Abstract
The facts of both positive and negative influences of cytokinins on stress resistance of plants are known today. Without pretending to a final choice between these points of view, we have made an attempt to analyze the details of the experiments that gave rise to conclusions about the nature of the effect of cytokinins on the resistance to stress-causing influences with a focus on their intensity and duration. The review deals with the data concerning the influence of different adverse factors on the content of endogenous cytokinins and transduction of cytokinin signals, examines the influence on plant resistance of treatment with exogenous hormone, and the effects of genetic modifications causing changes in cytokinin content and signaling. Resistance is considered not only as a mean of plant survival under severe stress but also as an instrument of maintaining growth rate in plants exposed to moderate stress. Literature data and our own results make it possible to conclude that cytokinins play an important role in formation of plant resistance to adverse influences; however, the effect of these hormones depends on stress intensity. Under moderate stress, cytokinins ensure maintenance of plant growth, whereas a drop in cytokinins hampers growth under a strong influence of adverse factors, which is a prerequisite for mobilization of limited resources characteristic of severe stress and ensures preservation of plant viability.
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Abbreviations
- CK:
-
cytokinins
References
Argueso, C.T., Ferreira, F.J., and Kieber, J.J., Environmental perception avenues: the interaction of cytokinin and environmental response pathways, Plant Cell Environ., 2009, vol. 32, pp. 1147–1160.
Cheikh, N. and Jones, R.J., Disruption of maize kernel growth and development by heat stress. Role of cytokinin/abscisic acid balance, Plant Physiol., 1994, vol. 106, pp. 45–51.
Pons, T.L., Jordi, W., and Kuiper, D., Acclimation of plants to light gradients in leaf canopies; evidence for a possible role for cytokinins transported in the transpiration stream, J. Exp. Bot., 2001, vol. 52, pp. 1–12.
Kang, N.Y., Cho, C., Kim, N.Y., and Kim, J., Cytokinin receptor-dependent and receptor-independent pathways in the dehydration response of Arabidopsis thaliana, J. Plant Physiol., 2012, vol. 169, pp. 1382–1391.
Arkhipova, T.N., Prinsen, E., Veselov, S.U., Martineko, E.V., Melentiev, A.I., and Kudoyarova, G.R., Cytokinin producing bacteria enhances plant growth in drying soil, Plant Soil, 2007, vol. 292, pp. 305–315.
Werner, T., Motyka, V., Laucou, V., Smets, R., van Onckelen, H., and Schmülling, T., Cytokinindeficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity, Plant Cell, 2003, vol. 15, pp. 2532–2550.
Nishiyama, R., Le, D.T., Watanabe, Y., Matsui, A., Tanaka, M., Seki, M., Yamaguchi-Shinozaki, K., Shinozaki, K., and Tran, L.S.P., Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency, PLoS One, 2012, vol. 7, p. e32124. doi 10.1371/journal.pone.0032124
Tran, L.S.P., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K., and Yamaguchi-Shinozaki, K., Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 20623–20628.
Rivero, R.M., Kojima, M., Gepstein, A., Sakakibara, H., Mittler, R., Gepstein, S., and Blumwald, E., Delayed leaf senescence induces extreme drought tolerance in a flowering plant, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp.19631–19636.
Xu, Y., Tian, J., Gianfagna, T., and Huang, B., Effects of SAG12-ipt expression on cytokinin production, growth and senescence of creeping bentgrass (A. stolonifera) under heat stress, Plant Growth Regul., 2009, vol. 57, pp. 281–291.
Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D.T., Kojima, M., Werner, T., Vankova, R., Yamaguchi-shinozaki, K., Shinozaki, K., Kakimoto, T., Sakakibara, H., Schmülling, T., and Tran, L.S., Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis, Plant Cell, 2011, vol. 23, pp. 2169–2183.
Li, W., Herrera-Estrella, L., and Tran, L.S., The yinyang of cytokinin homeostasis and drought acclimation/ adaptation, Trends Plant Sci., 2016, vol. 21, no. 7, pp. 548–550. doi 10.1016/j.tplants.2016.05.006
Zwack, P.J. and Rashotte, A.M., Interactions between cytokinin signaling and abiotic stress responses, J. Exp. Bot., 2015, vol. 66, pp. C. 4863–4871.
