Journal of Plant Growth Regulation

, Volume 34, Issue 4, pp 723–739 | Cite as

Tracking the Story of Cytokinin Research

Article

Abstract

Existence of compound(s) inducing cell division in excised plant tissues was spotted more than 100 years ago. Since then research of cytokinins (CKs), plant hormones which in cooperation with other phytohormones, namely auxin, control cytokinesis, and a number of other physiological processes in plants, has advanced correspondingly to the progress in other fields of life sciences. This historical overview is focused on major topics of CK research including (1) discovery of CKs, (2) search for natural CKs, (3) role of CKs in transfer RNA, (4) biosynthesis (5) metabolism, (6) signaling of CKs, and (7) molecular probing of the physiological functions of CKs. Some parts of these subjects can already be assessed within the context of an appropriate time span necessary for critical evaluation. I have used this opportunity to present also some personal recollections, namely those of Prof Folke Skoog, in whose laboratory the first CK, kinetin, was discovered.

Keywords

Cytokinin History Plant hormones t-RNA Cytokinin biosynthesis Cytokinin metabolism 

Notes

Acknowledgments

I would like to thank Prof. DS Letham, Australia, for providing me reprints of his publications and corrections of some parts of the manuscript, to Prof. DJ Armstrong, Oregon State University, Corwallis, Oregon, USA, for critical reading of the manuscript and refining of the English and to Prof. RM Napier, University of Warwick, Coventry, UK for checking the language of the part of the manuscript presenting my personal recollections.

References

  1. Akiyoshi DE, Morris RO, Hinz R, Mischke BS, Kosuge T, Garfinkel DJ, Gordon MP, Nester EW (1983) Cytokinin/auxin balance in grown gall tumors is regulated by specific loci in the T-DNA. Proc Natl Acad Sci USA 80:407–411PubMedCentralPubMedCrossRefGoogle Scholar
  2. Akiyoshi DE, Klee H, Amasino RM, Nestler EW, Gordon MP (1984) T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc Natl Acad Sci USA 81:5994–5998PubMedCentralPubMedCrossRefGoogle Scholar
  3. Akiyoshi DE, Regier DA, Gordon MP (1985) Cloning and nucleotide sequence of the tzs gene from Agrobacterium tumefaciens strain T37. Nucleic Acids Res 13:2773–2788PubMedCentralPubMedCrossRefGoogle Scholar
  4. Amasino R (2005) Kinetin arrives. The 50th anniversary of a new plant hormone. Plant Physiol 138:1177–1184PubMedCentralPubMedCrossRefGoogle Scholar
  5. Armstrong DJ (1994) Cytokinin oxidase and the regulation of cytokinin degradation. In: Mok DWS, Mok MC (eds) Cytokinins—chemistry, activity and function. CRC Press, Boca Raton, pp 139–154Google Scholar
  6. Armstrong DJ (2002) Folke Skoog: in memory and tribute. J Plant Growth Regul 21:3–16PubMedCrossRefGoogle Scholar
  7. Armstrong DJ, Burrows WJ, Skoog F, Roy KL, Söll D (1969) Cytokinins: distribution in transfer RNA species of Escherichia coli. Proc Natl Acad Sci USA 63:834–841PubMedCentralPubMedCrossRefGoogle Scholar
  8. Armstrong DJ, Murai N, Taller BJ, Skoog F (1976) Incorporation of cytokinin N6-benzyladenine into tobacco callus transfer ribonucleic acid and ribosomal ribonucleic acid preparations. Plant Physiol 57:15–22PubMedCentralPubMedCrossRefGoogle Scholar
  9. Astot C, Dolezal K, Nordstrom A, Wang Q, Kunkel T, Moritz T, Chua NH, Sandberg G (2000) An alternative cytokinin biosynthetic pathway. Proc Natl Acad Sci USA 97:14778–14783PubMedCentralPubMedCrossRefGoogle Scholar
  10. Barciszewska M, Kamínek M, Barciszewski J, Wiewiorowski M (1981) Lack of cytokinin activity of Y-type bases isolated from phenylalanine-specific tRNAs. Plant Sci Lett 20:287–392CrossRefGoogle Scholar
  11. Barciszewski J, Siboska GE, Pedersen BO, Clark BFC, Rattan SIS (1996) Evidence for the presence of kinetin in DNA and cell extracts. FEBS Lett 393:197–200PubMedCrossRefGoogle Scholar
  12. Barciszewski J, Siboska EG, Pedersen BO, Clark BFC, Rattan SIS (1997) A mechanism for the in vivo formation of N6-furfuryladenine, kinetin, as a secondary oxidative damage product of DNA. FEBS Lett 414:457–460PubMedCrossRefGoogle Scholar
