Plant hormones regulate numerous developmental and physiological processes. Abiotic stresses considerably affect production and distribution of phytohormones as the stress signal triggers. The homeostasis of plant hormones is controlled by their de novo synthesis and catabolism. The aim of this work was to analyse the contents of total and individual groups of endogenous cytokinins (CKs) as well as indole-3-acetic acid (IAA) in AtCKX overexpressing centaury plants grown in vitro on graded NaCl concentrations (0, 50, 100, 150, 200 mM). The levels of endogenous stress hormones including abscisic acid (ABA), salicylic acid (SA) and jasmonic acid (JA) were also detected. The elevated contents of total CKs were found in all analysed centaury shoots. Furthermore, increased amounts of all five CK groups, as well as enhanced total CKs were revealed on graded NaCl concentrations in non-transformed and AtCKX roots. All analysed AtCKX centaury lines exhibited decreased amounts of endogenous IAA in shoots and roots. Consequently, the IAA/bioactive CK forms ratios showed a significant variation in the shoots and roots of all AtCKX lines. In shoots and roots of both non-transformed and AtCKX transgenic centaury plants, salinity was associated with an increase of ABA and JA and a decrease of SA content.

Department for Plant Physiology Institute for Biological Research Siniša Stanković National Institute of Republic of Serbia University of Belgrade Bulevar despota Stefana 142 Belgrade 11060 Serbia

Faculty of Biology University of Belgrade Studentski trg 16 Belgrade 11000 Serbia

Institute of Experimental Botany of the Czech Academy of Sciences Rozvojová 263 16502 Prague 6 Czech Republic

Zobrazit více v PubMed

Hussain M, et al. Rice in saline soils: Physiology, biochemistry, genetics, and management. Adv. Agron. 2017;20:1.

Nguyen D, Rieu I, Mariani C, van Dam NM. How plants handle multiple stresses: Hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant. Mol. Biol. 2016;91:727–740. doi: 10.1007/s11103-016-0481-8. PubMed DOI PMC

Fahad S, et al. Phytohormones and plant responses to salinity stress: A review. Plant Growth Regul. 2015;75:391–404. doi: 10.1007/s10725-014-0013-y. DOI

Bielach A, Hrtyan M, Tognetti VB. Plants under stress: Involvement of auxin and cytokinin. Int. J. Mol. Sci. 2017;18:1427. doi: 10.3390/ijms18071427. PubMed DOI PMC

Mok DW, Mok MC. Cytokinin metabolism and action. Annual Rev. Plant Physiol. Plant Mol. Biol. 2001;52:89–118. doi: 10.1146/annurev.arplant.52.1.89. PubMed DOI

Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I. The role of phytohormones in alleviating salt stress in crop plants. Aust. J. Crop Sci. 2011;5:726–734.

Galuszka P, et al. Biochemical characterization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabacum L. Plant Growth Regul. 2007;26:255–267. doi: 10.1007/s00344-007-9008-5. DOI

Gajdošová S, 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

Schmülling T, Werner T, Riefler M, Krupková E, Bartrina y Manns I. Structure and funcyion of cytokinin oxidase dehydrogenase genes of maize, rice, Arabidopsis and other species. J. Plant Res. 2003;116:241–252. doi: 10.1007/s10265-003-0096-4. PubMed DOI

Werner T, et al. 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. 2003;15:2532–2550. doi: 10.1105/tpc.014928. PubMed DOI PMC

Tran LS, Shinozaki K, Yamaguchi-Shinozaki K. Role of cytokinin responsive two-component system in ABA and osmotic stress signalings. Plant Signal Behav. 2010;5:148–150. doi: 10.4161/psb.5.2.10411. PubMed DOI PMC

Nishiyama R, et al. Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS ONE. 2012;7:e32124. doi: 10.1371/journal.pone.0032124. PubMed DOI PMC

Nishiyama R, et al. 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;23:2169–2183. doi: 10.1105/tpc.111.087395. PubMed DOI PMC

