AJPS  Vol.10 No.12 , December 2019
Influence of Selenium on Growth, Antioxidants Production and Physiological Parameters of Rice (Oryza sativa L.) Seedlings and Its Possible Reversal by Coapplication of Sulphate
Abstract: The effect of selenate (Na2SeO4) and sulphate (Na2SO4) was studied on growth and metabolism in two rice cultivars cv. satabdi and cv. khitish. Selenate at low concentration (2 μM) expressed growth promoting effect on rice seedlings as opposed to its high concentration (≥20 μM) where the test seedlings showed stunted growth with browning at the apices of both roots and shoots. The chlorophyll contents showed a dose dependent effect. Both chlorophyll a and chlorophyll b contents were inhibited with increase in selenate concentrations. The effect was more pronounced in cv. satabdi compared to cv. khitish.The level of accessory pigments was deferentially affected by selenium treatment. Simultaneously, the fluorescence intensity and Hill activity decreased with increase in selenate concentrations in the test seedlings. It is assumed that selenium plays a protective role in plants subjected to stress and prevents the formation of reactive oxygen species (ROS) in the cells. Higher selenate concentrations (≥20 μM) exerted variable effect on the activities of enzymatic antioxidants viz.; superoxide dismutase (SOD), catechol peroxidase (CPX) and catalase (CAT) in the test seedlings. The activity of SOD increased with increase in selenate concentrations, whereas activities of CAT and CPX decreased. Under high selenate concentrations, the levels of oxidative stress markers, viz.; proline, H2O2 and MDA were also enhanced. Selenium induced accumulation of total soluble sugar and increased the level of both reducing and non reducing sugars in both the test cultivars. The starch contents concomitantly decreased with rise in selenate concentrations. Moreover, the nutrient contents of test seedlings were significantly influenced by selenium. The Na and K levels gradually increased whereas Ca, Mg and Fe levels decreased on application of selenate. Joint application of 10 mM sulphate and selenate showed significant alterations on all parameters tested with respect to selenate treatment alone. Partial to complete amelioration occurred in the test seedlings treated with high concentrations of selenate and sulphate. Our study shows that selenium at low concentration had a stimulatory effect on growth and metabolism as against high concentrations which proved to be toxic to the rice seedlings obtained from both the cultivars. Effects were more pronounced in cv. satabdi than in cv. khitish which is considered to be comparatively tolerant to selenium. The dose dependent influence of selenium on the physiological and biochemical responses of test seedlings may be reversed by co-application with sulphate.
Cite this paper: Das, D. , Seal, P. and Biswas, A. (2019) Influence of Selenium on Growth, Antioxidants Production and Physiological Parameters of Rice (Oryza sativa L.) Seedlings and Its Possible Reversal by Coapplication of Sulphate. American Journal of Plant Sciences, 10, 2236-2278. doi: 10.4236/ajps.2019.1012158.

[1]   Navarro-Alarcon, M. and Cabrera-Vique, C. (2008) Selenium in Food and the Human Body: A Review. Science of the Total Environment, 400, 115-141.

[2]   Terry, N., Zayed, A.M., de Souza, M.P. and Tarun, A.S. (2000) Selenium in Higher Plants. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 401-432.

[3]   Bodnar, M., Konieczka, P. and Namiesnik, J. (2012) The Properties, Functions, and Use of Selenium Compounds in Living Organisms. Journal of Environmental Science and Health Part C, 30, 225-252.

[4]   Turakainen, M. (2007) Selenium and Its Effects on Growth, Yield and Tuber Quality in Potato. PhD Dissertation, Department of Applied Biology, University of Helsinki, Helsinki.

[5]   Gigolashvili, T. and Kopriva, S. (2014) Transporters in Plant Sulphur Metabolism. Frontiers in Plant Science, 5, 422.

[6]   Kápolna, E., Laursen, K.H., Husted, S. and Larsen, E.H. (2012) Bio-Fortification and Isotopic Labelling of Se Metabolites in Onions and Carrots Following Foliar Application of Se and 77Se. Food Chemistry, 133, 650-657.

[7]   Hartikainen, H., Xue, T. and Piironen, V. (2000) Selenium as an Antioxidant and Prooxidant in Ryegrass. Plant and Soil, 225, 193-200.

