Cobalt+Salt-Stressed Salvia officinalis: ROS Scavenging Capacity and Antioxidant Potency

Main Article Content

Hülya Torun


Salvia officinalis L. (Lamiaceae) is one of the most widespread herbal species used in the food processing industry and for culinary and medicinal purposes. This work aimed to investigate changes in plant growth, water content, lipid peroxidation, H2O2, proline, and enzymes related to reactive oxygen species (ROS) detoxification including superoxide dismutase (SOD), peroxidase (POX), catalase (CAT), ascorbate peroxidase (APX) and glutathione reductase (GR). Phenolic contents and antioxidant capacity values such as ferric ion reducing antioxidant power (FRAP), cupric ion reducing antioxidant capacity (CUPRAC) and 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging were studied under stress conditions of salt, cobalt and a combination of the two. No significant differences were found in relative water content and chlorophyll fluorescence under salt, cobalt and their combination. However, the osmotic potential and relative growth rate were enhanced with salt+cobalt compared to salt-treated plants. Salt and cobalt individually stimulated high antioxidant activity. High APX and GR activities were associated with the high proline accumulation in the sage plants under the combined effect of salt+cobalt. The combination decreased lipid peroxidation (TBARS), while H2O2 content was increased. This increase with the combined salt+cobalt effect may be associated with the decrease in CAT activity. Moreover, a strong correlation was found between TPC and TF content and antioxidant capacity measured via FRAP, CUPRAC and DPPH. The TPC, TF and antioxidant capacity values also increased under the salt+cobalt combination, suggesting an increase in antioxidant content in the sage leaves. Therefore, the combination of salt and cobalt improved the stress tolerance of S. officinalis.

Article Details

Sending to International Journal of Secondary Metabolite


[1] Lopresti, A.L. (2017). Salvia (sage): a review of its potential cognitive-enhancing and protective effects. Drugs in R&D, 17(1), 53-64. doi: 10.1007/s40268-016-0157-5

[2] Jantová, S., Hudec, R., Sekretár, S., Kučerák, J., Melušová, M. (2014). Salvia officinalis L. extract and its new food antioxidant formulations induce apoptosis through mitochondrial/caspase pathway in leukemia L1210 cells. Interdisciplinary Toxicology, 7(3), 146–153. doi: 10.2478/intox-2014-0020

[3] Noctor, G., Paepe, R.D. Foyer, C.H. (2007). Mitochondrial redox biology and homeostasis in plants. Trends in Plant Science, 12, 125-134. doi: 10.1016/j.tplants.2007.01.005

[4] Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Rodermel, S., Inze, D., Mittler, R. (2002). Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase and catalase. Plant Jornal, 32, 329-342. doi: 10.1046/j.1365-313X.2002.01427.x

[5] Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F. (2004). The reactive oxygen gene network in plants. Trends in Plant Science, 9, 490–498. doi: 10.1016/j.tplants.2004.08.009

[6] 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. doi: 10.1016/j.plaphy.2010.08.016

[7] Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends in Plant Science, 11, 15–19. doi: 10.1016/j.tplants.2005.11.002

[8] Zandalinas, S.I., Mittler, R., Balfagón, D., Arbona, V., Gómez‐Cadenas, A. (2018). Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum, 162, 2–12. doi: 10.1111/ppl.12540

[9] Parida, A.K., Das, A.B. (2005). Salt tolerance and salinity effects on plants: a review, Ecotoxicology and Environmental Safety, 60, 324-349. doi: 10.1016/j.ecoenv.2004.06.010

[10] Jayakumara, K., Vijayarengan, P., Changxing, Z., Gomathinayagam, M., Jaleel, C.A. (2008). Soil applied cobalt alters the nodulation, leg-haemoglobin content and antioxidant status of Glycine max (L.) Merr. Colloids and Surfaces B: Biointerfaces, 67(2), 272-275. doi: 10.1016/j.colsurfb.2008.08.012

[11] Gopal, R., Dube, B.K., Sinha, P., Chatterjee, C. (2003). Cobalt toxicity effects on growth and metabolism of tomato. Communications in Soil Science and Plant Analysis, 34, 5-6, 619-628, doi: 10.1081/CSS-120018963

[12] Gad, N. (2005). Interactive effect of cobalt and salinity on tomato plants I- growth and mineral composition as affected by cobalt and salinity. Research Journal of Agriculture and Biological Sciences, 1(3): 261-269.

