Cytokinins (CKs) are a class of phytohormones affecting many aspects of plant growth and development. In the complex process of CK homeostasis in plants, N-glucosylation represents one of the essential metabolic pathways. Its products, CK N7- and N9-glucosides, have been largely overlooked in the past as irreversible and inactive CK products lacking any relevant physiological impact. In this work, we report a widespread distribution of CK N-glucosides across the plant kingdom proceeding from evolutionary older to younger plants with different proportions between N7- and N9-glucosides in the total CK pool. We show dramatic changes in their profiles as well as in expression levels of the UGT76C1 and UGT76C2 genes during Arabidopsis ontogenesis. We also demonstrate specific physiological effects of CK N-glucosides in CK bioassays including their antisenescent activities, inhibitory effects on root development, and activation of the CK signaling pathway visualized by the CK-responsive YFP reporter line, TCSv2::3XVENUS. Last but not least, we present the considerable impact of CK N7- and N9-glucosides on the expression of CK-related genes in maize and their stimulatory effects on CK oxidase/dehydrogenase activity in oats. Our findings revise the apparent irreversibility and inactivity of CK N7- and N9-glucosides and indicate their involvement in CK evolution while suggesting their unique function(s) in plants.

CEITEC Central European Institute of Technology Mendel University in Brno Zemědělská 1 613 00 Brno Czech Republic

Department of Biochemistry Faculty of Science Palacký University Šlechtitelů 11 783 71 Olomouc Czech Republic

Department of Biological Science Auburn University Auburn AL 36849 USA

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Šlechtitelů 27 783 71 Olomouc Czech Republic

Department of Molecular Biology and Radiobiology Faculty of AgriSciences Mendel University in Brno Zemědělská 1665 1 613 00 Brno Czech Republic

Institute of Biophysics of the Czech Academy of Sciences Královopolská 135 612 65 Brno Czech Republic

Isotope Laboratory Institute of Experimental Botany of the Czech Academy of Sciences Vídeňská 1083 142 20 Prague 4 Czech Republic

Laboratory of Growth Regulators Institute of Experimental Botany of the Czech Academy of Sciences and Faculty of Science of Palacký University Šlechtitelů 27 783 71 Olomouc Czech Republic

Laboratory of Hormonal Regulations in Plants Institute of Experimental Botany of the Czech Academy of Sciences Rozvojová 263 165 02 Prague 6 Czech Republic

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Osugi A., Sakakibara H. Q&A: How do plants respond to cytokinins and what is their importance? BMC Biol. 2015;13:102. doi: 10.1186/s12915-015-0214-5. PubMed DOI PMC

Kieber J.J., Schaller G.E. Cytokinin signaling in plant development. Development. 2018;145:dev149344. doi: 10.1242/dev.149344. PubMed DOI

Mok D.W., Mok M.C. Cytokinin metabolism and action. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 2001;52:89–118. doi: 10.1146/annurev.arplant.52.1.89. PubMed DOI

Auer C.A. Cytokinin inhibition of Arabidopsis root growth: An examination of genotype, cytokinin activity, and N6-benzyladenine metabolism. J. Plant. Growth Regul. 1996;15:201. doi: 10.1007/BF00190585. DOI

Strnad M. The aromatic cytokinins. Physiol. Plant. 1997;101:674–688. doi: 10.1111/j.1399-3054.1997.tb01052.x. DOI

Tarkowska D., Dolezal K., Tarkowski P., Astot C., Holub J., Fuksova K., Schmulling T., Sandberg G., Strnad M. Identification of new aromatic cytokinins in Arabidopsis thaliana and Populus x canadensis leaves by LC-(+)ESI-MS and capillary liquid chromatography/frit-fast atom bombardment mass spectrometry. Physiol. Plant. 2003;117:579–590. doi: 10.1034/j.1399-3054.2003.00071.x. PubMed DOI