  13. Barnes MF, Tien CL, Gray JS (1980) Biosynthesis of cytokinins by potato cell cultures. Phytochemistry 19:409–412CrossRefGoogle Scholar
  14. Barry GF, Rogers SG, Fraley RT, Brand L (1984) Identification of a cloned cytokinin biosynthetic gene. Proc Natl Acad Sci USA 81:4776–4780PubMedCentralPubMedCrossRefGoogle Scholar
  15. Beaty JS, Powell GK, Lica L, Regier DA, MacDonald EMS, Hommes NG, Morris RO (1986) Tzs, a nopaline Ti plasmid gene from Agrobacterium tumefaciens associated with trans-zeatin biosynthesis. Mol Gen Genet 203:274–280CrossRefGoogle Scholar
  16. Berridge MV, Ralph RK, Letham DS (1970) The binding of kinetin to plant ribosomes. Biochem J 119:75–84PubMedCentralPubMedCrossRefGoogle Scholar
  17. Bielach A, Duclercq J, Marhavý P, Benková E (2012) Genetic approach towards the identification of auxin and cytokinin crosstalk components involved in root development. Philos T Roy Soc B 367:1469–1478CrossRefGoogle Scholar
  18. Bilyeu KD, Cole JL, Laskey JG, Riekhof WR, Esparza TJ, Kramer MD, Morris RO (2001) Molecular and biochemical characterization of a cytokinin oxidase from maize. Plant Physiol 25:378–386CrossRefGoogle Scholar
  19. Blackwell JR, Horgan R (1994) Cytokinin biosynthesis by extracts of Zea mays. Phytochemistry 35:339–342CrossRefGoogle Scholar
  20. Braun AC (1947) Thermal studies on the factors responsible for tumor initiation in crown-gall. Am J Bot 3:234–240CrossRefGoogle Scholar
  21. Braun AC (1958) A physiological basis for autonomous growth of the crown-gall tumor cell. Proc Natl Acad Sci USA 44:344–349PubMedCentralPubMedCrossRefGoogle Scholar
  22. Braun AC, Laskaris T (1942) Tumor formation by attenuated crown-gall bacteria in the presence of growth-promoting substances. Proc Natl Acad Sci USA 28:468–477PubMedCentralPubMedCrossRefGoogle Scholar
  23. Braun AC, Mandale RJ (1948) Studies on the inactivation of the tumor-inducing principle in crown gall. Growth 12:255–269PubMedGoogle Scholar
  24. Braun AC, White PB (1943) Bacteriological sterility of tissues derived from secondary crown gall tumors. Phytopathology 33:85–100Google Scholar
  25. Brinegar C (1994) Cytokinin binding proteins and receptors. In: Mok DWS, Mok MC (eds) Cytokinins chemistry, activity, and function. CRC Press, Boca Raton, pp 217–232Google Scholar
  26. Brinegar AC, Fox JE (1987) Immunocytological localization of a wheat embryo-cytokinin-binding protein and its homology with proteins in other cereals. In: Klämbt D (ed) Plant hormone receptors, NATO ASI Series H, Cell Biol, vol 10. Springer-Verlag, Berlin, pp 177–184CrossRefGoogle Scholar
  27. Brownlee BG, Hall RH, Whitty CD (1975) 3-Methyl-2-butenal: an enzymatic degradation product of the cytokinin, N 6-(∆2-isopentenyl)adenine. Can J Biochem 53:37–41PubMedCrossRefGoogle Scholar
  28. Bruce MI, Zwar JA (1966) Cytokinin activity of some substituted ureas and thioureas. Proc R Soc Lond B Biol 165:245–265CrossRefGoogle Scholar
  29. Carlson BA, Kwon SY, Chamorro M, Oroszlan S, Hatfield DL, Lee BJ (1999) Transfer RNA modification status influences retroviral frameshifting. Virology 255:2–8PubMedCrossRefGoogle Scholar
  30. Cebalo T, Letham DS (1967) Synthesis of zeatin a factor inducing cell division. Nature 213:86CrossRefGoogle Scholar
  31. Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544PubMedCrossRefGoogle Scholar
  32. Chatfield JM, Armstrong DJ (1986) Regulation of cytokinin oxidase activity in callus tissues of Phaseolus vulgaris L. cv Great Northern. Plant Physiol 80:493–499PubMedCentralPubMedCrossRefGoogle Scholar
  33. Chatfield JM, Armstrong DJ (1988) Cytokinin oxidase from Phaseolus vulgaris callus culture. Affinity for concavalin-A. Plant Physiol 88:245–247Google Scholar
  34. Chen C-M, Hall RH (1969) Biosynthesis of N 6-( 2-isopentenyl)adenosine in the transfer ribonucleic acid of cultured tobacco pith tissue. Phytochemistry 8:1687–1695CrossRefGoogle Scholar
  35. Chen C-M, Melitz DK (1979) Cytokinin biosynthesis in cell-free system from cytokinin-autonomous tobacco tissue cultures. FEBS Lett 107:15–20PubMedCrossRefGoogle Scholar
  36. Chen C-M, Petschow B (1978) Cytokinin biosynthesis in cultured rootless tobacco plants. Plant Physiol 62:861–865PubMedCentralPubMedCrossRefGoogle Scholar
