Nikel’in Brokoli (Brassica oleracea L. var. italica) Tohumlarının Çimlenmesi ve Fide Gelişimi Üzerine Etkileri

Year 2021, Volume: 9 Issue: 3 - Additional Issue, 226 - 261, 29.05.2021

Çiğdem Çıngıl Barış Muammer Ünal

https://doi.org/10.29130/dubited.798455

Cited By: 3

Abstract

Bu araştırmada, brokoli bitkisinin tohum ve fidelerinde değişen konsantrasyonlardaki nikelin etkisi ve birikimi incelenmiştir. Tohumlarda çimlenme yüzdesi, bitkinin kök-gövde uzunlukları, ağırlık miktarları, klorofil, karotenoid, total çözünebilir protein ile MDA içerikleri, POD aktiviteleri ve Ni birikimi belirlenmiştir. 100 μM NiSO4 ün tohumlarda çimlenmeyi inhibe ettiği gözlenmiştir. Ni’nin büyümeyi etkilediği, ağırlık miktarlarında da değişikliklere neden olduğu belirlenmiştir. 9 günlük fidelerin klorofil içerikleri 1 μM NiSO4 de artarken, 30 günlük fidelerde ise 0.1 μM NiSO4 de artış tespit edilmiştir. Fidelerdeki total çözünebilir protein içeriğinde 10 ve 100 μM NiSO4 de azalışlar gözlenirken, POD aktivitesinde artışlar gözlenmiştir. Ayrıca, nikelin özellikle köklerde biriktiği belirlenmiştir. Nikelin brokolinin çimlenme ve büyüme-gelişmesi üzerine olan etkileri ile ilgili olarak, düşük konsantrasyonlardan (0.01, 0.1 ve 1 μM) bitkinin olumlu etkilendiği, yüksek konsantrasyonların ise (10 ve 100 μM) toksik etkilere neden olduğu tespit edilmiştir.
Anahtar Kelimeler: Nikel, Çimlenme, Bitki büyümesi, Brokoli, Brassica oleracea L. var. italica, Metal birikimi

Keywords

Nikel, Çimlenme, Bitki büyümesi, Brassica oleracea L. var. italica, Metal birikimi

Supporting Institution

İstanbul Üniversitesi Bilimsel Araştırma Projeleri Birimi

Project Number

2265

Thanks

Bu çalışma İstanbul Üniversitesi Bilimsel Araştırma Projeleri tarafından desteklenmiştir (Proje no: 2265).

The Effects of Nickel on Seed Germination and Seedling Development in Broccoli (Brassica oleracea L. var. italica)

Abstract

In this research, the effect and accumulation of nickel in varying concentrations in broccoli seeds and seedlings were investigated. Germination rate of seeds, root-stem length of the plant, weight amounts, contents of chlorophyll, carotenoid, total soluble protein and MDA, POD activities and Ni accumulation were determined. It was observed that 100 μM NiSO4 inhibited germination in seeds. It has been determined that Ni affect growth and also cause changes in weight amounts. While the chlorophyll content of 9-day-old seedlings increased in 1 μM NiSO4 was applied, an increase was found in 0.1 μM NiSO4 in 30-day-old seedlings. While decreases were observed in 10 and 100 μM NiSO4 in total soluble protein content in seedlings, increases in POD activity were observed. In addition, it was determined that nickel accumulated especially in the roots. Regarding the effects of nickel on the germination and growth-development of broccoli, it was determined that plant is affected positively in low concentrations (0.01, 0.1 and 1 μM), while high concentrations (10 and 100 μM) caused toxic effects.
Keywords: Nickel, Germination, Plant growth, Broccoli, Brassica oleracea L. var. italica, Metal accumulation

