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.
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References
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 80:407–411
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 81:5994–5998
Akiyoshi DE, Regier DA, Gordon MP (1985) Cloning and nucleotide sequence of the tzs gene from Agrobacterium tumefaciens strain T37. Nucleic Acids Res 13:2773–2788
Amasino R (2005) Kinetin arrives. The 50th anniversary of a new plant hormone. Plant Physiol 138:1177–1184
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 139–154
Armstrong DJ (2002) Folke Skoog: in memory and tribute. J Plant Growth Regul 21:3–16
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 63:834–841
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 57:15–22
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 97:14778–14783
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 20:287–392
Barciszewski J, Siboska GE, Pedersen BO, Clark BFC, Rattan SIS (1996) Evidence for the presence of kinetin in DNA and cell extracts. FEBS Lett 393:197–200
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 414:457–460
Barnes MF, Tien CL, Gray JS (1980) Biosynthesis of cytokinins by potato cell cultures. Phytochemistry 19:409–412
Barry GF, Rogers SG, Fraley RT, Brand L (1984) Identification of a cloned cytokinin biosynthetic gene. Proc Natl Acad Sci USA 81:4776–4780
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 203:274–280
Berridge MV, Ralph RK, Letham DS (1970) The binding of kinetin to plant ribosomes. Biochem J 119:75–84
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 367:1469–1478
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 25:378–386
Blackwell JR, Horgan R (1994) Cytokinin biosynthesis by extracts of Zea mays. Phytochemistry 35:339–342
Braun AC (1947) Thermal studies on the factors responsible for tumor initiation in crown-gall. Am J Bot 3:234–240
Braun AC (1958) A physiological basis for autonomous growth of the crown-gall tumor cell. Proc Natl Acad Sci USA 44:344–349
Braun AC, Laskaris T (1942) Tumor formation by attenuated crown-gall bacteria in the presence of growth-promoting substances. Proc Natl Acad Sci USA 28:468–477
Braun AC, Mandale RJ (1948) Studies on the inactivation of the tumor-inducing principle in crown gall. Growth 12:255–269
Braun AC, White PB (1943) Bacteriological sterility of tissues derived from secondary crown gall tumors. Phytopathology 33:85–100
Brinegar C (1994) Cytokinin binding proteins and receptors. In: Mok DWS, Mok MC (eds) Cytokinins chemistry, activity, and function. CRC Press, Boca Raton, pp 217–232
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 177–184
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 53:37–41
Bruce MI, Zwar JA (1966) Cytokinin activity of some substituted ureas and thioureas. Proc R Soc Lond B Biol 165:245–265
Carlson BA, Kwon SY, Chamorro M, Oroszlan S, Hatfield DL, Lee BJ (1999) Transfer RNA modification status influences retroviral frameshifting. Virology 255:2–8
Cebalo T, Letham DS (1967) Synthesis of zeatin a factor inducing cell division. Nature 213:86
Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544
Chatfield JM, Armstrong DJ (1986) Regulation of cytokinin oxidase activity in callus tissues of Phaseolus vulgaris L. cv Great Northern. Plant Physiol 80:493–499
Chatfield JM, Armstrong DJ (1988) Cytokinin oxidase from Phaseolus vulgaris callus culture. Affinity for concavalin-A. Plant Physiol 88:245–247
Chen C-M, Hall RH (1969) Biosynthesis of N 6-(∆ 2-isopentenyl)adenosine in the transfer ribonucleic acid of cultured tobacco pith tissue. Phytochemistry 8:1687–1695
Chen C-M, Melitz DK (1979) Cytokinin biosynthesis in cell-free system from cytokinin-autonomous tobacco tissue cultures. FEBS Lett 107:15–20
Chen C-M, Petschow B (1978) Cytokinin biosynthesis in cultured rootless tobacco plants. Plant Physiol 62:861–865
Chilton MD, Drummond MH, Merio DJ, Sciaky D, Montoya AL, Gordon MP, Nestler EW (1977) Cell 11:263–271
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–D121
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 4:325–334
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 33:327–336
Edwards CA, Armstrong DJ (1981) Cytokinin-active ribonucleosides in Phasoleus RNA. Plant Physiol 67:1185–1189
Erion JL, Fox E (1981) Purification and properties of a protein which binds cytokinin-active 6-substituted purines. Plant Physiol 67:156–162
Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525