Downes, B.P. and Crowell, D.N., Cytokinin regulates the expreßsion of a soybean ß-expansin gene by a posttranscriptional mechanism, Plant Mol. Biol., 1998, vol. 37, pp. 437–444.
Ružicka, K., Šimašková, M., Duclercq, J., Petrášek, J., Zažímalovaé, E., Simon, S., Friml, J., van Montagu, M.C., and Benková, E., Cytokinin regulates root meristem activity via modulation of the polar auxin transport, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 4284–4289.
Gordon, S.P., Chickarmane, V.S., Ohno, C., and Meyerowitz, E.M., Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 16529–16534.
Kulaeva, O.N., Tsitokininy, ikh struktura i funktsiya (Cytokinins, Their Structure and Function), Moscow: Nauka, 1973.
Kusnetsov, V.V., Oelmüller, R., Sarwat, M.I., Porfirova, S.A., Cherepneva, G.N., Herrmann, R.G., and Kulaeva, O.N., Cytokinins, abscisic acid and light affect on accumulation of chloroplast proteins in Lupinus luteus cotyledons without notable effect on steady state mRNA levels, Planta, 1994, vol. 194, pp. 318–327.
Zubo, Y.O., Yamburenko, M.V., Selivankina, S.Yu., Shakirova, F.M., Avalbaev, A.M., Kudryakova, N.V., Zubkova, N.K., Liere, K., Kulaeva, O.N., Kusnetsov, V.V., and Börner, Th., Cytokinins stimulate chloroplast transcription in detached barley leaves, Plant Physiol., 2008, vol. 148, pp. 1082–1093.
Kudoyarova, G.R., Dodd, I.C., Veselov, D.S., Rothwell, S.A., and Veselov, S.Y., Common and specific responses to availability of mineral nutrients and water, J. Exp. Bot., 2015, vol. 66, pp. 2133–2144.
Davies, W.J., Kudoyarova, G., and Hartung, W., Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought, J. Plant Growth Regul., 2005, vol. 24, pp. 285–295.
Kiba, T., Kudo, T., Kojima, M., and Sakakibara, H., Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin, J. Exp. Bot., 2011, vol. 62, pp. 1399–1409.
Dewitte, W., Chiappetta, A., Azmi, A., Witters, A., Strnad, M., Rembur, J., Noin, M., Chriqui, D., and van Onckelen, H.A., Dynamics of cytokinins in apical shoot meristems of a day-neutral tobacco during floral transition and flower formation, Plant Physiol., 1999, vol. 119, pp. 111–121.
Hwang, I., Sheen, J., and Muller, B., Cytokinin signaling networks, Annu. Rev. Plant Biol., 2012, vol. 63, pp. 353–380.
Kohli, A., Sreenivasulu, N., Lakshmanan, P., and Kumar, P.P., The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses, Plant Cell Rep., 2013, vol. 32, pp. 945–957.
Vysotskaya, L.B., Aval’baev, A.M., Yuldashev, R.A., Shakirova, F.M., Veselov, S.Yu., and Kudoyarova, G.R., Regulation of cytokinin oxidase activity as a factor affecting the content of cytokinins, Russ. J. Plant Physiol., 2010, vol. 57, pp. 494–500.
Ha, S., Vankova, R., Yamaguchi-Shinozaki, K., Shinozaki, K., and Tran, L.S., Cytokinins: metabolism and function in plant adaptation to environmental stresses, Trends Plant Sci., 2012, vol. 17, pp. 172–179.
Fricke, W., Akhiyarova, G., Wei, W., Alexandersson, E., Miller, A., Kjellbom, P.O., Richardson, A., Wojciechowski, T., Schreiber, L., Veselov, D., Kudoyarova, G., and Volkov, V., The short-term growth response to salt of the developing barley leaf, J. Exp. Bot., 2006, vol. 57, pp. 1079–1095.
