Genetic engineering of cytokinins and their application to agriculture

Critical Reviews in Biotechnology

Volumn 28, Issue 3, 2008, Pages 213-232

  Ma, Qing Hu ^a,b  

^a INSTITUTE OF BOTANY   (China)

^b Key Laboratory of Photosynthesis and Environmental Molecular Physiology   (China)

Author keywords

Agricultural applications; Cytokinins; Genetic engineering; Molecular breeding

Indexed keywords

AGRICULTURE; APPLICATIONS; BIOCHEMISTRY; BIOTECHNOLOGY; GENETIC ENGINEERING; MOLECULAR BIOLOGY; PLANT LIFE EXTENSION; PLANTS (BOTANY); SIGNAL TRANSDUCTION;

AGRICULTURAL APPLICATIONS; CYTOKININ METABOLISMS; CYTOKININS; FUTURE RESEARCH DIRECTIONS; MASTER REGULATORS; METABOLIC PROCESSES; MOLECULAR BREEDING; MOLECULAR BREEDINGS; MOLECULAR LEVELS; PLANT GROWTHS; RECENT PROGRESSES; TRANSGENIC APPROACHES;

ENGINEERING RESEARCH;

CYTOKININ; NITROGEN;

AGRICULTURE; APPLIED RESEARCH; BREEDING METHOD; FLORET; FLOWER; FLOWER DEVELOPMENT; FRUIT DEVELOPMENT; GENETIC ENGINEERING; HORTICULTURE; LEAF SENESCENCE; METABOLISM; MOLECULAR BIOLOGY; NITROGEN UTILIZATION; NODULATION; NONHUMAN; PLANT MORPHOLOGY; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; SEED PRODUCTION; SHOOT; SIGNAL TRANSDUCTION; STRESS; SYNTHESIS;

AGRICULTURE; BIOTECHNOLOGY; CYTOKININS; GENE EXPRESSION REGULATION, PLANT; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION;

EID: 54349097794     PISSN: 07388551     EISSN: 15497801     Source Type: Journal    
DOI: 10.1080/07388550802262205     Document Type: Review

References (149)