[13] Gad, N., Kandil, H. (2011). Maximizing the tolerance of wheat plants to soil salinity using cobalt I- growth and mineral composition. Journal of Applied Sciences Research, 7(11), 1569-1574.

[14] Gad, N., Abd El-Moez, M.R., Kandil, H. (2011). Barley response to salt stress at varied levels of cobalt ıı. some physiological and chemical characteristics. Journal of Applied Sciences Research, 7(11), 1447-1453.

[15] Gad, N., El–Metwally, I.M. (2015). Chemical and physiological response of maize to salinity using cobalt supplement. International Journal of ChemTech Research, 8(10), 45-52.

[16] Hunt, R., Causton, D.R., Shipley, B., Askew, A.P. (2002). A modern tool for classical plant growth analysis, Annals of Botany, 90, 485–488. doi: 10.1093/aob/mcf214

[17] Heath, R. L., Packer, L. (1968). Photoperoxidation in isolated chloroplasts, I. kinetics and stoichiometry of fatty acid peroxidation. Archives in Biochemistry and Biophysics, 125, 189-198. doi: 10.1016/0003-9861(68)90654-1

[18] Liu, J., Lu, B., Xun, A.L. (2000). An improved method for the determination of hydrogen peroxide in leaves. Progress in Biochemistry and Biophysics, 27, 548–551. doi: 10.1111/j.1365-2621.1977.tb01540.x

[19] Bates, L.S., Waldren, R.P., Teare, I.D. (1973). Rapid determination of free proline for water stress studies. Plant Soil, 39, 205–207. doi: 10.1007/BF00018060

[20] Bradford, M.M. (1976). A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of the protein-dye binding. Analytical Biochemistry, 72, 248–254. doi: 10.1016/0003-2697(76)90527-3

[21] Beauchamp, C., Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44, 276–287. doi: 10.1016/0003-2697(71)90370-8

[22] Mika, A., Lüthje, S. (2003). Properties of guaiacol peroxidase activities isolated from corn root plasma membranes. Plant Physiology, 132, 1489–1498. doi: 10.1104/pp.103.020396

[23] Aebi, H. Catalase in vitro, in S.P. Colowick, N.O. Kaplan (Eds.), Methods in Enzymology, Academic Press, Orlando, 1984, pp. 114–121.

[24] Nakano, Y., Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22, 867–880. doi: 10.1093/oxfordjournals.pcp.a076232

[25] Foyer, C.H., Halliwell, B. (1976). The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta, 133, 21–25. doi: 10.1007/BF00386001

[26] Singleton, V.L., Rossi, J.A. (1965). Colorimetry of total phenolics withphosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16, 144–158.

[27] Huang, D.-J., Chun-Der, L., Hsien-Jung, C., Yaw-Huei, L. (2004). Antioxidant and antiproliferative activities of sweet potato (Ipomoea batatas [L.] LamTainong 57') constituents. Botanical Bulletin- Academia Sinica Taipei, 45, 179–186.

[28] Benzie, I.F., Strain, J. (1999). Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods in Enzymology, 299, 15–27. doi: 10.1016/S0076-6879(99)99005-5

[29] Apak, R., Güçlü, K., Özyürek, M., Karademir, S.E. (2004). A novel total antioxidant capacity index for dietary polyphenols, vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. Journal of Agricultural and Food Chemistry, 52, 7970–7981. doi: 10.1021/jf048741x

[30] Blois, M.S. (1958). Antioxidant determinations by the use of a stable free radical. Nature, 181 (4617), 1199–1200. doi: 10.1038/1811199a0