Vyroubalová, S., Václaviková, K., Turecková, V., Novák, O., Smehilová, M., Hluska, T., Ohnoutková, L., Frébort, I., and 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, vol. 151, pp. 433–447.
Vankova, R., Gaudinova, A., Dobrev, P., Malbeck, J., Haisel, D., and Motyka, V., Comparison of salinity and drought stress effects on abscisic acid metabolites activity of cytokinin oxidase/dehydrogenase and chlorophyll levels in radish and tobacco, Ecol. Quest., 2011, vol. 14, pp. 99–100.
Ghanem, M.E., Albacete, A., Martínez-Andujar, C., Acosta, M., Romero-Aranda, R., Dodd, I.C., Lutts, S., and Perez-Alfocea, F., Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.), J. Exp. Bot., 2008, vol. 59, pp. 3039–3050.
Veselova, S.V., Farkhutdinov, R.G., Veselov, D.S., and Kudoyarova, G.R., Role of cytokinins in the regulation of stomatal conductance of wheat seedlings under conditions of rapidly changing local temperature, Russ. J. Plant Physiol., 2006, vol. 53, pp. 756–761.
Veselova, S.V., Farhutdinov, R.G., Veselov, S.Yu., Kudoyarova, G.R., Veselov, D.S., and Hartung, W., The effect of root cooling on hormone content, leaf conductance and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.), J. Plant Physiol., 2005, vol. 162, pp. 21–26.
Kosová, K., Prášil, I.T., Vitámvás, P., Dobrev, P., Motyka, V., Floková, K., Novák, O., Turecková, V., Rolcik, J., Pešek, B., Trávnicková, A., Gaudinová, A., Galiba, G., Janda, T., Vlasáková, E., et al., Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra, J. Plant Physiol., 2012, vol. 169, pp. 567–576.
Li, R., Sosa, J.L., and Zavala, M.E., Accumulation of zeatin O-glycosyltransferase in Phaseolus vulgaris and Zea mays following cold stress, Plant Growth Regul., 2000, vol. 32, pp. 295–305.
Maruyama, K., Urano, K., Yoshiwara, K., Morishita, M., Sakurai, N., Suzuki, H., Kojima, M., Sakakibara, H., Shibata, D., Saito, K., Shinozaki, K., and Yamaguchi-Shinozaki, K., Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts, Plant Physiol., 2014, vol. 164, pp. 1759–1771.
Jeon, J., Kim, N.Y., Kim, S., Kang, N.Y., Novak, O., Ku, S.J., Cho, C., Lee, D.J., Lee, E.J., Strnad, M., and Kim, J., A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis, J. Biol. Chem., 2010, vol. 285, pp. 23371–23386.
Dobrá, J., Cerný, M., Štorchová, H., Dobrev, P., Skalák, J., Jedelský, P.L., Lukšanová, H., Gaudinová, A., Pešek, B., Malbeck, J., Vanek, T., Brzobohatý, B., and Vanková, R., The impact of heat stress targeting on the hormonal and transcriptomic response in Arabidopsis, Plant Sci., 2015, vol. 231, pp. 52–61.
Liu, X. and Huang, B., Cytokinin effects on creeping bentgrass response to heat stress. II. Leaf senescence and antioxidant metabolism, Crop Sci., 2002, vol. 42, pp. 466–472.
Kudoyarova, G.R., Vysotskaya, L.B., Cherkozyanova, A., and Dodd, I.C., Effect of partial rootzone drying on the concentration of zeatin-type cytokinins in tomato (Solanum lycopersicum L.) xylem sap and leaves, J. Exp. Bot., 2007, vol. 58, pp. 161–168.
Brugiere, N., Jiao, S., Hantke, S., Zinselmeier, C., Roessler, J.A., Niu, X., Jones, R.J., and Habben, J.E., Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by CKs, abscisic acid, and abiotic stress, Plant Physiol., 2003, vol. 132, pp. 1228–1240.
Hansen, H. and Dörffling, K., Root-derived transzeatin riboside and abscisic acid in drought-stressed and rewatered sunflower plants: interaction in the control of leaf diffusive resistance? Funct. Plant Biol., 2003, vol. 30, pp. 365–375.