Spíchal L., Rakova N.Yu., Riefler M., Mizuno T., Romanov G.A., Strnad M., Schmülling T. Two Cytokinin Receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, Differ in their Ligand Specificity in a Bacterial Assay. Plant. Cell Physiol. 2004;45:1299–1305. doi: 10.1093/pcp/pch132. PubMed DOI

Hönig M., Plíhalová L., Husičková A., Nisler J., Doležal K. Role of Cytokinins in Senescence, Antioxidant Defence and Photosynthesis. IJMS. 2018;19:4045. doi: 10.3390/ijms19124045. PubMed DOI PMC

Lomin S.N., Krivosheev D.M., Steklov M.Yu., Arkhipov D.V., Osolodkin D.I., Schmülling T., Romanov G.A. Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands. J. Exp. Bot. 2015;66:1851–1863. doi: 10.1093/jxb/eru522. PubMed DOI PMC

Vaňková R. Advances in Regulation of Plant Growth and Development. Peres Publishers; London, UK: 1999. Cytokinin glycoconjugates—Distribution, metabolism and function.

Li Y., Baldauf S., Lim E.K., Bowles D.J. Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana. J. Biol. Chem. 2001;276:4338–4343. doi: 10.1074/jbc.M007447200. PubMed DOI

Bajguz A., Piotrowska A. Conjugates of auxin and cytokinin. Phytochemistry. 2009;70:957–969. doi: 10.1016/j.phytochem.2009.05.006. PubMed DOI

Vogt T., Jones P. Glycosyltransferases in plant natural product synthesis: Characterization of a supergene family. Trends Plant. Sci. 2000;5:380–386. doi: 10.1016/S1360-1385(00)01720-9. PubMed DOI

Ross J., Li Y., Lim E., Bowles D.J. Higher plant glycosyltransferases. Genome Biol. 2001;2:REVIEWS3004. doi: 10.1186/gb-2001-2-2-reviews3004. PubMed DOI PMC

Hou B., Lim E.-K., Higgins G.S., Bowles D.J. N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. J. Biol. Chem. 2004;279:47822–47832. doi: 10.1074/jbc.M409569200. PubMed DOI

Wang J., Ma X.-M., Kojima M., Sakakibara H., Hou B.-K. N-Glucosyltransferase UGT76C2 is Involved in Cytokinin Homeostasis and Cytokinin Response in Arabidopsis thaliana. Plant. Cell Physiol. 2011;52:2200–2213. doi: 10.1093/pcp/pcr152. PubMed DOI

Jin S.-H., Ma X.-M., Kojima M., Sakakibara H., Wang Y.-W., Hou B.-K. Overexpression of glucosyltransferase UGT85A1 influences trans-zeatin homeostasis and trans-zeatin responses likely through O-glucosylation. Planta. 2013;237:991–999. doi: 10.1007/s00425-012-1818-4. PubMed DOI

Wang J., Ma X.-M., Kojima M., Sakakibara H., Hou B.-K. Glucosyltransferase UGT76C1 finely modulates cytokinin responses via cytokinin N-glucosylation in Arabidopsis thaliana. Plant. Physiol. Biochem. 2013;65:9–16. doi: 10.1016/j.plaphy.2013.01.012. PubMed DOI

Li Y., Wang B., Dong R., Hou B. AtUGT76C2, an Arabidopsis cytokinin glycosyltransferase is involved in drought stress adaptation. Plant. Sci. 2015;236:157–167. doi: 10.1016/j.plantsci.2015.04.002. PubMed DOI

Šmehilová M., Dobrůšková J., Novák O., Takáč T., Galuszka P. Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance. Front. Plant. Sci. 2016;7 doi: 10.3389/fpls.2016.01264. PubMed DOI PMC

Lee S., Sergeeva L.I., Vreugdenhil D. Quantitative trait loci analysis of hormone levels in Arabidopsis roots. PLoS ONE. 2019;14:e0219008. doi: 10.1371/journal.pone.0219008. PubMed DOI PMC

Letham D., Tao G., Parker C.W. Plant Growth Substances 1982. Academic Press; London, UK: New York, NY, USA: 1982. An overview of cytokinin metabolism; p. 683.

