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Cytokinin metabolism: implications for regulation of plant growth and development

  • Břetislav Brzobohatý
  • Ian Moore
  • Klaus Palme

Abstract

This review describes recent advances in the study of cytokinin metabolism. It highlights how plant development is influenced by cytokinin synthesis, conjugation and conjugate hydrolysis, and what has been learned of the enzymes that regulate these processes. Although cytokinin metabolism and physiology are complex issues, some of the key enzymatic players are now being identified. This holds out the prospect of rapid progress in the near future. Just as much of what we know about the control of animal cell proliferation was learned by studying the cellular counterparts of viral oncogenes, so important information about the control of plant development by phytohormones has come from studying the genes of bacterial pathogens that subvert host phytohormone metabolism to their own advantage. We will focus on what has been learned from the use of such genes, and describe progress in identifying their functional counterparts in plants.

Key words

plant hormone cytokinin metabolism conjugation β-glucosidase transgenic plants 

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References

  1. 1.
    Banowetz GM: The effects of endogenous cytokinin content on benzyladenine-enhanced nitrate reductase induction. Physiol Plant 86: 341–348 (1992).CrossRefGoogle Scholar
  2. 2.
    Binns AN, Labriola J, Black RC: Initiation of auxin autonomy in Nicotiana glutinosa cells by the cytokininbiosynthesis gene from Agrobacterium tumefaciens. Planta 171: 539–548 (1987).CrossRefGoogle Scholar
  3. 3.
    Brinegar AC, Blumenthal S, Cooper G: Photoaffinity labeling of mung bean mitochondrial proteins using (3H)-2-azido-6-benzylaminopurine. In: Kaminek M, Mok DWS, Zazimalova E (eds), Physiology and Biochemistry of Cytokinins in Plants, pp. 301–307. SPB Academic Publishers, The Hague (1992).Google Scholar
  4. 4.
    Brzobohaty B, Moore I, Kristoffersen P, Bako L, Campos N, Schell J, Palme K: Release of active cytokinin by a β-glucosidase localized to the maize root meristem. Science 262: 1051–1054 (1993).PubMedCrossRefGoogle Scholar
  5. 5.
    Burch LR, Horgan R: The purification of cytokinin oxidase from Zea mays kernels. Phytochemistry 28: 1313–1319(1989).CrossRefGoogle Scholar
  6. 6.
    Burch LR, Horgan R: Cytokinin oxidase and the degradative metabolism of cytokinins. In: Kaminek M, Mok DWS, Zazimalova E (eds), Physiology and Biochemistry of Cytokinins in Plants, pp. 29–32. SPB Academic Publishers, The Hague (1992).Google Scholar
  7. 7.
    Campos N, Bako L, Feldwisch J, Schell J, Palme K: A protein from maize labeled with azido-IAA has novel β-glucosidase activity. Plant J 2: 675–684 (1992).CrossRefGoogle Scholar
  8. 8.
    Chatfield JM, Armstrong DJ: Regulation of cytokinin oxidase activity in callus tissues of Phaseolus vulgaris L. cv. Great Northern. Plant Physiol 80: 493–499 (1986).PubMedCrossRefGoogle Scholar
  9. 9.
    Chaudhury AM, Letham S, Craig S, Dennis ES: ampl — a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J 4: 907–916 (1993).CrossRefGoogle Scholar
  10. 10.
    Chen CM: Cytokinin biosynthesis in cell-free systems. In: Wareing PF (ed.), Plant Growth Substances, pp. 155–164. Academic Press, London (1982).Google Scholar
  11. 11.
    Chen CM, Melitz DK: Cytokinin biosynthesis in a cellfree system from cytokinin-autotrophic tobacco tissue cultures. FEBS Lett 107: 15–20 (1979).PubMedCrossRefGoogle Scholar
  12. 12.
    Claes B, Smalle J, Dekeyser R, Van Montagu M, Caplan A: Organ-dependent regulation of a plant promoter isolated from rice by ‘promoter-trapping’ in tobacco. Plant J 1: 15–26 (1991).PubMedCrossRefGoogle Scholar
  13. 13.
    Conn EE: β-Glycosidases in plants: substrate specificity. In: Essen A. (ed.), β -Glucosidases: Biochemistry and Molecular Biology. ACS Symposium Series 533, pp. 15–26. Maple Press, York, PA (1993).CrossRefGoogle Scholar
  14. 14.