  37. Chilton MD, Drummond MH, Merio DJ, Sciaky D, Montoya AL, Gordon MP, Nestler EW (1977) Cell 11:263–271PubMedCrossRefGoogle Scholar
  38. Czerwoniec A, Dunin-Horkawicz S, Purta E, Kaminska KH, Kasprzak JM, Bujnicki JM, Grosjean H, Rother K (2009) MODOMICS: a database of RNA modification pathways. 2008 update. Nucleic Acids Res 37:D118–D121PubMedCentralPubMedCrossRefGoogle Scholar
  39. Dickinson JR, Forsyth C, Van Staden J (1986) The role of adenine in the synthesis of cytokinins in tomato plants and cell-free root extracts. Plant Growth Regul 4:325–334CrossRefGoogle Scholar
  40. Dietrich JT, Kaminek M, Blevins DG, Reinbott TM, Morris RO (1995) Changes in cytokinins and cytokinin oxidase activity in developing maize kernels and the effects of exogenous cytokinins on kernel development. Plant Physiol Biochem 33:327–336Google Scholar
  41. Edwards CA, Armstrong DJ (1981) Cytokinin-active ribonucleosides in Phasoleus RNA. Plant Physiol 67:1185–1189PubMedCentralPubMedCrossRefGoogle Scholar
  42. Erion JL, Fox E (1981) Purification and properties of a protein which binds cytokinin-active 6-substituted purines. Plant Physiol 67:156–162PubMedCentralPubMedCrossRefGoogle Scholar
  43. Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525PubMedCrossRefGoogle Scholar
  44. Firn RD (1987) Too many binding proteins, not enough receptors. In: Plant hormone receptors, NATO ASI Series H, Cell Biology, Vol 10, p. 1, Springer-Verlag, BerlinGoogle Scholar
  45. Fittler F, Kline LK, Hall RH (1968) N6-(∆2-isopentenyl)adenosine: biosynthesis in vitro by an enzyme extract from yeast and rat liver. Biochem Biophys Res Commun 31:541–576Google Scholar
  46. Fox JE (1965) Incorporation of a kinin, N,6-benzyladenine into soluble RNA. Plant Physiol 41:75–82CrossRefGoogle Scholar
  47. Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452PubMedCrossRefGoogle Scholar
  48. Frébortová J, Fraaije MW, Galuszka P, Šebela M, Peč P, Hrbáč J, Novák O, Bilyeu KD, English JT, Frébort I (2004) Catalytic reaction of cytokinin dehydrogenase: preference for quinones as electron acceptors. Biochem J 380:121–130PubMedCentralPubMedCrossRefGoogle Scholar
  49. Gajdošová S, Spíchal L, Kamínek M, Hoyerová K, Novák O, Dobrev PI, Galuszka P, Klíma P, Gaudinová A, Žižková E, Hanuš J, Dančák M, Trávníček B, Pešek B, Krupička M, Vaňková R, Strnad M, Motyka V (2011) Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J Exp Bot 62:2827–2840PubMedCrossRefGoogle Scholar
  50. Galuszka P, Spíchal L, Kopečný D, Tarkowski P, Frébortová J, Šebela M, Frébort I (2008) Metabolism of plant hormones cytokinins and their functions in signaling, cell differentiation and plant development. In: Atta-ur-Rahman (ed) Studies in Natural Products Chemistry 34:203-264. Elsevier, AmsterdamGoogle Scholar
  51. Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988PubMedCrossRefGoogle Scholar
  52. Garfinkel DJ, Simpson RB, Ream LW, White FF, Gordon MP, Nestler EW (1981) Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell 27:143–153PubMedCrossRefGoogle Scholar
  53. Ge L, Yong JWH, Goh NK, Chia LS, Tan SN, Ong ES (2005) Identification of kinetin and kinetin riboside in coconut (Cocos nucifera L.) water using a combined approach of liquid chromatography-tandem mass spectrometry, high performance liquid chromatography and capillary electrophoresis. J Chromatogr B 829:26–34CrossRefGoogle Scholar
  54. Gefter ML, Russell RL (1969) Role of modifications in tyrosine transfer RNA—a modified base affecting ribosome binding. J Mol Biol 39:145–157PubMedCrossRefGoogle Scholar
  55. Gruhn N, Halawa M, Snel B, Seidl MF, Heyl A (2014) A subfamily of putative cytokinin receptors is revealed by an analysis of the evolution of the two-component signaling system in plants. Plant Physiol 165:227–237PubMedCentralPubMedCrossRefGoogle Scholar
  56. Gupta D, Bhargava S (2001) Thidiazuron induced regeneration in Cuminum cyminum L. J Plant Biochem Biot 10:61–62CrossRefGoogle Scholar
  57. Haberlandt G (1913) Zur Physiologie der Zellteilung. Sitzungsberichte der Königlich Preussischen Akademie der Wissenschaften, Berlin Phys Math Klasse 318–345Google Scholar
  58. Hall RH (1973) Cytokinins as a probe of developmental processes. Ann Rev Plant Physiol 24:415–444CrossRefGoogle Scholar