1. Abe, I., Tanaka, H., Abe, T., and Noguchi, H. 2007. Enzymatic formation of unnatural cytokinin analogs by adenylate isopentenyltransferase from mulberry. Biochem. Biophys. Res. Commun. 355: 795-800.
2. Ainley, W. M., McNeil, K. J., Hill, J. W., Simpson, R. B., Brenner, M. L., Nagao, R. T., and Key. J. L. 1993. Regulatable endogenous production of cytokinins up to 'toxic' levels in transgenic plants and plant tissues. Plant Mol. Biol. 22: 13-23.
3. Akiyoshi, D. E., Klee, H., Amasino, R. M., Nester, E. W., and Gordon, P. M. 1984. T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc. Nat. Acad. Sci. USA 81: 5994-98.
4. Allavena, A., Giovannini, A., Berio, T., Spena, A., Zottini, M., Accotto, G. P., and Vaira, A. M. 2000. Genetic engineering of Osteospermum spp: a case story. The 19th International Symposium on Improvement of Ornamental Plants, Acta Horticulturae. 508: 129-133.
5. Ando, S., Asano, T., Tsushima, S., Kamachi, S., Hagio, T., and Tabei, Y. 2005. Changes in gene expression of putative isopentenyltransferase during clubroot development in Chinese cabbage (Brassica rapa L.). Physiol. Mol. Plant Pathol. 67: 59-67.
6. Ashikari, M., Sakakibara, H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E. R., Qian, Q., Kitano, H., and Matsuoka, M. 2005. Cytokinin oxidase regulates rice grain production. Science. 309: 741-745.
7. Bai, F., and DeMason, D. A. 2008. Hormone interactions and regulation of PsPK2::GUS compared with DR5::GUS and PID::GUS in Arabidopsis thaliana. Amer. J. Bot. 95: 133-145.
8. Balibrea, L. M. E., Gonzalez, G. M. C., Fatima, T., Ehness, R., Lee, T. K., Proels, R., Tanner, W., and Roitsch, T. 2004. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16: 1276-1287.
9. Barry, G. F., Rogers, S. G., Fraley, R. T., and Brand, L. 1984. Identification of a cloned cytokinin biosynthetic gene. Proc. Nat. Acad. Sci. USA 81: 4776-4780.
10. Bassil, N. V., Mok, D. W. S., and Mok, M. 1993. Partial purification of a cis-trans-isomerase of zeatin from immature seed of Phaseolus vulgaris L. Plant Physiol. 102: 867-872.
11. Bell, R. L., Scorza, R., Srinivasan, C., and Webb, K. 1999. Transformation of "Beurre Bosc" pear with the rolC gene. J. Amer. Soc. Horticultural Sci. 124: 570-574.
12. Beveridge, C. A. 2006. Axillary bud outgrowth: sending a message. Curr. Opin. Plant Biol. 9: 35-40.
13. Beveridge, C. A., Mathesius, U., Rose, R. J., and Gresshoff, P. M. 2007. Common regulatory themes in meristem development and whole-plant homeostasis. Curr. Opin. Plant Biol. 10: 44-51.
14. Bilyeu, K. D., Cole, J. L., Laskey, J. G., Riekhof, W. R., Esparza, T. J., Kramer, M. D., and Morris, R. O. 2001. Molecular and biochemical characterization of a cytokinin oxidase from maize. Plant Physiol. 125: 378-386.
15. Boase, M. R., Winefield, C. S., Lill, T. A., and Bendall, M. J. 2004. Transgenic regal pelargoniums that express the rolC gene from Agrobacterium rhizogenes exhibit a dwarf floral and vegetative phenotype. In Vitro Cellular Dev. Biol. 40: 46-50.
16. Borochov, A., and Woodson, W. R. 1989. Physiology and biochemistry of flower petal senescence. Horticultural Rev. 11: 15-43.
17. Boyer, J. S. 1982. Plant productivity and environment. Science 218: 443-448.
18. Carabelli, M., Possenti, M., Sessa, G., Ciolfi, A., Sassi, M., Morelli, G., and Ruberti, I. 2007. Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev. 21: 1863-1868.
19. Chang, H., Jones, M. L., Banowetz, G. M., and Clark, D. G. 2003. Overproduction of cytokinins in Petunia flowers transformed with PSAG12-IPT delays corolla senescence and decreases sensitivity to ethylene. Plant Physiol. 132: 2174-2183.
20. Chefdor, F., Bénédetti, H., Depierreux, C., Delmotte, F., Morabito, D., and Carpin, S. 2006. Osmotic stress sensing in Populus: Components identification of a phosphorelay system. FEBS Lett. 580: 77-81.
21. Chen, C. M., and Melitz, D. K. 1979. Cytokinin biosynthesis in a cell-free system from cytokinin-autotrophic tobacco tissue cultures. FEBS Lett. 107: 15-20.