[31] Ma, X., Zheng, J., Zhang, X., Hu, Q., Qian, R. (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), 1–13. doi: 10.3389/fpls.2017.00600

[32] Karuppanapandian, T., Kim, W. (2013). Cobalt-induced oxidative stress causes growth inhibition associated with enhanced lipid peroxidation and activates antioxidant responses in Indian mustard (Brassica juncea L.) leaves. Acta Physiologia Plantarum, 35, 2429-2443. doi: 10.1007/s11738-013-1277-y

[33] Vanselow, A.P. Cobalt, in: H.D. Chapman, (Ed.), Diagnostic Criteria of Plants, Quality Printing Company, Abilene, TX, 1965, pp. 142–156.

[34] Lwalaba, J.L., Zvobgo, G., Fu, L., Zhang, X., Mwamba, T.M., Muhammad, N., Mundende, R.P., Zhang, G. (2017). Alleviating effects of calcium on cobalt toxicity in two barley genotypes differing in cobalt tolerance. Ecotoxicology and Environmental Safety, 139, 488-495. doi: 10.1016/j.ecoenv.2017.02.019

[35] Khalid, A.K., Shedeed, M.R. (2014). The effects of saline irrigation water and cobalt on growth and chemical composition in Nigella sativa. Nusantara Bioscience, 6(2), 146-151. doi: 10.13057/nusbiosci/n060207

[36] Gengmao, Z., Quanmei, S., Yu, H., Shihui, L., Changhai, W. (2014). The physiological and biochemical responses of a medicinal plant (Salvia miltiorrhiza L.) to stress caused by various concentrations of NaCl. PloS ONE, 9(2), e89624. doi: 10.1371/journal.pone.0089624

[37] Ksouri, R., Megdiche, V., Debez, A., Falleh, H., Grignon, C., Abdelly, C. (2007). Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritime. Plant Physiology and Biochemistry, 45, 244 - 249. doi: 10.1016/j.plaphy.2007.02.001

[38] Cuvelier, M.-E., Berset, C., Richard, H. (1994). Antioxidant constituents in sage (Salvia officinalis). Journal of Agricultural and Food Chemistry, 42, 665-669. doi: 10.1021/jf00039a012

[39] Taârit, M.B., Msaada, K., Hosni, K., Marzouk, B. (2012). Physiological changes, phenolic content and antioxidant activity of Salvia officinalis L. grown under saline conditions. Journal of the Science of Food and Agriculture, 92(8), 1614-1619. doi: 10.1002/jsfa.4746

[40] Duletić-Laušević, S., Alimpić, A., Pavlović, D., Marin, P.D., Lakušić, D. (2016). Salvia officinalis of different origins Antioxidant activity, phenolic and flavonoid content of extracts. Agro Food Industry Hi Tech, 27(1), 52-55.

[41] Bayan, Y., Genç, N. (2016). Determination of antioxidant capacity and total phenolic matter of Salvia verticillata subsp. amasiaca. Nevşehir Bilim ve Teknoloji Dergisi, 5(2), 158-166. doi: 10.17100/nevbiltek.284739

[42] Taârit, M.B., Msaada, K., Hosni, K., Marzouk, B. (2012). Fatty acids, phenolic changes and antioxidant activity of clary sage (Salvia sclarea L.) rosette leaves grown under saline conditions. Industrial Crops and Products, 38, 58– 63. doi:10.1016/j.indcrop.2012.01.002

[43] Valifard, M., Mohsenzadeh, S., Kholdebarin, B., Rowshan, V. (2014). Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. South African Journal of Botany, 93, 92 - 97.

[44] Başgel, S. Erdemoğlu, S.B. (2005). Determination of mineral and trace elements in some medicinal herbs and their infusions consumed in Turkey. Science of the Total Environment, 359, 82–89.

[45] Kiliçel, F., Karapinar, H.S., Uğuz, A. (2017). Determination of some heavy metal concentrations of sage tea with FAAS. International Journal of Secondary Metabolite, 4(3), 391-399. doi: 10.21448/ijsm.374637