Holub J., Hanuš J., Hanke D.E., Strnad M. Biological activity of cytokinins derived from Ortho- and Meta-Hydroxybenzyladenine. Plant. Growth Regul. 1998;26:109–115. doi: 10.1023/A:1006192619432. DOI

Beneš J., Vereš K., Chvojka L., Friedrich A. New Types of Kinins and their Action on Fruit Tree Species. Nature. 1965;206:830–831. doi: 10.1038/206830b0. DOI

Fox J.E., Cornette J., Deleuze G., Dyson W., Giersak C., Niu P., Zapata J., McChesney J. The Formation, Isolation, and Biological Activity of a Cytokinin 7-Glucoside. Plant. Physiol. 1973;52:627–632. doi: 10.1104/pp.52.6.627. PubMed DOI PMC

Letham D.S., Palni L.M.S., Tao G.-Q., Gollnow B.I., Bates C.M. Regulators of cell division in plant tissues XXIX. The activities of cytokinin glucosides and alanine conjugates in cytokinin bioassays. J. Plant. Growth Regul. 1983;2:103–115. doi: 10.1007/BF02042238. DOI

Van Staden J., Drewes F.E. The biological activity of cytokinin derivatives in the soybean callus bioassay. Plant. Growth Regul. 1991;10:109–115. doi: 10.1007/BF00024957. DOI

Hallmark H.T., Černý M., Brzobohatý B., Rashotte A.M. trans-Zeatin-N-glucosides have biological activity in Arabidopsis thaliana. PLoS ONE. 2020;15:e0232762. doi: 10.1371/journal.pone.0232762. PubMed DOI PMC

Kiba T., Takei K., Kojima M., Sakakibara H. Side-chain modification of cytokinins controls shoot growth in Arabidopsis. Dev. Cell. 2013;27:452–461. doi: 10.1016/j.devcel.2013.10.004. PubMed DOI

Mik V., Szüčová L., Spíchal L., Plíhal O., Nisler J., Zahajská L., Doležal K., Strnad M. N9-Substituted N6-[(3-methylbut-2-en-1-yl)amino]purine derivatives and their biological activity in selected cytokinin bioassays. Bioorg. Med. Chem. 2011;19:7244–7251. doi: 10.1016/j.bmc.2011.09.052. PubMed DOI

Hallmark H.T. The Roles of Cytokinins and Cytokinin-N-Glucosides in Development and Gene Expression of Arabidopsis Thaliana. [(accessed on 24 December 2020)];2020 Available online: https://etd.auburn.edu/handle/10415/7257.

Hošek P., Hoyerová K., Kiran N.S., Dobrev P.I., Zahajská L., Filepová R., Motyka V., Müller K., Kamínek M. Distinct metabolism of N-glucosides of isopentenyladenine and trans-zeatin determines cytokinin metabolic spectrum in Arabidopsis. New Phytol. 2020;225:2423–2438. doi: 10.1111/nph.16310. PubMed DOI

Podlešáková K., Zalabák D., Čudejková M., Plíhal O., Szüčová L., Doležal K., Spíchal L., Strnad M., Galuszka P. Novel Cytokinin Derivatives Do Not Show Negative Effects on Root Growth and Proliferation in Submicromolar Range. PLoS ONE. 2012;7:e39293. doi: 10.1371/journal.pone.0039293. PubMed DOI PMC

Campos N., Bako L., Feldwisch J., Schell J., Palme K. A protein from maize labeled with azido-IAA has novel β-glucosidase activity. Plant. J. 1992;2:675–684. doi: 10.1111/j.1365-313X.1992.tb00136.x. DOI