22. Chen, C. M., and Leisner, S. M. 1984. Modification of cytokinins by cauliflower microsomal enzymes. Plant Physiol. 75: 442-46.
23. SAG12-IPT Petunias. J. Amer. Soc. Horticultural Sci. 129: 93-99.
24. Connolly, D. M., and Winkler, M. E. 1991. Structure of Escherichia coli miaA and characterization of the mutator phenotype caused by miaA insertion mutation. J. Bacteriol. 173: 1711-1721.
25. Curtis, I. S., He, C., Jordi, W. J. R. M., Davelaar, E., Power, J. B., de Laat, A. M. M., and Davey, M. R. 1999. Promoter deletions are essential for transformation of lettuce by the T-cyt gene: The phenotypes of transgenic plants. Annals Bot. 83: 559-567.
26. D'Agostino, I. B., and Kieber, J. J. 1999. Molecular mechanisms of cytokinin action. Curr. Opin. Plant Biol. 2: 359-364.
27. Dietrich, J. T., Kaminek, M., Belvin, D. G., Beinbott, T. M., and Morris, R. O. 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: 289-294.
28. Ding, Y., and Ma, Q. H. 2006. Biosynthesis, signal transduction, and molecular regulation of cytokinins. Curr. Pharma. Anal. 2:169-182.
29. Dodd, I. C., and Beveridge, C. A. 2006. Xylem-borne cytokinins: still in search of a role? J. Exp. Bot. 57: 1-4.
30. Dun, E., Ferguson, B., and Beveridge, C. A. 2006. Apical dominance and shoot branching: divergent opinions or divergent mechanisms. Plant Phys. 142: 812-819.
31. Estruch, J. J., Chriqui, D., Grossmann, K., Schell, J., and Spena, A. 1991. The plant oncogene rolC is responsible for the release of cytokinins from glucoside conjugates. EMBO J. 10: 2889-2895.
32. Faiss, M., Strnad, M., Redig, P., Dolzak, K., Hanus, J., Van Onckelen, H., and Schmiilling, T. 1996. Chemically induced expression of the rolC-encoded beta-glucuronidase in transgenic tobacco plants and analysis of cytokinin metabolism: RolC does not hydrolyze endogenous cytokinin glucosides in planta. Plant J. 10: 33-46.
33. Ferreira, F. J., and Kieber, J. J. 2005. Cytokinin signaling. Curr. Opin. Plant Biol. 8: 518-525.
34. Foo, E., Morris, S. E., Parmenter, K., Young, N., Wang, H., Jones, A., Rameau, C., Turnbull, C. G. N., and Beveridge, C. A. 2007. Feedback regulation of xylem cytokinin content is conserved in pea and Arabidopsis. Plant Physol. 143: 1418-1428.
35. Forde, B. G. 2002. The role of long-distance signalling in plant responses to nitrate and other nutrients. J. Exp. Bot. 53: 39-43.
36. Franco-Zorrilla, J. M., Martin, A. C., Leyva, A., and Paz-Ares, J. 2005. Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physol. 138: 847-857.
37. Fu, Y., Ding, Y., Liu, X., Sun, C., Cao, S., Wang, D., He, S., Wang, X., Li, L., and Tian, W. 1998. Rice transformation with a senescence-inhibition chimeric gene. Chin. Sci. Bull. 43: 1810-1815.
38. Galuszka, P., Frebortova, J., Werner, T., Yamada, M., Strnad, M., Schmülling, T., and Frebort, I. 2004. Cytokinin oxidase/dehydrogenase genes in barley and wheat: Cloning and heterologous expression. Eur. J. Biochem. 271: 3990-4002.
39. Gan, S., and Amasino, R. M. 1997. Making sense of senescence: molecular genetic regulation of leaf senescence. Plant Physiol. 113: 313-319.
40. Gan, S., and Amasino, R. M. 1995. Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270: 1986-1988.
41. Geurts, R., and Bisseling, T. 2002. Rhizobium Nod factor perception and signaling. Plant Cell 14: S239-S249.
42. Gonzalez-Rizzo, S., Crespi, M., and Frugier, F. 2006. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18: 2680-2693.
43. Gotz, K.-P., Staroske, N., Radchuk, R., Emery, R. J. N., Wutzke, K.-D., Herzog, H., and Weber, H. 2007. Uptake and allocation of carbon and nitrogen in Vicia narbonensis plants with increased seed sink strength achieved by seed-specific expression of an amino acid permease. J. Exp. Bot. 58: 3183-3195.
44. Gray, J., Wang, J., and Gelvin, S. B. 1992. Mutation of the miaA gene of Agrobacterium tumefaciens results in reduced vir gene expression. J. Bacteriol. 174: 1086-1098.
