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Role and function of cytokinin oxidase in plants

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Abstract

Cytokinin oxidase (CK oxidase) is widely distributed in plants and is the only enzyme that has been shown unequivocally to catalyze the catabolism of specific cytokinins (CKs) to inactive products that lack the N6-unsaturated side chain. Thus, the enzyme is thought to play a major role in controlling the level or species of CKs in plant tissues. However, despite its discovery more than 25 years ago, little attention has been given to the elucidation of its role and function in plant growth and development. This review seeks to bring in to context the current state of knowledge regarding the biochemical and molecular properties, regulation in undifferentiated and differentiated tissues, and recent results from studies using transgenic plants in an attempt to provide a more comprehensive understanding of the physiological significance of the enzyme in plants. Notwithstanding species, tissue and other specific differences, in general, CK oxidase appears to contribute to CK homeostasis in plants. However, complete clarity as to its function awaits purification of the protein to homogeneity and the ultimate development of requisite molecular probes.

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References

  1. Akiyoshi DE, Morris, RO, Hinz R, Mischke BS, Kosuge T, Garfinkel DJ, Gordon MP and Nester EW (1983) Cytokinin/auxin balance in crown gall tumors is regulated by specific loci in the T-DNA. Proc Natl Acad Sci USA 80: 407–411

    Google Scholar 

  2. Armstrong DJ (1994) Cytokinin oxidase and the regulation of cytokinin degradation. In: Mok DWS and Mok MC (eds) Cytokinins: Chemistry, Activity, and Function, pp 139–154. Boca Raton, USA: CRC Press

    Google Scholar 

  3. Brownlee BG, Hall RH, and Whitty CD (1975) 3-Methyl-2-butenal; an enzymatic degradation product of the cytokinin, N6-(Δ2-isopentenyl)adenine. Can J Biochem 53: 37–41

    PubMed  Google Scholar 

  4. Burch LR and Horgan R (1989) The purification of cytokinin oxidase from Zea mays kernels. Phytochemistry 28: 1313–1319

    Article  Google Scholar 

  5. Burch LR and Horgan R (1992) Cytokinin oxidase and the degradative metabolism of cytokinins. In: Kamínek M, Mok DWS and Zažímalová E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp 29–32. The Hague, The Netherlands: SPB Academic Publ

    Google Scholar 

  6. Carmi A and Van Staden J (1983) Role of roots in regulating the growth rate and cytokinin content of leaves. Plant Physiol 73: 76–78

    Google Scholar 

  7. Cames MG and Wright MS (1988) Endosperm hormone levels of immature corn kernels of A188, Missouri 17, and DeKalb XL-12. Plant Sci 57: 195–203

    Article  Google Scholar 

  8. Chatfield JM and Armstrong DJ (1986) Regulation of cytokinin oxidase activity in callus tissues of Phaseolus vulgaris L. cv. Great Northern. Plant Physiol 80: 493–49

    Google Scholar 

  9. Chatfield JM and Armstrong DJ (1987) Cytokinin oxidase from Phaseolus vulgaris callus tissues: enhanced in vitro activity of the enzyme in the presence of copper-imidazole complexes. Plant Physiol 84: 726–731

    Google Scholar 

  10. Chatfield JM and Armstrong DJ (1988) Cytokinin oxidase from Phaseolus vulgaris callus cultures: affinity for concanavalin A. Plant Physiol 88: 245–247

    Google Scholar 

  11. Cheikh NC and Jones RJ (1994) Disruption of kernel growth and development by heat stress: role of cytokinin/ABA balance. Plant Physiol 106: 45–51

    PubMed  Google Scholar 

  12. Davey JE and Van Staden J (1979) Cytokinin activity in Lupinus albus L. IV. Distribution in seeds. Plant Physiol 163: 873–877

    Google Scholar 

  13. Dietrich JT, Kaminek M, Blevins DG, Reinbott TM and Morris RO (1995) Changes in cytokinins and cytokinin oxidase activity in developing maize kernels and the effects of exogenous cytokinin on kernel development. Plant Physiol Biochem 33: 327–336