Žižková E, et al. Tomato (Solanum lycopersicum L.) SlIPT3 and SlIPT4 isopentenyltransferases mediate salt stress response in tomato. BMC Plant Biol. 2015;15:85. doi: 10.1186/s12870-015-0415-7. PubMed DOI PMC

Trifunović-Momčilov M, et al. Salinity stress response of non-transformed and AtCKX transgenic centaury (Centaurium erythraea Rafn.) shoots and roots grown in vitro. Ann. App. Biol. 2020;177:74–89. doi: 10.1111/aab.12593. PubMed DOI PMC

Lau S, Jurgens G, De Smet I. The evolving complexity of the auxin pathway. Plant Cell. 2008;20:1738–1746. doi: 10.1105/tpc.108.060418. PubMed DOI PMC

Petersson SV, et al. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell. 2009;21:1659–1668. doi: 10.1105/tpc.109.066480. PubMed DOI PMC

Wang Y, Li K, Li X. Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J. Plant Physiol. 2009;166:1637–1645. doi: 10.1016/j.jplph.2009.04.009. PubMed DOI

Kazan K. Auxin and the integration of environmental signals into plant root development. Ann. Bot. 2013;112:1655–1665. doi: 10.1093/aob/mct229. PubMed DOI PMC

Gharbi E, et al. Phytohormone profiling in relation to osmotic adjustment in NaCl-treated plants of the halophyte tomato wild relative species Solanum chilense comparatively to the cultivated glycophyte Solanum lycopersicum. Plant Sci. 2017;258:77–89. doi: 10.1016/j.plantsci.2017.02.006. PubMed DOI

Vishwakarma K, et al. Abscisic acid signaling and abiotic stress tolerance in plants: A review on current knowledge and future prospects. Front. Plant Sci. 2017;8:161. PubMed PMC

Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant Biol. 2010;61:651–679. doi: 10.1146/annurev-arplant-042809-112122. PubMed DOI

Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI. Guard cell signal transduction network: Advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 2010;61:561–591. doi: 10.1146/annurev-arplant-042809-112226. PubMed DOI PMC

Mýtinová Z, et al. Effect of abiotic stresses on the activity of antioxidative enzymes and contents of phytohormones in wild type and AtCKX2 transgenic tobacco plants. Biol. Plant. 2010;54:461–470. doi: 10.1007/s10535-010-0082-3. DOI

Pospíšilová J. Interaction of cytokinins and abscisic acid during regulation of stomatal opening in bean leaves. Photosynthetica. 2003;41:49–56. doi: 10.1023/A:1025852210937. DOI

Wang Y, et al. Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J. 2011;68:249–261. doi: 10.1111/j.1365-313X.2011.04683.x. PubMed DOI

Verslues PE. ABA and cytokinins: Challenge and opportunity for plant stress research. Plant Mol. Biol. 2016;91:629–640. doi: 10.1007/s11103-016-0458-7. PubMed DOI

Jeon J, et al. A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J. Biol. Chem. 2010;M109:23371–23386. doi: 10.1074/jbc.M109.096644. PubMed DOI PMC

Kumar MN, Verslues PE. Stress physiology functions of the Arabidopsis histidine kinase cytokinin receptors. Physiol. Plantarum. 2015;154:369–380. doi: 10.1111/ppl.12290. PubMed DOI

Brugière N, et al. Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol. 2003;132:1228–1240. doi: 10.1104/pp.102.017707. PubMed DOI PMC

Nazar R, Iqbal N, Syeed S, Khan NA. Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J. Plant Physiol. 2011;168:807–815. doi: 10.1016/j.jplph.2010.11.001. PubMed DOI

Saraf, R., Saingar, S., Chaudhary, S. & Chakraborty, D. Response of plants to salinity stress and the role of salicylic acid in modulating tolerance mechanisms: Physiological and proteomic approach in Biotic and abiotic stress tolerance in plants (ed Vats, S.) 103–136 (Springer, 2018).