    Cowly DE, Duke CC, Liepa AJ, Mac Leod JK, Letham DS: The structure and synthesis of cytokinin metabolites. I. The 7- and 9-β -glucofuranosides and pyranosides of zeatin and 6-benzylaminopurine. Aust J Chem 31: 1095–1111 (1978).CrossRefGoogle Scholar
  15. 15.
    Dehio C, de Bruijn FJ: The early nodulation gene SrEnod2 from Sesbania rostrata is inducible by cytokinin. Plant J 2: 117–128 (1992).PubMedGoogle Scholar
  16. 16.
    Dixon SC, Martin RC, Mok MC, Shaw G, Mok DWS: Zeatin glycosylation enzymes in Phaseolus: isolation of O-glucosyltransferase from P. lunatus and comparison to O-xylosyltransferase from P vulgaris. Plant Physiol 90: 1316–1321 (1989).PubMedCrossRefGoogle Scholar
  17. 17.
    Dominov JA, Stenzler L, Lee S, Schwarz JJ, Leisner S, Howell SH: Cytokinins and auxins control the expression of a gene in Nicotiana plumbaginifolia cells by feedback regulation. Plant Cell 4: 451–461 (1992).PubMedGoogle Scholar
  18. 18.
    Doree M, Guern J: Short-term metabolism of some exogenous cytokinins in Acerpseudoplatanus cells. Biochim Biophys Acta 304: 611–622 (1993).CrossRefGoogle Scholar
  19. 19.
    Engelbrecht L: Cytokinins in leaf-cuttings of Phaseolus vulgaris L. during their development. Biochem Physiol Pflanzen 163: 335–343 (1972).Google Scholar
  20. 20.
    Entsch B, Parker CW, Letham DS, Summons RE: Preparation and characterization, using high performance liquid chromatography, of an enzyme forming glucosides of cytokinins. Biochim Biophys Acta 570: 124–139 (1979).PubMedCrossRefGoogle Scholar
  21. 21.
    Entsch B, Letham DS, Parker CW, Summons RE, Gollnow BI: Metabolites of cytokinins. In: Skoog F (ed), Plant Growth Substances 1979, pp. 109–118. Springer-Verlag, Berlin (1980).CrossRefGoogle Scholar
  22. 22.
    Entsch B, Parker CW, Letham DS: An enzyme from lupine seeds forming alanine derivatives of cytokinins. Phytochemistry 22: 375–381 (1983).CrossRefGoogle Scholar
  23. 23.
    Erion JL, Fox JE: Purification and properties of a protein which binds cytokinin-active 6-substituted purines. Plant Physiol 67: 156–162 (1981).PubMedCrossRefGoogle Scholar
  24. 24.
    Esen A, Cokmus C: Maize genotypes classified as null at the Glu locus have β-glucosidase activity and immunoreactive protein. Biochem Genet 28: 319–336 (1990).PubMedGoogle Scholar
  25. 25.
    Esen A: Purification and partial characterization of maize (Zea mays L.) β -glucosidase. Plant Physiol 98: 174–182 (1992).PubMedCrossRefGoogle Scholar
  26. 26.
    Estruch JJ, Chriqui D, Grossmann K, Schell J, Spena A: The plant oncogene rolC is responsible for the release of cytokinins from glucoside conjugates. EMBO J 10: 2889–2895 (1991).PubMedGoogle Scholar
  27. 27.
    Estruch JJ, Prinsen E, Van Onckelen H, Schell J, Spena A: Viviparous leaves produced by somatic activation of an inactive cytokinin-synthesizing gene. Science 254: 1364–1367 (1991).PubMedCrossRefGoogle Scholar
  28. 28.
    Estruch J J, Granell A, Hansen G, Prinsen E, Redig P, Van Onckelen H, Schwarz-Sommer Z, Sommer H, Spena A: Floral development and expression of floral homeotic genes are influenced by cytokinins. Plant J 4: 379–384 (1993).PubMedCrossRefGoogle Scholar
  29. 29.
    Firn RD: Too many binding proteins, not enough receptors? In: Klämbt D (ed), Plant Hormone Receptors. pp 1–11. NATO ASI Series H: Cell Biology Vol. 10. Springer-Verlag, Berlin/Heidelberg (1987).Google Scholar
  30. 30.