[8]   Sun, H.W., Ha, J., Liang, S.X. and Kang, W.J. (2010) Protective Role of Selenium on Garlic Growth under Cadmium Stress. Communications in Soil Science and Plant Analysis, 41, 1195-1204.

[9]   Khattab, H. (2004) Metabolic and Oxidative Responses Associated with Exposure of Eruca sativa (Rocket) Plants to Different Levels of Selenium. International Journal of Agriculture Biology, 6, 1101-1106.

[10]   Sors, T.G., Ellis, D.R. and Salt, D.E. (2005) Selenium Uptake, Translocation, Assimilation Metabolic Fate in Plants. Photosynthesis Research, 86, 373-389.

[11]   El Kassis, E., Cathala, E., Rouached, H., Fourcroy, P., Berthomieu, P., Terry, N., et al. (2007) Characterization of a Selenate-Resistant Arabidopsis Mutant. Root Growth as a Potential Target for Selenate Toxicity. Plant Physiology, 143, 1231-1241.

[12]   Cappa, J.J., Cappa, P.J., El Mehdawi, A.F., McAleer, J.M., Simmons, M.P. and Pilon-Smits, E.A. (2014) Characterization of Selenium and Sulfur Accumulation across the Genus Stanleya (Brassicaceae): A Field Survey and Common-Garden Experiment. American Journal of Botany, 101, 830-839.

[13]   Schiavon, M., Pittarello, M., Pilon-Smits, E.A.H., Wirtz, M., Hell, R. and Malagoli, M. (2012) Selenate and Molybdate Alter Sulfate Transport and Assimilation in Brassica juncea L. Czern.: Implications for Phytoremediation. Environmental and Experimental Botany, 75, 41-51.

[14]   Kuznetsov, V.V., Kholodova, V., Kuznetsov, V.V. and Yagodin, B. (2003) Selenium Regulates the Water Status of Plants Exposed to Drought. Doklady Biological Sciences, 390, 266-268.

[15]   Djanaguiraman, M., Prasad, P. and Seppanen, M. (2010) Selenium Protects Sorghum Leaves from Oxidative Damage under High Temperature Stress by Enhancing Antioxidant Defense System. Plant Physiology and Biochemistry, 48, 999-1007.

[16]   Cao, M.J., Wang, Z., Wirtz, M., Hell, R., Oliver, D.J. and Xiang, C.B. (2013) SULTR3;1 Is a Chloroplast-Localized Sulphate Transporter in Arabidopsis thaliana. The Plant Journal, 73, 607-616.

[17]   Wu, Y.Y., Lu, X.Y., Peng, Z.K. and Luo, Z.M. (2000) Effect of Se on Physiological and Biochemical Characters of Paddy Rice. Scientia Agricultura Sinica, 33, 100-103.

[18]   Hasanuzzaman, M., Hossain, M.A. and Fujita, M. (2011) Selenium-Induced Up-Regulation of the Antioxidant Defense and Methylglyoxal Detoxification System Reduces Salinity-Induced Damage in Rapeseed Seedlings. Biological Trace Element Research, 143, 1704-1721.

[19]   Hondal, R.J., Marino, S.M. and Gladyshev, V.N. (2012) Selenocysteine in Thiol/Disulfide-Like Exchange Reactions. Antioxidants & Redox Signaling, 18, 1675-1689.

[20]   Akbulut, M. and Cakir, S. (2010) The Effects of Se Phytotoxicity on the Antioxidant Systems of Leaf Tissues in Barley (Hordeum vulgare L.) Seedlings. Plant Physiology and Biochemistry, 48, 160-166.

[21]   Labanowska, M., Filek, M., Koscielniak, J., Kurdziel, M., Kulis, E. and Hartikainen, H. (2012) The Effects of Short-Term Selenium Stress on Polish and Finnish Wheat Seedlings-EPR, Enzymatic and Fluorescence Studies. Journal of Plant Physiology, 169, 275-284.

[22]   Balk, J. and Pilon, M. (2011) Ancient and Essential: The Assembly of Iron-Sulfur Clusters in Plants. Trends in Plant Science, 16, 18-26.