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, Berlin
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 31:541–576
Fox JE (1965) Incorporation of a kinin, N,6-benzyladenine into soluble RNA. Plant Physiol 41:75–82
Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452
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 380:121–130
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 62:2827–2840
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, Amsterdam
Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988
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 27:143–153
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 829:26–34
Gefter ML, Russell RL (1969) Role of modifications in tyrosine transfer RNA—a modified base affecting ribosome binding. J Mol Biol 39:145–157
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 165:227–237
Gupta D, Bhargava S (2001) Thidiazuron induced regeneration in Cuminum cyminum L. J Plant Biochem Biot 10:61–62
Haberlandt G (1913) Zur Physiologie der Zellteilung. Sitzungsberichte der Königlich Preussischen Akademie der Wissenschaften, Berlin Phys Math Klasse 318–345
Hall RH (1973) Cytokinins as a probe of developmental processes. Ann Rev Plant Physiol 24:415–444
Hall RH, De Ropp RS (1955) Formation of 6-furfurylaminopurine from DNA breakdown products. J Am Chem Soc 77:6400
Hall RH, Robins MJ, Stasiuk L, Thedford R (1966) Isolation of N6-(γ, γ -dimethylallyl)adenosine from soluble ribonucleic acid. J Am Chem Soc 88:2614–2618
Hall RH, Csonka L, David H, McLennan B (1967) Cytokinins in the soluble RNA of plant tissues. Science 156:69–71
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 51:76–83
Hare PD, Van Staden J (1994) Cytokinin oxidase: biochemical features and physiological significance. Physiol Plantarum 91:128–136
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 21:2008–2021
Holland MA (1997) Occam’s razor applied to hormonology. Plant Physiol 115:865–868
Holley RW, Everett GA, Madison JT, Zamir A (1965) Nucleotide sequences in the yeast alanine transfer ribonucleic acid. J Am Chem Soc 240:2122–2128
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 359:89–101
Horgan R, Hewett EW, Purse J, Wareing PF (1973) A new cytokinin from Populus robusta. Tetrahedron Lett 30:2827–2828
Hothorn M, Dabi T, Chory J (2011) Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat Chem Biol 7:766–768
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 17:615–626
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 409:1060–1063
Jacobs WP (1979) Plant hormones and plant development. Cambridge University Press, London
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 23:279–289
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
Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982–985
Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685
Kakimoto T (2003a) Biosynthesis of cytokinins. J Plant Res 116:233–239
Kakimoto T (2003b) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54:605–627
Kaminek M (1975) Die Zytokinine and ihre Beziehungen zu den Transfer-Ribonucleinsäuren. Biologische Rundschau 13:137–152
Kamínek M (1974) Evolution of tRNA and origin of two positional isomers of zeatin. J Theor Biol 48:489–492
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 215–224
Kamínek M, Armstrong DJ (1990) Genotypic variation in cytokinin oxidase from Phasoleus callus cultures. Plant Physiol 93:1530–1538
Kamínek M, Pačes V, Corse J, Challice JS (1979) Effects of stereospecific hydroxylation of N6-(Δ2-isopentenyl)adenosine on cytokinin activity. Planta 145:239–243
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 6:113–120
Kamínek M, Trčková M, Fox JE, Gaudinová A (2003) Comparison of cytokinin-binding proteins from wheat and oat grains. Physiol Plantarum 117:453–458
Kende H (1971) The cytokinins. Ann Rev Cytol 31:301–338
Kline LK, Fittler F, Hall RH (1969) N6-(Δ2-isopentenyl)adenosine. Biosynthesis in transfer ribonucleic acid in vitro. Biochemistry 8:4361–4371
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 51:1081–1084
Kögl F, Erxleben H, Haagen-Smit AJ (1933) Über ein Phytohomon der Zellstreckung. Zur Chemie des krystallisierten Auxins. V. Mitteilung. Zeitschift für Physiologische Chemie 216:31–46
Kögl F, Haagen-Smit AJ, Erxleben H (1934) Über eines neues Auxin („Heteroauxin“) aus Harn. XI. Mitteilung. Zeitschift für Physiologische Chemie 228:90–103