  59. Hall RH, De Ropp RS (1955) Formation of 6-furfurylaminopurine from DNA breakdown products. J Am Chem Soc 77:6400CrossRefGoogle Scholar
  60. Hall RH, Robins MJ, Stasiuk L, Thedford R (1966) Isolation of N6-(γ, γ -dimethylallyl)adenosine from soluble ribonucleic acid. J Am Chem Soc 88:2614–2618CrossRefGoogle Scholar
  61. Hall RH, Csonka L, David H, McLennan B (1967) Cytokinins in the soluble RNA of plant tissues. Science 156:69–71PubMedCrossRefGoogle Scholar
  62. Hamzi HQ, Skoog F (1964) Kinetin-like growth-promoting activity of 1-substituted adenines [1-benzyl-6-aminopurine and 1-(gama, gama-dimethylallyl)-6-aminopurine]. Proc Natl Acad Sci USA 51:76–83PubMedCentralPubMedCrossRefGoogle Scholar
  63. Hare PD, Van Staden J (1994) Cytokinin oxidase: biochemical features and physiological significance. Physiol Plantarum 91:128–136CrossRefGoogle Scholar
  64. Hejátko J, Ryu H, Kim G-T, Dobešová R, Choi S, Choi S-M, Souček P, Horák J, Pekárková B, Palme K, Brzobohatý B, Hwang I (2009) The histidine kinases CYTOKNIN-INDEPENDENT and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell 21:2008–2021PubMedCentralPubMedCrossRefGoogle Scholar
  65. Holland MA (1997) Occam’s razor applied to hormonology. Plant Physiol 115:865–868PubMedCentralPubMedGoogle Scholar
  66. Holley RW, Everett GA, Madison JT, Zamir A (1965) Nucleotide sequences in the yeast alanine transfer ribonucleic acid. J Am Chem Soc 240:2122–2128Google Scholar
  67. Holtz J, Klämbt D (1978) tRNA-Isopentenyltransferase fromZea mays L. Characterization of the isopentenylation reaction of tRNA, oligo(A) and other nucleic acids. H-S Z Physiol Chem 359:89–101Google Scholar
  68. Horgan R, Hewett EW, Purse J, Wareing PF (1973) A new cytokinin from Populus robusta. Tetrahedron Lett 30:2827–2828CrossRefGoogle Scholar
  69. Hothorn M, Dabi T, Chory J (2011) Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat Chem Biol 7:766–768PubMedCentralPubMedCrossRefGoogle Scholar
  70. Houba-Hérin N, Pethe C, d’Alayer J, Laloule M (1999) Cytokinin oxidase from Zea mays: purification, cDNA cloning and expression in moss protoplasts. Plant J 17:615–626PubMedCrossRefGoogle Scholar
  71. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063PubMedCrossRefGoogle Scholar
  72. Jacobs WP (1979) Plant hormones and plant development. Cambridge University Press, LondonGoogle Scholar
  73. Jordi W, Schapendonk A, Davelaar E, Stoopen GM, Pot CS, De Visser R, Van Rhijn JA, Gan S, Amasino RM (2000) Increased cytokinin levels in transgenic PSAG12-IPT tobacco plants have large direct and indirect effects on leaf senescence, photosynthesis and N partitioning. Plant, Cell Environ 23:279–289CrossRefGoogle Scholar
  74. Kado CI (2014) Historical account of gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens. Front Microbiol. doi:10.3389/fmicb.2014.00340 PubMedCentralPubMedGoogle Scholar
  75. Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982–985PubMedCrossRefGoogle Scholar
  76. Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685PubMedCrossRefGoogle Scholar
  77. Kakimoto T (2003a) Biosynthesis of cytokinins. J Plant Res 116:233–239PubMedCrossRefGoogle Scholar
  78. Kakimoto T (2003b) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54:605–627PubMedCrossRefGoogle Scholar
  79. Kaminek M (1975) Die Zytokinine and ihre Beziehungen zu den Transfer-Ribonucleinsäuren. Biologische Rundschau 13:137–152Google Scholar
  80. Kamínek M (1974) Evolution of tRNA and origin of two positional isomers of zeatin. J Theor Biol 48:489–492PubMedCrossRefGoogle Scholar
  81. Kamínek M (1982) Mechanisms preventing the interference of tRNA cytokinins in hormonal regulation. In: Wareing PF (ed) Plant Growth Substances 1982. Academic Press, London, pp 215–224Google Scholar
  82. Kamínek M, Armstrong DJ (1990) Genotypic variation in cytokinin oxidase from Phasoleus callus cultures. Plant Physiol 93:1530–1538PubMedCentralPubMedCrossRefGoogle Scholar
  83. Kamínek M, Pačes V, Corse J, Challice JS (1979) Effects of stereospecific hydroxylation of N6-(Δ2-isopentenyl)adenosine on cytokinin activity. Planta 145:239–243PubMedCrossRefGoogle Scholar