Rajeshwari V, Bhuvaneshwar V. Enhancing salinity tolerance in Brinjal plants by application of salicylic acid. J. Plant Sci. 2017;12:46–51. doi: 10.3923/jps.2017.46.51. DOI

Mohammadi M, Chaichi MR, Safikhani S. Salicylic acid application alleviates the salt stress effects in wheat. Int. J. Dev. Res. 2019;9:24976–24981.

Shaki F, Maboud HE, Niknam V. Effects of salicylic acid on hormonal cross talk, fatty acids profile, and ions homeostasis from salt-stressed safflower. J. Plant Inter. 2019;14:340–346.

Sawada H, Shim IS, Usui K. Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis modulation by salt stress in rice seedlings. Plant Sci. 2006;171:263–270. doi: 10.1016/j.plantsci.2006.03.020. DOI

Wasternack C, Hause B. Jasmonates and octadecanoids: Signals in plant stress responses and plant development. Prog. Nucleic Acid Res. Mol. Biol. 2002;72:165–221. doi: 10.1016/S0079-6603(02)72070-9. PubMed DOI

Wang Y, Mopper S, Hasentein KH. Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagona. J. Chem. Ecol. 2001;27:327–342. doi: 10.1023/A:1005632506230. PubMed DOI

Pedranzani H, et al. Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul. 2003;41:149–158. doi: 10.1023/A:1027311319940. DOI

Lomin SN, et al. 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

Kamínek M, et al. Purine cytokinins: A proposal for abbreviations. Plant Growth Regul. 2000;32:253–256. doi: 10.1023/A:1010743522048. DOI

Merewitz EB, Gianfagna T, Huang B. Photosynthesis, water use, and root viability under water stress as affected by expression of SAG12-ipt controlling cytokinin synthesis in Agrostis stolonifera. J. Exp. Bot. 2011;62:383–395. doi: 10.1093/jxb/erq285. PubMed DOI PMC

Alvarez S, Marsh EL, Schroeder SG, Schachtman DP. Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ. 2008;31:325–340. doi: 10.1111/j.1365-3040.2007.01770.x. PubMed DOI

Dobra J, et al. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J. Plant Physiol. 2010;167:1360–1370. doi: 10.1016/j.jplph.2010.05.013. PubMed DOI

Werner T, et al. Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and Tobacco. Plant Cell. 2010;22:3905–3920. doi: 10.1105/tpc.109.072694. PubMed DOI PMC

Macková H, et al. Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J. Exp. Bot. 2013;64:2805–2815. doi: 10.1093/jxb/ert131. PubMed DOI PMC

Lubovská Z, Dobrá J, Štorchová H, Wilhelmová N, Vanková R. Cytokinin oxidase/dehydrogenase overexpression modifies antioxidant defense against heat, drought and their combination in Nicotiana tabacum plants. J. Plant Physiol. 2014;171:1625–1633. doi: 10.1016/j.jplph.2014.06.021. PubMed DOI

Pospíšilová H, et al. Transgenic barley overexpressing a cytokinin dehydrogenase gene shows greater tolerance to drought stress. New Biotechnol. 2016;33:692–705. doi: 10.1016/j.nbt.2015.12.005. PubMed DOI

Vojta P, et al. Whole transcriptome analysis of transgenic barley with altered cytokinin homeostasis and increased tolerance to drought stress. New Biotechnol. 2016;33:676–691. doi: 10.1016/j.nbt.2016.01.010. PubMed DOI

Li S, et al. Overexpression of the cytokinin oxidase/dehydrogenase (CKX) from Medicago sativa enhanced salt stress tolerance of Arabidopsis. J. Plant Biol. 2019;62:374–386. doi: 10.1007/s12374-019-0141-z. DOI

Trifunović M, et al. Changes in cytokinin content and altered cytokinin homeostasis in AtCKX1 and AtCKX2-overexpressing centaury (Centaurium erythraea Rafn.) plants grown in vitro. Plant Cell Tiss. Organ Cult. 2015;120:767–777. doi: 10.1007/s11240-014-0646-6. DOI