Laloue M, Pethe C (1982) Dynamics of cytokinin metabolism in tobacco cells. In: Wareing PF (ed) Plant Growth Substances 1982. Academic Press, London, pp 185–195
Letham DS (1958) Cultivation of apple fruit tissues in vitro. Nature 182:473–474
Letham DS (1963a) Regulators of cell division in plant tissues. New Zeal J Bot 1:336–350
Letham DS (1963b) Purification of factors inducing cell division extracted from plum fruitlets. Life Sci 2:152–157
Letham DS (1963c) Zeatin, a factor inducing cell division isolated from Zea mays. Life Sci 8:569–573
Letham DS (1966) Regulators of cell division in plant tissues II. A cytokinin in plant extracts. Phytochemistry 5:269–286
Letham DS (1974) Regulators of cell division in plant tissues. XX. The cytokinins of coconut milk. Physiol Plantarum 32:66–70
Letham DS (1999) Cytokinins and plant growth. In: Hogan D, Williamson B (eds) New Zealand is different. Clerestory Press, New Zealand, pp 161–167
Letham DS, Bollard EG (1961) Stimulants of cell division in developing fruits. Nature 191:1119–1120
Letham DS, Miller CO (1965) Identity of kinetin-like factors from Zea mays. Plant Cell Physiol 6:355–359
Letham DS, Palni LMS (1983) The biosynthesis and metabolism of cytokinins. Annu Rev Plant Physiol 34:163–197
Letham DS, Ralph RK (1967) A cytokinin in soluble RNA from a higher plant. Life Sci 6:387–394
Letham DS, Shannon JS, McDonald IRC (1964) Structure of zeatin, a factor inducing cell division. Proc Chem Soc Lond, July issue, pp 230–261
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 65:2533–2543
Link GKK, Eggers V (1941) Hyperauxiny in crown gall of tomato—contributions from the hull botanical laboratory. Bot Gaz 103:87–106
Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plantarum 18:100–127
Lomin SN, Yonekura-Sakakibara K, Romanov GA, Sakakibara H (2011) Lingand-binding properties and subcellular localization of maize cytokinin receptors. J Exp Bot 62:5149–51159
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
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 24:1031–1037
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 7:211–220
Matand K, Prakash CS (2007) Evaluation of peanut genotypes for in vitro plant regeneration using thidiazuron. J Biotechnol 30:202–207
McLennan BD (1975) Enzymatic demodification of transfer RNA species containing N6-(∆2-isopentenyl)adenosine. Biochem Biophys Res Commun 65:345–351
Ménagé A, Morel G (1964) Sur la presence d’octopine dans les tissus de crown-gall. C R Acad Sci Paris 259:4795–4796
Miller CO (1961) Kinetin-like compound in maize. Proc Natl Acad Sci USA 47:170–174
Miller CO (1965) Evidence for the natural occurrence of zeatin and derivatives: compounds from maize which promote cell division. Proc Natl Acad Sci USA 54:1052–1058
Miller CO, Skoog F, von Saltza M, Strong FM (1955a) Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77:1392
Miller CO, Skoog F, von Saltza MH, Okumura FS, Strong FM (1955b) Structure and synthesis of kinetin. J Am Chem Soc 77:2662
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 103:16598–16603
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 155–166
Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118
Morris RO (1986) Genes specifying auxin and cytokinin biosynthesis in phytopahogens. Annu Rev Plant Physiol 37:509–538
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 20:621–637
Morris RO, Bilyeu KD, Laskey JG, Cheikh NN (1999) Isolation of a gene encoding a glycosylated cytokinin oxidase from maize. Biochem Biophys Res Co 255:328–333
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 112:1035–1043
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 117:11–21
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 87–100
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 18:100–127
Naylor J, Sander G, Skoog F (1954) Mitosis and cell enlargement without cell division in excised tobacco pith tissue. Physiol Plant 7:25–29
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 16:1365–1377
Nishinari N, Syono K (1980) Cell-free biosynthesis of cytokinins in cultured tobacco cells. Z Pflanzenphysiol 99:383–392
Nomura T, Tanakat Y, Abe H, Uchiyama M (1977) Cytokinin activity of discadenine: a spore germination inhibitor of Dictyostelium discoideum. Phytochemistry 16:1819–1820
Pačes V, Werdstiuk E, Hall RH (1971) Conversion of N 6-(∆2-isopentenyl)adenosine to adenosine by enzyme activity in tobacco tissue. Plant Physiol 48:775–778
Parker CW, Letham DS (1973) Regulators of cell division in plant tissues. XVI Metabolism of zeatin by radish cotyledons and hypocotyls. Planta 114:199–218
