Plant Growth Regulation

, Volume 34, Issue 1, pp 135–148

Metabolism and function of polyamines in plants: recent development (new approaches)

  • J. Martin-Tanguy
Article

Abstract

A review is presented of the recent developments in the metabolism andfunction of polyamines in plants. Polyamines appear to be involved in a widerange of plant processes so their exact role is not completely understood. Inthis review, the metabolic pathways involved in polyamine biosynthesis anddegradation are explained, along with the transport and conjugation of thesecompounds. The methodologies involved in the analysis of polyamine functionusing metabolic inhibitors and genetic and molecular approaches are described.The occurrence and distribution of polyamine-derived alkaloids are also dealtwith. The direction of future research in the study of plant polyamines isindicated.

Alkaloids Polyamine biosynthesis Polyamines Putrescine Spermidine Spermine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altabella T., Taylor M.A. and Tiburcio A.F. 1997. Recent advances in polyamine research. Trends Plant Sci. 2: 124–130.Google Scholar
  2. Altamura M.M. 1993. Cytological events induced by inhibition of polyamine biosynthesis in thin cell layers of tobacco. Protoplasma. 175: 9–16.Google Scholar
  3. Angelini R., Federico R. and D'Ovidi R. 1996. Spatial distribution and temporal accumulation of mRNA encoding diamine oxidase during lentil (Lens culinaris Medicus) seeling development. Plant Sci. 119: 103–113.Google Scholar
  4. Antognoni F., Pistocchi R., Casali P. and Bagni B. 1995. Does calcium regulate polyamine uptake in carrot protoplasts?. Plant Physiol. Biochem. 33: 701–702.Google Scholar
  5. Apelbaum A., Camellakis Z.N., Applewhite P.B., Kaur-Sawhney R. and Galston A.W. 1988. Binding of spermidine to a unique protein in thin-layer tobacco tissue culture. Plant Physiol. 88: 996–998.Google Scholar
  6. Aribaud M. and Martin-Tangu J. 1994. Polyamine metabolism in normal and sterile chrysanthemum plants. Phytochemistry. 37: 927–932.Google Scholar
  7. Aribaud M., Carré M. and Martin-Tanguy J. 1994. Polyamine metabolism and in vitro cell multiplication and differentiation of chrysanthemum leaf explants. Plant Growth Regul. 15: 143–155.Google Scholar
  8. Bagni N. and Pistocchi R. 1991. Uptake and transport of polyamines and inhibitors of polyamine metabolism in plants. In: Slocum R.D. and Flores H.E. (eds), Biochemistry and Physiology of Polyamines in plants. CRC Press, Boca Raton, pp. 105–118.Google Scholar
  9. Bajaj S. and Rajam M.V. 1995. Efficient plant regeneration from long-term callus cultures of rice by spermidine. Plant Cell. Rep. 14: 717–720.Google Scholar
  10. Baldwin I.T. 1988. Damage-induced alkaloids in tobacco: potbound plants are not inducible. J. Chem. Ecol. 14: 1113–1115.Google Scholar
  11. Bardocz S. 1993. The role of dietary polyamines. Eur. J. Clin. Nutr. 47: 683–690.Google Scholar
  12. Basu H.S., Schwietert H.C.A., Feuerstein B.G. and Marton L.J. 1990. Effect of variation in the structure of spermine on the association with DNA and the induction of DNA conformational changes. Biochem. J. 269: 329–334.Google Scholar
  13. Beigbeder A.R. 1995. Influence of polyamine inhibitors on light independent and light dependent chlorophyll biosynthesis and on the photosyntetic rate. J. Photochem. Photobiol. 28: 235–242.Google Scholar
  14. Besford R.T., Richardson C.M., Campos J.L. and Tiburcio A.F. 1993. Effect of polyamines on stabilization of molecular complexes of thylakoid membranes of osmotically stressed oat leaves. Planta. 189: 201–206.Google Scholar
