Abstract
Extracellular ATP (eATP) has been considered as signalling compound to mediate several physiological processes. Here we show that eATP played a role in alleviating the salicylic acid (SA)-induced inhibition of cell viability and respiration in tobacco (Nicotiana tabacum L. cv. Bright Yellow-2) suspension cells. Exogenous SA at higher concentrations (0.05, 0.1, 0.3, 0.5, or 0.7 mM) caused a significant reduction in respiratory O2 uptake or cell viability. The addition of exogenous ATP alleviated the SA-induced reductions in cell viability and respiration, but the effect was dependent on the concentrations of either exogenous SA or ATP. Further study shows that the alleviative effects of exogenous ATP were abolished by the addition of GdCl3 (an inhibitor of Ca2+ channels) or EGTA (a Ca2+ chelator). These results suggest that this role of extracellular ATP could be related to a Ca2+ signalling pathway.
Abbreviations
- eATP:
-
extracellular ATP
- SA:
-
salicylic acid
References
Alvarez, M.E.: Salicylic acid in the machinery of hypersensitive cell death and disease resistance. — Plant mol. Biol. 44: 429–442, 2000.
Bingham, I.J., Farrar, J.F.: Activity and capacity of respiratory pathways in barley roots deprived of inorganic nutrients. — Plant Physiol. Biochem. 27: 847–854, 1989.
Boyum, R., Guidotti, G.: Glucose-dependent, cAMP-mediated ATP efflux from Saccharomyces cerevisiae. — Microbiology 143: 1901–1908, 1997.
Chivasa, S., Murphy, A.M., Hamilton, J.M., Lindsey, K., Carr, J.P., Slabas, A.R.: Extracellular ATP is a regulator of pathogen defence in plants. — Plant J. 60: 436–448, 2009.
Choi, J., Tanaka, K., Cao, Y., Qi, Y., Qiu, J., Liang, Y., Lee, S.Y., Stacey, G.: Identification of a plant receptor for extracellular ATP. — Science 343: 290–294, 2014.
Delaney, T.P., Friedrich, L., Ryals, J.A.: Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. — Proc. nat. Acad. Sci. USA 92: 6602–6606, 1995.
Demidchik, V., Shang, Z., Shin, R., Thompson, E., Rubio, L., Laohavisit, A., Mortimer, J.C., Chivasa, S., Slabas, A.R., Glover, B.J., Schachtman, D.P., Shabala, S.N., Davies, J.M.: Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. — Plant J. 58: 903–913, 2009.
Dichmann, S., Idzko, M., Zimpfer, U., Hofmann, C., Ferrari, D., Luttmann, W., Virchow, C.J., Di Virgilio, F., Norgauer, J.: Adenosine triphosphate-induced oxygen radical production and CD11b up-regulation: Ca++ mobilization and actin reorganization in human eosinophils. — Blood 95: 973–978, 2000.
Foresi, N.P., Laxalt, A.M., Tonon, C.V., Casalongue, C.A., Lamattina, L.: Extracellular ATP induces nitric oxide production in tomato cell suspensions. — Plant Physiol. 145: 589–592, 2007.
Jouaville, L.S., Pinton, P., Bastianutto, C., Rutter, G.A., Rizzuto, R.: Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. — Proc. nat. Acad. Sci. USA 96: 13807–13812, 1999.
Kim, S.Y., Sivaguru, M., Stacey, G.: Extracellular ATP in plants. Visualization, localization, and analysis of physiological significance in growth and signaling. — Plant Physiol. 142: 984–992, 2006.
Klessig, D.F., Malamy, J.: The salicylic acid signal in plants. — Plant mol. Biol. 26: 1439–1458, 1994.
Logan, D.C., Knight, M.R.: Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. — Plant Physiol. 133: 21–24, 2003.
McCormack, J.G., Halestrap, A.P., Denton, R.M.: Role of calcium ions in regulation of mammalian intramitochondrial metabolism. — Physiol. Rev. 70: 391–425, 1990.
Moussa H.R., El-Gamal S.M.: Effect of salicylic acid pretreatment on cadmium toxicity in wheat. — Biol. Plant. 54: 315–320, 2010.
Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures. — Physiol. Plant. 15: 473–497, 1962.
Murphy, A.M., Chivasa, S., Singh, D.P., Carr, J.P: Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways? — Trends Plant Sci. 4: 155–160, 1999.
