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Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species

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Abstract

Cytokinin oxidases/dehydrogenases (CKX) catalyze the irreversible degradation of the cytokinins isopentenyladenine, zeatin, and their ribosides in a single enzymatic step by oxidative side chain cleavage. To date the sequences of 17 fully annotated CKX genes are known, including two prokaryotic genes. The CKX gene families of Arabidopsis thaliana and rice comprise seven and at least ten members, respectively. The main features of CKX genes and proteins are summarized in this review. Individual proteins differ in their catalytic properties, their subcellular localization and their expression domains. The evolutionary development of cytokinin-catabolizing gene families and the individual properties of their members indicate an important role for the fine-tuned control of catabolism to assure proper regulation of cytokinin functions. The use of CKX genes as a tool in studies of cytokinin biology and biotechnological applications is discussed.

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References

  • Angra R, Mandahar CL, Gulati A (1990) The possible involvement of cytokinins in the pathogenicity of Helminthosporium maydis. Mycopathologia 109:177–182

    CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    PubMed  Google Scholar 

  • Armstrong DJ (1994) Cytokinin oxidase and the regulation of cytokinin degradation. In: Mok DWS, Mok MC (eds) Cytokinin: chemistry, activity, and function. CRC, Boca Raton, pp 139–154

  • Armstrong DJ, Firtel RA (1989) Cytokinin oxidase activity in the cellular slime mold Dictyostelium discoideum. Dev Biol 136:491–499

    Google Scholar 

  • Benková E, Witters E, Van Dongen W, Kolář J, Motyka V, Brzobohatý B, Van Onckelen H, Macháčková I (1999) Cytokinins in tobacco and wheat chloroplasts: occurrence and changes due to light/dark treatment. Plant Physiol 121:245–251

    Article  CAS  PubMed  Google Scholar 

  • 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 125:378–386

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

  • Chatfield JM, Armstrong DJ (1986) Regulation of cytokin oxidase activity in callus tissues of Phaseolus vulgaris L. cv. Great Northern. Plant Physiol 80:493–499

    CAS  Google Scholar 

  • Cheikh N, Jones RJ (1994) Disruption of maize kernel growth and development by heat stress: role of cytokinin/abscisic acid balance. Plant Physiol 106:45–51

    CAS  PubMed  Google Scholar 

  • Crespi M, Messens E, Caplan AB, Van Montagu M, Desomer J (1992) Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J 11:795–804

    CAS  PubMed  Google Scholar 

  • Crespi M, Vereecke D, Temmerman W, Van Montagu M, Desomer J (1994) The fas operon of Rhodococcus fascians encodes new genes required for efficient fasciation of host plants. J Bacteriol 176:2492–2501

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Doree M, Guern J (1973) Short-time metabolism of some exogenous cytokinins in Acer pseudoplatanus cells. Biochim Biophys Acta 304:611–619

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Emanuelsson O, Heijne G von (2001) Prediction of organellar targeting signals. Biochim Biophys Acta 1541:114–119

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, Heijne G von (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Forsyth C, Staden J van (1987) Cytokinin metabolism in tomato plants. II. Metabolites of kinetin and benzyladenine in decapitated roots. Plant Growth Regul 6:277–292

    CAS  Google Scholar 

  • Fox JE, Dyson W, Sood D, McChesney JD (1972) Active forms of the cytokinins. In: Carr DJ (ed) Plant growth regulation. Springer, Berlin Heidelberg New York, pp 449–458

  • Frébort I, Šebela M, Galuszka P, Werner T, Schmülling T, Peč P (2002) Cytokinin oxidase/cytokinin dehydrogenase assay: optimized procedures and applications. Anal Biochem 306:1–7

    Article  PubMed  Google Scholar 

  • Galuszka P, Frébort I, Šebela M, Strnad M, Peč P (1999) Cytokinin oxidase: the key enzyme in the biodegradation of cytokinins. In: Strnad M, Peč P, Beck E (eds) Advances in regulation of plant growth and development. Peres, Prague, pp 39–48

  • Galuszka P, Frébort I, Šebela M, Sauer P, Jacobsen S, Peč P (2001) Cytokinin oxidase or dehydrogenease? Mechanism of cytokinin degradation in cereals. Eur J Biochem 268:450–461

    Article  CAS  PubMed  Google Scholar 

  • Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988

    CAS  PubMed  Google Scholar 

  • Gerhäuser D, Bopp M (1990) Cytokinin oxidases in mosses. 2. Metabolism of kinetin and benzyladenine in vivo. J Plant Physiol 135:714–718

    Google Scholar 

  • Gordon ME, Letham DS, Parker CW (1974) The metabolism and translocation of zeatin in intact radish seedlings. Ann Bot 38:809–825

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Houba-Hérin N, Pethe C, d'Alayer J, Laloue M (1999) Cytokinin oxidase from Zea mays: purification, cDNA cloning and expression in moss protoplasts. Plant J 17:615–626

