Dhiraj Kapur Kamal Jit Singh


The interaction between cadmium- a toxic metal and zinc- an essential micronutrient was investigated in influencing the activity of various antioxidant enzymes and related metabolites in soybean [Glycine max (L.) Merr.]. Higher levels of cadmium (Cd) stimulate the activity of potential enzymes like ascorbate peroxidase (APX), superoxide dismutase (SOD) accompanied by the buildup of non-enzymatic metabolites, hydrogen peroxide (H2O2), malondialdehyde (MDA) and proline due to rise in oxidative stress of plants.  Also, the reduced activity of catalase (CAT), glutathione reductase (GR) and ascorbic acid (AsA) content was based upon Cd treatment levels. Application of zinc (Zn) combination enhances the activity of enzymes like APX, GR, CAT and SOD in Cd treatments, also confirmed with the depleted levels of H2O2. Zn alone treatment had no significant effect on the activity of such enzymes indicating the toxicity owing to Cd treatments only. The accumulation behavior of other non-enzymatic metabolites like MDA, proline and ascorbic acid also get reversed with metal combination treatment. Moreover, the efficacy of Zn was more when applied in higher concentrations with low Cd. Thus, Zn plays a key role in plants to counter heavy metal stress by elevating antioxidative defense with higher activity of enzymes and reduced levels of non-enzymatic metabolites, and efficacy of Zn in combination is dose dependent.


Download data is not yet available.




Abiotic stress, Antagonistic interactions, Grains, Legumes, Pulses

Adriano, D.C. (1986). Trace elements in the terrestrial environment. Springer-Verlag, New York.
Ahmad, P., Jaleel, C.A., Salem, M.A., Nabi, G. and Sharma, S. (2010). Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology, 30: 161-175.  https://doi.org/10.3109/07388550903524243
Ahmad, P., Sarwat, M. and Sharma, S. (2008). Reactive oxygen species, antioxidants and signaling in plants. Journal of Plant Biology, 51: 167-173. https://doi.org/10.1007/BF03030694
Akay, A. and Koleli, N. (2007). Interaction between cadmium and zinc in barley (Hordeum vulgare L.) grown under field conditions. Bangladesh Journal of Botany, 36: 13-19. https://doi.org/10.3329/bjb.v36i1.1543
Alloway, B.J. (2004). Zinc in Soils and Crop Nutrition. Publ. of International Zinc Association.
Alscher, R.G., Erturk, N. and Heath, L.S. (2002). Role of superoxide dismutase (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany, 53: 1331-1341.
Angelone, M. and Bini, C. (1992). Trace elements concentrations in soils and plants of Western Europe. In: (Adriano DC, ed.) Biogeochemistry of trace metals. Boca Raton, FL: Lewis Publishers, 19-60.
Aravind, P. and Prasad, M.N.V. (2003). Zinc alleviates cadmium induced oxidative stress in Ceratophyllum demersum L.: A free floating freshwater macrophyte. Plant Physiology and Biochemistry, 41: 391-397. https://doi.org/10.1016/S0981-9428(03)00035-4
Aravind, P. and Prasad, M.N.V. (2005). Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiology and Biochemistry, 43: 107-116. https://doi.org/10.1016/j.plaphy.2005.01.002.
Aravind, P., Prasad, M.N.V., Malec, P., Waloszek, A. and Strza?-ka, K. (2009). Zinc protects Ceratophyllum demersum L. (free-floating hydrophyte) against reactive oxygen species induced by cadmium. Journal of Trace Elements in Medicine and Biology, 23: 50-60. https://doi.org/10.1016/j.jtemb.2008.10.002
Asada, K. (1992). Ascorbate peroxidase-a hydrogen peroxide scavenging enzyme in plants. Physiologia Plantarum, 85: 235-241. https://doi.org/10.1111/j.1399-3054.1992.tb04728.x
Ashraf, M. and Harris, P.J.C. (2004). Potential biochemical indicators of salinity tolerance in plants. Plant Science, 166: 3-16. https://doi.org/10.1016/j.plantsci.2003.10.024
Auld, D.S. (2001). Zinc coordination sphere in biochemical zinc sites. Biometals, 14: 271-313.