  15. Birecka H., Birecki M. and Frohlich M.W. 1987. Evidence for arginine as the endogenous precursor of necines in Heliotropiwn. 84: 42–46.Google Scholar
  16. Bonneau L., Carré M. and Martin-Tanguy J. 1994. Polyamines and related enzymes in rice differing in germination potential. 15: 75–82.Google Scholar
  17. Borrell A., Culianez-Macia F.A., Altabella T., Besford R.T., Flores D. and Tiburcio A.F. 1995. Arginine decarboxylase is localized in chloroplasts. Plant Physiol. 109: 771–776.Google Scholar
  18. Borrell A., Besford R.T., Altabella T., Masgrau C. and Tiburcio A.F. 1996. Regulation of arginine decarboxylase by spermine in osmotically-stressed oat leaves. Physiol. Plant. 98: 105–110.Google Scholar
  19. Burtin D., Martin-Tanguy J., Paynot M., Carré M. and Rossin M. 1990. Polyamines, hydroxycinnamoylputrescines, and root formation in leaf explants of tobacco cultivated in vitro. Effects of the suicide inhibitors of putrescine synthesis. Plant Physiol. 93: 1398–1404.Google Scholar
  20. Burtin D., Martin-Tanguy J. and Tepfer D. 1991. α-DL-difluoromethylornithine, a specific irreversible inhibitor of putrescine synthesis, induces a phenotype in tobacco similar to that ascribed to the root-inducing, left-hand transferred DNA of Agrobacterium rhizo genes. Plant Physiol. 95: 461–468.Google Scholar
  21. Campos J.L., Figueras X., Boronat A., Pinol M.T. and Tiburcio A.F. 1991. Changes in polyamine content of Arabidopsis thaliana after UV-C irradiation. In: Galston G.W. and Tiburcio A.F. (eds), Lecture Course on Polyamines as Regulators of Plant Development. Fundation Juan March, pp. 78–80.Google Scholar
  22. Del Duca S., Tidu V., Bassi R., Esposito C. and Serafini-Fracassini D. 1994. Identification of Chi a/b proteins as substrates of transglutaminase activity in isolated chloroplasts of Helianthus suberosus. L. Planta. 193: 283–289.Google Scholar
  23. Del Duca S., Beninati S. and Serafini-Fracassini D. 1995. Polyamines in chloroplast:Identification of their glutamyl and acetyl derivatives. Biochem J. 305: 233–237.Google Scholar
  24. De Scenzo R.A. and Minocha S.C. 1993. Modulation of cellular polyamines in tobacco by transfer and expression of mouse ornithine decarboxylase. Plant Mol. Biol. 22: 113–127.Google Scholar
  25. D'Oraci D. and Bagni N. 1987. In vitro interactions between polyamines and pectic substances. Biochem. Biophys. Res. Commun. 148: 1159–1163.Google Scholar
  26. Ecker J.R. 1994. The ethylene signal transduction pathways in plants. Science. 268: 327–338.Google Scholar
  27. Egea-Cortines M. and Mizrahi Y. 1991. Polyamines in cell division, fruit set and development, and seed germination. In: Slocum R.D. and Flores H.E. (eds), Biochemistry and Physiology of Polyamines in plants. CRC Press, Boca Raton, pp. 143–158.Google Scholar
  28. El Ghachtoul N., Martin-Tangu J., Paynot M. and Gianinazz S. 1996. First report of the inhibition of arbuscular mycorrhizal infection of Pisum sativum by specific and irreversible inhibition of polyamine biosynthesis or by gibberellic treatment. FEBS Lett. 385: 189–192.Google Scholar
  29. Evans P.T. and Malmberg R.L. 1989. Do polyamines have roles in plant development?. Ann. Rev. Plant Physiol. Plant Mol. Biol. 40: 235–269.Google Scholar
  30. Fecker L.F., Hiilebrandt S., Rügenhagen C., Herminghau S., Landsmann J. and Berlin J. 1992. Metabolic effects of a bacterial lysine decarboxylase gene expressed in a hairy root culture of Nicotiana glauca. Biotechnol. Lett. 14: 1035–1040.Google Scholar
  31. Federico R. and Angelini R. 1991. Polyamine catabolism. In: Slocum R.D. and Flores H.E. (eds), Biochemistry and Physiology of Polyamines in plants. CRC Press, Boca Raton, pp. 41–56.Google Scholar