Havlová, M., Dobrev, P.I., Motyka, V., Storchová, H., Libus, J., Dobrá, J., Malbeck, J., Gaudinová, H., and Vanková, R., The role of cytokinins in responses to water deficit in tobacco plants over-expressing transzeatin O-glucosyltransferase gene under 35S or SAG12 promoters, Plant Cell Environ., 2008, vol. 31, pp. 341–353.
Pospisilova, J., Vagner, M., Malbeck, J., Travnickova, A., and Batkova, P., Interactions between abscisic acid and cytokinins during water stress and subsequent rehydration, Biol. Plant., 2005, vol. 49, pp. 533–540.
Vysotskaya, L.B., Korobova, A.V., Veselov, S.Y., Dodd, I.C., and Kudoyarova, G.R., ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrient deprived durum wheat, Funct. Plant Biol., 2009, vol. 36, pp. 66–72.
Romanov, G.A., How do cytokinins affect the cell? Russ. J. Plant Physiol., 2009, vol. 56, pp. 268–290.
Brenner, W.G., Ramireddy, E., Heyl, A., and Schmülling, T., Gene regulation by cytokinin in Arabidopsis, Front. Plant Sci., 2012, vol. 3: 8, doi 10.3389/ fpls.2012.00008
Le, D.T., Nishiyama, R., Watanabe, Y., Vankova, R., Tanaka, M., Seki, M., Ham, L.H., Yamaguchi-Shinozaki, K., Shinozaki, K., and Tran, L.S., Identification and expression analysis of cytokinin metabolic genes in soybean under normal and drought conditions in relation to cytokinin levels, PLoS One, 2012, vol. 7, p. e42411. doi 10.1371/journal.pone.0042411
Jain, M., Tyagi, A.K., and Khurana, J.P., Differential gene expression of rice two-component signaling elements during reproductive development and regulation by abiotic stress, Funct. Integr. Genomics, 2008, vol. 8, pp. 175–180.
Wohlbach, D.J., Quirino, B.F., and Sussman, M.R., Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation, Plant Cell, 2008, vol. 20, pp. 1101–1117.
D’Agostino, I.B.D., Deruere, J., and Kieber, J.J., Characterization of the response of the Arabidopsis response regulator gene family to cytokinin, Plant Physiol., 2000, vol. 124, pp. 1706–1717.
Aloni, R., Langhans, M., Aloni, E., Dreieicher, E., and Ullrich, C.I., Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream, J. Exp. Bot., 2005, vol. 56, pp. 1535–1544.
Ali, Z., Basra, S.M.A., Munir, H., Mahmood, A., and Yousaf, S., Mitigation of drought stress in maize by natural and synthetic growth promoters, J. Agric. Soc. Sci., 2011, vol. 7, pp. 56–62.
Veerasamy, M., He, Y., and Huang, B., Leaf senescence and protein metabolism in creeping bentgrass exposed to heat stress and treated with cytokinins, J. Am. Soc. Hort. Sci., 2007, vol. 132, pp. 467–472.
Jespersen, D., Yu, J., and Huang, B., Metabolite responses to exogenous application of nitrogen, cytokinin, and ethylene inhibitors in relation to heat-induced senescence in creeping bentgrass, PLoS ONE, 2015, vol. 10, p. e0123744. doi 10.1371/journal.pone.0123744
Gadallah, M., Effects of kinetin on growth, grain yield and some mineral elements in wheat plants growing under excess salinity and oxygen deficiency, Plant Growth Regul., 1999, vol. 27, pp. 63–74.
Jeon, J. and Kim, J., Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein 2 (AHP2, AHP3, and AHP5) function in cold signaling, Plant Physiol., 2013, vol. 161, pp. 408–424.
Xia, J., Zhao, H., Liu, W., Li, L., and He, Y., Role of cytokinin and salicylic acid in plant growth at low temperatures, Plant Growth Regul., 2009, vol. 57, pp. 211–221.
