Biochemical and physiological responses of metal toxicity in some barley and wheat varieties from Central Anatolia

Year 2016, Volume: 9 Issue: 3, 12 - 25, 15.12.2016

Elif Öztetik

Abstract

The factors like increased traffic load due to population denstity, environmental pollution, industrial activities and improper practices of agricultural applications could be counted as a source of heavy metal accumulation in air, water and soil. The effects of heavy metals which accumulated in soils continue for a long period of time as a result of food chain between organisms and considered as a serious threat to human health. With this study, toxic effects of heavy metals on germination, roots and shoots lengths, water, protein, glutathione GSH contents and glutathione Stransferase GST activities of barley Hordeum vulgare cv. Ince 04 and wheat Triticum aestivum cv. Yunus varieties were investigated through different concentrations of single lead chloride PbCl2 and cadmium chloride CdCl2 0, 1.5 and 3.0 mM and combined PbCl2 + CdCl2 1.5 + 1.5 and 3.0 + 3.0 mM applications. In conclusion, it was shown that biochemical and physiological mechanisms were affected differently with varying concentrations of heavy metals and Ince 04 barley were found to be more tolerant to heavy metal stress by comparing to Yunus wheat . For more tolerant variety Ince 04 , the observed values as follows after 3.0 mM PbCl2 + CdCl2 treatment; 80% decrease in germination, 75 and 65% decrease of lengths in roots and shoots, 73 and 65 % decrease of water contents in roots and shoots, 134 and 40% increase of GSH contents in roots and shoots, 15 and 50 % increase of protein contents in roots and shoots and 70 and 39 % increase of GST activities in roots and shoots

Keywords

barley, germination, GST, heavy metals Cd, Pb, wheat

Orta Anadolu’ya ait bazı arpa ve buğday varyetelerinin metal toksitesine verdiği biyokimyasal ve fizyolojik tepkiler

Abstract

Nüfus yoğunluğu nedeniyle artan trafik yükü, çevresel kirlenme, endüstriyel aktiviteler ve yanlış tarım uygulamaları gibi faktörler, hava, su ve topraktaki ağır metal birikiminin kaynağı olarak sayılabilir. Toprakta biriken ağır metallerin etkileri, organizmalar arasındaki besin zinciri etkisi ile daha uzun süreli olmakta ve bu durum insan sağlığı için ciddi bir tehlike olarak kabul edilmektedir. Bu çalışmada, hem tekli kurşun klorid PbCl2 ve kadmiyum klorid CdCl2 0, 1.5 ve 3.0 mM ve hem de kombine PbCl+CdCl2 1.5 + 1.5 ve 3.0 + 3.0 mM uygulamaları ile ağır metallerin arpa Hordeum vulgare cv. Ince 04 ve buğday Triticum aestivum cv. Yunus varyetelerindeki çimlenme, kök ve yaprak uzunluğu, su, protein ve glutatyon GSH miktarları ile glutatyon S-transferaz GST aktiviteleri üzerindeki toksik etkileri araştırılmıştır. Sonuç olarak, farklı ağır metal konsantrasyonlarının biyokimyasal ve fizyolojik mekanizmaları farklı şekillerde etkilediği ve Ince 04 arpa çeşidinin ağır metal stresine Yunus buğday çeşidine nazaran daha toleranslı olduğu bulunmuştur. Daha toleranslı olan çeşit Ince 04 için, 3.0 mM PbCl2 +CdCl2uygulaması sonrasında gözlenen değerler; çimlenmede % 80 oranında azalma, kök ve yaprak uzunluklarında %75 ve 65 oranlarında azalma, su miktarlarında kökler ve yapraklarda %73 ve 65 oranlarında azalma, GSH miktarlarında kökler ve yapraklarda %134 ve 40 oranlarında artma, protein miktarlarında kökler ve yapraklarda %15 ve 50 oranlarında artma ile GST aktivitelerinde kökler ve yapraklarda %70 ve 39 oranlarında artma şeklindedir