    Google Scholar 

  14. Eklöf S, Astot C, Moritz T, Blackwell J, Olsson O and Sandberg G (1996) Cytokinin metabolites and gradients in wild type and transgenic tobacco with moderate cytokinin overproduction. Physiol Plant 98: 333–344

    Article  Google Scholar 

  15. Ekiöf S, Astot C, Blackwell J, Moritz T, Olsson O and Sandberg G (1997) Auxin-cytokinin interactions in wild-type and transgenic tobacco. Plant Cell Physiol 38: 225–235

    Google Scholar 

  16. Entsch B, Letham DS, Parker CW, Summons RE and Gollnow BI (1979) Metabolism of cytokinins. In: Skoog F (ed) Plant Growth Substances, pp 109–118. New York, USA: Springer-Verlag

    Google Scholar 

  17. Felker FC and Shannon JC (1980) Movement of 14C-labelled assimilates into kernels of Zea mays L. III. An anatomical examination and microautoradiographic study of assimilate transfer. Plant Physiol 65: 864–870

    Google Scholar 

  18. Griffith SM, Jones RJ and Brenner ML (1987) In vitro sugar transport in Zea mays L. kernels. I. Characteristics of sugar absorption and metabolism by developing maize endosperm. Plant Physiol 84: 467–471

    Google Scholar 

  19. Hansen CE, Meins F Jr and Milani A (1985) Clonal and physiological variation in the cytokinin content of tobacco cell lines differing in cytokinin requirement and capacity for neoplastic growth. Differentiation 29: 2–6

    Google Scholar 

  20. Hare PD and Van Staden J (1994) Cytokinin oxidase: biochemical features and physiological significance. Physiol Plant 91: 128–136

    Article  Google Scholar 

  21. Hare PD and Van Staden J (1994) Inhibitory effect of thidiazuron on the activity of cytokinin oxidase isolated from soybean callus. Plant Cell Physiol 35: 1121–1125

    Google Scholar 

  22. Henson IE (1978) Types, formation, and metabolism of cytokinins in leaves of Alnus glutinosa (L) Gaertn. J Exp Bot 29: 935–951

    Google Scholar 

  23. Hocart CH, Badenoch-Jones J, Parker CW, Lethan DS and Summons RE (1988) Cytokinin of dry Zea mays seed: quantification by radioimmunoassay and gas chromatography-mass spectrometry. J Plant Growth Regul 7: 179–196

    Google Scholar 

  24. Horgan R, Palni LMS, Scott IM and McGaw BA (1981) Cytokinin metabolism in Vinca rosea crown gall tissue. In: Guem J and Peaud-Lenoel C (eds) Metabolism and molecular activity of cytokinins, pp 56–65. New York, USA: Springer-Verlag

    Google Scholar 

  25. Iskikawa K, Karnada H, Yamaguchi I, Takahashi N and Harada H (1988) Morphology and hormone levels of tobacco and carrot tissues transformed by Agrobacterium tumefaciens. I. Auxin and cytokinin contents of cultured tissues transformed with wild-type and mutant Ti plasmids. Plant Cell Physiol 29: 461–466

    Google Scholar 

  26. Jameson PE (1994) Cytokinin metabolism and compartmentation. In: Mok DWS and Mok MC (eds) Cytokinins: Chemistry, Activity and Function, pp 113–128. Boca Raton, USA: CRC Press

    Google Scholar 

  27. Jameson PE, Letham DS, Zhang R, Parker CW and Badenoch-Jones J (1987) Cytokinin translocation and metabolism in lupin species. I. Zeatin riboside introduced into the xylem at the base of Lupinus angustifolius stems. Aust J Plant Physiol 14: 695–718

    Google Scholar 

  28. Jones RJ, Schreiber BMN, McNeil K, Brenner ML and Foxon G (1992) Cytokinin levels and oxidase activity during maize kernel development. In: Kamínek M, Mok DWS and Zažímalová E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp 29–32. The Hague, The Netherlands: SPB Academic Publishing