45. Guivarch, A., Rembur, J., Goetz, M., Roitsch, T., Noin, M., Schmülling, T., and Chriqui, D. 2002. Local expression of the ipt gene in transgenic tobacco (Nicotiana tabacum L. cv. SR1) axillary buds establishes a role for cytokinins in tuberization and sink formation. J. Exp. Bot. 53: 621-629.
46. He, P., Osaki, M., Takebe, M., Shinano, T., and Wasaki, J. 2005. Endogenous hormones and expression of senescence-related genes in different senescent types of maize. J. Exp. Bot. 56: 1117-1128.
47. Heyl, A., and Schmülling, T. 2003. Cytokinin signal perception and transduction. Curr. Opin. Plant Biol. 6: 480-488.
48. Higgins, T. J. V., Newbegin, E. J., Spencer, D., Llewellyn, D. J., and Craig, S. 1988. The sequence of a pea vicilin gene and its expression in transgenic tobacco plants. Plant Mol. Biol. 11: 683-695.
49. Higuchi, M., Pischke, M. S., Mahonen, A. P., Miyawaki, K., Hashimoto, Y., Seki, M., Kobayashi, M., Shinozaki, K., Kato, T., Tabata, S., Helariutta, Y., Sussman, M. R., and Kakimoto, T. 2004. In planta functions of the Arabidopsis cytokinin receptor family. Proc. Nat. Acad. Sci. USA 101: 8821-8826.
50. Hirose, N., Makita, N., Kojima, M., Kamada-Nobusada T., and Sakakibara H. 2007. Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol. 48: 523-539.
51. Hirose, N., Takei, K., Kuroha, T., Kamada-Nobusada, T., Hayashi H., and Sakakibara, H. 2008. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 59: 75-83.
52. Houba-Hérin, N., Pethe, C., d'Alayer, J., and Laloue, M. 1999. Cytokinin oxidase from Zea mays: Purification, cDNA cloning and expression in moss protoplasts. Plant J. 17: 615-626.
53. Huynh, L. N., Van Toai, T., Streeter, J., and Banowetz, G. 2005. Regulation of flooding tolerance of SAG12:ipt Arabidopsis plants by cytokinin. J. Exp. Bot. 56: 1397-1407.
54. Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., Taniguchi, M., Kiba, T., Ueguchi, C., Sugiyama, T., and Mizuno, T. 1999. Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol. 40: 733.
55. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K., and Kakimoto, T. 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060-1063.
56. Ishida, K., Yamashino, T., Yokoyama A., and Mizuno, T. 2008. Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant Cell Physiol. 49: 47-57.
57. Jones, R. J., and Schreiber, B. M. N. 1997. Role and function of cytokinin oxidase in plants. Plant Growth Regul. 23: 123-134.
58. Jordi, W., Schapendonk, A., Davelaar, E., Stoopen, G. M., Pot, C. S., De Visser, R., Van Rhijn, J. A., Gan, S., and Amasino, R. M. 2000. Increased cytokinin levels in transgenic P-SAG12-IPT tobacco plants have large direct and indirect effects on leaf senescence, photosynthesis and N partitioning. Plant, Cell Environ. 23: 279-289.
59. Kakimoto, T. 1996. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274: 982-985.
60. Kakimoto, T. 2001. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyl transferases. Plant Cell Physiol. 42: 677-685.
61. Kaminek, M. 1992. Progress in cytokinin research. Trends Biotechnol. 10: 159-164.
62. Kaneyoshi, J., and Kobayashi, S. 1999. Characteristics of transgenic trifoliate orange (Poncirus trifoliata Raf.) possessing the rolC gene of Agrobacterium rhizogenes Ri plasmid. J. Japanese Soc. Horticultural Sci. 68: 734-738.
63. Khodakovskaya, M., Li, Y., Li, J., Vankova, R., Malbeck, J., and McAvoy, R. 2005. Effects of cor15a-IPT gene expression on leaf senescence in transgenic Petunia x hybrida and Dendranthema x grandiflorum. J. Exp. Bot. 56: 1165-1175.
64. Kim, H. J., Ryu, H., Hong, S. H., Woo, H. R., Lim, P. O., Lee, I. C., Sheen, J., Nam, H. G., and Hwang, I. 2006. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc. Nat. Acad. Sci. USA 103: 814-819.
65. Koshita, Y., Nakamura, Y., Kobayashi, S., and Morinaga, K. 2002. Introduction of the rolC gene into the genome of the Japanese persimmon causes dwarfism. J. Japanese Soc. Horticultural Sci. 71: 529-531.
66. Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K., Kojima, M., Nagato, Y., Sakakibara, H., and Kyozuka, J. 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445: 652-655.
