Abstract
The plant hormone ethylene or the gaseous signalling molecule nitric oxide (NO) may enhance salt stress tolerance by maintaining ion homeostasis, first of all K+/Na+ ratio of tissues. Ethylene and NO accumulation increased in the root apices and suspension culture cells of tomato at sublethal salt stress caused by 100 mM NaCl, however, the induction phase of programmed cell death (PCD) was different at lethal salt concentration. The production of ethylene by root apices and the accumulation of NO in the cells of suspension culture did not increase during the initiation of PCD after 250 mM NaCl treatment. Moreover, cells in suspension culture accumulated higher amount of reactive oxygen species which, along with NO deficiency contributed to cell death induction. The absence of ethylene in the apical root segments and the absence of NO accumulation in the cell suspension resulted in similar ion disequilibrium, namely K+/Na+ ratio of 1.41 ± 0.1 and 1.68 ± 0.3 in intact plant tissues and suspension culture cells, respectively that was not tolerated by tomato.
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Abeles, F. B., Morgan, P. W., Salveit, M. E. (1992) Regulation of ethylene production by internal, environmental, and stress factors. In: Abeles, F. B., Morgan, P. W., Salveit, M. E. (eds). Ethylene in Plant Biology. Academic Press, San Diego, pp. 56–119.
Ayarpadikannan, S., Chung, E., Kim, K., So, H.-A., Schraufnagle, K. R., Lee, J.-H. (2014) RsERF1 derived from wild radish (Raphanus sativus) confers salt stress tolerance in Arabidopsis. Acta Physiol. Plant doi: 10.1007s11738-013-1478-4
Biddington, N. L. (1992) The influence of ethylene in plant tissue culture. Plant Growth Regul. 11, 173–187.
Cao, W. H., Liu, J., He, X. J., Mu, R. L., Zhou, H. L., Chen, S. Y., Zhang, J. S. (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol. 143, 707–719.
Carimi, F., Zottini, M., Formentin, E., Terzi, M., Lo Schiavo, F. (2003) Cytokinins: new apoptotic inducers in plants. Planta 216, 413–421.
Chae, S. C., Kim, H. H., Park, S. U. (2012) Ethylene inhibitors enhance shoot organogenesis of gloxinia (Sinningia speciosa). Sci. World J. Vol. 2012, Article ID859381, doi: 10.1100/2012/859381
Chae, H. S., Faure, F., Kieber, J. J. (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15, 545–559.
Cheng, M. C., Liao, P. M., Kuo, W. W., Lin, T. P. (2013) The Arabidopsis ETHYLENE RESPONSE FACT OR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol. 162, 1566–1582.
Csiszár, J., Szabó, M., Erdei, L., Márton, L., Horváth, F., Tari, I. (2004) Auxin autotrophic tobacco callus tissues resists oxidative stress: the importance of glutathione S-transferase and glutathione peroxidase activities in auxin heterotrophic and autotrophic calli. J. Plant Physiol. 161, 691–699.
Demidchik, V., Straltsova, D., Medvedev, S. S., Pozhvanov, G. A., Sokolik, A., Yurin, V. (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. J. Exp. Bot. 65, 1259–1270.
Ederli, L., Morettini, R., Borgogni, A., Wasternack, C., Miersch, O., Reale, L., Ferranti, F., Tosti, N., Pasqualini, S. (2006) Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol. 142, 595–608.
Fukuda, H., Komamine, A. (1980) Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol. 65, 57–60.
Gamborg, O., Miller, R., Ojima, K. (1968) Nutrient requirement suspensions cultures of soybean root cells. Exp. Cell Res. 50, 151–158.
Garcia-Gonzales, R., Quiroz, K., Carrasco, B., Caligari, P. (2010) Plant tissue culture: Current status, opportunities and challenges. Cienc. Investig. Agrar. 37, 5–30.
Gémes, K., Poór, P., Horváth, E., Kolbert, Z., Szopkó, D., Szepesi, Á., Tari, I. (2011) Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiol. Plant. 142, 179–192.
Huh, G. H., Damsz, B., Matsumoto, T. K., Reddy, M. P., Rus, A. M., Ibeas, J. I., Narasimhan, M. L., Bressan, R. A., Hasegawa, P. M. (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J. 29, 649–659.
Jones, M. L., Chaffin, G. S., Eason, J. R., Clark, D. G. (2005) Ethylene-sensitivity regulates proteolytic activity and cysteine protease gene expression in petunia corollas. J. Exp. Bot. 56, 2733–2744.
Kamiyoshihara, Y., Tieman, D. M., Huber, D. J., Klee, H. J. (2012) Ligand-induced alterations in the phosphorylation state of ethylene receptors in tomato fruit. Plant Physiol. 160, 488–497.
Kende, H., Zeevaart, J. A. D. (1997) The five “classical” plant hormones. Plant Cell 9, 1197–1210.
Khan, M. N., Siddiqui, M. H., Mohammad, F., Naeem, M. (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide-Biol. Ch. 27, 210–218.