Hyoung S, et al. Cytokinin oxidase PpCKX1 plays reg-ulatory roles in development and enhances dehydration and salt tolerance in Physcomitrella patens. Plant Cell Rep. 2020;39:419–430. doi: 10.1007/s00299-019-02500-3. PubMed DOI

Schachtman DP, Goodger JQ. Chemical root to shoot signaling under drought. Trends Plant Sci. 2008;13:281–287. doi: 10.1016/j.tplants.2008.04.003. PubMed DOI

Nakabayashi R, et al. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 2014;77:367–379. doi: 10.1111/tpj.12388. PubMed DOI PMC

Liao X, et al. Overexpression of MsDREB6.2 results in cytokinin-deficient developmental phenotypes and enhances drought tolerance in transgenic apple plants. Plant J. 2017;89:510–526. doi: 10.1111/tpj.13401. PubMed DOI

Ramireddy E, et al. Root engineering in barley: Increasing cytokinin degradation produces a larger root system, mineral enrichment in the shoot and improved drought tolerance. Plant Physiol. 2018;177:1078–1095. doi: 10.1104/pp.18.00199. PubMed DOI PMC

Xu S, et al. Wild tobacco genomes reveal the evolution of nicotine biosynthesis. Proc. Natl. Acad. Sci. USA. 2017;114:6133–6138. doi: 10.1073/pnas.1700073114. PubMed DOI PMC

Jang G, Choi YD. Drought stress promotes xylem differentiation by modulating the interaction between cytokinin and jasmonic acid. Plant Signal Behav. 2018;13(3):e1451707. doi: 10.1080/15592324.2018.1451707. PubMed DOI PMC

Zörb C, Geilfus CM, Mühling K, Ludwing-Müller J. The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J. Plant Physiol. 2013;170:220–224. doi: 10.1016/j.jplph.2012.09.012. PubMed DOI

Llanes A, Masciarelli O, Ordoñez R, Isla MI, Luna V. Differential growth responses to sodium salts involve different ABA catabolism and transport in the halophyte Prosopis strombulifera. Biol. Plantarum. 2014;58:80–88. doi: 10.1007/s10535-013-0365-6. DOI

Bishopp A, Benková E, Helariutta Y. Sending mixed messages: Auxin-cytokin in crosstalk in roots. Curr. Opin. Plant. Biol. 2011;14:10–16. doi: 10.1016/j.pbi.2010.08.014. PubMed DOI

Vanstraelen M, Benková E. Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. 2012;28:463–487. doi: 10.1146/annurev-cellbio-101011-155741. PubMed DOI

Werner T, Köllmer I, Bartrina I, Holst K, Schmülling T. New insights into the biology of cytokinin degradation. Plant Biol. 2006;8:371–381. doi: 10.1055/s-2006-923928. PubMed DOI

Jones B, et al. Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell. 2010;22:2956–2969. doi: 10.1105/tpc.110.074856. PubMed DOI PMC

Polanská L, et al. Altered cytokinin metabolism affects cytokinin, auxin, and abscisic acid contents in leaves and chloroplasts, and chloroplast ultrastructure in transgenic tobacco. J. Exp. Bot. 2007;58:637–649. doi: 10.1093/jxb/erl235. PubMed DOI

Prerostova S, et al. Hormonal dynamics during salt stress responses of salt-sensitive Arabidopsis thaliana and salt-tolerant Thellungiella salsuginea. Plant Sci. 2017;264:188–198. doi: 10.1016/j.plantsci.2017.07.020. PubMed DOI

Yang Z, Yu L, Merewitz E, Huang B. Differential effects of abscisic acid and glycine betaine on physiological responses to drought and salinity stress for two perennial grass species. J. Am. Soc. Hortic. Sci. 2012;137:96–106. doi: 10.21273/JASHS.137.2.96. DOI