  32. Feth F., Wagner R. and Wagner K.G. 1986. Regulation in tobacco callus of enzyme activities of the nicotine pathway. Planta. 108: 402–410.Google Scholar
  33. Flores H.E. and Filner P. 1985. Polyamine catabolism in higher plants: characterization of pyrroline dehydrogenase. Plant Growth Regul. 3: 277–291.Google Scholar
  34. Flores H.E., Protacio C.M. and Signs M.W. 1989. Primary and secondary metabolism of polyamines in plants. Recent. Adv. Phytochem. 23: 329–393.Google Scholar
  35. Flores H.E. and Martin-Tanguy J. 1991. Polyamines and Plant Secondary Metabolites. In: Slocum R.D. and Flores H.E. (eds), Biochemistry and Physiology of Polyamines in Plants. CRC Press, Boca Raton, pp. 57–72.Google Scholar
  36. Folk J.E. 1980. Transglutaminases. Annu. Rev. Biochem. 49: 517–531.Google Scholar
  37. Fritze K., Czaja I. and Walden R. 1995. T-DNA tagging of genes influencing polyamine metabolism: isolation of mutant plant lines and rescue of DNA promoting growth in the presence of a polyamine biosynthetic inhibitor. Plant. 7: 261–271.Google Scholar
  38. Galston A.W. and Kaur-Sawhney R.K. 1990. Polyamines in plant physiology. Plant Physiol. 94: 406–410.Google Scholar
  39. Galston A.W. and Flores H.E. 1991. Polyamines in plant morphogenesis. In: Slocum R.D. and Flores H.E. (eds), Biochemistry and Physiology of Polyamines in plants. CRC Press, Boca Raton, pp. 175–183.Google Scholar
  40. Galston A.W. and Kaur-Sawhney R. 1995. Polyamines as endogenous growth regulators. In: Davies P.J. (ed.), Plant Hormones. Physiology, Biochemistry and Molecular Biologiy. 2nd edn. Kluwer Academic Publishers, Dordrecht, pp. 158–178.Google Scholar
  41. Geny L., Broquedis M., Martin-Tanguy J. and Bouard J. 1997. Free, conjugated and wall-bound polyaniines in various parts of fruiting cuttings of Vitis vinifera at different stages of development. Am. J. Enol. Vitic. 48: 80–84.Google Scholar
  42. Gilad G.M., Gilad V.H. and Rabey J.M. 1996. Arginine and ornithine decarboxylation in rodent brain-coincidental changes during development and after ischemia. Neurosci. Lett. 216: 33–36.Google Scholar
  43. Guggisberg A. and Hesse M. 1983. Putrescine, spermidine, spermine and related polyamine alkaloids. In: Brossi A. (ed.), The Alkaloids, Chemistry and Pharmacology. vol. XXII Academic Press, New York, p. 85.Google Scholar
  44. Hachiya A., Yamamoto Y. and Matsumoto H. 1996. Inhibitory effect of phenylpropanoids on aluminium toxicity in cultured tobacco cells. Plant Cell Physiol. 37: 53.Google Scholar
  45. Hartman T., Sander H., Adolph M. and Toppel G. 1988. Metabolic links between the biosynthesis of pyrrolizidine alkaloids and polyamines in root cultures of Senecio vulgaris. Planta. 175: 82–90.Google Scholar
  46. Havelange A., Lejeune P., Bernier A., Kaur-Sawhney R. and Galston A.W. 1996. Putrescine export from leaves in relation to floral transition in Sinapis alba. Physiol. Plant. 96: 59–65.Google Scholar
  47. Hayashi S. and Murakami Y. 1995. Rapid and regulated degradation of ornithine decarboxylase. Biochem. J. 306: 221–230.Google Scholar
  48. Heby O. and Persson L. 1990. Molecular genetics of polyamine synthesis in eukaryotic cells. Trends. Biochem. Sci. 15: 153–158.Google Scholar
  49. Hibi N., Fujita T., Hatamo M., Hashimoto T. and Gamada Y. 1992. Putrescine N-methyl transferase in cultured roots of Hyoscyanius albus. n-Butylamine as a potent inhibitor of the transferase both in vitro and in vivo. Plant Physiol. 100: 826–835.Google Scholar
  50. Hibi N., Higashiguchi S., Hashimoto T. and Yamada Y. 1994. Gene expression in tobacco low-nicotine mutants. Plant Cell. 6: 723–735.Google Scholar