Brzobohaty B., Moore I., Kristoffersen P., Bako L., Campos N., Schell J., Palme K. Release of active cytokinin by a beta-glucosidase localized to the maize root meristem. Science. 1993;262:1051–1054. doi: 10.1126/science.8235622. PubMed DOI

Brzobohatý B., Moore I., Palme K. Cytokinin metabolism: Implications for regulation of plant growth and development. Plant. Mol. Biol. 1994;26:1483–1497. doi: 10.1007/BF00016486. PubMed DOI

Filipi T., Mazura P., Janda L., Kiran N.S., Brzobohatý B. Engineering the cytokinin-glucoside specificity of the maize β-d-glucosidase Zm-p60.1 using site-directed random mutagenesis. Phytochemistry. 2012;74:40–48. doi: 10.1016/j.phytochem.2011.10.008. PubMed DOI

Perilli S., Moubayidin L., Sabatini S. The molecular basis of cytokinin function. Curr. Opin. Plant. Biol. 2010;13:21–26. doi: 10.1016/j.pbi.2009.09.018. PubMed DOI

Hwang I., Sheen J., Müller B. Cytokinin signaling networks. Annu. Rev. Plant. Biol. 2012;63:353–380. doi: 10.1146/annurev-arplant-042811-105503. PubMed DOI

Armstrong D.J. Cytokinins: Chemistry, Activity, and Function. CRC Press; Boca Raton, FL, USA: 1994. Cytokinin oxidase and the regulation of cytokinin degradation; p. 360.

Hai N.N., Chuong N.N., Tu N.H.C., Kisiala A., Hoang X.L.T., Thao N.P. Role and Regulation of Cytokinins in Plant Response to Drought Stress. Plants. 2020;9:422. doi: 10.3390/plants9040422. PubMed DOI PMC

Galuszka P., Popelková H., Werner T., Frébortová J., Pospíšilová H., Mik V., Köllmer I., Schmülling T., Frébort I. Biochemical Characterization of Cytokinin Oxidases/Dehydrogenases from Arabidopsis thaliana Expressed in Nicotiana tabacum L. J. Plant. Growth Regul. 2007;26:255–267. doi: 10.1007/s00344-007-9008-5. DOI

Kowalska M., Galuszka P., Frébortová J., Šebela M., Béres T., Hluska T., Šmehilová M., Bilyeu K.D., Frébort I. Vacuolar and cytosolic cytokinin dehydrogenases of Arabidopsis thaliana: Heterologous expression, purification and properties. Phytochemistry. 2010;71:1970–1978. doi: 10.1016/j.phytochem.2010.08.013. PubMed DOI

Mrízová K., Jiskrová E., Vyroubalová Š., Novák O., Ohnoutková L., Pospíšilová H., Frébort I., Harwood W.A., Galuszka P. Overexpression of Cytokinin Dehydrogenase Genes in Barley (Hordeum vulgare cv. Golden Promise) Fundamentally Affects Morphology and Fertility. PLoS ONE. 2013;8:e79029. doi: 10.1371/journal.pone.0079029. PubMed DOI PMC

Zalabák D., Pospíšilová H., Šmehilová M., Mrízová K., Frébort I., Galuszka P. Genetic engineering of cytokinin metabolism: Prospective way to improve agricultural traits of crop plants. Biotechnol. Adv. 2013;31:97–117. doi: 10.1016/j.biotechadv.2011.12.003. PubMed DOI

Záveská Drábková L., Dobrev P.I., Motyka V. Phytohormone Profiling across the Bryophytes. PLoS ONE. 2015;10:e0125411. doi: 10.1371/journal.pone.0125411. PubMed DOI PMC

Žižková E., Kubeš M., Dobrev P.I., Přibyl P., Šimura J., Zahajská L., Záveská Drábková L., Novák O., Motyka V. Control of cytokinin and auxin homeostasis in cyanobacteria and algae. Ann. Bot. 2017;119:151–166. doi: 10.1093/aob/mcw194. PubMed DOI PMC