  84. Kamínek M, Vaněk T, Motyka V (1987) Cytokinin activities of N 6-benzyladenosine derivatives hydroxylated on the side-chain phenyl ring. J Plant Growth Regul 6:113–120CrossRefGoogle Scholar
  85. Kamínek M, Trčková M, Fox JE, Gaudinová A (2003) Comparison of cytokinin-binding proteins from wheat and oat grains. Physiol Plantarum 117:453–458CrossRefGoogle Scholar
  86. Kende H (1971) The cytokinins. Ann Rev Cytol 31:301–338CrossRefGoogle Scholar
  87. Kline LK, Fittler F, Hall RH (1969) N6-(Δ2-isopentenyl)adenosine. Biosynthesis in transfer ribonucleic acid in vitro. Biochemistry 8:4361–4371PubMedCrossRefGoogle Scholar
  88. Kobayashi H, Morisaki N, Tago Y, Hashimoto Y, Iwasaki S, Kawachi E, Nagata R, Shudo K (1995) Identification of a major cytokinin in coconut milk. Experientia 51:1081–1084PubMedCrossRefGoogle Scholar
  89. Kögl F, Erxleben H, Haagen-Smit AJ (1933) Über ein Phytohomon der Zellstreckung. Zur Chemie des krystallisierten Auxins. V. Mitteilung. Zeitschift für Physiologische Chemie 216:31–46CrossRefGoogle Scholar
  90. Kögl F, Haagen-Smit AJ, Erxleben H (1934) Über eines neues Auxin („Heteroauxin“) aus Harn. XI. Mitteilung. Zeitschift für Physiologische Chemie 228:90–103CrossRefGoogle Scholar
  91. Laloue M, Pethe C (1982) Dynamics of cytokinin metabolism in tobacco cells. In: Wareing PF (ed) Plant Growth Substances 1982. Academic Press, London, pp 185–195Google Scholar
  92. Letham DS (1958) Cultivation of apple fruit tissues in vitro. Nature 182:473–474CrossRefGoogle Scholar
  93. Letham DS (1963a) Regulators of cell division in plant tissues. New Zeal J Bot 1:336–350CrossRefGoogle Scholar
  94. Letham DS (1963b) Purification of factors inducing cell division extracted from plum fruitlets. Life Sci 2:152–157CrossRefGoogle Scholar
  95. Letham DS (1963c) Zeatin, a factor inducing cell division isolated from Zea mays. Life Sci 8:569–573PubMedCrossRefGoogle Scholar
  96. Letham DS (1966) Regulators of cell division in plant tissues II. A cytokinin in plant extracts. Phytochemistry 5:269–286CrossRefGoogle Scholar
  97. Letham DS (1974) Regulators of cell division in plant tissues. XX. The cytokinins of coconut milk. Physiol Plantarum 32:66–70CrossRefGoogle Scholar
  98. Letham DS (1999) Cytokinins and plant growth. In: Hogan D, Williamson B (eds) New Zealand is different. Clerestory Press, New Zealand, pp 161–167Google Scholar
  99. Letham DS, Bollard EG (1961) Stimulants of cell division in developing fruits. Nature 191:1119–1120PubMedCrossRefGoogle Scholar
  100. Letham DS, Miller CO (1965) Identity of kinetin-like factors from Zea mays. Plant Cell Physiol 6:355–359Google Scholar
  101. Letham DS, Palni LMS (1983) The biosynthesis and metabolism of cytokinins. Annu Rev Plant Physiol 34:163–197CrossRefGoogle Scholar
  102. Letham DS, Ralph RK (1967) A cytokinin in soluble RNA from a higher plant. Life Sci 6:387–394PubMedCrossRefGoogle Scholar
  103. Letham DS, Shannon JS, McDonald IRC (1964) Structure of zeatin, a factor inducing cell division. Proc Chem Soc Lond, July issue, pp 230–261Google Scholar
  104. Lindner A-C, Lang D, Seifert M, Podlešáková K, Novák O, Strnad M, Reski R, von Schwartzenberg K (2014) Isopentenyltransferase-1 (IPT1) knockout in Physcomitrella together with phylogenetic analyses of IPTs provide insights into evolution of plant cytokinin biosynthesis. J Expt Bot 65:2533–2543CrossRefGoogle Scholar
  105. Link GKK, Eggers V (1941) Hyperauxiny in crown gall of tomato—contributions from the hull botanical laboratory. Bot Gaz 103:87–106CrossRefGoogle Scholar
  106. Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plantarum 18:100–127CrossRefGoogle Scholar
  107. Lomin SN, Yonekura-Sakakibara K, Romanov GA, Sakakibara H (2011) Lingand-binding properties and subcellular localization of maize cytokinin receptors. J Exp Bot 62:5149–51159PubMedCentralPubMedCrossRefGoogle Scholar
  108. Lomin SN, Krivosheev DM, Steklov MYu, Arkhipov DV, Osolodkin DI, Schmülling T, Romanov GA (2015) Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands. J Exp Bot. doi:10.1093/jxb/eru522 PubMedCentralPubMedGoogle Scholar
  109. Marhavý P, Duclercq J, Weller B, Feraru E, Bielach A, Offriga R, Friml J, Schwechheimer C, Murphy A, Benková E (2014) Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Current Biol 24:1031–1037CrossRefGoogle Scholar
