Cytokinins are well-known to be involved in processes responsible for plant growth and development. More recently, these hormones have begun to be associated with stress responses as well. However, it is unclear how changes in cytokinin biosynthesis, signaling, or transport relate to stress effects. This study examines in parallel how two different stresses, salt, and oxidative stress, affect changes in both cytokinin levels and whole plant transcriptome response. Solanum lycopersicum seedlings were given a short-term (6 hr) exposure to either salt (150 mM NaCl) or oxidative (20 mM H2O2) stress and then examined to determine both changes in cytokinin levels and transcriptome. LC-MS/MS was used to determine the levels of 22 different types of cytokinins in tomato plants including precursors, active, transported, and conjugated forms. When examining cytokinin levels we found that salt treatment caused an increase in both active and inactive cytokinin levels and oxidative stress caused a decrease in these levels. RNA-sequencing analyses of these same stress-treated tissues revealed 6,643 significantly differentially expressed genes (DEGs). Although many DEGs are similar between the two stresses, approximately one-third of the DEGs in each treatment were unique to that stress. Several cytokinin-related genes were among the DEGs. Examination of photosystem II efficiency revealed that cytokinins affect physiological response to stress in tomato, further validating the changes in cytokinin levels seen in planta.

Department of Biological Sciences Auburn University Auburn Alabama

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science of Palacký University and Institute of Experimental Botany of the Czech Academy of Sciences Olomouc Czech Republic

National Center for Genome Resources Santa Fe New Mexico

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Acosta‐Motos, J. R. , Ortuño, M. F. , Bernal‐Vicente, A. , Diaz‐Vivancos, P. , Sanchez‐Blanco, M. J. , & Hernandez, J. A. (2017). Plant responses to salt stress: Adaptive mechanisms. Agronomy, 23, 18 10.3390/agronomy7010018 DOI

Anders, S. , & Huber, W. (2012). Differential Expression of RNA‐Seq Data at the Gene Level–the DESeq Package. Heidelberg, Germany: European Molecular Biology Laboratory (EMBL).

Apel, K. , & Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 373–399. 10.1146/annurev.arplant.55.031903.141701 PubMed DOI

Bar, M. , Israeli, A. , Levy, M. , Gera, H. B. , Jiménez‐Gómez, J. , Kouril, S. , … Ori, N. (2016). CLAUSA is a MYB transcription factor that promotes leaf differentiation by attenuating cytokinin signaling. The Plant Cell, 28, 1602–1615. 10.1105/tpc.16.00211 PubMed DOI PMC

Bose, J. , Rodrigo‐Moreno, A. , & Shabala, S. (2014). ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany, 65, 1241–1257. 10.1093/jxb/ert430 PubMed DOI

Capua, Y. , & Eshed, Y. (2017). Coordination of auxin‐triggered leaf initiation by tomato LEAFLESS. PNAS, 114, 3246–3251. 10.1073/pnas.1617146114 PubMed DOI PMC

Davies, P. J. (2004). Plant Hormones: Biosynthesis, Signal Transduction, Action!. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Duque, A. S. , deAlmeida, A. M. , da Silva, A. B. , da Silva, J. M. , Farinha, A. P. , Santos, D. , … deSousa Araújo, S. (2013). Abiotic stress responses in plants: Unraveling the complexity of genes and networks to survive In Vahdati K. (Ed.), Abiotic Stress ‐ Plant Responses and Applications in Agriculture. London, UK: InTech. ISBN: 978‐953‐51‐1024‐8.

Ghanem, M. E. , Albacete, A. , Martínez‐Andújar, C. , Acosta, M. , Romero‐Aranda, R. , Dodd, I. C. , … Pérez‐Alfocea, F. (2008). Hormonal changes during salinity‐induced leaf senescence in tomato (Solanum lycopersicum L.). Journal of Experimental Botany, 59, 3039–3050. 10.1093/jxb/ern153 PubMed DOI PMC

Ghanem, M. E. , Albacete, A. , Smigocki, A. C. , Frébort, I. , Pospíšilová, H. , Martínez‐Andújar, C. , … Pérez‐Alfocea, F. (2011). Root‐synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. Journal of Experimental Botany, 62, 125–140. 10.1093/jxb/erq266 PubMed DOI PMC

Gill, S. S. , & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909–930. 10.1016/j.plaphy.2010.08.016 PubMed DOI

Gupta, S. , Shi, X. , Lindquist, I. E. , Devitt, N. P. , Mudge, J. , & Rashotte, A. M. (2013). Transcriptome profiling of cytokinin and auxin regulation in tomato root. Journal of Experimental Botany, 64, 695–704. 10.1093/jxb/ers365 PubMed DOI PMC

Ismail, A. M. , & Horie, T. (2017). Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annual Review of Plant Biology, 68, 1 10.1146/annurev-arplant-042916-040936 PubMed DOI