Gajdošová S., Spíchal L., Kamínek M., Hoyerová K., Novák O., Dobrev P.I., Galuszka P., Klíma P., Gaudinová A., Zizková E., et al. Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J. Exp. Bot. 2011;62:2827–2840. doi: 10.1093/jxb/erq457. PubMed DOI

Jiskrová E., Novák O., Pospíšilová H., Holubová K., Karády M., Galuszka P., Robert S., Frébort I. Extra- and intracellular distribution of cytokinins in the leaves of monocots and dicots. N. Biotechnol. 2016;33:735–742. doi: 10.1016/j.nbt.2015.12.010. PubMed DOI

Vyroubalová S., Václavíková K., Turecková V., Novák O., Smehilová M., Hluska T., Ohnoutková L., Frébort I., Galuszka P. Characterization of new maize genes putatively involved in cytokinin metabolism and their expression during osmotic stress in relation to cytokinin levels. Plant. Physiol. 2009;151:433–447. doi: 10.1104/pp.109.142489. PubMed DOI PMC

Benjamini Y., Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. Ser. B (Methodological) 1995;57:289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x. DOI

Kamínek M., Vaněk T., Motyka V. Cytokinin activities ofN6-benzyladenosine derivatives hydroxylated on the side-chain phenyl ring. J. Plant. Growth Regul. 1987;6:113–120. doi: 10.1007/BF02026460. DOI

Sumanta N., ImranulHaque C., Nishika J., Suprakash R. Spectrophotometric Analysis of Chlorophylls and Carotenoids from Commonly Grown Fern Species by Using Various Extracting Solvents. Res. J. Chem. Sci. 2014;4:63–69.

Dobrev P.I., Kamínek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J. Chromatogr. A. 2002;950:21–29. doi: 10.1016/S0021-9673(02)00024-9. PubMed DOI

Dobrev P.I., Vankova R. Quantification of abscisic Acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol. Biol. 2012;913:251–261. doi: 10.1007/978-1-61779-986-0_17. PubMed DOI

Djilianov D.L., Dobrev P.I., Moyankova D.P., Vankova R., Georgieva D.Ts., Gajdošová S., Motyka V. Dynamics of Endogenous Phytohormones during Desiccation and Recovery of the Resurrection Plant Species Haberlea rhodopensis. J. Plant. Growth Regul. 2013;32:564–574. doi: 10.1007/s00344-013-9323-y. DOI

Hanuš J., Siglerová V., Matucha M. N6-alkyladenosines and adenines labelled with tritium. J. Label. Compd. Radiopharm. 2000;43:523–531. doi: 10.1002/(SICI)1099-1344(200004)43:5<523::AID-JLCR339>3.0.CO;2-O. DOI

Motyka V., Vaňková R., Čapková V., Petrášek J., Kamínek M., Schmülling T. Cytokinin-induced upregulation of cytokinin oxidase activity in tobacco includes changes in enzyme glycosylation and secretion. Physiol. Plant. 2003;117:11–21. doi: 10.1034/j.1399-3054.2003.1170102.x. DOI

Gaudinová A., Dobrev P.I., Šolcová B., Novák O., Strnad M., Friedecký D., Motyka V. The Involvement of Cytokinin Oxidase/Dehydrogenase and Zeatin Reductase in Regulation of Cytokinin Levels in Pea (Pisum sativum L.) Leaves. J. Plant. Growth Regul. 2005;24:188–200. doi: 10.1007/s00344-005-0043-9. DOI

Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Motyka V., Kamínek M. Physiology and Biochemistry of Cytokinins in Plants: Developed from the Symposium Held at Liblice, Czechoslovakia, 10–14 September 1990. SPB Academic Publishing; The Hague, The Netherlands: 1992. Characterization of Cytokinin Oxidase from Tobacco and Poplar Callus Cultures.