    Fladung M: Transformation of diploid and tetraploid potato clones with the rolC gene of Agrobacterium rhizogenes and characterization of transgenic plants. Plant Breed 104: 295–304 (1990).CrossRefGoogle Scholar
  31. 31.
    Fox JE, Cornette J, Deleuze G, Dyson W, Giersak G, Niu P, Zapata J, McChesney J: The formation, isolation and biological activity of a cytokinin 7-glucoside. Plant Physiol 52: 627–632 (1973).PubMedCrossRefGoogle Scholar
  32. 32.
    Haberlandt G: Zur Physiologie der Zellteilungen. Sitzungsber K Preuss Akad Wiss: 318–345 (1913).Google Scholar
  33. 33.
    Hall RH: N6-(Δ2-isopentenyl) adenosine: chemical reactions, biosynthesis, metabolism and significance to the structure and function of tRNA. In: Davidson JN, Cohn WE (eds) Progress in Nucleic Acid Research and Molecular Biology, Vol 10, pp. 57–86. Academic Press, New York (1970).CrossRefGoogle Scholar
  34. 34.
    Hamaguchi N, Iwamura H, Fujita T: Fluorescent anticytokinins as a probe for binding. Isolation of cytokininbinding proteins from the soluble fraction and identification of a cytokinin-binding site on ribosomes of tobacco {Nicotiana tabacum cultivar Wisconsin No. 38) callus cells. Eur J Biochem 153: 565–572 (1985).PubMedCrossRefGoogle Scholar
  35. 35.
    Hansen CE, Meins F Jr, Milani A: Clonal and physiological variation in the cytokinin content of tobacco cell lines differing in cytokinin requirements and capacity for neoplastic growth. Differentiation 29: 1–6 (1985).CrossRefGoogle Scholar
  36. 36.
    Henson I.E., Wareing PF: Cytokinins mXanthium strumarium L.: Distribution in the plant and production in the root system. J Exp Bot 27: 1268–1278 (1976).CrossRefGoogle Scholar
  37. 37.
    Hepler PK, Wayne RO: Calcium and plant development. Ann Rev Plant Physiol 36: 397–439 (1985).CrossRefGoogle Scholar
  38. 38.
    Ivanova M, Todorov IT, Atanassova L, Dewitte W, Van Onckelen HA: Co-localization of cytokinins with proteins related to cell proliferation in developing somatic embryos of Dactylis glomerata L. J Exp Bot 45: 1009–1017 (1994).CrossRefGoogle Scholar
  39. 39.
    Jones RJ, Schreiber BM, McNeil K, Brenner ML, Foxon G: Cytokinin levels and oxidase activity during maize kernel development. In: Kaminek M, Mok DWS, Zazimalova E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp. 235–239. SPB Academic Publishers, The Hague (1992).Google Scholar
  40. 40.
    Kaminek M, Armstrong DJ: Genotypic variation in cytokinin oxidase from Phaseolus callus cultures. Plant Physiol 93: 1530–1538 (1990).PubMedCrossRefGoogle Scholar
  41. 41.
    Kares C, Prinsen E, Van Onckelen H, Otten L: IAA synthesis and root induction with iaa genes under heat shock promoter control. Plant Mol Biol 15: 225–236 (1990).PubMedCrossRefGoogle Scholar
  42. 42.
    Klee HJ, Horsch RB, Hinchee MA, Hein MB, Hoffmann NL: The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic petunia plants. Genes Devel 1: 86–96 (1987).CrossRefGoogle Scholar
  43. 43.
    Kobayashi K, Zbell B, Reinert J: A high affinity binding site for cytokinin to a particulate fraction in carrot suspension cells. Protoplasma 106: 145–155 (1981).CrossRefGoogle Scholar
  44. 44.
    Laloue M, Fox JE: Cytokinin oxidase from wheat: partial purification and general properties. Plant Physiol 90: 899–906 (1989).PubMedCrossRefGoogle Scholar
  45. 45.
    Lee YH, Mok MO, Mok DWS, Griffin DA, Shaw G: Cytokinin metabolism in Phaseolus embryos. Plant Physiol 77: 635–641 (1985).PubMedCrossRefGoogle Scholar
  46. 46.
    Letham DS: Zeatin, a factor inducing cell division from Zea mays. Life Sci 8: 569–573 (1963).PubMedCrossRefGoogle Scholar
  47. 47.