Balen, B., Tkalec, M., Šiki?, S., Toli?, S., Cvjetko, P., Pavlica, M. and Vidakovic´-Cifrek, Z. (2011). Biochemical responses of Lemna minor experimentally exposed to cadmium and zinc. Ecotoxicology, 20: 815-826. https://doi.org/10.1007/s10646-011-0633-1
Bates, L.S., Waldren, R.P. and Teare, I.D. (1973). Rapid determination of free proline for water stress studies. Plant Soil, 39: 205-207. https://doi.org/10.1007/BF00018060
Brahim, S., Joke, D., Ann, C., Jean-Paul, N., Marjo, T., Arja, T., Sirpa, K., Frank, V.B., Karen, S. and Jaco, V. (2010). Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. Journal of Plant Physiology, 167(4): 247-254. https://doi.org/10.1016/j.jplph.2009.09.015
Broadley, M.R., White, P.J., Hammond, J.P., Zelko, I. and Lux, A. (2007). Zinc in plants. New Phytologist, 173: 677-702. https://doi.org/10.1111/j.1469-8137.2007.01996.x
Cakmak, I. (2000). Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytologist, 146: 185-205. http://dx.doi.org/10.1046/j.1469-8137.2000.00630.x
Chasapis, C.T., Loutsidou, A.C., Spiliopoulou, C.A. and Stefanidou, M.E. (2012). Zinc and human health: an update. Archives of Toxicology, 86: 521-534.  https://doi.org/10.1007/s00204-011-0775-1
Chen, C.T., Chen, T.H., Lo, K.F. and Chiu, C.Y. (2004). Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Science, 166: 103-111.
Cherif, J., Mediouni, C., Ammar, W. and Jemal, F. (2011). Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicum). Journal of Environmental Science, 23: 837-844.
Cho, Un-H. and Seo, Nam-H. (2005). Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Science, 168: 113-120. https://doi.org/10.1016/j.plantsci.2004.07.021
Dhindsa, R.S., Plumb-Dhindsa, P. and Thorpe, T.A. (1981). Leaf senescence: correlated with increased level of membrane permeability and lipid peroxidation and decreased level of superoxide dismutase and catalase. Journal of Experimental Botany, 23: 93-101. https://doi.org/10.1093/jxb/32.1.93
Dikkaya, E.T. and Ergün, N. (2014). Effects of cadmium and zinc interactions on growth parameters and activities of ascorbate peroxidase on maize (Zea mays L. MAT 97). European Journal of Experimental Biology, 4(1): 288-295.
Foyer, C.H. and Noctor, G. (2003). Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum, 119: 355-364. https://doi.org/10.1034/j.1399-3054.2003.00223.x
Gallego, S.M., Pena, L.B., Barcia, R.A., Azpiliceuta, C.E., Iannone, M.F., Rosales, E.P., Zawoznik, M.S., Groppa, M.D. and Benavides, M.P. (2012). Unraveling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environmental and Experimental Botany, 83: 33-46. https://doi.org/10.1016/j.envexpbot.2012.04.006
Galloway, J.N., Thornton, J.D., Norton, S.A., Volcho, H.L. and McLean, R.A. (1982). Trace metals in atmospheric deposition: a review and assessment. Atmospheric Environement, 16: 1677-1700. https://doi.org/10.1016/0004-6981(82)90262-1
Gill, S.S., Khan, N.A. and Tuteja, N. (2012). Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Science, 182: 112-120.
