Distinct metabolism of N-glucosides of isopentenyladenine and trans-zeatin determines cytokinin metabolic spectrum in Arabidopsis.

Arabidopsis thaliana UGT cytokinin N-glucoside cytokinin isomerase cytokinin metabolism isopentenyladenine metabolic network zeatin

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
03 2020
Historique:
received: 28 08 2019
accepted: 26 10 2019
pubmed: 5 11 2019
medline: 15 5 2021
entrez: 5 11 2019
Statut: ppublish

Résumé

The diversity of cytokinin (CK) metabolites suggests their interconversions are the predominant regulatory mechanism of CK action. Nevertheless, little is known about their directionality and kinetics in planta. CK metabolite levels were measured in 2-wk-old Arabidopsis thaliana plants at several time points up to 100 min following exogenous application of selected CKs. The data were then evaluated qualitatively and by mathematical modeling. Apart from elevated levels of trans-zeatin (tZ) metabolites upon application of N

Identifiants

pubmed: 31682013
doi: 10.1111/nph.16310
doi:

Substances chimiques

Cytokinins 0
Glucosides 0
N(6)-(delta(2)-isopentenyl)adenine 2365-40-4
Isopentenyladenosine 7724-76-7
Zeatin 7I6OOJ9GR6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2423-2438

Informations de copyright

© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.