    Letham DS, Palni LMS: The biosynthesis and metabolism of cytokinins. Ann Rev Plant Physiol 34: 163–197 (1983).CrossRefGoogle Scholar
  48. 48.
    Li Y, Shi X, Strabala TJ, Hagen G, Guilfoyle TJ: Transgenic tobacco plants that overproduce cytokinins show increased tolerance to exogenous auxin and auxin transport inhibitors. Plant Sci 100: 9–14 (1994).CrossRefGoogle Scholar
  49. 49.
    Martin RC, Martin RR, Mok MC, Mok DWS: A monoclonal antibody specific to zeatin O-glycosyltransferases of Phaseolus. Plant Physiol 94: 1290–1294 (1990).PubMedCrossRefGoogle Scholar
  50. 50.
    Martin RC, Mok MC, Mok DWS: Cytolocalization of zeatin O-xylosyltransferase in Phaseolus. Proc Natl Acad Sci USA 90: 953–957 (1993).PubMedCrossRefGoogle Scholar
  51. 51.
    McGaw BA, Horgan R: Cytokinin oxidase from Zea mays kernels and Vicia rosea crown-gall tissue. Planta 159: 30–37 (1983).CrossRefGoogle Scholar
  52. 52.
    McGaw BA, Heald JK, Horgan R: Dihydrozeatin metabolism in radish seedlings. Phytochemistry 23: 1373- 1377 (1984).CrossRefGoogle Scholar
  53. 53.
    McGaw BA, Horgan R, Heald JK, Wullems GJ, Schilperoort RA: Mass-spectrometric quantitation of cytokinins in tobacco crown-gall tumours by mutated octopine Ti plasmids of Agrobacterium tumefaciens. Planta 176: 230–234 (1988).CrossRefGoogle Scholar
  54. 54.
    Medford JI, Horgan R, El-Sawi Z, Klee HJ: Alterations of endogenous cytokinins in transgenic plants using a chimeric isopentenyl transferase gene. Plant Cell 1: 403- 413 (1989).PubMedGoogle Scholar
  55. 55.
    Miernyk J A: Abscisic acid inhibition of kinetin nucleotide formation in germinating lettuce seeds. Physiol Plant 45: 63–66 (1979).CrossRefGoogle Scholar
  56. 56.
    Miller CO, Skoog F, Saltza MH von, Strong FM: Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77: 1329–1334 (1955).Google Scholar
  57. 57.
    Miller CO, Skoog F, Okomura FS, von Saltza MH, Strong FM: Isolation, structure and synthesis of kinetin, a substance promoting cell division. J Am Chem Soc 78: 1345–1350 (1956).Google Scholar
  58. 58.
    Mok MC, Mok DWS, Marsden KE, Shaw G: The biological activity and metabolism of a novel cytokinin metabolite, O-xylosylzeatin, in callus tissue of Phaseolus vulgaris and P. lunatus. J Plant Physiol 130: 423–431 (1987).CrossRefGoogle Scholar
  59. 59.
    Mok DWS, Mok MC, Martin RC, Bassil NV, Lightfoot DA: Zeatin metabolism in Phaseolus: enzymes and genes. In: Karsen CM, van Loon LC, Vreugdenhil D (eds) Progress in Plant Growth Regulation, pp. 597–606, Kluwer Academic Publishers, Dordrecht (1992).Google Scholar
  60. 60.
    Mok DWS, Mok MC, Martin RC, Bassil N, Shaw G: Immuno-analysis of zeatin metabolic enzymes ofPhaseolus. In: Kaminek M, Mok DWS, Zazimalova E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp. 17–23. SPB Academic Publishers, The Hague (1992).Google Scholar
  61. 61.
    Montague MI, Enns RK, Siegel NZ, Jaworski EG: Inhibition of 2,4-dichlorophenoxyacetic acid conjugation to amino acids by treatment of cultured soybean cells with cytokinins. Plant Physiol 67: 701–704 (1981).PubMedCrossRefGoogle Scholar
  62. 62.
    Moore FH: A cytokinin-binding protein from wheat germ. Isolation by affinity chromatography and properties. Plant Physiol 64: 594–599 (1979).PubMedCrossRefGoogle Scholar
  63. 63.