Keywords

arpa, çimlenme, GST, ağır metaller Cd, Pb, buğday

References

• Ali, G., Srivastava, P. S., Iqbal, M. (1998). Morphogenic response and proline content in Bacopa monnieri cultures grown under copper stress. Plant Science, 138(2), 191-195.
• Arora, A., Sairam, R.K., Srivastava, G.C. (2002). Oxidative stress and antioxidative system in plants. Current Science, 82(10), 1227- 1238.
• Backor, M., Loppi, S. (2009). Interactions of lichens with heavy metals. Biologia Plantarum, 53(2), 214-222.
• Barcelo, J., Poschenrieder, C. (2002). Fast root growth responses, root exudates, and internal detoxication as clues to the mechanisms of aluminium toxicity and resistance: a review. Environmental and Experimental Botany, 48(1), 75-92.
• Becerril, J.M., Gonzalez-Murua, C., Munoz-Rueda, A., De Felipe, M.R. (1989). Changes induced by cadmium and lead in gas exchange and water relations of clover and lucerne. Plant Physiology and Biochemistry, 27(6), 913-918.
• Chandra, R., Bharagava, R.N. Yadav, S., Mohan, D. (2009). Accumulation and distribution of toxic metals in wheat (Triticum aestivum L.) and Indian mustard (Brassica campestris L.) irrigated with distillery and tannery effluents. Journal of Hazardous Materials, 162(2-3), 1514-1521.
• Cobbett, C., Goldsbrough, P. (2002). Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology, 53, 159-182.
• Costa, G., Morel, J.L. (1994). Water relations, gas exchange and amino acid content in Cd-treated lettuce. Plant Physiology and Biochemistry, 32(4), 561-570.
• Dalcorso, G., Farinati, S., Furini, A. (2010). Regulatory networks of cadmium stress in plants. Plant Signaling and Behavior, 5(6), 1- 5.
• DalCorso, G., Farinati, S., Maistri, S., Furini, A. (2008). How plants cope with cadmium: staking all on metabolism and gene expression. Journal of Integrative Plant Biology, 50(10), 1268-1280.
• Das, P., Samantaray, S., Rout, G.R. (1997). Studies on cadmium toxicity in plants: A review. Environmental Pollution, 98(1), 29-36.
• De Dorlodot, S., Lutts, S., Bertin, P. (2005). Effects of ferrous iron toxicity on the growth and mineral composition of an interspecific rice. Journal of Plant Nutrition, 28(1), 1-20.
• Dubey, R.S. (2011). Metal toxicity, oxidative stress and antioxidative defense system in plants. In S.D. Gupta (Ed.), Reactive oxygen species and antioxidants in higher plants (pp. 177-203). Boca Raton, Fla, USA: CRC Press.
• Edwards, R., Dixon, D. (2005). Plant glutathione transferases. Methods in Enzymology, 401, 169-186.
• Ellman, G.L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82(1), 70-77.
• Frear, D.S., Swanson, H.R. (1970). Biosynthesis of S-(4-ethylamino-6-isopropylamino-2-s-triazine) glutathione: Partial purification and properties of glutathione S-transferase from corn. Phytochemistry, 9(10), 2123-2132.
• Freeman, J.L., Persans, M.W., Nieman, K., Albrecht, C., Peer,W., Pickering, I.J., Salt, D.E. (2004). Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell, 16(8), 2176-2191.
• Freeman, J.L., Garcia, D., Kim, D., Hopf, A., Salt, D.E. (2005). Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiology, 137(3), 1082- 1091.
• Foyer, C.H., Noctor, G. (2005). Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell, 17(7), 1866-1875.
• Gamalero, E., Lingua, G., Berta, G., Glick B. R. (2009). Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Canadian. Journal of Microbiology, 55(5), 501-514.
• Gill, M. (2014). Heavy metal stress in plants: a review. International Journal of Advanced Research, 2(6), 1043-1055.
• Gill S.S., Tuteja N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stres tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909-930.
• Gohar, Z.N., Ahmad, R., Gul, H. (2003). Growth and development of cotton roots at various soil textures under soil conditions. Pakistan Journal of Botany, 35(5), 949-959.