[23]   Schiavon, M., Moro, I., Pilon-Smits, E.A., Matozzo, V., Malagoli, M. and Dalla Vecchia, F. (2012) Accumulation of Selenium in Ulva sp. and Effects on Morphology, Ultrastructure and Antioxidant Enzymes and Metabolites. Aquatic Toxicology, 122-123, 222-231.

[24]   Horsfall, M.J., Abia, A.A. and Spiff, A.I. (2003) Removal of Cu(II) and Zn(II) Ions from Waste Water by Cassava (Manihot esculenta Cranz) Waste Biomass. African Journal of Biotechnology, 2, 360-364.

[25]   Arinola, O.G., Nwozo, S.O., Ajiboye, J.A. and Oniye, A.H. (2008) Evaluation of Trace Elements and Total Antioxidant Status in Nigerian Cassava Processors. Pakistan Journal of Nutrition, 7, 770-772.

[26]   Garousi, F., Kovacs, B., Andrasi, D. and Veres, S. (2016) Selenium Phytoaccumulation by Sunflower Plants under Hydroponic Conditions. Water Air and Soil Pollution, 227, 382.

[27]   Soetan, K.O., Olaiya, C.O. and Oyewole, O.E. (2010) The Importance of Mineral Elements for Humans, Domestic Animals and Plants: A Review. African Journal of Food Science, 4, 200-222.

[28]   Barberon, M., Berthomieu, P., Clairotte, M., Shibagaki, N., Davidian, J.C. and Gosti, F. (2008) Unequal Functional Redundancy between the Two Arabidopsis thaliana High-Affinity Sulphate Transporters SULTR1;1 and SULTR1;2. New Phytologist, 180, 608-619.

[29]   White, P.J. and Broadley, M.R. (2009) Biofortification of Crops with Seven Mineral Elements Often Lacking in Human Diets—Iron, Zinc, Copper, Calcium, Magnesium, Selenium and Iodine. New Phytologist, 182, 49-84.

[30]   Velu, G., Ortiz-Monasterio, I., Cakmak, I., Hao, Y. and Singh, R.P. (2013) Biofortification Strategies to Increase Grain Zinc and Iron Concentrations in Wheat. Journal of Cereal Science, 59, 365-372.

[31]   Barrs, H.D. and Weatherly, P.E. (1962) A Re-Examination of Relative Turgidity for Estimating Water Deficits in Leaves. Australian Journal of Biological Sciences, 15, 413-428.

[32]   Paech, K. and Tracey, M.V. (1956) Modern Methods of Plant Analysis. Springer-Verlag, Berlin, Vol. 4, 143-196.

[33]   Arnon, D.I. (1949) Copper Enzyme in Isolated Chloroplast. Plant Physiology, 24, 1-15.

[34]   Mukherji, S. and Biswas, A.K. (1979) Modulation of Chlorophyll, Carotene and Xanthophyll Formation by Penicillin, Benzyladenine and Embryonic Axis in Mung Bean (Phaseolus aureus L.) Cotyledons. Annals of Botany, 43, 225-229.

[35]   Vishniac, W. (1957) Methods for the Study of Hill Reaction. In: Colowick, S.P. and Kaplan, N.O., Eds., Methods in Enzymology, Academic Press, New York, Vol. 4, 342-355.

[36]   Giannopolitis, C.N. and Ries, S.K. (1977) Superoxide Dismutases I. Occurrence in Higher Plants. Plant Physiology, 59, 309-314.

[37]   Gasper, T. and Laccoppe, J. (1968) The Effect of CCC and AMO-1618 on Growth, Catalase, Peroxidase, IAA Oxidase Activity of Young Barley Seedlings. Physiologia Plantarum, 21, 1104-1109.

[38]   Chance, B. and Maehly, A.C. (1955) Assay of Catalases and Peroxidases. Methods in Enzymology, 2, 764-817.

[39]   Bates, L.S., Waldren, R.P. and Treare, I.D. (1973) Rapid Estimation of Free Proline for Water Stress Determination. Plant and Soil, 39, 205-207.

[40]   Vellikova, V., Yordanov, I. and Edreva, A. (2000) Oxidative Stress and Some Antioxidant Systems in Acid Rain-Treated Bean Plants. Plant Science, 151, 59-66.