    Google Scholar 

  29. Kaminek M and Armstrong DJ (1990) Genotypic variation in cytokinin oxidase from Phaseolus callus cultures. Plant Physiol 93: 1530–1538

    Google Scholar 

  30. Karanov EN, Iliev LK and Alexieva VS (1992) Phenylurea cytokinins — chemistry physiology and application. In: Karnínek M, Mok DWS and Zažímalová E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp 199–204. The Hague, The Netherlands: SPB Academic Publ

    Google Scholar 

  31. Laloue M, Terrine C, and Guem J (1977) Cytokinin metabolism and biological activity of N6-(Δ2-isopentenyl)adenosine and N6-(Δ2-isopentenyl)adenine in tobacco cells and callus. Plant Physiol 59: 478–483

    Google Scholar 

  32. Laloue M and Fox JE (1985) Characterization of an imine intermediate in the degradation of isopentenylated cytokinins by a cytokinin oxidase from wheat. In: Bopp M, Knoop B and Rademacher W (eds) Abstracts of the 12th International Conference on Plant Growth Substances, p 23. Heidelberg

  33. Laloue M, and Fox JE (1989) Cytokinin oxidase from wheat: partial purification and general properties. Plant Physiol 90: 899–906

    Google Scholar 

  34. Letham DS and Zhang R (1989) Cytokinin translocation and metabolism in lupin species. II. New nucleotides metabolites of cytokinins. Plant Sci 64: 161–165

    Article  Google Scholar 

  35. Lewis DH, Burge GK, Hopping ME and Jameson PE (1996) Cytokinin and fruit development in the kiwifruit (Actinidia deliciosa). II. Effects of reduced pollination and CPPU application. Physiol Plant 98: 187–195

    Article  Google Scholar 

  36. Libreros-Minotta CA and Tipton PA (1995) A colorimetric assay for cytokinin oxidase. Anal Biochem 231: 339–341

    Article  PubMed  Google Scholar 

  37. Lur HS and Setter TL (1993) Role of auxin in maize endosperm development. Plant Physiol 103: 273–280

    PubMed  Google Scholar 

  38. McGaw BA and Horgan R (1983) Cytokinin oxidase from Zea mays and Vinca rosea crown gall tissue. Planta 159: 30–37

    Google Scholar 

  39. McGaw BA and Horgan R (1983) Cytokinin catabolism and cytokinin oxidase. Phytochemistry 22: 1103–1105

    Article  Google Scholar 

  40. McGaw BA, Heald JM and Horgan R (1984) Dihydrozeatin metabolism in radish seedlings. Phytochemistry 23: 1373–1377

    Article  Google Scholar 

  41. McGaw BA, Horgan R and Heald JK (1985) Cytokinin metabolism and the modulation of cytokinin activity in radish. Phytochemistry 24: 9–13

    Article  Google Scholar 

  42. McGaw BA, Horgan R, Heald JK, Wullems GJ and Schilperoort RA (1988) Mass spectrometric quantitation of cytokinins in tobacco crown gall tumors induced by mutated octopine Ti plasmids of Agrobacterium tumefaciens. Planta 176: 230–243

    Google Scholar 

  43. McNeil KJ, Brenner ML and Jones RJ (1991) Effect of benzylamino-purine and thidiazuron on maize kernel development. Proc Plant Growth Reg Soc of Amer 17: 16–17

    Google Scholar 

  44. Meilan R and Morris RO (1994) Cloning the cytokinin oxidase gene. Plant Physiol (suppl) 105: 68

    Google Scholar 

  45. Mok DWS, Armstrong DJ, Isogai Y and Okamoto T (1982) Cytokinin activity of N-phenyl-N'-1,2,3,-thidiazol-5-ylurea (Thidiazuron). Phytochemistry 21: 1509–1511