Wang, Y., Shen, W., Chan, Z., and Wu, Y., Endogenous cytokinin overproduction modulates ROS homeostasis and decreases salt stress resistance in Arabidopsis thaliana, Front. Plant Sci., 2015, vol. 6, p. 1004. doi 10.3389/fpls.2015.01004
Reguera, M., Peleg, Z., Abdel-Tawab, Y.M., Tumimbang, E.B., Delatorre, C.A., and Blumwald, E., Stress-induced cytokinin synthesis increases drought tolerance through the coordinated regulation of carbon and nitrogen assimilation in rice, Plant Physiol., 2013, vol. 163, pp. 1609–1622.
Zhang, P., Wang, W.Q., Zhang, G.L., Kaminek, M., Dobrev, P., Xu, J., and Gruissem, W., Senescenceinducible expression of isopentenyl transferase extends leaf life, increases drought stress resistance and alters cytokinin metabolism in cassava, J. Integr. Plant Biol., 2010, vol. 52, pp. 653–659.
Qin, H., Gu, Q., Zhang, J., Sun, L., Kuppu, S., Zhang, Y., Burow, M., Payton, P., Blumwald, E., and Zhang, H., Regulated expression of an isopentenyltransferase gene (IPT) in peanut significantly improves drought tolerance and increases yield under field conditions, Plant Cell Physiol., 2011, vol. 52, pp. 1904–1914.
Macková, H., Hronková, M., Dobrá, J., Turecková, V., Novák, O., Lubovská, Z., Motyka, V., Haisel, D., Hájek, T., Prášil, I.T., Gaudinová, A., Štorchová, H., Ge, E., Werner, T., Schmülling, T., et al., Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression, J. Exp. Bot., 2013, vol. 64, pp. 2805–2815.
Cerný, M., Kuklová, A., Hoehenwarter, W., and Brzobohaty, B., Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and upregulation, J. Exp. Bot., 2013, vol. 64, pp. 4193–4206.
Vysotskaya, L.B., Kudoyarova, G.R., and Veselov, S.Yu., Effect on shoot water relations, and cytokinin and abscisic acid levels of inducing expression of a gene coding for isopentenyltransferase in roots of transgenic tobacco plants, J. Exp. Bot., 2010, vol. 61, pp. 3709–3717.
Karan, R., Singla-Pareek, S.L., and Pareek, A., Histidine kinase and response regulator genes as they relate to salinity tolerance in rice, Funct. Integr. Genomics, 2009, vol. 9, pp. 411–417.
Kumar, M.N. and Verslues, P.E., Stress physiology functions of the Arabidopsis histidine kinase cytokinin receptors, Physiol. Plant., 2015, vol. 154, pp. 369–380.
Shi, Y., Tian, S., Hou, L., Huang, X., Zhang, X., Guo, H., and Yang, S., Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis, Plant Cell, 2012, vol. 24, pp. 2578–2595.
Mason, M.G., Jha, D., Salt, D.E., Tester, M., Hill, K., Kieber, J.J., and Schaller, G.E., Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1;1 and accumulation of sodium in Arabidopsis shoots, Plant J., 2010, vol. 64, pp. 753–763.
Lichtenthaler, H.K. and Burkart, S., Photosynthesis and high light stress, Bulg. J. Plant Physiol., 1999, vol. 25, pp. 3–16.
Cortleven, A., Nitschke, S., Klaumünzer, M., Abdelgawad, H., Asard, H., Grimm, B., Riefler, M., and Schmülling, T., A novel protective function for cytokinin in the light stress response is mediated by the Arabidopsis histidine kinase 2 and Arabidopsis histidine kinase 3 receptors, Plant Physiol., 2014, vol. 164, pp. 1470–1483.
Danilova, M.N., Kudryakova, N.V., Voronin, P.Yu., Oelmü ller, R., Kusnetsov, V.V., and Kulaeva, O.N., Membrane receptors of cytokinin and their regulatory role in Arabidopsis thaliana plant response to photooxidative stress under conditions of water deficit, Russ. J. Plant Physiol., 2014, vol. 61, pp. 434–442.