    CAS  PubMed  Google Scholar 

  • Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–389

    Google Scholar 

  • Jones RJ, Schreiber BMN (1997) Role and function of cytokinin oxidase in plants. Plant Growth Regul 23:123–134

    CAS  Google Scholar 

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

  • Kamínek M, Armstrong DJ (1990) Genotypic variation in cytokinin oxidase from Phaseolus callus cultures. Plant Physiol 93:1530–1538

    Google Scholar 

  • Kamínek M, Trčková M, Motyka V, Gaudinová A (1994) Role of cytokinins in control of wheat grain development and utilization of nutrients. Biol Plant 36:135

    Google Scholar 

  • Kamínek M, Motyka V, Vaňková R (1997) Regulation of cytokinin content in plant cells. Physiol Plant 101:689–700

    Article  Google Scholar 

  • Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M, Tabata S (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 (supplement). DNA Res 8:205–213

    CAS  PubMed  Google Scholar 

  • Kapoor K, Sharma VK (1981) Effect of growth-promoting chemicals on growth, nitrogen fixation and heterocyst frequency of a blue-green alga. Z Allg Mikrobiol 21:305–311

    CAS  PubMed  Google Scholar 

  • Laloue M, Fox JE (1985) Characterization of an imine intermediate in the degradation of isopentenylated cytokinins by a cytokinin oxidase from wheat. In: Boop M, Knoop B, Rademacher W (eds) Abstracts of the 12th international conference on plant growth substances, Heidelberg, p 23

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

    CAS  Google Scholar 

  • Laloue M, Pethe C (1982) Dynamics of cytokinin metabolism in tobacco cells. In: Wareing PF (ed) Plant growth substances 1982. Academic Press, London, pp 186–195

  • Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56

    Article  CAS  PubMed  Google Scholar 

  • Lejeune P, Prinsen E, Van Onckelen HA, Bernier G (1998). Hormonal control of ear abortion in a stress-sensitive maize (Zea mays) inbred. Aust J Plant Physiol 25:481–488

    CAS  Google Scholar 

  • Letham DS, Wilson MM, Parker CW, Jenkins ID, Macleod JK, Summons RE (1975) Regulators of cell division in plant tissue. XXIII. The identity of an unusual metabolite of 6-benzylaminopurine. Biochim Biophys Acta 399:61–70

    Article  CAS  PubMed  Google Scholar 

  • Letham DS, Tao GQ, Parker CW (1982) An overview of cytokinin metabolism. In: Wareing PF (ed) Plant growth substances. Academic Press, London, pp 143–152

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

    Article  CAS  PubMed  Google Scholar 

  • Lohrmann J, Sweere U, Zabaleta E, Bäuerle I, Keitel C, Kozma-Bognar L, Brennicke A, Kudla J, Schäfer E, Harter K (2001) The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear-encoded mitochondrial complex I genes. Mol Gen Genomics 265:2–13

    Article  CAS  Google Scholar 

  • Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13

    CAS  PubMed  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Miernyk JA (1979) Abscisic acid inhibition of kinetin nucleotide formation in germinating lettuce seeds. Physiol Plant 45:63–66

    CAS  Google Scholar 

  • Miernyk JA, Blaydes (1977) Short term metabolism of radioactive kinetin during lettuce seed germination. Physiol Plant 39:4–8

    CAS  Google Scholar 

  • Mills LJ, Van Staden J (1978) Extraction of cytokinins from maize, smut tumors of maize and Ustilago maydis cultures. Physiol Plant Pathol 13:73–80

    CAS  Google Scholar 

  • Mok MC (1994) Cytokinins and plant development: an overview. In Mok, DWS, Mok MC (eds) Cytokinins: Chemistry, activity, and function. CRC, Boca Raton, pp 155–166

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    Google Scholar 

  • Morris RO (1995) Genes specifying auxin and cytokinin biosynthesis in prokaryotes. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic, Dordrecht, pp 318–339

  • Morris RO, Bilyeu KD, Laskey JG, Cheikh N (1999) Isolation of a gene encoding a glycosylated cytokinin oxidase from maize. Biochem Biophys Res Comm 255:328–333

    CAS  PubMed  Google Scholar 

  • Motyka V, Kamínek M (1994) Cytokinin oxidase from auxin and cytokinin-dependent callus cultures of tobacco Nicotiana tabacum L.). J Plant Growth Regul 13:1–9

    CAS  Google Scholar 

  • Motyka V, Faiss M, Strnad M, Kamínek M, Schmülling T (1996) Changes in 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

    CAS  PubMed  Google Scholar 

  • 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 Plant 117:11–21

    CAS  Google Scholar 

  • Mushegian AR, Koonin EV (1995) A putative FAD-binding domain in a distinct group of oxidases including a protein involved in plant development. Protein Sci 4:1243–1244