  51. Jansen N.A.K., Gaba V. and Greenberg M. 1998. Higher plants and UV-B radiation balancing damage, repair and acclimation. Trends. Plant Sci. 3: 119–159.Google Scholar
  52. Kallio A., McCann P. and Bey P. 1981. DL_α(Difluoromethyl)arginine: a potent enzyme activated irreversible inhibitor of bacterial arginine decarboxylase. Biochemistry. 20: 3163–3166.Google Scholar
  53. Kumar A., Taylor M.A., Mad Arif S.A. and Davies H.V. 1996. Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: Antisense plants display abnormal phenotypes. Plant J. 9: 147–158.Google Scholar
  54. Kupchan S.M., Davies A.P., Barboutis S.J., Schnoes H.K. and Burlingame A.L. 1969. Tumor inhibitors. XLIII. Solapalmitine and solapalmitenine, two novel alkaloid tumor inhibitors from Solanum tripartitum. J. Org. Chem. 34: 3888–3898.Google Scholar
  55. Langebartels C., Kerner K.J., Leonardi S., Schraudner M., Trost M., Heller W. et al. 1991. Biochemical plant response to ozone. I. Differential induction of polyamine and ethylene biosynthesis in tobacco. Plant Physiol. 91: 882–887.Google Scholar
  56. Li G., Regunathan S., Barrow C.J., Eshraghi J., Cooper R. and Reiss D.J. 1994. Agmatine – An endogenous clonidine-displacing substance in the brain. Science. 263: 966–969.Google Scholar
  57. Mad Arif S.A., Taylor M.A., George L.A., Buder A.R., Burch L.R., Davies H.U. et al. 1994. Characterisation of the S-adenosylmethionine decarboxylase (SAM DC) gene of potato. Plant Mol. Biol. 26: 327–338.Google Scholar
  58. Malmberg R.L. and Cellino M.L. 1994. Arginine decarboxylase of oat is activated by enzymatic cleavage into two polypeptides. J. Biol. Chem. 28: 2703–2706.Google Scholar
  59. Martin-Tanguy J. 1985. The occurrence and possible functions of hydroxycinnamoyl acid amides in plant. Plant Growth Regul. 3: 381–399.Google Scholar
  60. Martin-Tanguy J. 1987. Hydroxycinnamic acid amides, hypersensitivity, flowering and sexual organogenesis in plants. In: Von Wettstein D. and Chua D.N. (eds), Plant Molecular Biology. Plenum Publishing Corporation, New York, pp. 253–263.Google Scholar
  61. Martin-Tanguy J., Tepfer D., Paynot M., Burtin D., Heisler I. and Martin C. 1990. Inverse relationship between polyamine levels and the degree of phenotypic alteration induced by the root-inducing left-hand transferre DNA from Agrobacterium rhizogenes. Plant Physiol. 92: 912–918.Google Scholar
  62. Martin-Tanguy J., Corbineau F., Burtin D., Ben Hayyim G. and Tepfer D 1993. Genetic transformation with a derivative of rol C from Agrobacterium rhizogenes or treatment with α-aminoisobutyric acid reduces ethylene production and the accumulation of water-insoluble polyaminehydroxycinnamic acid conjugates in tobacco flowers. Plant Sci. 93: 63–76.Google Scholar
  63. Martin-Tanguy J., Sun L.Y., Burtin D., Vernoy R., Rossin N. and Tepfer D. 1996. Attenuation of the phenotypes caused by rootinducing, left-hand transferred DNA and its rol A gene. Correlations with changes in polyamine metabolism and DNA methylation. Plant Physiol. 111: 259–267.Google Scholar
  64. Martin-Tanguy J. 1997. Conjugated polyamines and reproductive development: biochemical, molecular and physiological approaches. Physiol. Plant. 100: 675–688.Google Scholar
  65. Masgrau C., Mtabella T., Farras R., Flores P., Thompson A.J., Besford R.T. et al. 1997. Inducible overexpression of oat arginine decarboxylase in transgenic tobacco plants. Plant J. 11: 465–473.Google Scholar
  66. Mehta H.S., Saftner R.A., Mehta R.A. and Davies P.J. 1994. Identification of posttranscriptionally modified 18-kilodalton protein from rice as eukaryotic translocation initiation factor 5A. Plant Physiol. 106: 1413–1419.Google Scholar