    Article  Google Scholar 

  46. Motyka V and Kaminek M (1992) Characteristics of cytokinin oxidase from tobacco and poplar callus cultures. In: Kamínek M, Mok DWS and Zažímalová E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp 33–39. The Hague, The Netherlands: SPB Academic Publ

    Google Scholar 

  47. Motyka V, Faiss M, Strnad M, Kaminek M and Schmülling T (1996) Changes in cytokinin content and cytokinin oxidase activity in response to depression of ipt gene transcription in transgenic tobacco calli and plants. Plant Physiol 112: 1035–1043

    PubMed  Google Scholar 

  48. Muhitch MJ (1988) Glutamine synthetase activity of the endosperm, embryo, and pedicel-placento-chalazal regions of developing maize (Zea mays) kernels. Physiol Plant 74: 176–180

    Google Scholar 

  49. Pačes V, Werstiuk E and Hall RH (1971) Conversion of N6-(2-isopentenyl)adenosine to adenosine by enzyme activity in tobacco tissue. Plant Physiol 48: 775–778

    Google Scholar 

  50. Palmer MV, Scott IM and Horgan R (1981) Cytokinin metabolism in Phaseolus vulgaris L. II. Comparative metabolism of exogenous cytokinins by detached leaves. Plant Sci Lett 22: 187–195

    Google Scholar 

  51. Palmer M, Horgan R and Wareing PF (1981) Cytokinin metabolism in Phaseolus vulgaris L.: identification of endogenous cytokinin and metabolism of [8-14C]-dihydrozeatin in stems of decapitated plants. Planta 153: 297–302

    Google Scholar 

  52. Palmer M and Palni LMS (1987) Substrate effects on cytokinin metabolism in soybean callus tissue. J Plant Physiol 126: 365–371

    Google Scholar 

  53. Palni LMS, Burch L and Horgan R (1988) The effect of auxin concentration on cytokinin stability and metabolism. Planta 174: 231–234

    Google Scholar 

  54. Parker CW and Letham DS (1973) Regulation of cell division in plant tissues. XVI. Metabolism of zeatin by radish cotyledons and hypocotyls. Planta 114: 199–218

    Google Scholar 

  55. Parker CW and Letham DS (1974) Regulation of cell division in plant tissues. XVIII. Metabolism of zeatin in Zea mays seedlings. Planta 115: 337–344

    Google Scholar 

  56. Porter GA, Knievel DP and Shannon JC (1985) Sugar efflux from maize (Zea mays L.) pedicel tissue. Plant Physiol 77: 524–531

    Google Scholar 

  57. Roessler JA, Jones RJ, Schreiber BMN and Vance CP (1996) Molecular cloning and characterization of maize seedling cytokinin oxidase. In: Abstracts of the American Society of Agronomy p 170

  58. Schreiber BMN (1990) The role of cytokinins in maize kernel development. Ph.D. Diss., Univ. of Minnesota, St. Paul, MN, USA

    Google Scholar 

  59. Schreiber BMN, Roessler JA and Jones RJ (1995) Polyclonal antibodies to maize seedling cytokinin oxidase. Plant Physiol 108(suppl): 80

    Google Scholar 

  60. Scott RA, McGaw BA, Horgan R and Williams PE (1982) Biochemical studies on cytokinins in Vinca rosea crown gall tissues. In: Wareing PE (ed) Plant Growth Substances, pp 165–174. London: Academic Press

    Google Scholar 

  61. Shudo K, Okamoto T, Isogai Y and Ohshima K (1992) Structure-activity relationship and agricultural application of synthetic cytokinins. In: Kamínek M, Mok DWS and Zažímalová E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp 189–193. The Hague, The Netherlands: SPB Academic Publ

    Google Scholar 

  62. Shudo K (1994) Chemistry of phenylurea cytokinins. In: Mok DWS and Mok MC (eds) Cytokinins: Chemistry, Activity, and Function, pp 35–42. Boca Raton, USA: CRC Press