Gomes, D.S., Fragoso, L.C., Riger, C.J., Panek, A.D. and Eleutherio, E.C.A. (2002). Regulation of cadmium uptake by Saccharomyces cerevisiae. Biochimica et Biophysica Acta (BBA) Bioenergetics, 1573(1): 21-25. https://doi.org/10.1016/S0304-4165(02)00324-0
Guerinot, M.L. and Eide, D. (1999). Zeroing in on zinc uptake in yeast and plants. Current Opinion in Plant Biology, 2: 244-249. https://doi.org/10.1016/S1369-5266(99)80042-9
Hart, J.J., Welch, R.M., Norvell, W.A. and Kochian, L.V. (2002). Transport interactions between cadmium and zinc in roots of bread and durum wheat seedlings. Physiologia Plantarum, 116(1):73-78. https://doi.org/10.1034/j.1399-3054.2002.1160109.x
Hassan, M.J., Shao, G. and Zhang, G. (2005a). Influence of cadmium toxicity on antioxidant enzymes activity in rice cultivars with different grain Cd accumulation. Journal of Plant Nutrition, 28: 1259-1270. https://doi.org/10.1081/PLN-200063298
Hassan, M.J., Zhang, G., Wu, F., Wie, K. and Chen, Z. (2005b). Zinc alleviates growth inhibition and oxidative stress caused by cadmium in rice. Journal of Plant Nutrition and Soil Science, 168: 255-261. https://doi.org/10.1002/jpln.200420403
Heath, R.L. and Packer, L. (1968). Photoperoxidation in isolated chloroplast-I: Kinetics stoichiometery of fatty peroxidation. Archives of Biochemistry and Biophysics, 125: 189-198. https://doi.org/10.10 16/0 003-9861(68)90654-1
Hussain, A., Ali, S., Rizwan, M., Rehman, M.Z., Javed, M.R., Imran, M., Chatha, S.A.S. and Nazir, R. (2018). Zinc oxide nanoparticles alter the wheat physiological response and reduce the cadmium uptake by plants. Environment Pollution, 242: 1518-1526. https://doi.org/10.1016/j.envpol.2018.08.036
Kalai, T., Khamassi, K., Silva, J.A.T.d., Gouia, H. and Ben-Kaab, L.B. (2014). Cadmium and copper stress affect seedling growth and enzymatic activities in germinating barley seeds. Archives of Agronomy and Soil Science, 60(6): 765-783. https://doi.org/10.1080/03650340.2013.838001
Kapoor, D., Rattan, A., Bhardwaj, R., Kaur, S., Gupta, A. and Manoj (2016). Antioxident defence responses and activation of phenolic compounds in Brassica juncea exposed to cadmium stress. International Journal of Green Pharmacy, 10(4): 228-234. http://dx.doi.org/10.22377/ijgp.v10i04.760
Kawano, T., Kawano, N., Muto, S. and Lapeyrie, F. (2001). Cation-induced superoxide generation in tobacco cell suspension culture is dependent on ion valence. Plant Cell Environment, 24: 1235-1241. https://doi.org/10.1046/j.1365-3040.2001.00766.x
Khalid, K.A. and Hendawy, S.F. (2005). Response of Sage (Salvia Officinalis L.) plants to zinc application under different salinity levels. Journal of Applied Sciences Research, 1(2): 147-155.
Khan, N.A., Anjum, N.A., Nazar, R. and Iqbal, N. (2009). Increased activity of ATP-sulfurylase and increased contents of cysteine and glutathione reduce high cadmium-induced oxidative stress in mustard cultivar with high photosynthetic potential. Russian Journal of Plant Physiology, 56(5): 670-677. https://doi.org/10.1134/S1021443709050136
Lantzy, R.J. and Mackenzie, F.T. (1979). Atmospheric trace metals: global cycles and assessment of man’s impact. Geochimica et Cosmochimica Acta, 43: 511.
Lux, A., Martinka, M., Vaculík, M. and White, P.J. (2011). Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany, 62: 21-37.
Ma, D., Sun, D., Wang, C., Ding, H., Qin, H., Hou, J., Huang, X., Xie, Y. and Guo, T. (2017). Physiological responses and yield of wheat plants in zinc-mediated alleviation of drought stress. Frontiers in Plant Science, 8: 860. https://doi.org/10.3389/fpls.2017.00860
Markovska, Y.K., Gorinova, N.I., Nedkovska, M.P. and Miteva, K.M. (2009). Cadmium-induced oxidative damage and antioxidant responses in Brassica juncea plants. Biologia Plantarum, 53(1): 151-154. https://doi.org/10.1007/s10535-009-0023-1
Marschner, H. and Marschner, P. (2012). Marschner’s mineral nutrition of higher plants, 3rd ed. Academic, London/Waltham.
Mavis, R.D. and Stellwagen, E. (1968). Purification and subunit structure of glutathione reductase from baker’s yeast. Journal of Biological Chemistry, 243: 809-814.
Minchin, F.R. and Pate, J.S. (1975). Effects of water, aeration and salt regime on nitrogen fixation in a nodulated legume: definition of an optimum root environment. Journal of Experimental Botany, 26: 60-80. https://doi.org/10.1093/jxb/26.1.60
Mishra, S. and Dubey, R.S. (2006). Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: Role of proline as enzyme protectant. Journal of Plant Physiology, 163: 927-936. https://doi.org/10.1016/j.jplph.2005.08.003
Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7: 405-410. https://doi.org/10.1016/S1360-1385(02)02312-9
Mobin, M. and Khan, N.A. (2006). Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. Journal of Plant Physiology, 164: 601-610. https://doi.org/10.1016/j.jplph.2006.03.003
Morkunas, I., Wozniak, A., Mai, V.C., Rucinska-Sobkowiak, R. and Jeandet, P. (2018). The role of heavy metals in plant response to biotic stress. Molecules, 23(9): 2309-2320. https://doi.org/10.3390/molecules23092320
Mukherji, S.P. and Chaudhari, M.A. (1983). Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Plant Physiology, 58: 166-170. https://doi.org/10.1111/j.1399-3054.1983.tb04162.x
Nakano, Y. and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology, 22: 867-880.