Références

Allen M, Qin W, Moreau F, Moffatt B. 2002. Adenine phosphoribosyltransferase isoforms of Arabidopsis and their potential contributions to adenine and cytokinin metabolism. Physiologia Plantarum 115: 56-68.
Åstot C, Dolezal K, Nordström A, Wang Q, Kunkel T, Moritz T, Chua NH, Sandberg G. 2000. An alternative cytokinin biosynthesis pathway. Proceedings of the National Academy of Sciences, USA 97: 14778-14783.
Axelos M, Curie C, Mazzolini L, Bardet C, Lescure B. 1992. A protocol for transient gene expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiology and Biochemistry 30: 123-128.
Bassil NV, Mok D, Mok MC. 1993. Partial purification of a cis-trans-isomerase of zeatin from immature seed of Phaseolus vulgaris L. Plant Physiology 102: 867-872.
Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang Y, Schaller GE, Loraine A, Kieber JJ. 2013. Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-seq in Arabidopsis. Plant Physiology 162: 272-294.
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 Physiology 125: 378-386.
Brenner WG, Ramireddy E, Heyl A, Schmülling T. 2012. Gene regulation by cytokinin in Arabidopsis. Frontiers in Plant Science 3: 1-22.
Brenner WG, Schmülling T. 2015. Summarizing and exploring data of a decade of cytokinin-related transcriptomics. Frontiers in Plant Science 6: 1-13.
Brzobohatý B, Moore I, Kristoffersen P, Bako L, Campos N, Schell J, Palme K. 1993. Release of active cytokinin by a beta-glucosidase localized to the maize root meristem. Science 262: 1051-1054.
Dobrev PI, Hoyerová K, Petrášek J. 2017. Analytical determination of auxins and cytokinins. In: Dandekar T, Naseem M, eds. Methods in molecular biology. Auxins and cytokinins in plant biology. New York, NY, USA: Humana Press, 31-39.
Dobrev PI, Vankova R. 2012. Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. In: Shabala S, Cuin TA, eds. Methods in molecular biology. Plant salt tolerance. Totowa, NJ, USA: Humana Press, 251-261.
Falk A, Rask L. 1995. Expression of a zeatin-O-glucoside-degrading beta-glucosidase in Brassica napus. Plant Physiology 108: 1369-1377.
Fox JE, Cornette J, Deleuze G, Dyson W, Giersak C, Niu P, Zapata J, McChesney J. 1973. The formation, isolation, and biological activity of a cytokinin 7-glucoside. Plant Physiology 52: 627-632.
Gajdošová S, Spíchal L, Kamínek M, Hoyerová K, Novák O, Dobrev PI, Galuszka P, Klíma P, Gaudinová A, Žižková E et al. 2011. Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. Journal of Experimental Botany 62: 2827-2840.
Galichet A, Hoyerova K, Kaminek M, Gruissem W. 2008. Farnesylation directs AtIPT3 subcellular localization and modulates cytokinin biosynthesis in Arabidopsis. Plant Physiology 146: 1155-1164.
Galuszka P, Popelková H, Werner T, Frébortová J, Pospíšilová H, Mik V, Köllmer I, Schmülling T, Frébort I. 2007. Biochemical characterization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabacum L. Journal of Plant Growth Regulation 26: 255-267.
Gaudinová A, Dobrev PI, Šolcová B, Novák O, Strnad M, Friedecký D, Motyka V. 2005. The involvement of cytokinin oxidase/dehydrogenase and zeatin reductase in regulation of cytokinin levels in pea (Pisum sativum L.) leaves. Journal of Plant Growth Regulation 24: 188-200.
Gillissen B, Bürkle L, André B, Kühn C, Rentsch D, Brandl B, Frommer WB. 2000. A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis. Plant Cell 12: 291-300.
Hirose N, Makita N, Yamaya T, Sakakibara H. 2005. Functional characterization and expression analysis of a gene, OsENT2, encoding an equilibrative nucleoside transporter in rice suggest a function in cytokinin transport. Plant Physiology 138: 196-206.
Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H. 2008. Regulation of cytokinin biosynthesis, compartmentalization and translocation. Journal of Experimental Botany 59: 75-83.
Hluska T, Šebela M, Lenobel R, Frébort I, Galuszka P. 2017. Purification of maize nucleotide pyrophosphatase/phosphodiesterase casts doubt on the existence of zeatin cis-trans isomerase in plants. Frontiers in Plant Science 8: 1-13.
Hou B, Lim EK, Higgins GS, Bowles DJ. 2004. N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. Journal of Biological Chemistry 279: 47822-47832.
Kakimoto T. 2001. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant and Cell Physiology 42: 677-685.
Kasahara H, Takei K, Ueda N, Hishiyama S, Yamaya T, Kamiya Y, Yamaguchi S, Sakakibara H. 2004. Distinct isoprenoid origins of cis- and trans-zeatin biosyntheses in Arabidopsis. Journal of Biological Chemistry 279: 14049-14054.
Kiba T, Takei K, Kojima M, Sakakibara H. 2013. Side-chain modification of cytokinins controls shoot growth in Arabidopsis. Developmental Cell 27: 452-461.
Kowalska M, Galuszka P, Frébortová J, Šebela M, Béres T, Hluska T, Šmehilová M, Bilyeu KD, Frébort I. 2010. Vacuolar and cytosolic cytokinin dehydrogenases of Arabidopsis thaliana: heterologous expression, purification and properties. Phytochemistry 71: 1970-1978.
Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J. 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445: 652-655.
Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H. 2009. Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21: 3152-3169.