Parker CW, Cowley DE, Letham DS, MacLeod JK (1972) Raphanatin, an unusual purine derivative and a metabolite of zeatin. Biochem Biophys Res Commun 49:460–466
Parker CW, Wilson MM, Letham DS, Cowley DE, MacLeod JK (1973) The glucosylation of cytokinins. Biochem Biophys Res Co 55:1370–1376
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 142:239–251
Persson BC, Esberg B, Ólavsson Ó, Bjōrk GR (1994) Synthesis and function of isopentenyl adenosine derivatives in tRNA. Biochimie 76:1152–1160
Peterkofsky A (1968) Incorporation of mevalonic acid into the N6-(Δ2-isopentenyl)adenosine of transfer ribonucleic acid in. Biochemistry 7:472–482
Pils B, Heyl A (2009) Unraveling the evolution of cytokinin signalling. Plant Physiol 151:782–791
Romanov GA (2011) The discovery of cytokinin receptors and biosynthesis of cytokinins: a true story. Russ J Plant Physiol 58:743–747
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 102:9972–9977
Schmitz RY, Skoog F, Playtis AJ, Leonard NJ (1972) Cytokinins: synthesis and biological activity of geometric and positional isomers of zeatin. Plant Physiol 50:702–705
Shantz EM, Steward FC (1955) The identification of compound A from coconut milk as 1,3-diphenylurea. J Amer Chem Soc 77:6351–6353
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 10:921
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 1–14
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 11:118–131
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 263–285
Smith EF, Townsend CO (1907) A plant tumor of bacterial origin. Science 25:671–673
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 47:516–520
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 45:1299–1305
Starling EH (1905) The Crotonian Lectures, I. On chemical correlation of the functions of the body. Lancet 166:339–341
Strnad M (1997) The aromatic cytokinins. Physiol Plantarum 101:674–688
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 45:213–218
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 63:35–41
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 59:377–387
Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thalinana. J Biol Chem 276:26405–26410
Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyse the biosynthesis of trans-zeatin. J Biol Chem 279:41866–41872
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 101–112
Taya Y, Tanaka Y, Nishimura S (1978) 5′-AMP is a direct precursor of cytokinin in Dictyostelium discoideum. Nature 271:545–547
Terrine C, Laloule M (1980) Kinetics of N6-(∆2-isopentenyl)adenosine degradation in tobacco cells. Plant Physiol 65:1090–1095
Van Overbeek J, Conklin ME, Blakeslee AF (1941) Factors in coconut milk essential for growth and development of very young datura embryos. Science 94:350–351
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 167:872–886
Went FW, Thimann KV (1937) Phytohormones. MacMillan Co, New York, pp 7–8
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 59:2659–2672
White PR (1943) Nutrient deficiency studies and improved inorganic nutrient medium for cultivation of of excised tomato roots. Growth 7:53
White PR, Braun AC (1941) Crown gall production by bacteria-free tumor tissues. Science 94:239–241
White PR, Braun AC (1942) A cancerous neoplasm of plants-autonomous bacteria-free crown-gall tissue. Cancer Res 2:597–617
Whitty CD, Hall RH (1974) A cytokinin oxidase in Zea mays. Can J Biochem 52:789–799
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 287:458–461
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 42:1017–1023
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 134:1654–1661
Young AP, Bandarian V (2013) Radical mediated ring formation in the biosynthesis of the hypermodified tRNA base wybutosine. Curr Opin Chem Biol 17:613–618
Zachau HG, Dütting D, Feldmann H (1966) The structures of two serine transfer ribonucleic acids. Hoppe-Seylers Zeit Physiol Chem 347:212–235
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 86:109–127
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 209:1385–1391
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 2:2143–2150
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.
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Kamínek, M. Tracking the Story of Cytokinin Research. J Plant Growth Regul 34, 723–739 (2015). https://doi.org/10.1007/s00344-015-9543-4
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DOI: https://doi.org/10.1007/s00344-015-9543-4