    Motyka V, Kaminek M: Characterization of cytokinin oxidase from tobacco and poplar callus cultures. In: Kaminek M, Mok DWS, Zazimalova E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp. 33–39. SPB Academic Publishers, The Hague (1992).Google Scholar
  64. 64.
    Nandi SK, De Klerk GJM, Parker CW, Palni LMS: Endogenous cytokinin levels and metabolism of zeatin riboside in genetic tumour tissues and non-tumorous tissues of tobacco. Physiol Plant 78: 197–204 (1990).CrossRefGoogle Scholar
  65. 65.
    Olsen KW, Zaluzec EJ, Zaluzec MM, Fernandez EJ, Pavkovic SF: Crystallographic and binding studies on a cytokinin peanut agglutinin complex. Biophys J 59:296A (1991).Google Scholar
  66. 66.
    Paces V, Werstiuk E, Hall RH: Conversion of N6-(Δ2- isopentenyl) adenosine to adenosine by enzyme activity in tobacco tissue. Plant Physiol 48: 775–778 (1971).PubMedCrossRefGoogle Scholar
  67. 67.
    Paces V, Kaminek M: Effect of ribosylzeatin on the enzymatic degradation of N6-(Δ2-isopentenyl) adenosine. Nucl Acids Res 3: 2309–2314 (1976).PubMedCrossRefGoogle Scholar
  68. 68.
    Palmer MV, Horgan R, Wareing PF: Cytokinin metabolism in Phaseolus vulgaris L. I. Variations in cytokinin levels in leaves of decapitated plants in relation to lateral bud outgrowth. J Exp Bot 32: 1231–1241 (1981).CrossRefGoogle Scholar
  69. 69.
    Palmer MV, Palni LMS: Substrate effects on cytokinin metabolism in soybean callus tissue. J Plant Physiol 126: 365–371 (1987).CrossRefGoogle Scholar
  70. 70.
    Palni LMS, Burch L, Horgan R: The effect of auxin concentration on cytokinin stability and metabolism. Planta 174: 231–234 (1988).CrossRefGoogle Scholar
  71. 71.
    Parker CW, Letham DS: Regulators of cell division in plant tissues. XVI. Metabolism of zeatin by radish cotyledons and hypocotyls. Planta 114: 199–218 (1973).CrossRefGoogle Scholar
  72. 72.
    Parker CW, Wilson MM, Letham DS, Cowley DE, MacLeod JK: The glucosylation of cytokinins. Biochem Biophys Res Commun 55: 1370–1376 (1973).CrossRefGoogle Scholar
  73. 73.
    Parker CW, Letham DS: Regulators of cell division in plant tissues. XVIII. Metabolism of zeatin in Zea mays seedlings. Planta 115: 337–344 (1974).CrossRefGoogle Scholar
  74. 74.
    Parker CW, Entsch B, Letham DS: Inhibitors of two enzymes which metabolize cytokinins. Phytochemistry 25: 303–310(1986).Google Scholar
  75. 75.
    Polya GM, Davis AW: Properties of a high affinity cytokinin-binding protein from wheat germ. Planta 139: 139–147 (1978).CrossRefGoogle Scholar
  76. 76.
    Reinecke DM, Brenner ML, Rubenstein I: Cytokinin biosynthesis in developing Zea mays kernels. Plant Physiol 99 (Suppl): 66 (1992).Google Scholar
  77. 77.
    Roberts DD, Goldstein IJ: Adenine binding sites of the lectin from lima beans (Phaseolus lunatus). J Biol Chem 258: 13820–13824 (1983).PubMedGoogle Scholar
  78. 78.
    Romano C, Hein M, Klee H: Inactivation of auxin in tobacco transformed with the indole acetic acid-lysine synthetase gene of Pseudomonas savastanoi. Genes Devel 5: 438–446 (1991).PubMedCrossRefGoogle Scholar
  79. 79.
    Romanov GA, Taran VY, Chvojka L, Kulaeva ON: Receptor-like cytokinin-binding protein(s) from barley leaves. J Plant Growth Regul 7: 1–7 (1988).CrossRefGoogle Scholar
  80. 80.
    Romanov GA, Taran VY, Venis MA: Cytokinin-binding protein from maize shoots. J Plant Physiol 136: 208–212 (1990).CrossRefGoogle Scholar
  81. 81.