67. Lee, D., and Natesan, E. 2006. Evaluating genetic containment strategies for transgenic plants. Trends Biotechnol. 24: 109-114.
68. Letham, D. S. 1963. Zeatin, a factor inducing cell division from Zea mays. Life Sci. 8: 569-573.
69. Letham, D. S., and Palni, L. M. S. 1983. Cytokinin metabolism and biosynthesis. Ann. Rev. Plant Physiol. 34: 163-197.
70. Li, Q., Robson, P. R. H., Bettany, A. J. E., Donnison, I. S., Thomas, H., and Scott, I. M. 2004. Modification of senescence in ryegrass transformed with IPT under the control of a monocot senescence-enhanced promoter. Plant Cell Rep. 22: 816-821.
71. Li, X., Qian, Q., Fu, Z., Wang, Y., Xiong, G., Zeng, D., Wang, X., Liu, X., Teng, S., Hiroshi, F., Yuan, M., Luok, D., Han, B., and Li, J. 2003. Control of tillering in rice. Nature 422: 618-621.
72. Lopez-Bucio J., Millan-Godinez, M., Mendez-Bravo, A., Morquecho-Contreras, A., Ramirez-Chavez, E., Molina-Torres, J., Perez-Torres, A., Higuchi, M., Kakimoto, T., and Herrera-Estrella, L. 2007. Cytokinin receptors are involved in alkamide regulation of root and shoot development in Arabidopsis. Plant Physiol. 145: 1703-1713.
73. Ma, Q. H., Lin, Z. B., and Fu, D. Z. 2002. Increased seed cytokinin levels in transgenic tobacco influence embryo and seedling development. Funct. Plant Biol. 29: 1107-1113.
74. Ma, Q. H., and Song, Y. R. 1993. Genetic engineering of plant hormones. Acta Bot. Sinica. 35: 18-28.
75. Ma, Q. H., and Tian, B. 2005. Characterization of a wheat histidine-containing phosphotransfer protein (HP) that is regulated by cytokinin-mediated inhibition of leaf senescence. Plant Sci. 168: 1507-1514.
76. Ma, Q. H., Wang, X. M., and Wang, Z. M. 2008. Expression of isopentenyl transferase gene controlled by seed-specific lectin promoter in transgenic tobacco influences seed development. J. Plant Growth Regul. 27: 68-76.
77. Ma, Q. H., Zhang, R., Hocart, C. H., Letham, D. S., and Higgins, T. J. V. 1998. Seed-specific expression of the isopentenyl transferase gene (ipt) in transgenic tobacco. Aust. J. Plant Physiol. 25: 53-59.
78. Mahonen, A. P., Bishopp, A., Higuchi, M., Nieminen, K. M., Kinoshita, K., Tormakangas, K., Ikeda, Y., Oka, A., Kakimoto, T., and Helariutta1, Y. 2006. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311: 94-97.
79. McCabe, M. S., Garratt, L., Schepers, F., Jordi, W. J. R. M., Stoopen, G. M., Davelaar, E., van Rhijn, J. H. A., Power, J. B., and Davey, M. 2001. Effects of PSAG12-IPT gene expression on development and senescence in transgenic lettuce. Plant Physiol. 127: 505-516.
80. Martin, R. C., Mok, M. C., Habben, J. E., and Mok, D. W. S. 2001. A maize cytokinin gene encoding an O-glucosyltransferase specific to cis-zeatin. Proc. Nat. Acad. Sci. USA 98: 5922-5926.
81. Martineau, B., Houck, C. M., Sheehy, R. E., and Hiatt, W. R. 1994. Fruit-specific expression of the A. tumefaciens isopentenyl transferase gene in tomato: effects on fruit ripening and defence-related gene expression in leaves. Plant J. 5: 11-19.
82. Martineau, B., Summerfelt, K. R., Adams, D. F., and Deverma, J. W. 1995. Production of high solid tomatoes through molecular modification of levels of the plant growth regulator cytokinin. Bio/Technology 13: 250-254.
83. Massonneau, A., Houba-Herin, N., Pethe, C., Madzak, C., Falque, M., Mercy, M., Kopecny, D., Majira, A., Rogowsky, P., and Laloue, M. 2004. Maize cytokinin oxidase genes: differential expression and cloning of two new cDNAs. J. Exp. Bot. 55: 2549-2557.
84. Matthews, L. J., Morris, R. O., and Blevins, D. G. 1992. Genetic mechanisms for Rhizobium cytokinin biosynthesis, and their relationship to nodule development. Plant Physiol. 99(suppl): 37.
85. Maul, P., Bausher, M., McCollum, G., Mozoruk, J., and Niedz, R. 2006. CsHPt1, a putative histidine-containing phosphotransmitter protein induced during early somatic embryogenesis in Valencia sweet orange. Plant Sci. 170: 44-53.
86. Miller, C. O., Skoog, F., von Saltza, M. H., and Strong, F. 1955. Kinetin, a cell division factor from deoxyribonucleic acid. J. Amer. Chem. Soc. 77: 1392.