• Gonzalez, L., Reigosa Roger, M.J. (2001). Plant water status. In M.J. Reigosa Roger (Ed.). Handbook of Plant Ecophysiology Techniques (pp.185-191). Dordrecht, The Netherlands: Kluwer Academic Publisher.
• Gonzalez, L., Gonzalez-Vilar, M. (2001). Determination of relative water content. In M.J. Reigosa Roger (Ed.), Handbook of Plant Ecophysiology Techniques (pp. 207-212). Dordrecht, The Netherlands: Kluwer Academic Publisher.
• Guo, J., Dai, X., Xu, W., Ma, M. (2008). Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere, 72(7), 1020-1026.
• Habig, W.H., Pabst, M.J., Jakoby, W.B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130-7139.
• Habig, W.H., Jakoby, W.B. (1981). Assays for differentiation of glutathione S-transferases. Methods in Enzymology, 77, 398-405.
• Hagemeyer, J., Breckle, S.W. (1996). Growth under trace element stress. In Y. Waisel, U. Kafkafi (Ed.), Plant roots: The hidden half (pp. 415-433). New York, USA: Marcel Dekker.
• Hall, J.L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53(366), 1-11.
• Halliwell, B. (1995). How to characterize an antioxidant: An update? Biochemistry Society Symposium, 61, 73-101.
• Haluskova, L , Valentovicova, K., Huttova, J., Mistrik, I., Tamas, L. (2009). Effect of abiotic stresses on glutathione peroxidase and glutathione S-transferase activity in barley root tips. Plant Physiology and Biochemistry, 47(11-12), 1069-1074.
• Hoagland, D. R., Arnon, D. I. (1950). The water-culture method for growing plants without soil. California Agricultural Experiment Station, Berkeley.
• Klein, M., Burla, B., Martinoia, E. (2006). The multidrug resistance-associated proteins (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Letters, 580(4), 1112-1122.
• Kositsin, A.V. (1991). Interaction between metals and enzymes. In N.V. Alekseeva-Popova (Ed.), Tolerance of plant species grown in the wild to heavy metals (pp. 15-22). Leningrad: Lenuprizdat.
• Kranner, I., L. Colville, L. (2011). Metals and Seeds: Biochemical and molecular implications and their significance for seed germination. Environmental and Experimental Botany, 72(1), 93-105.
• Lamhamdi, M. Bakrim, A. Aarab, A., Lafont, R., Sayah, F. (2011). Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth. Comptes Rendus Biologies, 334(2),118-126.
• Levetin, E., McMahon, K. (2011). Plants and Society. USA: McGraw-Hill.
• Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randal, R.J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193(1), 265-275.
• Navarro, L,. Guitian, J. (2003). Seed germination and seedling survival of two threatened endemic species of the northwest Iberian Peninsula. Biological Conservation, 109(3), 313-320.
• Mahmood, T., Islam, K.R. Muhammad, S. (2007). Toxic effects of heavy metals on early growth and tolerance of cereal crops. Pakistan Journal of Botany, 39(2), 451-462.
• Manmathan, H., Lapitan, N. L. (2013). Measuring germination percentage in wheat. Bio-protocol 3(16): e 866. http://www.bio- protocol.org/e866. (Date of access: 29.11.2016).
• Mannervik, B., Danielson, U. H. (1988). Glutathione transferases- structure and catalytic activity. CRC Critical Reviews in Biochemistry and Molecular Biology, 23(3), 283-337.
• May, M.J., Vernoux, T., Leaver, C., Van Montagu, M., Inze, D. (1998). Glutathione homeostasis in plants: Implications for environmental sensing and plant development. Journal of Experimental Botany, 49(321), 649-667.
• Mel’nichuk, Yu.P. (1990). The effect of cadmium ions on the cell division and plant growth. Kiev: Naukova Dumka.
• Mendoza-Cozatl, D., Devars, S., Loza-Tavera, H., Moreno-Sanchez, R. (2002). Cadmium accumulation in the chloroplast of Euglena gracilis. Physiologia Plantarum, 115(2), 276-283.
• Mesmar, M.N., K. Jaber, K. (1991).The toxic effect of lead on seed germination, growth, chlorophyll and protein contents of wheat and lens. Acta Biologica Hungarica, 42(4), 331-344.