Nishizawa, N.K. (2005). The uptake and translocation of minerals in rice plants, in Triyaka K, Heong KL (eds.): Rice is life: Scientific perspectives for the 21st century. IRRI, Manila, Philippines, pp. 90-93.
Ozturk, L., Eker, S. and Ozkutlu, F. (2003). Effect of Cadmium on Growth and Concentrations of Cadmium, Ascorbic Acid and Sulphydryl Groups in Durum Wheat Cultivars. Turkish Journal of Agriculture and Forestry, 27: 161-168
Ozturk, Z.N., Talame, V., Deyholos, M., Michalowski, C.B., Galbraith, D.W., Gozukirmizi, N., Tuberosa, R. and Bohnert, H.J. (2002). Monitoring large-scale changes in transcript abundance in drought- and salt stressed barley. Plant Molecular Biology, 48: 551-573. https://doi.org/10.1023/A:1014875215580
Pierart, A., Shahid, M., Sejalon-Delmas, N. and Dumat, C. (2015). Antimony bioavailability: knowledge and research perspectives for sustainable agricultures. Journal of Hazardous Materials, 289: 219-234. https://doi.org/10.1016/j.jhazmat.2015.02.011
Powell, S.R. (2000). The antioxidant properties of zinc. Journal of Nutrition, 130: 1447-1454. https://doi.org/10.1093/jn/130.5.1447S
Qayyum, M.F., Rehman, M.Z., Ali, S., Rizwan, M., Naeem, A., Maqsood, M.A., Khalid, H., Rinklebe, J. and Ok, Y.S. (2017). Residual effects of monoammonium phosphate, gypsum and elemental sulfur on cadmium phytoavailability and translocation from soil to wheat in an effluent irrigated field. Chemosphere, 174: 515-523. https://doi.org/10.1016/j.chemosphere. 2017.02.006
Qiao, X., Wang, P., Shi, G. and Yang, H. (2015). Zinc conferred cadmium tolerance in Lemna minor L. via modulating polyamines and proline metabolism. Plant Growth Regulators, 77: 1-9. https://doi.org/10.1007/s10725-015-0027-0
Rascio, N. and Navari-Izzo, F. (2011). Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Science, 180: 169-181. https://doi.org/10.1016/j.plantsci.2010.08.016
Rehman, M.Z., Rizwan, M., Khalid, H., Ali, S., Naeem, A., Yousaf, B., Liu, G., Sabir, M. and Farooq, M. (2018). Farmyard manure alone and combined with immobilizing amendments reduced cadmium accumulation in wheat and rice grains grown in field irrigated with raw effluents. Chemosphere, 199: 468-476. https://doi.org/10.1016/j.chemosphere. 2018. 02. 030
Rizwan, M., Ali, S., Rehman, M.Z., Adrees, M., Arshad, M., Qayyum, M.F., Ali, L., Hussain, A., Chatha, S.A.S. and Imran, M. (2019). Alleviation of cadmium accumulation in maize (Zea mays L.) by foliar spray of zinc oxide nanoparticles and biochar to contaminated soil. Environmental Pollution, 248: 358-367. https://doi.org/10.1016/j.envpol.2019.02.031
Sarwar, N., Saifullah, S.S.M., Munir, H.Z., Asif, N., Sadia, B. and Ghulam, F. (2010). Role of mineral nutrition in minimizing cadmium accumulation by plants. Journal of the Science of Food and Agriculture, 90: 925-937. https://doi.org/10.1002/jsfa.3916
Seminario, A., Song, L., Zulet, A., Nguyen, H.T., González, E.M. and Larrainzar, E. (2017). Drought Stress Causes a Reduction in the Biosynthesis of Ascorbic Acid in Soybean Plants. Frontiers in Plant Science, 8: 1042. https://doi.org/10.3389/fpls.2017.01042
Shi, G., Liu, C., Cai, Q., Liu, Q. and Hou, C. (2010). Cadmium Accumulation and Tolerance of Two Safflower Cultivars in Relation to Photosynthesis and Antioxidantive Enzymes. Bulletin of Environmental and Contamination Toxicology, 85(3): 256-263. https://doi.org/10.1007/s00128-010-0067-0
Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y. and Yoshimura, K. (2002). Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany, 53: 1305-1319.https://doi.org/10.1093/jexbot/53.372.