Parish, R.W., Weibel, M.: Extracellular ATP, ecto-ATPase and calcium influx in Dictyostelium discoideum cells. — FEBS Lett. 118: 263–266, 1980.
Robson, C.A., Vanlerberghe, G.C.: Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. — Plant Physiol. 129: 1908–1920, 2002.
Rutter, G.A., Rizzuto, R.: Regulation of mitochondrial metabolism by ER Ca2+ release: an intimate connection. — Trends Biochem. Sci. 25: 215–221, 2000.
Sun, J., Zhang, C.L., Deng, S.R., Lu, C.F., Shen, X., Zhou, X.Y., Zheng, X.J., Hu, ZM., Chen, S.L.: An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica. — Plant Cell Environ. 35: 893–916, 2012.
Tanaka, K., Gilroy, S., Jones, A.M., Stacey, G.: Extracellular ATP signaling in plants. — Trends Cell Biol. 20: 601–608, 2010.
Tang, W., Brady, S.R., Sun, Y., Muday, G,K., Roux, S.J.: Extracellular ATP inhibits root gravitropism at concentrations that inhibit polar auxin transport. — Plant Physiol. 131: 147–154, 2003.
Tari, I., Kiss, G., Deér, A.K., Csiszár, J., Erdei, L., Gallé, Á., Gémes, K., Horváth, F., Poór, P., Szepesi, Á., Simon, L. M. Salicylic acid increased aldose reductase activity and sorbitol accumulation in tomato plants under salt stress. — Biol. Plant. 54: 677–683, 2010.
Tari, I., Poór, P., Gémes, K.: Sublethal concentrations of salicylic acid decrease the formation of reactive oxygen species but maintain an increased nitric oxide production in the root apex of the ethylene-insensitive never ripe tomato mutants. — Plant Signal. Behav. 6: 1263–1266, 2011.
Thomas, C., Rajagopal, A., Windsor, B., Dudler, R., Lloyd, A., Roux, S.J.: A role for ectophosphatase in xenobiotic resistance. — Plant Cell 12: 519–533, 2000.
Tonón, C., Terrile, C.M., Iglesias J.M., Lamattina, L., Casalongué, C.: Extracellular ATP, nitric oxide and superoxide act coordinately to regulate hypocotyl growth in etiolated Arabidopsis seedlings. — J. Plant Physiol. 167: 540–546, 2010.
Wang, D.H., Li, X.X., Su, Z.K., Ren H.X.: The role of salicylic acid in response of two rice cultivars to chilling stress. — Biol. Plant. 53: 545–552, 2009.
Weerasinghe, R.R., Swanson, S.J., Okada, S.F., Garrett, M.B., Kim, S.Y., Stacey, G., Boucher, R. C., Gilroy, S., Jones, A.M.: Touch induces ATP release in Arabidopsis roots that is modulated by the heterotrimeric G-protein complex. — FEBS Lett. 583: 2521–2526, 2009.
Wolf, C., Hennig, M., Romanovicz, D., Steinebrunner, I.: Developmental defects and seedling lethality in apyrase AtAPY1 and AtAPY2 double knockout mutants. — Plant mol. Biol. 64: 657–672, 2007.
Xie, Z., Chen, Z.: Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells. — Plant Physiol. 120: 217–226, 1999.
Yang, S.W., Kim, S.K., Kim, W.T.: Perturbation of NgTRF1 expression induces apoptosis-like cell death in tobacco BY-2 cells and implicates NgTRF1 in the control of telomere length and stability. — Plant Cell 16: 3370–3385, 2004.
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Acknowledgements: We thank Prof. Jiang Liwen (The Chinese University of Hong Kong) for the supply of the tobacco cell culture. This work was supported by the National Natural Science Foundation of China (Nos. 31260059 and 30900105), the Key Project of Chinese Ministry of Education (No. 211190), the Fundamental Research Funds for the Gansu Universities of Gansu Provincial Department of Finance, and NWNU-kjcxgc-03-77 and 49.
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Feng, H.Q., Guan, D.D., Bai, J.Y. et al. Extracellular ATP alleviates the salicylic acid-induced inhibition of cell viability and respiration through a Ca2+-dependent mechanism. Biol Plant 59, 193–197 (2015). https://doi.org/10.1007/s10535-014-0464-z
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DOI: https://doi.org/10.1007/s10535-014-0464-z