  67. Metcalf B.W., Bey P., Danzin C., Jung M.J., Casara P. and Vevert J.P. 1978. Catalytic irreversible inhibition of mammalian ornithine decarboxylase by substrat and product analogues. J. Am. Chem. Soc. 100: 2251–2253.Google Scholar
  68. Meurer-Grimes B., Berlin J. and Strack D. 1989. Hydroxycinnamoyl-CoA: putrescine hydroxycinnamoyl transferase in tobacco cell cultures with high and low levels of caffeoylputrescine. Plant Physiol. 89: 488–492.Google Scholar
  69. Michael A.J., Furze J.M., Rhodes J.C. and Burtin D. 1996. Molecular cloning and functional identification of a plan ornithine decarboxylase cDNA. Biochem. J. 314: 241–248.Google Scholar
  70. Minocha S.C. and Minocha R.C. 1996. Role of polyamines in somatic embryogenesis. In: Bajaj Y.P.S. (ed.), Biotechnology in Agriculture and Forestry: Somatic Embryogenesis and Synthetic Seeds. vol. 30 Springer-Verlag, New York, pp. 53–70.Google Scholar
  71. Mueller S. 1996. QTL analysis of polyamines in potato leaves. In: Struick P.C. (ed.), Abstracts of 13th Triennial Conference of the European Association for Potato Research. Veldhoven, pp. 73–74.Google Scholar
  72. Negrel J. and Martin C. 1984. The biosynthesis of feruloyl tyramine in Nicotiana tabacum. Phytochemistry. 23: 2797–2801.Google Scholar
  73. Negrel J. and Lherminier J. 1987. Peroxidase-mediated integration of tyramine into xylem cell walls of tobacco leaves. Planta. 72: 494–501.Google Scholar
  74. Negrel J. 1989. The biosynthesis of cinnamoylputrescines in callus tissue cultures of Nicotiana tabacum. Phytochemistry. 28: 477–481.Google Scholar
  75. Pelosi L.A., Rother A. and Edwards J.M. 1986. Lysine decarboxylase activity and alkaloid production in Heimia saliczfolia cultures. Phytochemistry. 25: 2319–2915.Google Scholar
  76. Perez-Amador M.A., Carbonell J. and Granell A. 1995. Expression of arginine decarboxylase is induced during early fruit development and in young tissues of Pisum sativum (L.)-. Plant Mol. Biol. 28: 997–1009.Google Scholar
  77. Philipps G.C. and Kuehn G.D. 1991. Uncommon polyamines in plants and other organisms. In: Slocum R.D. and Flores H.E. (eds), Biochemistry and Physiology of Polyamines in Plants. CRC Press, Boca Raton, pp. 121–133.Google Scholar
  78. Pistoochi R., Antognoni F., Bagni N. and Zannoni D. 1990. Spermidine uptake by mitochondria of Hehanthus tuberosus. Plant Physiol. 92: 690–695.Google Scholar
  79. Pistocchi R. and Bagni N. 1990. Effect of calcium on spermine uptake in carrot cell cultures and protoplasts. J. Plant Physiol. 136: 728–733.Google Scholar
  80. Pohjanpelto P. and Höltta E. 1996. Phosphorylation of Okazaki-like DNA fragments in mammalian cells and role of polyamines in the processing of this DNA. EMBO J. 15: 1193–1200.Google Scholar
  81. Robins R.J., Parr A.J. and Walton N.J. 1991. Studies on the biosynthesis of tropane alkaloids in Datura stramornum L. transformed root cultures. 2. On the relative contributions of L-arginine and L-ornithine to the formation of the tropane ring. Planta. 183: 196.Google Scholar
  82. Schoofs G., Teichman S., Hartmann T. and Wink M. 1983. Lysine decarboxylase activity and alkaloid production in Heimia salicifolia cultures. Phytochemistry. 25: 2315–2317.Google Scholar
  83. Schröder G. and Schröder J. 1995. CDNAs from Catharanthus roseus heterologous expression, identification of the proenzymeprocessing site, evidence for the presence of both subunits in the active enzyme, and a conserved region in the 5′-mRNA leader. Eur. J. Biochem. 228: 74–78.Google Scholar
  84. Schuber F., Hong K., Duözgünes N. and Papahadjopoulos D. 1983. Polyamines as regulators of membrane fusion: aggregation and fusion of liposomes. Biochemistry. 22: 6134–6140.Google Scholar