[41]   Hodges, D.M., DeLong, J.M., Forney, C.F. and Prange, R.K. (1999) Improving the Thiobarbituric Acid-Reactive-Substances Assay as for Estimating Lipid Peroxidation in Plant Tissues Containing Anthocyanin and Other Interfering Compounds. Planta, 207, 604-611.

[42]   Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956) Colorimetric Method for Determination of Sugars and Related Substances. Analytical Chemistry, 28, 350-356.

[43]   Miller, G.L. (1972) Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugars. Analytical Chemistry, 31, 426-428.

[44]   McCready, R.M., Guggolz, J., Silviera, V. and Owens, H.S. (1950) Determination of Starch and Amylase in Vegetables. Analytical Chemistry, 22, 1156-1158.

[45]   Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein Measurement with the Folin Phenol Reagent. The Journal of Biological Chemistry, 193, 265-275.

[46]   Simaei, M., Khavarinejad, R.A., Saadatmand, S., et al. (2011) Interactive Effects of Salicylic Acid and Nitric Oxide on Soybean Plants under NaCl Salinity. Russian Journal of Plant Physiology, 58, Article No. 783.

[47]   Hawrylak-Nowak, B. (2009) Beneficial Effects of Exogenous Selenium in Cucumber Seedlings Subjected to Salt Stress. Biological Trace Element Research, 132, 259-269.

[48]   Broadley, M.R., Alcock, J., Alford, J., Cartwright, P., Foot, I., Fairweather-Tait, S.J., et al. (2010) Selenium Biofortification of High-Yielding Winter Wheat (Triticum aestivum L.) by Liquid or Granular Se Fertilisation. Plant Soil, 332, 5-18.

[49]   Freeman, J.L., Tamaoki, M., Stushnoff, C., Quinn, C.F., Cappa, J.J., Devonshire, J., Fakra, S.F., Marcus, M.A., McGrath, S.P., Van Hoewyk, D., et al. (2010) Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata. Plant Physiology, 153, 1630-1652.

[50]   Valkama, E., Kivimaenpaa, M., Hartikainen, H. and Wulff, A. (2003) The Combined Effects of Enhanced UV-B Radiation and Selenium on Growth, Chlorophyll Fluorescence and Ultrastructure in Strawberry (Fragaria × ananassa) and Barley (Hordeum vulgare) Treated in the Field. Agricultural and Forest Meteorology, 120, 267-278.

[51]   Xue, T., Hartikainen, H. and Piironen, V. (2001) Antioxidative and Growth Promoting Effect of Selenium in Senescing Lettuce. Plant Soil, 237, 55-61.

[52]   Fargasová, A., Pastierová, J. and Svetková, K. (2006) Effect of Se-Metal Pair Combinations (Cd, Zn, Cu, Pb) on Photosynthetic Pigments Production and Metal Accumulation in Synapis alba L. Seedlings. Plant, Soil and Environment, 52, 8-15.

[53]   Lichtenthaler, H.K. and Miehé, J.A. (1997) Fluorescence Imaging as a Diagnostic Tool for Plant Stress. Trends in Plant Science, 2, 316-320.

[54]   Huseynova, I.M. (2012) Photosynthetic Characteristics and Enzymatic Antioxidant Capacity of Leaves from Wheat Cultivars Exposed to Drought. Biochimica et Biophysica Acta, 1817, 1516-1523.

[55]   Baek, S., Han, T., Ahn, S., et al. (2012) Effects of Heavy Metals on Plant Growths and Pigment Contents in Arabidopsis thaliana. The Plant Pathology Journal, 28, 446-452.

[56]   Ghasemi, F., Heidari, R., Jameii, R. and Purakbar, L. (2012) Effects of Ni2+ Toxicity on Hill Reaction and Membrane Functionality in Maize. Journal of Stress Physiology & Biochemistry, 8, 55-61.

[57]   Boisvert, S., Joly, D., Leclerc, S., Govindachary, S., Harnois, J. and Carpentier, R. (2007) Inhibition of the Oxygen-Evolving Complex of Photo-System II and Depletion of Extrinsic Polypeptides by Nickel. Biometals, 20, 879-889.