  110. Martin D, Lewis TL, Cerny J (1954) The physiology of growth in apple fruits. 7. Between tree variation of cell physiology in relation to disorder incidence. Aust J Biol Sci 7:211–220PubMedGoogle Scholar
  111. Matand K, Prakash CS (2007) Evaluation of peanut genotypes for in vitro plant regeneration using thidiazuron. J Biotechnol 30:202–207CrossRefGoogle Scholar
  112. McLennan BD (1975) Enzymatic demodification of transfer RNA species containing N6-(∆2-isopentenyl)adenosine. Biochem Biophys Res Commun 65:345–351CrossRefGoogle Scholar
  113. Ménagé A, Morel G (1964) Sur la presence d’octopine dans les tissus de crown-gall. C R Acad Sci Paris 259:4795–4796PubMedGoogle Scholar
  114. Miller CO (1961) Kinetin-like compound in maize. Proc Natl Acad Sci USA 47:170–174PubMedCentralPubMedCrossRefGoogle Scholar
  115. Miller CO (1965) Evidence for the natural occurrence of zeatin and derivatives: compounds from maize which promote cell division. Proc Natl Acad Sci USA 54:1052–1058PubMedCentralPubMedCrossRefGoogle Scholar
  116. Miller CO, Skoog F, von Saltza M, Strong FM (1955a) Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77:1392CrossRefGoogle Scholar
  117. Miller CO, Skoog F, von Saltza MH, Okumura FS, Strong FM (1955b) Structure and synthesis of kinetin. J Am Chem Soc 77:2662CrossRefGoogle Scholar
  118. Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103:16598–16603PubMedCentralPubMedCrossRefGoogle Scholar
  119. Mok MC (1994) Cytokinins and plant development—an overview. In: Mok DWS, Mok MC (eds) Cytokinins—chemistry, activity, and function. CRC Press, Boca Raton, pp 155–166Google Scholar
  120. Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118PubMedCrossRefGoogle Scholar
  121. Morris RO (1986) Genes specifying auxin and cytokinin biosynthesis in phytopahogens. Annu Rev Plant Physiol 37:509–538CrossRefGoogle Scholar
  122. Morris RO, Blevins DG, Dietrich JT, Durley RC, Gelvin SB, Gray J, Hommes NG, Kaminek M, Mathesius U, Meilan R, Reinbott TM, Sayavedra-Soto I (1993) Cytokinin in plant pathogenic bacteria and developing cereal grains. Aust J Plant Physiol 20:621–637CrossRefGoogle Scholar
  123. Morris RO, Bilyeu KD, Laskey JG, Cheikh NN (1999) Isolation of a gene encoding a glycosylated cytokinin oxidase from maize. Biochem Biophys Res Co 255:328–333CrossRefGoogle Scholar
  124. Motyka V, Faiss M, Strnad M, Kamínek M, Schmülling T (1996) Changes in the cytokinin content and cytokinin oxidase activity in response to derepression of ipt gene transcription in transgenic tobacco calli and plants. Plant Physiol 112:1035–1043PubMedCentralPubMedGoogle Scholar
  125. Motyka V, Vaňková R, Čapková V, Petrášek J, Kamínek M, Schmülling T (2003) Cytokinin-induced upregulation of cytokinin oxidase activity in tobacco includes changes in enzyme glycosylation and secretion. Physiol Plantarum 117:11–21CrossRefGoogle Scholar
  126. Murai N (1994) Cytokinin biosynthesis in tRNA and cytokinin incorporation into plant RNA. In: Mok DWS, Mok MC (eds) Cytokinins—chemistry, activity, and function. CRC Press, Boca Raton, pp 87–100Google Scholar
  127. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 18:100–127Google Scholar
  128. Naylor J, Sander G, Skoog F (1954) Mitosis and cell enlargement without cell division in excised tobacco pith tissue. Physiol Plant 7:25–29CrossRefGoogle Scholar
  129. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Genetic analysis of Arabidopsis histidine kinase genes encoding cytokinin receptors reveals their overlapping biological functions in the regulation of shoot and root growth. Plant Cell 16:1365–1377PubMedCentralPubMedCrossRefGoogle Scholar
  130. Nishinari N, Syono K (1980) Cell-free biosynthesis of cytokinins in cultured tobacco cells. Z Pflanzenphysiol 99:383–392CrossRefGoogle Scholar
  131. Nomura T, Tanakat Y, Abe H, Uchiyama M (1977) Cytokinin activity of discadenine: a spore germination inhibitor of Dictyostelium discoideum. Phytochemistry 16:1819–1820CrossRefGoogle Scholar
  132. Pačes V, Werdstiuk E, Hall RH (1971) Conversion of N 6-(∆2-isopentenyl)adenosine to adenosine by enzyme activity in tobacco tissue. Plant Physiol 48:775–778PubMedCentralPubMedCrossRefGoogle Scholar