    CAS  PubMed  Google Scholar 

  • Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–36

    CAS  PubMed  Google Scholar 

  • Pačes V, Werstiuk E, Hall RH (1971) Conversion of N6-(Δ2-isopentenyl)adenosine to adenosine by enzyme activity in tobacco tissue. Plant Physiol 48:775–778

    Google Scholar 

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Peeters N, Small I (2001) Dual targeting to mitochondria and chloroplasts. Biochim Biophys Acta 1541:54–63

    Article  CAS  PubMed  Google Scholar 

  • Redig P, Schmülling T, Van Onckelen H (1996a) Analysis of cytokinin metabolism in ipt transgenic tobacco by liquid chromatography-tandem mass spectrometry. Plant Physiol: 112:141–148

    Google Scholar 

  • Redig P, Shaul O, Inze D, Van Montagu M, Van Onckelen H (1996b) Levels of endogenous cytokinins, indole-3-acetic acid and abscisic acid during the cell cycle of synchronized tobacco BY-2 cells. FEBS Lett 391:175–180

    CAS  PubMed  Google Scholar 

  • Redig P, Motyka V, Van Onckelen H, Kamínek M (1997) Regulation of cytokinin oxidase activity in tobacco callus expressing the T-DNA ipt gene. Physiol Plant 99:89–96

    Article  CAS  Google Scholar 

  • Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu J, Niimura Y, Cheng Z, Nagamura Y, Antonio BA, Kanamori H, Hosokawa S, Masukawa M, Arikawa K, Chiden Y, Hayashi M, Okamoto M, Ando T, Aoki H, Arita K, Hamada M, Harada C, Hijishita S, Honda M, Ichikawa Y, Idonuma A, Iijima M, Ikeda M, Ikeno M, Itoh S, Itoh T, Itoh Y, Iwabuchi A, Kamiya K, Karasawa W, Katagiri S, Kikuta A, Kobayashi N, Kono I, Machita K, Maehara T, Mizuno H, Mizubayashi T, Mukai Y, Nagasaki H, Nakashima, M, Nakama Y, Nakamichi Y, Nakamura M, Namiki N, Negishi M, Ohta I, Ono N, Saji S, Sakai K, Shibata M, Shimokawa T, Shomura A, Song J, Takazaki Y, Terasawa K, Tsuji K, Waki K, Yamagata H, Yamane H, Yoshiki S, Yoshihara R, Yukawa K, Zhong H, Iwama H, Endo T, Ito H, Hahn JH, Kim HI, Eun MY, Yano M, Jiang J, Gojobori T (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316

    Article  CAS  PubMed  Google Scholar 

  • Schmülling T (2001) CREam of cytokinin signalling: receptor identified. Trends Plant Sci 6:281–284

    Article  PubMed  Google Scholar 

  • Schmülling T, Schäfer S, Romanov G (1997) Cytokinins as regulators of gene expression. Physiol Plant 100:505–519

    Article  Google Scholar 

  • Schwacke R, Schneider A, Graaff E van der, Fischer K, Catoni E, Desimone M, Frommer WB, Flügge UI, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131:16–26

    Article  CAS  PubMed  Google Scholar 

  • Shudo K (1994) Chemistry of phenylurea cytokinins. In: Mok DWS, Mok MC (eds) Cytokinins: chemistry, activity, and function. CRC, Boca Raton, pp 35–42

  • Singh S, Palni LMS, Letham DS (1992) Cytokinin biochemistry in relation to leaf senescence. V. Endogeneous cytokinin levels and metabolism of zeatin riboside in leaf discs from green and senescent tobacco (Nicotiana rustica) leaves. J Plant Physiol 139:279–283

    CAS  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215

    Google Scholar 

  • Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410

    Article  CAS  PubMed  Google Scholar 

  • Terrine C, Laloue M (1980) Kinetics of N6-(Δ2-isopentenyl)adenosine degradation in tobacco cells: evidence of regulatory mechanism under the control of cytokinins. Plant Physiol 65:1090–1095

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Van Kast CA, Laten H (1987) Cytokinin utilization by adenine requiring mutants of the yeast Saccharomyces cerevisiae. Plant Physiol 83:726–727

    Google Scholar 

  • Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Wilkins MR, Lindskog I, Gasteiger E, Bairoch A, Sanchez JC, Hochstrasser DF, Appel RD (1997) Detailed peptide characterisation using PEPTIDEMASS: a World-Wide Web accessible tool. Electrophoresis 18:403–408

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Yang SH, Yu H, Goh CJ (2002) Isolation and characterization of the orchid cytokinin oxidase DSCKX1 promoter. J Exp Bot 53:1899–1907

    Article  CAS  PubMed  Google Scholar 

  • Yang SH, Yu H, Goh CJ (2003) Functional characterisation of a cytokinin oxidase gene DSCKX1 in Dendrobium orchid. Plant Mol Biol 51:237–248

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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Schmülling, T., Werner, T., Riefler, M. et al. Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J Plant Res 116, 241–252 (2003). https://doi.org/10.1007/s10265-003-0096-4

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