• Mullineaux, P., Rausch, T. (2005). Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthesis Research, 86(3), 459-474.
• Munzuroglu, O., Zengin, F.K. (2006). Effect of cadmium on germination, coleoptile and root growth of barley seeds in the presence of gibberellic acid and kinetin. Journal of Environmental Biology, 27(4), 671-677.
• Nagajyoti, P. C., Lee, K. D., Sreekanth, T.V.M. (2010). Heavy metals, occurrence and toxicity for plants: A review. Environmental Chemistry Letters, 8(3), 199-216.
• Obroucheva, N.V. Bystrova, E.I. Ivanov, V.B. Anupova, O.V. Seregin, I.V. (1998). Root growth responses to lead in young maize seedling. Plant and Soil, 200(1), 55-61.
• Ogawa, K., Iwabuchi, M. (2001). A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide. Plant and Cell Physiology, 42(3), 286-291.
• Ono, H., Ozaki, K., Yoshikawa, H. (2005). Identification of cytochrome P450 and glutathione-S-transferase genes preferentially expressed in chemosensory organs of the swallowtail butterfly, Papilio xuthus L. Insect Biochemistry and Molecular Biology, 35(8), 837-846.
• Opik, H., Rolfe, S. A. (2005). The Physiology of flowering plants. Cambridge: Cambridge University Press.
• Öncel, I., Keleş, Y. Ustun, A.S. (2000). Interactive effects of temperature and heavy metal stress on the growth and some biochemical compounds in wheat seedling. Environmental Pollution, 107(3), 315-320.
• Oztetik, E. (2005). Purification of glutathione S-transferases and genetic characterization of zeta isozyme from Pinus brutia, Ten. (PhD Dissertation). Ankara, Turkey: Middle East Technical University.
• Oztetik, E. (2015). Biomarkers of ecotoxicological oxidative stress in an urban environment: using evergreen plant in industrial areas. Ecotoxicology, 24(4), 903-914.
• Oztetik, E., Cakir, A. (2014). New food for an old mouth: New enzyme for an ancient archaea. Enzyme and Microbial Technology, 55, 58-64.
• Ozturk, L., Eker, S., 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(3), 161-168.
• Parys, E., Romanowska, E., Siedlecka, M., Poskuta, J.W. (1998). The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiologiae Plantarum, 20(3), 313-322.
• Patra, M., Bhowmik, N.,Bandopadhyay, B., Sharma, A. (2004). Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environmental and Experimental Botany, 52(3), 199-223.
• Rausch, T., Gromes, R., Liedschulte, V., Muller, I., Bogs, J., Galovic, V., Wachter, A. (2007). Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biology, 9(5), 565-572.
• Rea, P. A. (1999). MRP subfamily ABC transporters from plants and yeast. Journal of Experimental Botany, 50 (Special issue), 895- 913.
• Reddy, A.M., Kumar, S.G., Jyotsnakumari, G., Thimmanayak, S., Sudhakar, C. (2005). Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemospher, 60(1), 97-104.
• Salt, D.E., Rauser, W.E. (1995). MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiology, 107(4), 1293-1301.
• Seregin, I.V., V. B. Ivanov, V.B. (2001). Physiological Aspects of Cadmium and Lead Toxic Effects on Higher Plants. Russian Journal of Plant Physiology, 48(4), 523-544.
• Seregin, I.V., A.D. Kozhevnikova, A.D. (2008). Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium. Russian Journal of Plant Physiology, 55(1), 1-22.
• Shafi, M., Guoping, Z., Bakht, J., Khan, M.A., Islam, E.U., Dawood, M. K. (2010). Effect of cadmium and salinity stresses on root morphology of wheat. Pakistan Journal of Botany, 42(4), 2747-2754.
• Shao, H.B., Liang, Z.S., Shao, M.A., Sun, Q., Hu, Z.M. (2005). Investigation on dynamic changes of photosynthetic characteristics of 10 wheat (Triticum aestivum L.) genotypes during two vegetative-growth stages at water deficits. Colloids and Surfaces B: Biointerfaces, 43(3-4), 221-227.