Sripinyowanicha S, et al. Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): The role of OsP5CS1 and OsP5CR gene expression during salt stress. Environ. Exp. Bot. 2013;86:94–105. doi: 10.1016/j.envexpbot.2010.01.009. DOI

Sales L, et al. Salt tolerance in apple seedlings is affected by exogenous ABA application. Acta Hortic. 2018;1206:121–128. doi: 10.17660/ActaHortic.2018.1206.17. DOI

Qiun ZB, Guo JL, Zhu AJ, Zhang L, Zhang MM. Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol. Environ. Saf. 2014;104:202–208. doi: 10.1016/j.ecoenv.2014.03.014. PubMed DOI

Yuan F, Liang X, Li Y, Yin S, Wang B. Methyl jasmonate improves tolerance to high salt stress in the recretohalophyte Limonium bicolor. Fun. Plant. Biol. 2018;46:82–92. doi: 10.1071/FP18120. PubMed DOI

Yang Y, Qi M, Mei C. Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J. 2004;40:909–919. doi: 10.1111/j.1365-313X.2004.02267.x. PubMed DOI

Zubo YO, Schaller GE. Role of the cytokinin-activated type-B response regulators in hormone crosstalk. Plants. 2020;9(2):166. doi: 10.3390/plants9020166. PubMed DOI PMC

Hao L, et al. Role of endogenous salicylic acid in Arabidopsis response to elevated sulfur dioxide concentration. Biol. Plant. 2011;55:297–304. doi: 10.1007/s10535-011-0042-6. DOI

Devinar G, Llanes A, Masciarelli O, Luna V. Abscisic acid and salicylic acid levels induced by different relative humidity and salinity conditions in the halophyte Prosopis strombulifera. Plant Growth Regul. 2013;70:247–256. doi: 10.1007/s10725-013-9796-5. DOI

Miura K, Sato A, Ohta M, Furukawa J. Increased tolerance to salt stress in the 873 phosphate-accumulating Arabidopsis mutants siz1 and pho2. Planta. 2011;234:1191–1199. doi: 10.1007/s00425-011-1476-y. PubMed DOI

La VH, et al. Antagonistic shifting from abscisic acid- to salicylic acid-mediated sucrose accumulation contributes to drought tolerance in Brassica napus. Environ. Exp. Bot. 2019;162:38–47. doi: 10.1016/j.envexpbot.2019.02.001. DOI

Azooz MM. Salt stress mitigation by seed priming with salicylic acid in two faba bean genotypes differing in salt tolerance. Int. J. Agric. Biol. 2009;11:343–350.

Syeed S, et al. Salicylic acid-mediated changes in photosynthesis, nutrients content and antioxidant metabolism in two mustard (Brassica juncea L.) cultivars differing in salt tolerance. Acta Physiol. Plant. 2011;33:877–886. doi: 10.1007/s11738-010-0614-7. DOI

Trifunović M, et al. Overexpression of Arabidopsis cytokinin oxidase/dehydrogenase genes AtCKX1 and AtCKX2 in transgenic Centaurium erythraea Rafn. Plant Cell Tiss. Organ Cult. 2013;115:139–150. doi: 10.1007/s11240-013-0347-6. DOI

Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plantarum. 1962;15:473–479. doi: 10.1111/j.1399-3054.1962.tb08052.x. DOI

Dobrev PI, 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., Hoyerova, K., Petrasek, J. Analytical Determination of Auxins and Cytokinins in Auxins and Cytokinins in Plant Biology: Methods and Protocols, Book Series: Methods in Molecular Biology vol. 1569, (eds. Dandekar, T., Naseem, M.) 31–39 (Springer, 2017). PubMed

Cytokinin deficiency confers enhanced tolerance to mild, but decreased tolerance to severe salinity stress in in vitro grown potato

Phytohormone profiles in non-transformed and AtCKX transgenic centaury (Centaurium erythraea Rafn) shoots and roots in response to salinity stress in vitro