87. Mitiouchkina, T. Y., and Dolgov, S. V. 2000. Modification of chrysanthemum flower and plant architecture by rolC gene from Agrobacterium rhizogenes introduction. The 19th International Symposium on Improvement of Ornamental Plants, Acta Horticulturae. 508: 163-169.
88. Miyawaki, K., Tarkowski, P., Matsumoto-Kitano, M., Kato, T., Sato, S., Tarkowska, D., Tabata, S., Sandberg, G., and Kakimoto, T. 2006. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Nat. Acad. Sci. USA 103: 16598-16603.
89. Mok, D. W., and Mok, M. C. 2001. Cytokinin metabolism and action. Annual Review Plant Physiol. Plant Mol. Biol. 52: 89-118.
90. Morris, R. O., Bilyeu, K. D., Laskey, J. G., and Cheikh, N. N. 1999. Isolation of a gene encoding a glycosylated cytokinin oxidase from maize. Biochem. Biophys. Res. Commun. 255: 328-333.
91. Morris, G. C., Mirunalni, T., and Kim, D. 2006. A possible role of cytokinin in mediating long-distance nitrogen signaling in the promotion of sylleptic branching in hybrid poplar. J. Plant Physiol. 163: 684-68.
92. Müller, B., and Sheen, J., 2007. Advances in cytokinin signaling. Science 318: 68-69.
93. Murray, J. D., Karas, B. J., Sato, S., Tabata, S., Amyot, L., and Szczyglowski, K. 2007. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315: 101-104.
94. Nam, H. G. 1997. The molecular genetic analysis of leaf senescence. Curr. Opin. Biotechnol. 8: 200-207.
95. Nilsson, O., Moritz, T., Sundberg, B., Sandberg, G., and Olsson, O. 1996. Expression of the Agrobacterium rhizogenes rolC gene in a deciduous forest tree alters growth and development and leads to stem fasciation. Plant Physiol. 112: 493-502.
96. Nordstrom, A., Tarkowski, P., Tarkowska, D., Norbaek, R., Åstot, C., Dolezal, K., and Sandberg, G. 2004. Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana. A factor of potential importance for auxin-cytokinin-regulated development. Proc. Nat. Acad. Sci. USA 101: 8039-8044.
97. Oh, S. A., Park, J. H., Lee, G. I., Paek, K. H., Park, S. K., and Hong, G. N. 1997. Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 12: 527-535.
98. Oka, A. 2003. Newinsights into cytokinins. J. Plant Res. 116: 217-220.
99. Ongaro V., and Leyser, O. 2008. Hormonal control of shoot branching. J. Exp. Bot. 59: 67-74.
100. Papon, N., Oudin, A., Vansiri, A., Rideau, M., Chénieux, J. C., and Crèche, J. 2003. Differential expression of two type-A response regulators in plants and cell cultures of Catharanthus roseus (L.) G. Don. J. Exp. Bot. 54: 1793-1795.
101. Papon, N., Vansiria, A., Ganteta, P., Chenieux, J. C., Rideau, M., and Creche, J. 2004. Histidine-containing phosphotransfer domain extinction by RNA interference turns off a cytokinin signalling circuitry in Catharanthus roseus suspension cells. FEBS Lett. 558: 85-88.
102. Pepper, A. N., Morse, A. P., and Guinel, F. C. 2007. Abnormal root and nodule vasculature in R50 (sym16), a pea nodulation mutant which accumulates cytokinins. Annals Bot. 99: 765-776.
103. Pogány, M., Koehl, J., Heiser, I., Elstner, E. F., and Barna, B. 2004. Juvenility of tobacco induced by cytokinin gene introduction decreases susceptibility to Tobacco necrosis virus and confers tolerance to oxidative stress. Physiol. Mol. Plant Pathol. 65: 39-47.
104. Popelková, H., Galuszka, P., Frébortová, J., Bilyeu, K. D., and Frébort, I. 2004. Cytokinin dehydrogenase: characterization and structure homology modeling of the flavoprotein catabolizing plant hormones cytokinins. In: Recent Research Developments in Proteins, vol. 2. pp. 63-81. Pandalai, S. G. ed., Transworld Research Network, Kerala, India.
105. Reiser, L., Sanchez-Baracaldo, P., and Hake, S. 2000. Knots in the family tree: evolutionary relationships and functions of knox homeobox genes. Plant Mol. Biol. 42: 151-166.
106. Riefler, M., Novak, O., Strnad, M., and Schmülling, T. 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18: 40-54.