Motyka V., Kamínek M. Cytokinin oxidase from auxin- and cytokinin-dependent callus cultures of tobacco (Nicotiana tabacum L.) J. Plant. Growth Regul. 1994;13:1–9. doi: 10.1007/BF00210700. DOI

Suzuki T., Miwa K., Ishikawa K., Yamada H., Aiba H., Mizuno T. The Arabidopsis Sensor His-kinase, AHK4, Can Respond to Cytokinins. Plant. Cell Physiol. 2001;42:107–113. doi: 10.1093/pcp/pce037. PubMed DOI

Yamada H., Suzuki T., Terada K., Takei K., Ishikawa K., Miwa K., Yamashino T., Mizuno T. The Arabidopsis AHK4 Histidine Kinase is a Cytokinin-Binding Receptor that Transduces Cytokinin Signals Across the Membrane. Plant. Cell Physiol. 2001;42:1017–1023. doi: 10.1093/pcp/pce127. PubMed DOI

Romanov G.A., Spíchal L., Lomin S.N., Strnad M., Schmülling T. A live cell hormone-binding assay on transgenic bacteria expressing a eukaryotic receptor protein. Anal. Biochem. 2005;347:129–134. doi: 10.1016/j.ab.2005.09.012. PubMed DOI

Capua Y., Eshed Y. Coordination of auxin-triggered leaf initiation by tomato LEAFLESS. Proc. Natl. Acad. Sci. USA. 2017;114:3246–3251. doi: 10.1073/pnas.1617146114. PubMed DOI PMC

Keshishian E.A., Hallmark H.T., Ramaraj T., Plačková L., Sundararajan A., Schilkey F., Novák O., Rashotte A.M. Salt and oxidative stresses uniquely regulate tomato cytokinin levels and transcriptomic response. Plant. Direct. 2018;2:e00071. doi: 10.1002/pld3.71. PubMed DOI PMC

Byng J.W., Chase M.W., Christenhusz M.J.M., Fay M.F., Judd W.S., Mabberley D.J., Sennikov A.N., Soltis D.E., Stevens P.F., Stevens P.F., et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 2016;181:1–20. doi: 10.1111/boj.12385. DOI

Stirk W.A., Ördög V., Novák O., Rolčík J., Strnad M., Bálint P., Staden J. van Auxin and cytokinin relationships in 24 microalgal strains1. J. Phycol. 2013;49:459–467. doi: 10.1111/jpy.12061. PubMed DOI

Morrison E.N., Knowles S., Hayward A., Thorn R.G., Saville B.J., Emery R.J.N. Detection of phytohormones in temperate forest fungi predicts consistent abscisic acid production and a common pathway for cytokinin biosynthesis. Mycologia. 2015;107:245–257. doi: 10.3852/14-157. PubMed DOI

Trdá L., Barešová M., Šašek V., Nováková M., Zahajská L., Dobrev P.I., Motyka V., Burketová L. Cytokinin Metabolism of Pathogenic Fungus Leptosphaeria maculans Involves Isopentenyltransferase, Adenosine Kinase and Cytokinin Oxidase/Dehydrogenase. Front. Microbiol. 2017;8:1374. doi: 10.3389/fmicb.2017.01374. PubMed DOI PMC

Tarakhovskaya E.R., Maslov Yu.I., Shishova M.F. Phytohormones in algae. Russ. J. Plant. Physiol. 2007;54:163–170. doi: 10.1134/S1021443707020021. DOI

Sakakibara H. Cytokinins: Activity, biosynthesis, and translocation. Annu. Rev. Plant. Biol. 2006;57:431–449. doi: 10.1146/annurev.arplant.57.032905.105231. PubMed DOI

Zalabák D., Galuszka P., Mrízová K., Podlešáková K., Gu R., Frébortová J. 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. Physiol. Biochem. 2014;74:283–293. doi: 10.1016/j.plaphy.2013.11.020. PubMed DOI

Skoog F., Armstrong D.J. Cytokinins. Annu. Rev. Plant. Physiol. 1970;21:359–384. doi: 10.1146/annurev.pp.21.060170.002043. DOI