  133. Parker CW, Letham DS (1973) Regulators of cell division in plant tissues. XVI Metabolism of zeatin by radish cotyledons and hypocotyls. Planta 114:199–218PubMedCrossRefGoogle Scholar
  134. Parker CW, Cowley DE, Letham DS, MacLeod JK (1972) Raphanatin, an unusual purine derivative and a metabolite of zeatin. Biochem Biophys Res Commun 49:460–466PubMedCrossRefGoogle Scholar
  135. Parker CW, Wilson MM, Letham DS, Cowley DE, MacLeod JK (1973) The glucosylation of cytokinins. Biochem Biophys Res Co 55:1370–1376CrossRefGoogle Scholar
  136. Parker CW, Letham DS, Gollnow BI, Summons RE, Duke CC, MacLeod JK (1978) Regulators of cell division in plant tissues. XXV. Metabolism of zeatin by lupin seedlings. Planta 142:239–251PubMedCrossRefGoogle Scholar
  137. Persson BC, Esberg B, Ólavsson Ó, Bjōrk GR (1994) Synthesis and function of isopentenyl adenosine derivatives in tRNA. Biochimie 76:1152–1160CrossRefGoogle Scholar
  138. Peterkofsky A (1968) Incorporation of mevalonic acid into the N6-(Δ2-isopentenyl)adenosine of transfer ribonucleic acid in. Biochemistry 7:472–482PubMedCrossRefGoogle Scholar
  139. Pils B, Heyl A (2009) Unraveling the evolution of cytokinin signalling. Plant Physiol 151:782–791PubMedCentralPubMedCrossRefGoogle Scholar
  140. Romanov GA (2011) The discovery of cytokinin receptors and biosynthesis of cytokinins: a true story. Russ J Plant Physiol 58:743–747CrossRefGoogle Scholar
  141. Sakakibara H, Kasahara H, Ueda N, Kojima M, Takei K, Hishiyama S, Asami T, Okada K, Kamiya Y, Yamaya T, Ymaguchi S (2005) Agrobacterium tumefaciens increases cytokinin production in plastids by modifying the biosynthetic pathway in the host plant. Proc Natl Acad Sci USA 102:9972–9977PubMedCentralPubMedCrossRefGoogle Scholar
  142. Schmitz RY, Skoog F, Playtis AJ, Leonard NJ (1972) Cytokinins: synthesis and biological activity of geometric and positional isomers of zeatin. Plant Physiol 50:702–705PubMedCentralPubMedCrossRefGoogle Scholar
  143. Shantz EM, Steward FC (1955) The identification of compound A from coconut milk as 1,3-diphenylurea. J Amer Chem Soc 77:6351–6353CrossRefGoogle Scholar
  144. Shaw G, Smallwood BM, Wilson DV (1966) Purines, pyrimidines and imidazoles. 24. Synthesis of zeatin a naturally occurring adenine derivative with plant cell division promoting activity and its 9-β-D ribofuranoside. J Chem Soc C 10:921CrossRefGoogle Scholar
  145. Skoog F (1994) A personal history of cytokinin and plant hormones research. In: Mok WS, Mok MD (eds) Cytokinins—chemistry, activity and function. CRC Press, Boca Raton, pp 1–14Google Scholar
  146. Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. No XI, Biological action of growth substances. Symp Soc Exp Biol 11:118–131PubMedGoogle Scholar
  147. Skoog F, Tsui C (1951) Growth substances and the formation of buds in plant tissues. In: Skoog F (ed) Plant Growth Substances. University of Wisconsin Press, Madison, pp 263–285Google Scholar
  148. Smith EF, Townsend CO (1907) A plant tumor of bacterial origin. Science 25:671–673PubMedCrossRefGoogle Scholar
  149. Sondheimer E, Tzou D-S (1971) The metabolism of hormones during seed germination and dormancy. II. The metabolism of 8-14C-zeatin in bean axes. Plant Physiol 47:516–520PubMedCentralPubMedCrossRefGoogle Scholar
  150. Spíchal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Strnad M, Schmülling T (2004) Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol 45:1299–1305PubMedCrossRefGoogle Scholar
  151. Starling EH (1905) The Crotonian Lectures, I. On chemical correlation of the functions of the body. Lancet 166:339–341CrossRefGoogle Scholar
  152. Strnad M (1997) The aromatic cytokinins. Physiol Plantarum 101:674–688CrossRefGoogle Scholar
  153. Strnad M, Hanuš J, Vaněk T, Kamínek M, Ballantine JA, Fussell B, Hanke DE (1997) meta-Topolin, a highly active aromatic cytokinin from poplar leaves (Populus x canadensis Moech., cv. Robusta). Phytochemistry 45:213–218CrossRefGoogle Scholar
  154. Struxness LA, Armstrong DJ, Gillam I, Tener GM, Burrows WJ, Skoog F (1979) Distribution of cytokinin-active ribonuclesides in wheat germ tRNA species. Plant Physiol 63:35–41PubMedCentralPubMedCrossRefGoogle Scholar