13 05
Singh, A. and Prasad, S.M. (2015). Remediation of heavy metal contaminated ecosystem: an overview on technology advancement. International Journal of Environmental Science and Technology, 12: 353-366. https://doi.org/10.1007/s13762-014-0542-y
Singh, S., Eapen, S. and D’Souza, S.F. (2006). Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere, 62: 233-246. https://doi.org/10.1016/j.chemosphere.2005.05.017
Smeets, K., Cuypers, A., Lambrechts, A., Semane, B., Hoet, P., Laere, A.V. and Vangronsveld, J. (2005). Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiology and Biochemistry, 43: 437-444. https://doi.org/10.1016/j.plaphy.2005.03.007
Smith, I.K., Vierheller, T.L. and Thorne, C.A. (1989). Proprieties and functions of glutathione reductase in plants. Physiologia Plantarum, 77: 449-456. https://doi.org/10.1111/j.1399-3054.1989.tb05666.x
Smolders, E., Brans, K., Foldi, A. and Merckx, R. (1999). Cadmium fixation in soils measured by isotopic dilution. Soil Science Society of American Journal, 63(1): 78-85. https://doi.org/10.2136/sssaj1999.03615995006300010013x
Subba, P., Mukhopadhyay, M., Mahato, S.K., Bhutia, K.D., Mondal, T.K. and Ghosh, S.K. (2014). Zinc stress induces physiological, ultra-structural and biochemical changes in mandarin orange (Citrus reticulata Blanco) seedlings. Physiology and Molecular Biology of Plants, 20(4): 461-473. https://doi.org/10.1007/s12298-014-0254-2
Tavallali, V., Rahemi, M., Eshgh, S., Kholdebarin, B. and Ramezanian, A. (2010). Zinc alleviates salt stress and increases antioxidant enzyme activity in the leaves of pistachio (Pistacia vera L. ‘Badami’) seedlings. Turkish Journal of Agriculture and Forestry, 34: 349-359.
Teranishi, Y., Tanaka, A., Osumi, M. and Fukui, S. (1974). Catalase activity of hydrocarbon utilizing Candida yeast. Agricultural and Biological Chemistry, 38: 1213-1216. https://doi.org/10.1080/0002 1369. 1974.10861301
Tkalec, M., Štefani?, P.P., Cvjetko, P., Šiki?, S., Pavlica, M. and Balen, B. (2014). The effects of cadmium-zinc interactions on biochemical response in tobacco seedlings and adult plants. PLoS ONE, 9(1): e87582. https://doi.org/10.1371/journal.pone. 00875 82
Trakal, L., Komárek, M., Száková, J., Tlustoš, P., Tejnecký, V. and Drábek, O. (2012). Sorption behavior of Cd, Cu, Pb, and Zn and their interactions in phytoremediated soil. International Journal of Phytoremediation, 14: 806-819.
Ullrich, S.M., Ramsey, M.H. and Helios-Rybicka, E. (1999). Total and exchangeable concentrations of heavy metal in soils near Bytom, an area of Pb/Zn mining and smelting in upper Silesia, Poland. Applied Geochemistry, 14: 187-196. https://doi.org/10.1016/S0883-2927(98)00042-0
Velikova, V., Yordanov, I. and Edreva, A. (2000). Oxidative stress and some antioxidative systems in acid rain treated bean plants: Protective role of exogenous polyamines. Plant Science, 151: 59-66. https://doi.org/10.1016/S0168-9452(99)00197-1
Weisany, W., Sohrabi, Y., Heidari, G., Siosemardeh, A. and Ghassemi-Golezani, K. (2012). Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L.). Plant Omics Journal, 5(2): 60-67.
Wu, F. and Zhang, G. (2002). Alleviation of cadmium-toxicity by application of zinc and ascorbic acid in barley. Journal of Plant Nutrition, 25: 2745-2761. https://doi.org/10.1081/PLN-120015536
Citation Format
How to Cite
Kapur, D., & Singh, K. J. (2019). Zinc alleviates cadmium induced heavy metal stress by stimulating antioxidative defense in soybean [Glycine max (L.) Merr.] crop. Journal of Applied and Natural Science, 11(2), 338- 345. https://doi.org/10.31018/jans.v11i2.2054
More Citation Formats:
Research Articles