Varga A., Bruinsma J. Effects of Different Cytokinins on the Senescence of Detached Oat Leaves. Planta. 1973;111:91–93. doi: 10.1007/BF00386739. PubMed DOI

Dumbroff E.B., Walker M.A. The Oat-leaf Senescence Test for Cytokinins Reconsidered. Ann. Bot. 1979;44:767–769. doi: 10.1093/oxfordjournals.aob.a085791. DOI

Mik V., Szüčová L., Smehilová M., Zatloukal M., Doležal K., Nisler J., Grúz J., Galuszka P., Strnad M., Spíchal L. N9-substituted derivatives of kinetin: Effective anti-senescence agents. Phytochemistry. 2011;72:821–831. doi: 10.1016/j.phytochem.2011.02.002. PubMed DOI

Szücová L., Spíchal L., Dolezal K., Zatloukal M., Greplová J., Galuszka P., Krystof V., Voller J., Popa I., Massino F.J., et al. Synthesis, characterization and biological activity of ring-substituted 6-benzylamino-9-tetrahydropyran-2-yl and 9-tetrahydrofuran-2-ylpurine derivatives. Bioorg. Med. Chem. 2009;17:1938–1947. doi: 10.1016/j.bmc.2009.01.041. PubMed DOI

Stenlid G. Cytokinins as inhibitors of root growth. Physiol. Plant. 1982;56:500–506. doi: 10.1111/j.1399-3054.1982.tb04546.x. DOI

Ivanov V.B., Filin A.N. Cytokinins regulate root growth through its action on meristematic cell proliferation but not on the transition to differentiation. Funct. Plant. Biol. 2018;45:215–221. doi: 10.1071/FP16340. PubMed DOI

Doležálková L. Characterization and significance of N-glucosyltransferase pathway as a tool for regulation of cytokinin homeostasis in plants. [(accessed on 3 September 2019)];2019 Available online: https://dspace.cuni.cz/handle/20.500.11956/108837.

Conrad K., Motyka V., Schlüter T. Increase in activity, glycosylation and expression of cytokinin oxidase/dehydrogenase during the senescence of barley leaf segments in the dark. Physiol. Plant. 2007;130:572–579. doi: 10.1111/j.1399-3054.2007.00914.x. DOI

Motyka V., Kamínek M. Regulation of Cytokinin Catabolism in Tobacco Callus Cultures. In: Nijkamp H.J.J., Van Der Plas L.H.W., Van Aartrijk J., editors. Progress in Plant Cellular and Molecular Biology: Proceedings of the VIIth International Congress on Plant Tissue and Cell Culture, Amsterdam, The Netherlands, 24–29 June 1990. Springer; Dordrecht, The Netherlands: 1990. pp. 492–497. Current Plant Science and Biotechnology in Agriculture.

Kamínek M., Motyka V., Vaňková R. Regulation of cytokinin content in plant cells. Physiol. Plant. 1997;101:689–700. doi: 10.1111/j.1399-3054.1997.tb01053.x. DOI

Dynamic changes of endogenous phytohormones and carbohydrates during spontaneous morphogenesis of Centaurium erythraea Rafn

Desiccation as a Post-maturation Treatment Helps Complete Maturation of Norway Spruce Somatic Embryos: Carbohydrates, Phytohormones and Proteomic Status

Hormonome Dynamics During Microgametogenesis in Different Nicotiana Species

Integrating the Roles for Cytokinin and Auxin in De Novo Shoot Organogenesis: From Hormone Uptake to Signaling Outputs

Evolutionary diversification of cytokinin-specific glucosyltransferases in angiosperms and enigma of missing cis-zeatin O-glucosyltransferase gene in Brassicaceae

The Hulks and the Deadpools of the Cytokinin Universe: A Dual Strategy for Cytokinin Production, Translocation, and Signal Transduction