  85. Serafini-Fracassini D., Del Duca S. and Beninati S. 1995. Plant transglutaminases. Phytochemistry. 40: 355–365.Google Scholar
  86. Slocum R.D. 1991. Tissue and subcellular localisation of polyamines and enzymes of polyamine metabolism. In: Slocum R.D. and Flores H.E. (eds), Biochemistry and Physiology of Polyamines in plants. CRC Press, Boca Raton, pp. 93–105.Google Scholar
  87. Smith T.A., Negrel J. and Bird C.R. 1983. The cinnamic acid amides of the di-and polyamines. In: Bachrach U., Kayc A. and Chayen R. (eds), Advances in Polyamine Research. Raven Press, New York, pp. 347–370.Google Scholar
  88. Tabor C.W. and Tabor H. 1984. Polyamines. Annu. Rev. Biochem. 53: 749–790.Google Scholar
  89. Tarenghi E. and Martin-Tanguy J. 1995. Polyamines, floral induction and floral development of strawberry (Fragaria ananassa Duch.). Plant Growth Regul. 17: 157–165.Google Scholar
  90. Tassoni A., Antognoni F. and Bagni N. 1996. Polyamine binding to plasma membrane vesicles from zucchini hypocotyls. Plant Physiol. 110: 817–824.Google Scholar
  91. Tepfer D. 1984. Transformation of several species of higher plants by Agrobacterium rhizo genes: Sexual transmission of the transformed genotype and phenotype. Cell. 47: 959–967.Google Scholar
  92. Tiburcio A.F., Kaur-Sawhney R., Ingersoll R.B. and Oalston A.W. 1985. Correlation between polyamines and pyrrolidine alkaloids in developing tobacco callus. Plant Physiol. 78: 323–326.Google Scholar
  93. Tiburcio A.F., Kaur-Sawhney R. and Galston A.W. 1987. Effect of polyamine biosynthetic inhibitors on alkaloids and organogenesis in tobacco callus cultures. Plant Cell Tissue Organ Culture. 9: 111–120.Google Scholar
  94. Tiburcio A.F., Kaur-Sawhney R. and Galston A.W. 1990. Polyamine metabolism. In: Miflin B.J. and Lea P.J. (eds), The Biochemistry of Plants, Intermediary Nitrogen Fixation. Academic Press, New York, pp. 283–325.Google Scholar
  95. Tiburcio A.F., Altabella T., Borrell A. and Masgraw C. 1997. Polyamine metabolism and its regulation. Physiol. Plant. 100: 664–674.Google Scholar
  96. Tipping A.J. and McPherson M.J. 1995. Cloning and molecular analsyis of pea seedling copper amine oxidase. J. Biol. Chem. 270: 16939–16946.Google Scholar
  97. Twardowski T., Puhkowska J. and Wiewiorowski M. 1982. Inhibitory effect of selected quinolizidine alkaloids and their derivatives and analogues on the Phe-tRNA binding to ribosomes. Bull. Acad. Pol. Sc. 29: 129–140.Google Scholar
  98. Watson M. and Malmberg R.L. 1996. Regulation of Arabidopsis thaliana (L.) Heynh arginine decarboxylase by potassium defi-ciency stress. Plant Physiol. 111: 1077–1083.Google Scholar
  99. Wink M. and Hartman T. 1982. Localization of the enzyme of quinolizidine alkaloid biosynthesis in leaf chloroplasts of Lupinus polyphyllus. Plant Physiol. 70: 74–77.Google Scholar
  100. Wink M. 1985. Metabolism of quinolizidine alkaloids in plants and cell suspension cultures. Induction and degradation. In: Neumann K.H., Barz W. and Reinhand E. (eds), Primary and secondary metabolism of plant cell cultures. Springer-Verlag, Heidelberg, pp. 107–116.Google Scholar
  101. Ye X.S., Avdiushko S.A. and Kuc J. 1994. Effect of polyamines on in vitro phosphorylation of soluble and plasma membrane proteins in tobacco, cucumber and Arabidopsis thaliana. Plant Sci. 97: 109–118.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • J. Martin-Tanguy
    • 1
  1. 1.Groupe de Physiologie et Biochimie Végétales, UMR CNRS 6553, Campus Scientifique de BeaulieuUniversité de Rennes IRennes CedexFrance

Personalised recommendations