    Sano H, Youssefian S: Light and nutritional regulation of transcripts encoding a wheat protein kinase homolog is mediated by cytokinins. Proc Natl Acad Sci USA 91: 2582–2586 (1994).PubMedCrossRefGoogle Scholar
  82. 82.
    Schmitt JM, Piepenbrock M: Regulation of phosphoenolpyruvate carboxylase and crassulacean acid metabolism induction in Mesembryanthenum crystallinum L. by cytokinin. Modulation of leaf gene expression by roots? Plant Physiol 99: 1664–1669 (1992).PubMedCrossRefGoogle Scholar
  83. 83.
    Schmulling T, Schell J, Spena A: Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 2621–2629 (1988).Google Scholar
  84. 84.
    Schmulling T, Beinsberger S, De Greef J, Schell J, Van Onckelen H, Spena A: Construction of heat-inducible chimaeric gene to increase the cytokinin content in transgenic plant tissue. FEBS Lett 2: 401–406 (1989).CrossRefGoogle Scholar
  85. 85.
    Schmulling T, Fladung M, Grossman K, Schell J: Hormonal content and sensitivity of transgenic tobacco and potato plants expressing single rol genes of Agrobacterium rhizogenes T-DNA. Plant J 3: 371–382 (1993).CrossRefGoogle Scholar
  86. 86.
    Singh S, Palni LMS, Letham DS: Cytokinin biochemistry in relation to leaf senescence. V. Endogenous cytokinin levels and metabolism of zeatin riboside in leaf discs from green and senescent tobacco (Nicotiana rustica) leaves. J Plant Physiol 139: 279–283 (1992).CrossRefGoogle Scholar
  87. 87.
    Skoog F, Miller CO: Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11: 118–130 (1957).PubMedGoogle Scholar
  88. 88.
    Skoog F, Armstrong DJ: Cytokinins. Ann Rev Plant Physiol 21: 359–384 (1970).CrossRefGoogle Scholar
  89. 89.
    Smart C, Scofield S, Bevan M, Dyer T: Delayed leaf senescence in tobacco plants transformed with tmr, a gene for cytokinin production in Agrobacterium. Plant Cell 3: 647–656 (1991).PubMedGoogle Scholar
  90. 90.
    Smigocki AC: Cytokinin content and tissue distribution in plants transformed by a reconstructed isopentenyl transferase gene. Plant Mol Biol 16: 105–115 (1991).PubMedCrossRefGoogle Scholar
  91. 91.
    Smigocki AC, Owens LD: Cytokinin gene fused with a strong promoter enhances shoot organogenesis and zeatin levels in transformed plant cells. Proc Natl Acad Sci USA 85: 5131–5135 (1988).PubMedCrossRefGoogle Scholar
  92. 92.
    Smith AR, Van Staden J: Changes in endogenous cytokinin levels in kernels of Zea mays L. during imbibition and germination. J Exp Bot 29: 1067–1075 (1978).CrossRefGoogle Scholar
  93. 93.
    Sondheimer E, Tzou D: The metabolism of 8-14C-zeatin in bean axes. Plant Physiol 47: 516–520 (1971).PubMedCrossRefGoogle Scholar
  94. 94.
    Sossountzov L, Maldiney R, Sotta B, Sabbagh I, Habricot Y, Bonnet M, Miginiac E: Immunocytochemical localization of cytokinins in Craigella tomato and a sideshootless mutant. Planta 175: 291–304 (1988).CrossRefGoogle Scholar
  95. 95.
    Spena A, Aalen RB, Schulze SC: Cell autonomous behavior of the rolC gene of Agrobacterium rhizogenes during leaf development: a visual assay for transposon excision in transgenic plants. Plant Cell 1: 1157–1164 (1989).PubMedGoogle Scholar
  96. 96.
    Spena A, Prinsen E, Fladung M, Schulze SC, Van Onckelen H: The indoleacetic acid-lysine synthetase gene of Pseudomonas syringae subsp. savastanoi induces developmental alterations in transgenic tobacco and potato plants. Mol Gen Genet 227: 205–212 (1991).PubMedCrossRefGoogle Scholar
  97. 97.
    Stuber CW, Goodmann MM, Johnson FM: Genetic control and racial variation of β -glucosidase isozymes in maize (Zea mays L.). Biochem Genet 15: 383–394 (1977).PubMedCrossRefGoogle Scholar
  98. 98.