  155. Sýkorová B, Kurešová G, Daskalova S, Trčková M, Hoyerová K, Raimanová I, Motyka V, Trávníčková A, Elliott MC, Kamínek M (2008) Senescence-induced ectopic expression of A. tumefaciens ipt gene in wheat delays leaf senescence, increases cytokinin content, nitrate influx and nitrate reductase activity but does not affect grain yield. J Exp Bot 59:377–387PubMedCrossRefGoogle Scholar
  156. Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thalinana. J Biol Chem 276:26405–26410PubMedCrossRefGoogle Scholar
  157. Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyse the biosynthesis of trans-zeatin. J Biol Chem 279:41866–41872PubMedCrossRefGoogle Scholar
  158. Taller BJ (1994) Distribution, biosynthesis, and function of cytokinins in tRNA. In: Mok DWS, Mok MC (eds) Cytokinins—chemistry, activity and function. CRC Press, Boca Raton, pp 101–112Google Scholar
  159. Taya Y, Tanaka Y, Nishimura S (1978) 5′-AMP is a direct precursor of cytokinin in Dictyostelium discoideum. Nature 271:545–547PubMedCrossRefGoogle Scholar
  160. Terrine C, Laloule M (1980) Kinetics of N6-(∆2-isopentenyl)adenosine degradation in tobacco cells. Plant Physiol 65:1090–1095PubMedCentralPubMedCrossRefGoogle Scholar
  161. Van Overbeek J, Conklin ME, Blakeslee AF (1941) Factors in coconut milk essential for growth and development of very young datura embryos. Science 94:350–351CrossRefGoogle Scholar
  162. Wang C, Liu Y, Li S-S, Han G-Z (2015) Insights into the origin and evolution of the plant hormone signalling machinery. Plant Physiol 167:872–886PubMedCrossRefGoogle Scholar
  163. Went FW, Thimann KV (1937) Phytohormones. MacMillan Co, New York, pp 7–8Google Scholar
  164. Werner T, Holst K, Pörs Y, Guivarc’h A, Mustroph A, Chriqui D, Grimm B, Schmülling T (2008) Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots. J Exp Bot 59:2659–2672PubMedCentralPubMedCrossRefGoogle Scholar
  165. White PR (1943) Nutrient deficiency studies and improved inorganic nutrient medium for cultivation of of excised tomato roots. Growth 7:53Google Scholar
  166. White PR, Braun AC (1941) Crown gall production by bacteria-free tumor tissues. Science 94:239–241PubMedCrossRefGoogle Scholar
  167. White PR, Braun AC (1942) A cancerous neoplasm of plants-autonomous bacteria-free crown-gall tissue. Cancer Res 2:597–617Google Scholar
  168. Whitty CD, Hall RH (1974) A cytokinin oxidase in Zea mays. Can J Biochem 52:789–799PubMedCrossRefGoogle Scholar
  169. Yadav NS, Postle K, Saiki RK, Thomashow MF, Chilton M-D (1980) T-DNA of a crown gall teratoma is covalently joined to host plant DNA. Nature 287:458–461PubMedCrossRefGoogle Scholar
  170. Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023PubMedCrossRefGoogle Scholar
  171. Yonekura-Sakakibara K, Kojima M, Yamaya T, Sakakibara H (2004) Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol 134:1654–1661PubMedCentralPubMedCrossRefGoogle Scholar
  172. Young AP, Bandarian V (2013) Radical mediated ring formation in the biosynthesis of the hypermodified tRNA base wybutosine. Curr Opin Chem Biol 17:613–618PubMedCentralPubMedCrossRefGoogle Scholar
  173. Zachau HG, Dütting D, Feldmann H (1966) The structures of two serine transfer ribonucleic acids. Hoppe-Seylers Zeit Physiol Chem 347:212–235CrossRefGoogle Scholar
  174. Zaenen I, van Larebeke N, Teuchy H, van Montagu M, Schell J (1974) Supercoiled circular DNA in crown-gall inducing Agrobacterium strains. J Mol Biol 86:109–127PubMedCrossRefGoogle Scholar
  175. Zambryski P, Holsters M, Kruger K, Depicker A, Schell J, Van Montagu M, Goodman HM (1980) Tumor DNA structure in plant cells transformed by A. tumefaciens. Science 209:1385–1391PubMedCrossRefGoogle Scholar
  176. Zambryski P, Joos H, Genetello C, Leemans J, Van Montagu M, Shell J (1983) Ti plasmid vector for the induction of DNA into plant cells without alternation of their normal regeneration capacity. EMBO J 2:2143–2150PubMedCentralPubMedGoogle Scholar

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Institute of Experimental BotanyAcademy of Sciences of the Czech RepublicPrague 6Czech Republic

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