Joshi, R. , Sahoo, K. K. , Tripathi, A. K. , Kumar, R. , Gupta, B. K. , Pareek, A. , & Singla‐Pareek, S. L. (2018). Knockdown of an inflorescence meristem‐specific cytokinin oxidase‐OsCKX2 in rice reduces yield penalty under salinity stress condition. Plant, Cell and Environment, 41, 936–946. 10.1111/pce.12947 PubMed DOI

Letham, D. S. (1971). Regulators of cell division in plant tissues XII. A cytokinin bioassay using excised radish cotyledons. Physiologia Plantarum, 25, 391–396. 10.1111/j.1399-3054.1971.tb01462.x DOI

Mackova, H. , Hronkova, M. , Dobra, J. , Tureckova, V. , Novak, O. , Lubovska, Z. , … Vankova, R. (2013). Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. Journal of Experimental Botany, 64, 2805–2815. 10.1093/jxb/ert131 PubMed DOI PMC

Miller, N. A. , Kingsmore, S. F. , Farmer, A. , Langley, R. J. , Mudge, J. , Crow, J. A. , … May, G. D. (2008). Management of high‐throughput DNA sequencing projects: Alpheus. Journal of Computer Science and Systems Biology, 1, 132. PubMed PMC

Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405–410. 10.1016/S1360-1385(02)02312-9 PubMed DOI

Mittler, R. , Finka, A. , & Goloubinoff, P. (2012). How do plants feel the heat? Trends in Biochemical Sciences, 37, 118–125. 10.1016/j.tibs.2011.11.007 PubMed DOI

Mittler, R. , Vanderauwera, S. , Gollery, M. , & Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends in Plant Science, 9, 490–498. 10.1016/j.tplants.2004.08.009 PubMed DOI

Mittova, V. , Tal, M. , Volokita, M. , & Guy, M. (2003). Up‐regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt‐induced oxidative stress in the wild salt‐tolerant tomato species Lycopersicon pennellii. Plant, Cell and Environment, 26, 845–856. 10.1046/j.1365-3040.2003.01016.x PubMed DOI

Mok, D. W. , & Mok, M. C. (2001). Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology, 89, 89–118. 10.1146/annurev.arplant.52.1.89 PubMed DOI

Muller, B. (2011). Generic signal‐specific responses: Cytokinin and context‐dependent cellular responses. Journal of Experimental Botany, 62, 3273‐3288. PubMed

Nishiyama, R. , Watanabe, Y. , Fujita, Y. , Le, D. T. , Kojima, M. , Werner, T. , … Tran, L.‐S. P. (2011). 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. The Plant Cell, 23, 2169–2183. 10.1105/tpc.111.087395 PubMed DOI PMC

Ouyang, B. , Yang, T. , Li, H. , Zhang, L. , Zhang, Y. , Zhang, J. , … Ye, Z. (2007). Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. Journal of Experimental Botany, 58, 507–520. 10.1093/jxb/erl258 PubMed DOI

Pandey, S. K. , Nookaraju, A. , Upadhyaya, C. P. , Gururani, M. A. , Venkatesh, J. , Kim, D.‐H. , & Park, S. W. (2011). An update on biotechnological approaches for improving abiotic stress tolerance in tomato. Crop Science, 51, 2303–2324. 10.2135/cropsci2010.10.0579 DOI

Peleg, Z. , & Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop plants. Current Opinion in Plant Biology, 14, 290–295. 10.1016/j.pbi.2011.02.001 PubMed DOI

Pineda, B. , Garcia‐Abellan, J. O. , Anton, T. , Perez, F. , Moyano, E. , Sogo, B. G. , … Atares, A. (2012). Tomato: Genomic approaches for salt and drought stress tolerance In Tuteja N., Gill S. S., Tiburcio A. F. & Tuteja R. (Eds.), Improving Crop Resistance to Abiotic Stress. Singapore: Wiley‐VCH.

Prerostova, S. , Dobrev, P. I. , Gaudinova, A. , Hosek, P. , Soudek, P. , Knirsch, V. , & Vankova, R. (2017). Hormonal dynamics during salt stress responses of salt‐sensitive Arabidopsis thaliana and salt‐tolerant Thellungiella salsuginea . Plant Science, 264, 188–198. 10.1016/j.plantsci.2017.07.020 PubMed DOI

Qin, F. , Shinozaki, K. , & Yamaguchi‐Shinozaki, K. (2011). Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant and Cell Physiology, 52, 1569–1582. 10.1093/pcp/pcr106 PubMed DOI

R Core Team (2013). R: A Language and Environment for Statistical, Computing. Vienna, Austria: R Foundation for Statistical Computing.