107. Rivero, R. M., Kojima, M., Gepstein, A., Sakakibara, H., Mittler, R., Gepstein, S., and Blumwald, E. 2007. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Nat. Acad. Sci. USA 104: 19631-19636.
108. Robson, P. R. H., Donnison, I. S., Wang, K., Frame, B., Pegg, S. E., Thomas, A., and Thomas, H. 2004. Leaf senescence is delayed in maize expressing the Agrobacterium IPT gene under the control of a novel maize senescence-enhanced promoter. Plant Biotechnol. J. 2: 101-112.
109. Roeckel, P., Oancia, T., and Drevet, J. 1997. Effects of seed-specific expression of a cytokinin biosynthetic gene on canola and tobacco phenotypes. Transgenic Res. 6: 133-141.
110. Rolletschek, H., Hosein, F., Miranda, M., Heim, U., Gotz, K. P., Schlereth, A., Borisjuk, L., Saalbach, I., Wobus, U., and Weber, H. 2005. Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and Pisum sativum increases storage proteins. Plant Physiol. 137: 1236-1249.
111. Sakakibara, H. 2003. Nitrate-specific and cytokinin-mediated nitrogen signaling pathways in plants. J. Plant Res. 116: 253-257.
112. Sakakibara, H., Hayakawa, A., Deji, A., Gawronski, S., and Sugiyama, T. 1999. His-Asp phosphotransfer possibly involved in a nitrogen signal transduction mediated by cytokinin in maize: molecular cloning of cDNAs for two-component regulatory factors and demonstration of phosphotransfer activity in vitro. Plant Mol. Biol. 41: 563-573.
113. Sakakibara, H., Kasahara, H., Ueda, N., Kojima, M., Takei, K., Hishiyama, S., Asami, T., Okada, K., Kamiya, Y., Yamaya, T., and Yamaguchi, S. 2005. Agrobacterium tumefaciens increases cytokinin production in plastids by modifying the biosynthetic pathway in the host plant. Proc. Nat. Acad. Sci. USA 102: 9972-9977.
114. Sakakibara, H., Suzuki, M., Takei, K., Deji, A., Taniguchi, M., and Sugiyama, T. 1998. A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J. 14: 337-344.
115. Sakakibara, H., and Takei, K. 2002. Identification of cytokinin biosynthesis genes in Arabidopsis: A breakthrough for understanding the metabolic pathway and the regulation in higher plants. J. Plant Growth Regul. 21: 17-23.
116. Sakakibara, H., Takei, K., and Hirose, N. 2006. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 11: 440-448.
117. Sakamoto, T., Sakakibara, H., Kojima, M., Yamamoto, Y., Nagasaki, H., Inukai, Y., Sato, Y., and Matsuoka, M. 2006. Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol. 142: 54-62.
118. Sakano, Y., Okada, Y., Matsunaga, A., Suwama, T., Kaneko, T., Ito, K., Noguchi, H., and Abe, I. 2004. Molecular cloning, expression, and characterization of adenylate isopentenyltransferase from hop (Humulus lupulus L.). Phytochemistry 65: 2439-2446.
119. Sheen, J. 2002. Phosphorelay and transcription control in cytokinin signal transduction. Science 296: 1650-1652.
120. Schroeder, H. E. 1984. Effects of applied growth regulators on pod growth and seed protein composition in Pisum sativum L. J. Exp. Bot. 35: 813-821.
121. Schmülling, T., Schell, J., and Spena, A. 1988. Single genes from Agrobacterium rhizogenes influence plant development. EMBO J. 7: 2621-2629.
122. Schwartz, S. H., Qin, X., and Loewen, M. C. 2004. The Biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J. Biol. Chem. 279: 46940-46945.
123. Scorza, R., Zimmerman, T. W., Cordts, J. M., Footen, K. J., and Ravelonandro, M. 1994. Horticultural characteristics of transgenic tobacco expressing the rolC gene from Agrobacterium rhizogenes. J. Amer. Soc. Horticultural Sci. 119: 1091-1098.
124. Stougaard, J. 2000. Regulators and regulation of legume root nodule development. Plant Physiol. 124: 531-540.
125. Suzuki, T., Imamura, A., Ueguchi, C., and Mizuno, T. 1998. Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol. 39: 1258-1268.
126. Suzuki, T., Sakurai, K., Imamura, A., Nakamura, A., Ueguchi, C., and Mizuno, T. 2000. Compilation and characterization of Histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana. Biosci., Biotechnol. Biochem. 64: 2486-2489.