• Shao, H.B., Chu, L.Y., Lu, Z.H., Kang, C.M. (2008). Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. International Journal of Biological Science, 4(1), 8-14.
• Sharma, R.K., Agrawal, M. (2005). Biological effects of heavy metals: An overview. Journal of Environmental Biology, 26(2), 301- 313.
• Sharma, S.S., Dietz, K.J. (2009). The relationship between metal toxicity and cellular redox imbalance. Trends in Plant Science, 14(1), 43-50.
• Sharma, P., Dubey R.S. (2004). Ascorbate peroxidase from rice seedlings: Properties of enzyne isoforms, effects of stresses and protective roles of osmolytes. Plant Science, 167(3), 541-550.
• Sharma, P., Dubey, R.S. (2005). Lead toxicity in plants. Brazilian Journal of Plant Physiology, 17(1), 35-52.
• Sharma, P., Dubey, R.S. (2007). Involvement of oxidative stress and role of antioxidative defense systemin growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Reports, 26(11), 2027-2038.
• Singh, P.K., Tewari, R.K. (2003). Cadmium toxicity induced chnages in plant water relations and oxidative metabolism of Brassica juncea L. plants. Journal of Environmental Biology, 24(1), 107-112.
• Srivastava, S., Tripathi, R.D., Dwivedi, U.N. (2004). Synthesis of phytochelatins and modulation of antioxidants in response to cadmium stress in Cuscuta reflexa – an angiospermic parasite. Journal of Plant Physiology, 161(6), 665-674.
• Titov, A.F. Talanova, V.V., Boeva, N.P. (1996). Growth responses of barley and wheat seedlings to lead and cadmium. Biologia Plantarum, 38(3), 431-436. Transitional Zone Agricultural Research http://arastirma.tarim.gov.tr/gktaem/Menu/12/Tescilli-Cesitlerimiz (Date of access: 07.12.2016). Institute website. (2016). Registered Varieties.
• USDA Foreign Agricultural Service. (2016). Turkey Grain and Feed Annual Report, 2016. E. Leonardi. (Ed). (GAIN Report No. TR6015). http://gain.fas.usda.gov/Recent%20GAIN%20Publications/Grain%20and%20Feed%20Annual_Ankara_Turkey_3-29- 2016.pdf (Date of access: 10.12.2016).
• Vassilev, A., Yordanov, I., Tsonev, T. (1997). Effects of Cd2+ on the physiological state and photosynthetic activity of young barley plants. Photosynthetica, 34(2), 293-302.
• Verma, S., Dubey, R.S. (2003). Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Science, 164(4), 645-655.
• Villiers, F. Ducruix, C., Hugouvieux, V. (2011). Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics. 11(9), 1650-1663.
• Weckx, J.E.J., Clijsters, H.M.M. (1997). Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiology and Biochemistry, 35(5), 405-410.
• Wojcik, M., Tukendorf, A. (1999). Cd-tolerance of maize, rye and wheat seedlings. Acta Physiologiae Plantarum, 21(2), 99-107.
• Wu, F., Zhang, G., Dominy, P. (2003). Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. Environmental and Experimental Botany, 50(1), 67-78.
• Wu, F.B., G.P. Zhang. (2002). Alleviation of cadmium-toxicity by application of zinc and ascorbic acid in barley. Journal of Plant Nutrition, 25(12), 2745-2761.
• Xiang, C., Werner, B.L., Christensen, E.M., Oliver, D.J. (2001). The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiology, 126(2), 564-574.
• Yadav, S.K. (2010). Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South African Journal of Botany, 76(2), 167-179.
• Yazaki, K. (2006). ABC transporters involved in the transport of plant secondary metabolites. FEBS Letters, 580(4), 1183-1191.
• Yücel, E. (2000). Ebe Karaçamın biyolojik ve ekolojik özellikleri. Eskisehir; Birlik Ofset Matbaacılık.
• Yücel, M., Yücel, E. (2013). On the ecotoxicological effects of heavy metal pollution of industrial origin determination of wheat varieties. Biological Diversity and Conservation, 6(3), 6-11.
• Zhu, Y.L. Pilon-Smits, E.A.H. Tarun, A.S., Weber, S.U., Jouanin, L. Terry, N. (1999). Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing g-Glutamylcysteine synthetase. Plant Physiology, 121(4), 1169-1177.