Laloue M, Pethe C. 1982. Dynamics of cytokinin metabolism in tobacco cells. In: Wareing PW, ed. Plant growth substances. London, UK: Academic Press, 185-195.
Lee D, Moffatt BA. 1993. Purification and characterization of adenine phosphoribosyltransferase from Arabidopsis thaliana. Physiologia Plantarum 87: 483-492.
Letham DS, Palni LMS, Tao G-Q, Gollnow BI, Bates CM. 1983. Regulators of cell division in plant tissues XXIX. The activities of cytokinin glucosides and alanine conjugates in cytokinin bioassays. Journal of Plant Growth Regulation 2: 103-115.
Lexa M, Genkov T, Malbeck J, Macháčková I, Brzobohatý B. 2003. Dynamics of endogenous cytokinin pools in tobacco seedlings: a modelling approach. Annals of Botany 91: 585-597.
Martin RC, Mok MC, Shaw G, Mok DW. 1989. An enzyme mediating the conversion of zeatin to dihydrozeatin in Phaseolus embryos. Plant Physiology 90: 1630-1635.
Miyawaki K, Matsumoto-Kitano M, Kakimoto T. 2004. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. The Plant Journal 37: 128-138.
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. Proceedings of the National Academy of Sciences, USA 103: 16598-16603.
Moffatt BA, Wang L, Allen MS, Stevens YY, Qin W, Snider J, von Schwartzenberg K. 2000. Adenosine kinase of Arabidopsis. Kinetic properties and gene expression. Plant Physiology 124: 1775-1785.
Mok DW, Mok MC. 2001. Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology 52: 89-118.
Motyka V, Kamínek M. 1994. Cytokinin oxidase from auxin- and cytokinin-dependent callus cultures of tobacco (Nicotiana tabacum L.). Journal of Plant Growth Regulation 13: 1-9.
Motyka V, Vankova R, Capkova V, Petrasek J, Kaminek M, Schmulling T. 2003. Cytokinin-induced upregulation of cytokinin oxidase activity in tobacco includes changes in enzyme glycosylation and secretion. Physiologia Plantarum 117: 11-21.
Romanov GA, Lomin SN, Schmülling T. 2006. Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. Journal of Experimental Botany 57: 4051-4058.
Sakakibara H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57: 431-449.
Samsonova Z, Kuklova A, Mazura P, Rotkova G, Novak O, Brzobohaty B, Kiran NS. 2012. Natural variation in the cytokinin metabolic network in Arabidopsis thaliana. Mendelnet 2012: 881-886.
Šimura J, Antoniadi I, Široká J, Tarkowska D, Strnad M, Ljung K, Novak O. 2018. Plant hormonomics: multiple phytohormone profiling by targeted metabolomics. Plant Physiology 177: 476-489.
Šmehilová M, Dobrůšková J, Novák O, Takáč T, Galuszka P. 2016. Cytokinin-specific glycosyltransferases possess different roles in cytokinin homeostasis maintenance. Frontiers in Plant Science 7: 1264.
Šmehilová M, Galuszka P, Bilyeu KD, Jaworek P, Kowalska M, Šebela M, Sedláová M, English JT, Frébort I. 2009. Subcellular localization and biochemical comparison of cytosolic and secreted cytokinin dehydrogenase enzymes from maize. Journal of Experimental Botany 60: 2701-2712.
Spíchal L. 2012. Cytokinins - recent news and views of evolutionally old molecules. Functional Plant Biology 39: 267-284.
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 and Cell Physiology 45: 1299-1305.
Van Staden J, Drewes FE. 1991. The biological activity of cytokinin derivatives in the soybean callus bioassay. Plant Growth Regulation 10: 109-115.
Takei K. 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 and Cell Physiology 42: 85-93.
Takei K, Sakakibara H, Sugiyama T. 2001. Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. Journal of Biological Chemistry 276: 26405-26410.
Takei K, Yamaya T, Sakakibara H. 2004. Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyse the biosynthesis of trans-zeatin. Journal of Biological Chemistry 279: 41866-41872.
Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling 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.
Yamada H, Koizumi N, Nakamichi N, Kiba T, Yamashino T, Mizuno T. 2004. Rapid response of Arabidopsis T87 cultured cells to cytokinin through His-to-Asp phosphorelay signal transduction. Bioscience, Biotechnology, and Biochemistry 68: 1966-1976.
Zalabák D, Galuszka P, Mrízová K, Podlešáková K, Gu R, Frébortová J. 2014. Biochemical characterization of the maize cytokinin dehydrogenase family and cytokinin profiling in developing maize plantlets in relation to the expression of cytokinin dehydrogenase genes. Plant Physiology and Biochemistry 74: 283-293.
Zürcher E, Liu J, Di Donato M, Geisler M, Müller B. 2016. Plant development regulated by cytokinin sinks. Science 353: 1027-1030.

Auteurs

Petr Hošek (P)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Klára Hoyerová (K)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Nagavalli S Kiran (NS)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Petre I Dobrev (PI)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Lenka Zahajská (L)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Roberta Filepová (R)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Václav Motyka (V)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Karel Müller (K)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

Miroslav Kamínek (M)

The Czech Academy of Sciences, Institute of Experimental Botany, Rozvojová 263, 165 02, Praha 6, Czech Republic.

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