMedGoogle Scholar

Copyright information

© The Society for In Vitro Biology 2008

Authors and Affiliations

  1. 1.University of ManitobaWinnipegCanada

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