Effects of exogenous salicylic acid on antioxidative responses, phenolic metabolism and photochemical activity of strawberry under salt stress

Document Type : Original Article


Department of Biology, Payame Noor University (PNU), 19395-3697 Tehran, Iran



To further clarify the specific photochemical mechanisms of salicylic acid (SA)-mediated adaptation to salt stress, this experiment was conducted to examine the effect of SA (100 and 500 μM) on photosynthesis, antioxidative capacity and phenolic metabolism in strawberry plants under salt stress (50 mM). The results showed that high SA had a negative effect on strawberry plants as reduced leaf dry weight in plants that exposed to 500 μM SA under non-salt stress conditions. Salt stress negatively affected the leaf dry weight, whereas foliar spray of 100 μM SA alleviated the salt-induced inhibitory effects on the plant growth. Salt stress caused a significant decrease in photosystem performance index (PIabs); however, plants exposed to salt stress after SA pretreatment conserved their photosynthetic electron transport rate, compared with NaCl-alone treated plants, relating to the improvement of water-splitting complex on the donor side of PSII (Fv/Fo). The application of 100 μM SA in saline condition also increased the accumulation of soluble sugars like trehalose (Tre). Lipid peroxidation was observed in plants subjected to salinity stress, as evidenced by higher malondialdehyde (MDA) levels. In contrast, foliar spray of SA at a concentration of 100 μM promoted catalase (CAT) activity as well as phenolic content, thus reducing MDA and, consequently oxidative damage to membranes. Hence, foliar application of SA at 100 μM was effective in alleviation of salt stress in strawberry by improving PSII functioning, induction of compatible osmolytes and phenol metabolism, and mitigating membrane damage.