Guan, C., Wang, X., Feng, J., Hong, S., Liang, Y., Ren, B., and Zuo, J., Cytokinin antagonizes abscisic acid-mediated inhibition of cotyledon greening by promoting the degradation of abscisic acid insensitive 5 protein in Arabidopsis, Plant Physiol., 2014, vol. 164, pp. 1515–1526.
Cerný, M., Jedelský, P.L., Novák, J., Schlosser, A., and Brzobohatý, B., Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis, Plant Cell Environ., 2014, vol. 37, pp. 1641–1655.
Nguyen, K.H., Ha, C.V., Nishiyama, R., Watanabe, Y., Leyva-González, M.A., Fujita, Y., Tran, U.T., Li, W., Tanaka, M., Seki, M., Schaller, G.E., Herrera-Estrella, L., and Tran, L.S., Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought, Proc. Natl. Acad. Sci. USA, 2016, vol. 113, pp. 3090–3095.
Qin, F., Shinozaki, K., and Yamaguchi-Shinozaki, K., Achievements and challenges in understanding plant abiotic stress responses and tolerance, Plant Cell Physiol., 2011, vol. 52, pp. 1569–1582.
Farkhutdinov, R., Veselova, S., Veselov, D.S., Mitrichenko, A., Dedov, A., and Kudoyarova, G.R., The effect of rapid temperature increase on the growth rate of wheat leaves, Russ. J. Plant Physiol., 2003, vol. 50, pp. 247–250.
Tardieu, F., Plant tolerance to water deficit: physical limits and possibilities for progress, C. R. Geosci., 2005, vol. 337, pp. 57–67.
Jones, P., Keane, E.M., and Osborne, B.A., Effects of alien cytoplasmic variation on carbon assimilation and productivity in wheat, J. Exp. Bot., 1998, vol. 49, pp. 1519–1528.
Žižková, E., Dobrev, P.I., Muhovski, Y., Hošek, P., Hoyerová, K., Haisel, D., Procházková, D., Lutts, S., Motyka, V., and Hichri, I., Tomato (Solanum lycopersicum L.) SlIPT3 and SlIPT4 isopentenyltransferases mediate salt stress response in tomato, BMC Plant Biol., 2015, vol. 15, p. 85. doi 10.1186/s12870-015- 0415-7
Werner, T., Nehnevajova, E., Köllmer, I., Novák, O., Strnad, M., Krämer, U., and Schmülling, T., Rootspecific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco, Plant Cell, 2010, vol. 22, pp. 3905–3920.
Marhavý, P., Bielach, A., Abas, L., Abuzeineh, A., Duclercq, J., Tanaka, H., Parezová, M., Petrášek, J., Friml, J., Kleine-Vehn, J., and Benková, E., Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis, Dev. Cell, 2011, vol. 21, pp. 796–804.
Sun, L., Zhang, Q., Wu, J., Zhang, L., Jiao, X., Zhang, S., Zhang, Z., Sun, D., Lu, T., and Sun, Y., Two rice authentic histidine phosphotransfer proteins,OsAHP1 and OsAHP2,mediate cytokinin signaling and stress responses in rice, Plant Physiol., 2014, vol. 165, pp. 335–345.
Moya, J.L., Primo-Millo, E., and Talon, M., Morphological factors determining salt tolerance in citrus seedlings: the shoot to root ratio modulates passive root uptake of chloride ions and their accumulation in leaves, Plant Cell Environ., 1999, vol. 22, pp. 1435–1433.
Werner, T., Holst, K., Pörs, Y., Guivarc’h, A., Mustroph, A., Chriqui, D., Grimm, B., and Schmülling, T., Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots, J. Exp. Bot., 2008, vol. 59, pp. 2659–2672.
Brenner, W.G., Romanov, G.A., Köllmer, I., Bürkle, L., and Schmülling, T., Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokininsensitive processes and suggest cytokinin action through transcriptional cascades, Plant J., 2005, vol. 44, pp. 314–333.