Ramireddy, E. , Chang, L. , & Schmülling, T. (2014). Cytokinin as a mediator for regulating root system architecture in response to environmental cues. Plant Signaling and Behavior, 9, 5021–5032. 10.4161/psb.27771 PubMed DOI PMC

Sakakibara, H. (2006). Cytokinins: Activity, biosynthesis, and translocation. Annual Review of Plant Biology, 57, 431–449. 10.1146/annurev.arplant.57.032905.105231 PubMed DOI

Saxena, I. , Srikanth, S. , & Chen, Z. (2016). Cross talk between H2O2 and interacting signal molecules under plant stress response. Frontiers in Plant Science, 7, 570 10.3389/fpls.2016.00570 PubMed DOI PMC

Schäfer, M. , Brütting, C. , Meza‐Canales, I. D. , Großkinsky, D. K. , Vankova, R. , Baldwin, I. T. , & Meldau, S. (2015). The role of cis‐zeatin‐type cytokinins in plant growth regulation and mediating responses to environmental interactions. Journal of Experimental Botany, 66, 4873–4884. 10.1093/jxb/erv214 PubMed DOI PMC

Shi, X. , Gupta, S. , Lindquist, I. E. , Cameron, C. T. , Mudge, J. , & Rashotte, A. M. (2013). Transcriptome analysis of cytokinin response in tomato leaves. PLoS ONE, 8, e55090 10.1371/journal.pone.0055090 PubMed DOI PMC

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, 10.1104/pp.18.00293 10.1104/pp.18.00293 PubMed DOI PMC

Singh, M. , Singh, A. , Prasad, S. M. , & Singh, R. K. (2017). Regulation of plants metabolism in response to salt stress: An omics approach. Acta Physiologiae Plantarum, 39, 48 10.1007/s11738-016-2345-x DOI

Sun, Y. , Ji, K. , Liang, B. , Du, Y. , Jiang, L. , Wang, J. , … Wang, H. (2017). Suppressing ABA uridine diphosphate glucosyltransferase (SlUGT75C1) alters fruit ripening and the stress response in tomato. The Plant Journal, 91, 574–589. 10.1111/tpj.13588 PubMed DOI

Sun, W. , Xu, X. , Zhu, H. , Liu, A. , Liu, L. , Li, J. , & Hua, X. (2010). Comparative transcriptomic profiling of a salt‐tolerant wild tomato species and a salt‐sensitive tomato cultivar. Plant and Cell Physiology, 51, 997–1006. 10.1093/pcp/pcq056 PubMed DOI

Svačinová, J. , Novák, O. , Lenka Plačková, L. , Lenobel, R. , Holík, J. , Strnad, M. , & Doležal, K. (2012). A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: Pipette tip solid‐phase extraction. Plant Methods, 8, 17. PubMed PMC

To, J. P. C. , & Kieber, J. J. (2008). Cytokinin signaling: Two‐components and more. Trends in Plant Science, 13, 85–92. 10.1016/j.tplants.2007.11.005 PubMed DOI

Veselov, D. S. , Kudoyarova, G. R. , Kudryakova, N. V. , & Kusnetsov, V. V. (2017). Role of cytokinins in stress resistance of plants. Russian Journal of Plant Physiology, 64, 15–27. 10.1134/S1021443717010162 DOI

Wilkinson, S. , Kudoyarova, G. R. , Veselov, D. S. , Arkhipova, T. N. , & Davies, W. J. (2012). Plant hormone interactions: Innovative targets for crop breeding and management. Journal of Experimental Botany, 63, 3499–3509. 10.1093/jxb/ers148 PubMed DOI

Wu, T. D. , & Watanabe, C. K. (2005). GMAP: A genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics, 21(9), 1859–1875. 10.1093/bioinformatics/bti310 PubMed DOI

Žižková, E. , Dobrev, P. I. , Muhovski, Y. , Hošek, P. , Hoyerová, K. , Haisel, D. , … Hichri, I. (2015). Tomato (Solanum lycopersicum L.) SlIPT3 and SlIPT4 isopentenyltransferases mediate salt stress response in tomato. BMC Plant Biology, 15, 85. PubMed PMC

Zürcher, E. , Tavor‐Deslex, D. , Lituiev, D. , Enkerli, K. , Tarr, P. T. , & Müller, B. (2013). A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiology, 161, 1066–1075. 10.1104/pp.112.211763 PubMed DOI PMC

Zwack, P. J. , De Clercq, I. , Howton, T. C. , Hallmark, H. T. , Hurny, A. , Keshishian, E. A. , … Rashotte, A. M. (2016). Cytokinin response factor 6 represses cytokinin‐associated genes during oxidative stress. Plant Physiology, 172, 1249–1258. PubMed PMC

Zwack, P. J. , & Rashotte, A. M. (2015). Interactions between cytokinin signalling and abiotic stress responses. Journal of Experimental Botany, 66, 4863–4871. 10.1093/jxb/erv172 PubMed DOI

Zwack, P. J. , Robinson, B. R. , Risley, M. G. , & Rashotte, A. M. (2013). Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to cytokinin and numerous abiotic stresses. Plant and Cell Physiology, 54, 971–981. 10.1093/pcp/pct049 PubMed DOI

Cytokinin N-glucosides: Occurrence, Metabolism and Biological Activities in Plants