    Sugiharto B, Burnell JN, Sugiyama T: Cytokinin is required to induce the nitrogen-dependent accumulation of mRNAs for phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaves. Plant Physiol 100: 153–156 (1992).PubMedCrossRefGoogle Scholar
  99. 99.
    Takegami T, Yoshida K: Isolation and purification of cytokinin binding protein from tobacco leaves by affinity column chromatography. Biochem Biophys Res Commun 67: 782–789 (1975).PubMedCrossRefGoogle Scholar
  100. 100.
    Taran VY, Romanov GA, Venis MA: Purification of soluble zeatin-binding proteins from maize shoots. In: Kaminek M, Mok DWS, Zazimalova E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp. 165–167. SPB Academic Publishers, The Hague (1992).Google Scholar
  101. 101.
    Taya T, Tanaka Y, Nishimura S: 5’ AMP is a direct precursor of cytokinin in Dictyostelium discoideum. Nature 271: 545–547 (1978).PubMedCrossRefGoogle Scholar
  102. 102.
    Terrine C, Laloue M: Kinetics of N6-(A2-isopentenyl) adenosine degradation in tobacco cells. Plant Physiol 65: 1090–1095 (1980).PubMedCrossRefGoogle Scholar
  103. 103.
    Trewavas AJ: Growth substances in context: a decade of sensitivity. Biochem Soc Transact 20: 102–108 (1992).Google Scholar
  104. 104.
    Turner JE, Mok MC, Mok DWS: Zeatin metabolism in fruits of Phaseolus: comparison between embryos, seedcoat, and pod tissue. Plant Physiol 79: 321–322 (1985).PubMedCrossRefGoogle Scholar
  105. 105.
    Turner JE, Mok DWS, Mok MC, Shaw G: Isolation and partial purification of an enzyme catalyzing the formation of O-xylosylzeatin in Phaseolus vulgaris embryos. Proc Natl Acad Sci USA 84: 3714–3717 (1987).PubMedCrossRefGoogle Scholar
  106. 106.
    Van Staden J, Dimalla GG: Endogenous cytokinins and the breaking of dormancy and apical dominance in potato tubers. J Exp Bot 29: 1077–1084 (1978).CrossRefGoogle Scholar
  107. 107.
    Van Staden J, Smith AR: The synthesis of cytokinins in excised roots of maize and tomato under aseptic conditions. Ann Bot 42: 751–753 (1978).Google Scholar
  108. 108.
    Van Staden J, Mooney PA: The effect of cytokinin preconditioning on the metabolism of adenine derivatives in soybean callus. J Plant Physiol 133: 466–469 (1988).CrossRefGoogle Scholar
  109. 109.
    Wang TL, Thompson AG, Horgan R: A cytokinin glucoside from leaves of Phaseolus vulgaris L. Planta 135: 285–288 (1977).CrossRefGoogle Scholar
  110. 110.
    Whenam RJ: Effect of systemic tobacco mosaic virus infection on endogenous cytokinin concentration in tobacco (Nicotiana tabacum L.) leaves: consequences for the control of resistance and symptom development. Physiol Mol Plant Pathol 35: 85–95 (1989).CrossRefGoogle Scholar
  111. 111.
    Whitty CD, Hall RH: A cytokinin oxidase in Zea mays. Can J Biochem 52: 781–799 (1974).Google Scholar
  112. 112.
    Wyndaele R, Christiansen J, Horseele R, Rudelsheim P, Van Onckelen H: Functional correlation between endogenous phytohormone levels and hormone autotrophy of transformed and habituated soybean cell lines. Plant Cell Physiol 29: 1095–1101 (1988).Google Scholar
  113. 113.
    Zhang R, Letham DS, Wong OC, Nooden LD, Parker CW: Cytokinin biochemistry in relation to leaf senescence. II. The metabolism of benzylaminopurine in soybean leaves and the inhibition of conjugation. Plant Physiol 83: 334–340 (1987).PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 1994

Authors and Affiliations

  • Břetislav Brzobohatý
    • 1
    • 2
  • Ian Moore
    • 2
    • 3
  • Klaus Palme
    • 2
  1. 1.Institute for BiophysicsAS CRBrnoCzech Republic
  2. 2.Max-Planck-Institut für ZüchtungsforschungKölnGermany
  3. 3.Department of Plant SciencesUniversity of OxfordOxfordUK

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