Gupta, S., Shi, X., Lindquist, I.E., Devitt, N.P., Mudge, J., and Rashotte, A.M., Transcriptome profiling of cytokinin and auxin regulation in tomato root, J. Exp. Bot., 2013, vol. 64, pp. 695–704.
Lee, D.J., Park, J.Y., Ku, S.J., Ha, Y.M., Kim, S., Kim, M.D., Oh, M.H., and Kim, J., Genome-wide expression profiling of Arabidopsis response regulator 7 (ARR7) overexpression in cytokinin response, Mol. Gen. Genomics, 2007, vol. 277, pp. 115–137.
Huang, D., Wu, W., Abrams, S.R., and Cutler, A.J., The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors, J. Exp. Bot., 2008, vol. 59, pp. 2991–3007.
Mortimer, J.C., Laohavisit, A., Macpherson, N., Webb, A., Brownlee, C., Battey, N.H., and Davies, J.M., Annexins: multifunctional components of growth and adaptation, J. Exp. Bot., 2008, vol. 59, pp. 533–544.
Rashotte, A.M., Carson, S.D.B., To, J.P.C., and Kieber, J.J., Expression profiling of cytokinin action in Arabidopsis, Plant Physiol., 2003, vol. 132, pp. 1998–2011.
Sappl, P.G., Carroll, A.J., Clifton, R., Lister, R., Whelan, J., Millar, A.H., and Singh, K.B., The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress, Plant J., 2009, vol. 58, pp. 53–68.
Zavaleta-Mancera, H.A., López-Delgado, H., Loza-Tavera, H., Mora-Herrera, M., Trevilla-García, C., Vargas-Suárez, M., and Ougham, H., Cytokinin promotes catalase and ascorbate peroxidase activities and preserves the chloroplast integrity during ark-senescence, J. Plant Physiol., 2007, vol. 164, pp. 1572–1582.
Procházková, D., Haisel, D., and Wilhelmová, N., Antioxidant protection during ageing and senescence in chloroplasts of tobacco with modulated life span, Cell Biochem. Funct., 2008, vol. 26, pp. 582–590.
Köhler, K.-H. and Conrad, K., Zur Spezifitat des Amaranthus- cytokinintests. III. Benzimidazolderivate und andere Verbindungen, Flora, 1968, vol. 159, pp. 293–298.
Khokhlova, V.A., Karavaiko, N.N., Podergina, T.A., and Kulaeva, O.N., Antagonism in abscisic acid and cytokinin action on the structural and biochemical differentiation of chloroplasts in isolated pumpkin cotyledons, Tsitologiya, 1978, vol. 20, no. 9, pp. 1033–1052.
Kravtsov, A.K., Zubo, Ya.O., Yamburenko, M.V., Kulaeva, O.N., and Kusnetsov, V.V., Cytokinin and abscisic acid control plastid gene transcription during barley seedling de-etiolation, Plant Growth Regul., 2011, vol. 64, pp. 173–183. doi 10.1007/s10725-010- 9553-y
Li, W.X., Oono, Y., Zhu, J., He, X.J., Wu, J.M., Iida, K., Lu, X.Y., Cui, X., Jin, H., and Zhu, J.K., The Arabidopsis nfya5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance, Plant Cell, 2008, vol. 20, pp. 2238–2251.
Zeevaart, J.A.D. and Creelman, R.A., Metabolism and physiology of abscisic acid, Annu. Rev. Plant. Physiol., 1988, vol. 39, pp. 439–473.
Munns, R., Why measure osmotic adjustment? Aust. J. Plant Physiol., 1988, vol. 15, pp. 717–726.
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Original Russian Text © D.S. Veselov, G.R. Kudoyarova, N.V. Kudryakova, V.V. Kusnetsov, 2017, published in Fiziologiya Rastenii, 2017, Vol. 64, No. 1, pp. 19–32.
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Veselov, D.S., Kudoyarova, G.R., Kudryakova, N.V. et al. Role of cytokinins in stress resistance of plants. Russ J Plant Physiol 64, 15–27 (2017). https://doi.org/10.1134/S1021443717010162
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DOI: https://doi.org/10.1134/S1021443717010162