127. Takei, K., Sakakibara, H., and Sugiyama, T. 2001. Identification of genes encoding adenylate isopentenyl-transferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J. Biol. Chem. 276: 26405-26410.
128. Takei, K., Sakakibara, H., Taniguchi, M., and Sugiyama, T. 2001. Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: Implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol. 42: 85-93.
129. Takei, K., Yamaya, T., and Sakakibara, H. 2004. Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J. Biol. Chem. 279: 41866-41872.
130. Takei, K., Ueda, N., Aoki, K., Kuromori, T., Hirayama, T., Shinozaki, K., Yamaya, T., and Sakakibara, H. 2004. AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol. 45: 1053-1062.
131. Taya, Y., Tanaka, Y., and Nishimura, S. 1978. 5′-AMP is a direct precursor of cytokinin in Dictyostelium discoidum. Nature 271: 545-54.
132. Tirichine, L., Sandal, N., Madsen, L. H., Radutoiu, S., Albrektsen, A. S., Sato, S., Asamizu, E., Tabata, S., and Stougaard, J. 2007. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315: 104-107.
133. Tran, L. P., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K., and Yamaguchi-Shinozaki, K. 2007. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Nat. Acad. Sci. USA 104: 20623-20628.
134. Ueguchi, C., Koizumi, H., Suzuki, T., and Mizuno, T. 2001. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 42: 231-235.
135. 14C]adenine into pea fruits. J. Plant Physiol. 141: 380-382.
136. Van Toai, T. T., Saglio, P., Ricard, B., and Pradet, A. 1995. Developmental regulation of anoxic stress tolerance in maize. Plant, Cell Environ. 18: 937-942.
137. Vasil, I. K. 2005. The story of transgenic cereals: the challengen, the debate, and the solution - A historical perspective. In Vitro Plant 41: 577-583.
138. Veach, Y. K., Martin, R. C., Mok, D. W. S., Malbeck, J., Vankova, R., and Mok, M. C. 2003. O-Glucosylation of cis-zeatin in maize. Characterization of genes, enzymes, and endogenous cytokinins. Plant Physiol. 131: 1374-1380.
139. Werner. T., Motyka, V., Laucou, V., Smets, R., Van Onckelen, H., and Schmülling, T. 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15: 2532-2550.
140. Werner, T., Motyka, V., Strnad, M., and Schmülling, T. 2001. Regulation of plant growth by cytokinin. Proc. Nat. Acad. Sci. USA 98: 10487-10492.
141. Winefield, C., Lewis, D., Arathoon, S., and Deroles, S. 1999. Alterations of Petunia plant form through the introduction of the rolC gene from Agrobacterium rhizogenes. Mol. Breed. 5: 543-551.
142. White, F. F., Taylor, B. H., Huffman, G. A., Gordon, M. P., and Nester, E. W. 1985. Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J. Bacteriol. 164: 33-44.
143. Yang, S. H., Yu, H., and Goh, C. J. 2003. Functional characterisation of a cytokinin oxidase gene DSCKX1 in Dendrobium orchid. Plant Mol. Biol. 51: 237-248.
144. Ye, C. J., Wu, S. W., Kong, F. N., Zhou, C. J., Yang, Q. K., Sun, Y., and Wang, B. 2006. Identification and characterization of an isopentenyltransferase (IPT) gene in soybean (Glycine max L.). Plant Sci. 170: 542-550.
145. Yokoyama, A., Yamashino, T., Amano, Y., Tajima, Y., Imamura, A., Sakakibara. H., and Mizuno T. 2007. Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. Plant Cell Physiol. 48: 84-96.
146. Young, T. E., Giesler-Lee, J., and Gallie, D. R. 2004. Senescence-induced expression of cytokinin reverses pistil abortion during maize flower development. Plant J. 38: 910-922.
147. Zhang, J., Van Toai, T., Huynh, L., and Preiszner, J. 2000. Development of flooding-tolerant Arabidopsis thaliana by autoregulated cytokinin production. Mol. Breed. 6: 135-144.
148. Zubko, E., Adams, C. J., Macháèková, I., Malbeck, J., Scollan, C., and Meyer, P. 2002. Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J. 29: 797-808.
149. Zuker, A., Tzfira, T., Scovel, G., Ovadis, M., Shklarman, E., Itzhaki, H., and Vainstein, A. 2001. rolC-transgenic carnation with improved agronomic traits: Quantitative and qualitative analyses of greenhouse-grown plants. J. Amer. Soc. Horticultural Sci. 126:13-18.