Köves, E., Szabó, M. (1987) Ethylene production in habituated and auxin-requiring tobacco calluscultures–Does ethylene play a role in the habituation. Physiol. Plant. 69, 351–355.
Li, J. S., Jia, H. L., Wang, J. (2014) cGMP and ethylene are involved in maintaining ion homeostasis under salt stress in Arabidopsis roots. Plant Cell Rep. 33, 447–459.
Lieberman, M. (1979) Biosynthesis and action of ethylene. Annu. Rev. Plant Phyiol. 30, 533–591.
Lu, C. W., Shao, Y., Li, L., Chen, A. J., Xu, W. Q., Wu, K. J., Luo, Y., B., Zhu, B. Z. (2011) Ove_expression of SLERF1 tomato gene encoding an ERF-type transcription enhances salt tolerance. Russ. J. Plant Physiol. 58, 118–125.
Merchante, C., Alonso, J. M., Stepanova, A. N. (2013) Ethylene signaling: simple ligand, complex regulation. Current Opin. Plant Biol. 16, 554–560.
Murashige, T., Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473–497.
Nagendra-Prasad, D., Sudhakar, N., Murugesan, K., Mohan, N. (2008) Pre-exposure of calli to ozone promotes tolerance of regenerated Lycopersicon esculentum cv. PKM1 plantlets against acute ozone stress. J. Plant Physiol. 165, 1288–1299.
Ozden, M., Karaslaan, M. (2011) Effect of cytokinin on callus proliferation associated with physiological and biochemical changes in Vitis vinifera L. Acta Physiol. Plant. 33, 1451–1459.
Poór, P., Gémes, K., Horváth, F., Szepesi, A., Simon, M. L., Tari, I. (2011) Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol. 13, 105–114.
Poór, P., Szopkó, D., Tari, I. (2012) Ionic homeostasis disturbance is involved in tomato cell death induced by NaCl and salicylic acid. In Vitro Cell Dev-Pl 48, 377–382.
Poór, P., Kovács, J., Szopkó, D., Tari, I. (2013) Ethylene signaling in salt stress- and salicylic acid-induced programmed cell death in tomato suspension cells. Protoplasma 250, 273–284.
Purnhauser, L., Medgyesy, P., Czakó, M., Dix, P. J., Márton, L. (1987) Stimulation of shoot regeneration in Triticum aestivum and Nicotiana plumbaginifolia Viv tissue cultures using the ethylene inhibitor AgNO3. Plant Cell Rep. 6, 1–4.
Redig, P., Shaul, O., Inze, D., VanMontagu, M., VanOnckelen, H. (1996) Levels of endogenous cytokinins, indole-3-acetic acid and abscisic acid during the cell cycle of synchronized tobacco BY-2 cells. FEBS Lett. 391, 175–180.
Shabala, S. (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J. Exp. Bot. 60, 709–711.
Shi, C., Zhang, Y. Q., Bian, K., Xu, L. L. (2011) Amount and activity changes of 20S proteasome modified by oxidation in salt-treated wheat root tips. Acta Physiol. Plant 33, 1227–1237.
Szabó, M., Köves, E., Somogyi, I. (1994) Development of auxin autotrophy in Nicotiana tabacum callus cultures. Physiol. Plant. 90, 348–352.
Tari, I., Szalai, G., Lőrincz, Z., Bálint, A. (2002) Changes in thiol content in roots of wheat cultivars exposed to copper stress. Biol. Plant. 45, 255–260.
Trobacher, C. P. (2009) Ethylene and programmed cell death in plants. Botany 87, 757–769.
Wang, H. H., Liang, X. L., Wan, Q., Wang, X. M., Bi, Y. R. (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230, 293–307.
Yakimova, E. T., Kapchina-Toteva, V. M., Woltering, E. J. (2007) Signal transduction events in aluminum-induced cell death in tomato suspension cells. J. Plant Physiol. 164, 702–708.
Yang, S. F., Hoffman, N. E. (1984) Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35, 155–189.
Zhao, L. Q., Zhang, F., Guo, J. K., Yang, Y. L., Li, B. B., Zhang, L. X. (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol. 134, 849–857.
Zhao, X. C., Schaller, G. E. (2004) Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett. 562, 189–192.
Acknowledgements
This work was financially supported by a grant from the Hungarian Scientific Research Fund (OTKA K 101243). Péter Po#x00F3;r, #x00C1;gnes Szepesi and Judit Kov#x00E1;cs were supported by the European Union and the State of Hungary, co-financed by the European Social Fund in the framework of TÁAMOP 4.2.4. A/2-11-1-2012-0001 ‘National Excellence Program’.
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Poór, P., Borbély, P., Kovács, J. et al. Opposite Extremes in Ethylene/Nitric Oxide Ratio Induce Cell Death in Suspension Culture and Root Apices of Tomato Exposed to Salt Stress. BIOLOGIA FUTURA 65, 428–438 (2014). https://doi.org/10.1556/ABiol.65.2014.4.7
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DOI: https://doi.org/10.1556/ABiol.65.2014.4.7