[58]   Józwiak, W. and Politycka, B. (2019) Effect of Selenium on Alleviating Oxidative Stress Caused by a Water Deficit in Cucumber Roots. Plants (Basel, Switzerland), 8, 217.

[59]   Kubala, S., Garnczarska, M., Wojtyla, L., Clippe, A., Kosmala, A. and Zmienko, A. (2015a) Deciphering Priming-Induced Improvement of Rapeseed (Brassica napus L.) Germination through an Integrated Transcriptomic and Proteomic Approach. Plant Science, 231, 94-113.

[60]   Kubala, S., Wojtyla, L., Quinet, M., Lechowska, K., Lutts, S. and Garnczarska, M. (2015b) Enhanced Expression of the Proline Synthesis Gene P5CSA in Relation to Seed Osmo Priming Improvement of Brassica napus Germination under Salinity Stress. Plant Science, 183, 1-12.

[61]   Shalaby, T., Bayoumi, Y., Alshaal, T., Elhawat, N., Sztrik, A. and El-Ramady, H. (2017) Selenium Fortification Induces Growth, Antioxidant Activity, Yield and Nutritional Quality of Lettuce in Salt-Affected Soil Using Foliar and Soil Applications. Plant Soil, 421, 245-258.

[62]   Wang, C.Q. (2011) Water-Stress Mitigation by Selenium in Trifolium repens L. Journal of Plant Nutrition and Soil Science, 174, 276-282.

[63]   Malik, J.A., Goel, S., Kaur, N., Sharma, S., Singh, I. and Nayyar, H. (2012) Selenium Antagonises the Toxic Effects of Arsenic on Mungbean (Phaseolus aureus Roxb.) Plants by Restricting Its Uptake and Enhancing the Antioxidative and Detoxification Mechanisms. Environmental and Experimental Botany, 77, 242-248.

[64]   Proietti, P., Luigi, N., Buono, D.D., D’Amato, R., Tedeschini, E., Daniele, D.B., et al. (2013) Selenium Protects Olive (Olea europaea L.) from Drought Stress. Scientia Horticulturae, 164, 165-171.

[65]   Iqbal, M., Hussain, I., Liaqat, H., Ashraf, M.A., Rasheed, R. and Rehman, A.U. (2015) Exogenously Applied Selenium Reduces Oxidative Stress and Induces Heat Tolerance in Spring Wheat. Plant Physiology and Biochemistry, 94, 95-103.

[66]   Shekari, F., Abbasi, A. and Mustafavi, S.H. (2017) Effect of Silicon and Selenium on Enzymatic Changes and Productivity of Dill in Saline Condition. Journal of the Saudi Society of Agricultural Sciences, 16, 367-374.

[67]   Subramanyam, K., Arun, M., Mariashibu, T.S., Theboral, J., Rajesh, M., Singh, N.K., et al. (2012) Overexpression of Tobacco Osmotin (Tbosm) in Soybean Conferred Resistance to Salinity Stress and Fungal Infections. Planta, 236, 1909-1925.

[68]   Nawaz, F., Ashraf, M.Y., Ahmad, R., Waraich, E.A., Shabbir, R.N. and Bukhari, M.A. (2015) Supplemental Selenium Improves Wheat Grain Yield and Quality through Alterations in Biochemical Processes under Normal and Water Deficit Conditions. Food Chemistry, 175, 350-357.

[69]   Hashem, H.A., Hassanein, R.A., Bekheta, M.A. and El-Kady, F.A. (2013) Protective Role of Selenium in Canola (Brassica napus L.) Plant Subjected to Salt Stress. The Egyptian Journal of Experimental Biology, 9, 199-211.

[70]   Houot, V., Etienne, P., Petitot, A.S., Barbier, S., Blein, J.P. and Suty, L. (2001) Hydrogen Peroxide Induces Programmed Cell Death Features in Cultured Tobacco BY-2 Cells, in a Dose-Dependent Manner. Journal of Experimental Botany, 52, 1721-1730.

[71]   Farmer, E.E. and Mueller, M.J. (2013) ROS-Mediated Lipid Peroxidation and RES-Activated Signaling. Annual Review of Plant Biology, 64, 429-450.