    Google Scholar 

  63. Singh S, Letham DS, Jameson PE, Zhang R, Parker CW, Badenoch-Jones J and Nooden D (1988) Cytokinin biochemistry in relation to senescence. IV. Cytokinin metabolism in soybean explants. Plant Physiol 88: 787–794

    Google Scholar 

  64. Singh S, Palni LMS and Letham DS (1992) Cytokinin 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

    Google Scholar 

  65. Summons RE, Entsch B, Letham DS, Gollnow BI and MacLeod JK (1980) Regulation of cell division in plants tissues. XXVIII. Metabolites of zeatin in sweet-corn kernels: purification and identification using high-perfonnance liquid chromatography and chemical-ionization mass spectrometry. Planta 147: 422–434

    Google Scholar 

  66. Terrine C and Laloue M (1980) Kinetics of N 6-(Δ2-isopentenyl)adenosine degradation in tobacco cells. Evidence of regulatory mechanism under the control of cytokinins. Plant Physiol 65: 1090–1095

    Google Scholar 

  67. Thomas JC and Katterman RF (1986) Cytokinin activity induced by thidiazuron. Plant Physiol 81: 681–683

    Google Scholar 

  68. Turner JE, Mok MC and Mok DWS (1985) Zeatin metabolism in fruits of Phaseolus: comparison between embryo, seedcoat, and pod tissues. Plant Physiol 79: 321–322

    Google Scholar 

  69. Van Staden J and Davey JE (1979) The synthesis transport and metabolism of exogenous cytokinins. Plant Cell Environ 2: 93–106

    Google Scholar 

  70. Van Staden J and Crouch NR (1996) Benzyladenine and derivatives — their significance and interconversion in plants. Plant Growth Regul 19: 153–175

    Google Scholar 

  71. Vaňková R, Gaudinova A, Kamínek M and Eder J (1992) The effect of interaction of synthetic cytokinin and auxin on the production of natural cytokinins by immobilized tobacco cells. In: Kamínek M, Mok DWS and Zažímalová E (eds) Physiology and Biochemistry of Cytokinins in Plants, pp 47–51. The Hague, The Netherlands: SPB Academic Publ

  72. Wang J and Letham DS (1995) Cytokinin oxidase — purification by affinity chromatography and activation by caffeic acid. Plant Sci 112: 161–166

    Article  Google Scholar 

  73. Whitty CD and Hall RH (1974) A cytokinin oxidase in Zea mays. Can J Biochem 52: 787–799

    Google Scholar 

  74. Wyndaele R, Christian J, Horseele R, Rudelsheim P and Van Onckelen HA (1988) Functional correlation between endogenous phytohormone levels and hormone autotrophy of transformed and habituated soybean cell lines. Plant Cell Physiol 29: 1095–1101

    Google Scholar 

  75. Zhang R and Letham DS (1990) Cytokinin translocation and metabolism in lupin species. III. Translocation of xylem cytokinin into the seed of lateral shoots of Lupinus angustifolius. Plant Sci 70: 65–71

    Article  Google Scholar 

  76. Zhang R, Zhang X, Wang J, Letham DS, Mckinney SA and Higgins TJV (1995) The effect of auxin on cytokinin levels and metabolism in transgenic tobacco tissues expressing an ipt gene. Planta 196: 84–94

    Article  Google Scholar 

  77. Zhang R, Letham DS, Wong OC, Nooden LD and Parker CW (1987) Cytokinin biochemistry in relation to leaf senescence. II. The metabolism of 6-benzyl-aminopurine in soybean leaves and the inhibition of its conjugation. Plant Physiol 83: 334–340

    Google Scholar 

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  1. Department of Agronomy and Plant Genetics, University of Minnesota, 411 Borlaug Hall, 1991 Buford Circle, St. Paul, Minnesota, 55108, USA

    Robert J. Jones & Beth M.N. Schreiber

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Jones, R.J., Schreiber, B.M. Role and function of cytokinin oxidase in plants. Plant Growth Regulation 23, 123–134 (1997). https://doi.org/10.1023/A:1005913311266

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