Ashraf, M., N. A. Akram, R. N. Arteca and M. R. Foolad. 2010. 'The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance'. Critical Reviews in Plant Sciences, 29(3):162-190. 
Bates, L. S., R. P. Waldern and I. D. Teare. 1973. 'Rapid determination of free proline for water stress studies'. Journal of Plant Nutrition and Soil Science, 39 (1): 205-207.
Bradford, M.M. 1976. 'A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding'. Annual Biochemistry, 72: 248-254.
Chandra, A., A. Anand, and A. Dubey. 2007. 'Effect of salicylic acid on morphological and biochemical attributes in cowpea'. Journal of Environmental Biology, 28: 193-196.
Chu, J., X., Yao and Z. Zhang. 2010. 'Responses of wheat seedlings to exogenous selenium supply under cold stress'. Biological Trace Element Research, 136: 355-363.
Diao, M., L. Ma, J. Wang, J. Cui, A. Fu, and H. Y.  Liu. 2014. 'Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system'. Journal of Plant Growth Regulation, 33: 671-682.
Elguera, J.C.T.,  E.Y. Barrientos, K. Wrobel and K. Wrobel. 2013. 'Effect of cadmium (Cd (II)), selenium (Se (IV)) and their mixtures on phenolic compounds and antioxidant capacity in Lepidium sativum'. Acta Physiologiae Plantarum,35: 431-441.
Feng, R., C. Wei, and S. Tu. 2013. 'The roles of selenium in protecting plants against abiotic stresses'. Environmental and Experimental Botany, 87: 58-68.
Gengmao, Z., L. Shihui, S. Xing, W. Yizhou, and C. Zipan. 2015. 'The role of silicon in physiology of the medicinal plant (Lonicera japonica L.) under salt stress'. Scientific Reports, 5: 12696.
Lee, S., S.G. Kim, and C.M. Park. 2010. 'Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis'. New Phytologist, 188: 626-637
Li, T., Y. Hu, X. Du, H.Tang, C. Shen, and J. Wu. 2014. 'Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems'. PLOS ONE, 9(10), e109492.
Li, Z.G., L.J. Luo and L.P. Zhu. 2014. 'Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings'. Botanical Studies, 55: 20-31.
Habibi, G. and N. Ajory. 2015. 'The effect of drought on photosynthetic plasticity in Marrubium vulgare plants growing at low and high altitudes'. Journal of Plant Research, 128(6): 987-994.
Habibi, G. and R. Hajiboland. 2012. 'Comparison of photosynthesis and antioxidative protection in Sedum album and Sedum stoloniferum (Crassulaceae) under water stress'. Photosynthetica, 50: 508-518.
Habibi, G. 2017. 'Physiological, photochemical and ionic responses of sunflower seedlings to exogenous selenium supply under salt stress'. Acta Physiologiae Plantarum, 39(10): 213.
Hao, L., Y. Zhao, D. Jin, L. Zhang, X. Bi, H. Chen, Q. Xu, C. Ma, and G. Li. 2012. 'Salicylic acid-altering Arabidopsis mutant’s response to salt stress'.Plant and Soil, 354: 81-95.
Hasanuzzaman, M., K. Nahar, and M.Fujita, 2013. 'Ecophysiology and responses of plants under salt stress. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and Responses of Plants under Salt Stress'. Springer Science & Business Media, 25-87.
Hayat, Q., S. Hayat, M. Irfan, and A. Ahmad. 2010. 'Effect of exogenous salicylic acid under changing environment: a review'. Environmental and Experimental Botany, 68: 14-25.
Jamalian, S., Gholami, M. and M. Esna-Ashari, 2013'. Abscisic acid-mediated leaf phenolic compounds, plant growth and yield is strawberry under different salt stress regimes'. Theoretical and Experimental Plant Physiology 25(4):291-299.
Jayakannan, M., J. Bose, O. Babourina, Z. Rengel, and S. Shabala. 2013. 'Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel'. Journal of Experimental Botany, 64: 2255-2268.
Jiang, C., Q. Cui, K. Feng, D. Xu, C. Li, and Q. Zheng. 2016. 'Melatonin improves antioxidant capacity and ion homeostasis and enhances salt tolerance in maize seedlings'.Acta Physiologiae Plantarum, 38: 1-9.
Jiang, C., C. Zu, D. Lu, Q. Zheng, J. Shen and H. Wang. 2017. 'Effect of exogenous selenium supply on photosynthesis, Na+ accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress'. Nature Publishing Group, p. 1–14.
Jini, D. and B. Joseph. 2017. 'Physiological mechanism of salicylic acid for alleviation of salt stress in rice'.Rice Science, 24: 97-108.
Kalaji, H.M., K. Bosa, J. Kościelniak and K. Żuk-Gołaszewska. 2011. 'Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces'. Environmental and Experimental Botany, 73: 64-72.
Kalaji, H.M., A. Jajoo, A.Oukarroum, M. Brestic, M. Zivcak, I.A. Samborska, M.D. Cetner, I. Łukasik, V. Goltsev and R.J. Ladle. 2016. 'Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions'. Acta Physiologiae Plantarum, 38: 102.
Karlidag, H., E. Yildirim, and M. Turan. 2009. 'Salicylic acid ameliorates the adverse effect of salt stress on strawberry'. Scientia Agricola, 66: 180-187.
Krizek, D.T., G.F. Kramer, A. Upadhyaya, and R.M. Mirecki. 1993. 'UV‐B response of cucumber seedlings grown under metal halide and high pressure sodium/deluxe lamps'. Physiologia Plantarum, 88: 350-358.
Lichtenthaler, H.K. and A.R. Wellburn. 1983. 'Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents’. Biochemical Society Transactions, 11 (5): 591-592.
Magné, C., Saladin, G. and C. Clément. 2006. 'Transient effect of the herbicide flazasulfuron on carbohydrate physiology in Vitis vinifera'.Chemosphere, 62: 650-657.
Ma, X., J. Zheng , X. Zhang , Q. Hu and R. Qian. 2017. 'Salicylic acid alleviates the adverse effects of salt stress on Dianthus superbus (Caryophyllaceae) by activating photosynthesis, protecting morphological structure, and enhancing the antioxidant system'. Frontiers in Plant Science, 8: 600.
Meda, A., C.E. Lamien, M. Romito, J. Millogo, and O.G. Nacoulma. 2005. 'Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity'. Food Chemistry, 91: 571-577.
Miura, K. and Y. Tada. 2014. 'Regulation of water, salinity, and cold stress responses by salicylic acid'.  Frontiers in Plant Science, 5: 4.
Munns, R. and M. Tester. 2008. 'Mechanisms of salinity tolerance." Annual Review of Plant Biology, 59: 651-681.
Noreen, S., A. Siddiq, K. Hussain, S. Ahmad and M. Hasanuzzaman .2017.  'Foliar application of salicylic acid with salinity stress on physiological and biochemical attributes of sunflower (Helianthus annuus L.) crop'. Acta Scientiarum Polonorum-Hortorum Cultus, 16: 57-74.
Pirlak, L. and A. Eşitken.2004. 'Salinity effects on growth, proline and ion accumulation in strawberry plants'. Plant Soil Sci, 54: 189-192.
Saied, A.S., A.J. Keutgen, and G. Noga. 2005. 'The influence of NaCl salinity on growth, yield and fruit quality if strawberry CVS: Elsanta and Korona'. Scientia Horticulturae, 103: 289-303.
Shen, C., Y. Hu, X. Du, T. Li, H.Tang and J. Wu. 2014. 'Salicylic acid induces physiological and biochemical changes in Torreya grandis cv. Merrillii seedlings under drought stress'. Trees, 28: 961-970.
Shu, S., Y. Yuan, J. Chen, J. Sun, W. Zhang, Y. Tang, M. Zhong and S. Guo. 2015. 'The role of putrescine in the regulation of proteins and fatty acids of thylakoid membranes under salt stress'. Scientific Reports, 5:14390.
Strasser, R.J., M. Tsimilli-Michael, and A. Srivastava. 2004. 'Analysis of the chlorophyll a fluorescence transient'. In: Chlorophyll a fluorescence." Springer, Netherlands, 321-362.
Velikova, V., I. Yordanov and A. Edreva. 2000. 'Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines'. Plant Science, 151: 59-66.
Velioglu, Y.S., G. Mazza, L. Gao and B.D. Oomah. 1998. 'Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products'. Journal of Agricultural and Food Chemistry, 46: 4113-4117.
Wei, W., Q.T. Li, Y.N. Chu, R.J. Reiter, X.M. Yu, D.H. Zhu, W.K. Zhang , B. Ma , Q. Lin, J.S. Zhang, and S.Y. Chen.  2014. 'Melatonin enhances plant growth and abiotic stress tolerance in soybean plants'. Journal of Experimental Botany, 66: 695-707.
Xu, Z. and S.J. Rothstein. 2018. 'ROS-Induced anthocyanin production provides feedback protection by scavenging ROS and maintaining photosynthetic capacity in Arabidopsis'. Plant Signaling & Behavior, 13: 1364-1377.
Zhang, Y., L. Wang, Y.Liu, Q. Zhang, Q. Wei and W. Zhang, 2006. 'Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast'. Planta 224: 545-555.
Zucker, M. 1965. 'Induction of phenylalanine deaminase by light and its relation to chlorogenic acid synthesis in potato tuber tissue'. Plant Physiology, 40(5): 779–784.