[72]   Rosa, M., Prado, C., Podazza, G., Interdonato, R., González, J.A., Hilal, M. and Prado, F.E. (2009) Soluble Sugars—Metabolism, Sensing and Abiotic Stress: A Complex Network in the Life of Plants. Plant Signaling Behaviour, 4, 388-393.

[73]   Zeeman, S.C., Smith, S.M. and Smith, A.M. (2004) The Breakdown of Starch in Leaves. New Phytologist, 163, 247-261.

[74]   Zhou, R., Silcher, R.C. and Quebedeau, B. (2002) Apple Leaf Sucrose Phosphatesynthase Is Inhibited by Sorbitol-6-Phosphate. Functional Plant Biology, 29, 569-574.

[75]   Dubey, R.S. and Singh, A.K. (1999) Salinity Induces Accumulation of Soluble Sugars and Alter the Activity of Sugar Metabolizing Enzymes in Rice Plants. Biologia Plantarum, 42, 233-239.

[76]   Devi, R., Munjral, N., Gupta, A.K. and Kaur, N. (2007) Cadmium Induced Changes in Carbohydrate Status and Enzymes of Carbohydrate Metabolism, Glycolysis and Pentose Phosphate Pathway in Pea. Environmental and Experimental Botany, 61, 167-174.

[77]   Couée, I., Sulmon, C., Gouesbet, G. and El Amrani, A. (2006) Involvement of Soluble Sugars in Reactive Oxygen Species Balance and Responses to Oxidative Stress in Plants. Journal of Experimental Botany, 57, 449-459.

[78]   Rahoui, S., Chaoui, A. and El Ferjani, E. (2010) Reserve Mobilization Disorder in Germinating Seeds of Vicia faba L. Exposed to Cadmium. Journal of Plant Nutrition, 33, 809-817.

[79]   Hasegawa, P.M., Bressan, R.A., Zhu, J.K. and Bohnert, H.J. (2000) Plant Cellular and Molecular Responses to High Salinity. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 463-499.

[80]   López-Berenguer, C., García-Viguera, C. and Carvajal, M. (2006) Are Root Hydraulic Conductivity Responses to Salinity Controlled by Aquaporins in Broccoli Plants? Plant Soil, 279, 13-23.

[81]   Fu, L., Shen, Q., Kuang, L., Yu, J., Wu, D. and Zhang, G. (2018) Metabolite Profiling and Gene Expression of Na/K Transporter Analyses Reveal Mechanisms of the Difference in Salt Tolerance between Barley and Rice. Plant Physiology and Biochemistry, 130, 248-257.

[82]   Ríos, J.J., Rosales, M.A., Blasco, B., Cervilha, L., Romero, L. and Ruiz, J.M. (2008) Biofortification of Se and Induction of the Antioxidant Capacity in Lettuce Plants. Scientia Horticulturae, 116, 248-255.

[83]   Yao, X.Q., Chu, J.Z., He, X.L., Liu, B.B., Li, J.M., et al. (2013) Effects of Selenium on Agronomical Characters of Winter Wheat Exposed to Enhanced Ultra-Violet-B. Ecotoxicology and Environmental Safety, 92, 320-326.

[84]   Filek, M., Keskinen, R., Hartikainen, H., Szarejko, I., Janiak, A., Miszalski, Z., et al. (2008) The Protective Role of Selenium in Rape Seedlings Subjected to Cadmium Stress. Journal of Plant Physiology, 165, 833-844.

[85]   Nouet, C.C., Motte, P. and Hanikenne, M. (2011) Chloroplastic and Mitochondrial Metal Homeostasis. Trends in Plant Science, 16, 395-404.

[86]   Feng, R., Wei, C. and Tu, S. (2013) The Roles of Selenium in Protecting Plants against Abiotic Stresses. Environmental and Experimental Botany, 87, 58-68.

[87]   Pazurkiewicz-Kocot, K., Galas, W. and Kita, A. (2003) The Effect of Selenium on the Accumulation of Some Metals in Zea mays L. Plants Treated with Indole-3-Acetic Acid. Cellular & Molecular Biology Letters, 8, 97-103.