Project Number

2265

References

• [1] H. Marschner, Mineral Nutrition of Higher Plants, 2nd ed., Academic Press, London, pp 889, 1995.
• [2] K. Mengel, E.A. Kirkby, H. Kosegarten ve T. Appel, Principles of Plant Nutrition, Dordrecht: Kluwer Academic, 2001.
• [3] P.J. White ve P.H. Brown, Plant Nutrition for Sustainable Development and Global Health, Ann. of Bot., 105(7), 1073-1080. 2010.
• [4] D.L. Eskew, R.M. Welch, ve W.A. Norvell, Nickel, an Essential Micronutrient for Legumes and Possibly All Higher Plants, Science, 222, 621-623, 1983.
• [5] P.H. Brown, , R.M. Welch ve E.E. Cary, Nickel a Micronutrient Essential for All Higher Plants, Plant Physiology, 85, 801-803, 1987.
• [6] A. Banerjee ve A. Roychoudhury, Plant Responses to Environmental Nickel Toxicity. In: Aftab T., Hakeem K.R. (eds) Plant Micronutrients. Springer, Cham., 2020.
• [7] D.L. Eskew, R.M. Welch ve W.A. Norvell, Nickel in Higher Plants: Further Evidence for an Essential Role, Plant Physiol., 76, 671-693, 1984.
• [8] J. Molas, Changes in Morphological and Anatomical Structure of Cabbage (Brassica oleracea L.) Outer Leaves and in Ultrastructure of Their Chloroplasts Caused by an in vitro Excess of Nickel, Photosynthetica, 34 (4), 513-522, 1997.
• [9] P. Zornoza, S. Robles ve N.Martin, Alleviation of Nickel Toxicity by Ammonium Supply to Sunflower Plants, Plant and Soil, 208, 221-226, 1999.
• [10] P.H. Brown, R.M. Welch ve J. Madison, Effect of Nickel Deficiency on Soluble Anion, Amino Acid and Nitrogen Levels in Barley, Plant and Soil, 125, 19-27, 1990.
• [11] T. Pandolfini, R. Gabbrielli ve C.Comparini, Nickel Toxicity and Peroxidase Activity in Seedlings of Triticum aestivum L., Plant Cell and Environment, 15, 719-725, 1992.
• [12] E. Gajewska ve M. Sklodowska, Antioxidative Responses and Proline Level in Leaves and Roots of Pea Plants Subjected to Nickel Stress, Acta Physiologia Plantarum, 27(3), 329-339, 2005.
• [13] A.M. Mayer ve A. Mayber, The Germination of Seeds, 3rd edition, Pergamon Pres Ltd., U.K., 0-08-028854-5, 1982.
• [14] H. Thomas, D.P. Webb ve P.F. Wareing, Seed dormancy in Acer: maturation in relation to dormancy in Acer pseudoplatanus L., Journal of Experimental Botany, 24, 958-967, 1973.
• [15] W.E. Finch-Savage ve G. Leubner-Metzger, Seed Dormancy and the Control of Germination, New Phytologist, 171, 501-523, 2006.
• [16] M.T. Mooring, A.W. Cooper ve E.D. Senaca, Seed Germination Response and Evidence for Height Ecophenes in Spartina alterniflora from North Carolina, American Journal of Botany, 58, 48-55, 1971.
• [17] J.D. Bewley ve M.Black, Seeds: Physiology of Development and Germination, 2nd edition, Plenum Pres, New York, 1994.
• [18] B. Veer, Effect of Phasic Treatment of Ni on Seedling Growth and Activities of Certain Hydrolytic Enzymes of Seeds, J. Ind. Bot. Soc., 5, 351-354, 1988.
• [19] E.J. Underwood, Trace Elements in Human and Animal Nutrition, 3rd Edn., Academic Press, New York, pp: 461-479, 1971.
• [20] D. Bertrand ve A. De Wolf, Importance in Nickel, Comme Okigoelement Pour les Rhizobium des Nodules Leguminueses, C.R. Hend. Acad. Sci., Paris, 79, 1855-1858, 1973.
• [21] S.N. Singh, Effects of Nickel on Germination, Growth, Total Nitrogen and Phosphate Levels of Cicer arietinum L. Seedlings, Trop. Ecol., 25, 90-94, 1984.
• [22] W.P. Bushnell, Delay of Senescence in Wheat Leaves by Cytokinins, Nickel and other substances, Can. J. Bot., 44, 1485-1493, 1966.
• [23] R.M. Welch, The Biological Significance of Nickel, J. Plant Nutr., 3, 345-356, 1981.
• [24] P. Pelosi, R. Fiorentini ve C. Galoppini, On the Nature of Nickel Compounds in Alyssum bertolonii desv-II, Agric. Biol. Chem., 40, 1641-1642, 1976.
• [25] J. Gerendás, J. Polacco, S.K. Freyermuth ve B. Sattelmacher, Significance of Nickel for Plant Growth and Metabolism, Z. Pflanzenernaehr Bodenkd, 162, 241-256, 1999.
• [26] A.J. Bloom, Mineral Nutrition, In: Plant Physiology, Taiz, L. and E. Zeiger (Eds.). Sinauer Associates, Sunderland, MA, pp: 67-86, 2002.
• [27] J.C. Polacco, Is Nickel a Universal Component of Plant Urease?, Plant Sci. Lett., 10, 249-255, 1977.
• [28] J.E. Dixon, C. Gazzola, R.B. Blakely ve B. Zerner, Jack-bean Urease (EC 3.5.1.5.3). A Metalloenzyme, A Simple Biological Role for Nickel, J. Am. Chem. Soc., 97, 4131-4133, 1975.
• [29] C. Tsui, Effect of Seed Treatment with Micro-elements on the Germination and Early Growth of Wheat, Scientia Sinica, 4, 129-135, 1955.
• [30] I. Pais, A. Somos, L. Duda, F. Tarjanyi ve F. Nagymihaly, Trace Elements Experiments with Tomato and Paprika, I. Kiserletugyi Kozlem, 62, 25-40, 1970.
• [31] F.A. Bazzaz, R.B. Carlson ve G.L. Rolfe, The Effect of Heavy Metals on Plants, I Inhibition of Gas Exchange in Sunflower by Pb, Cd, Ni and Ti, Environ. Pollut., 7, 241-246, 1974.
• [32] W.R. Gordon, S.S. Schwemmer ve W.S. Hillman, Nickel and the Metabolism of Urea by Lemna paucicostata Hegelm. 6746, Planta, 140, 265-268, 1978.
• [33] D.R. Hoagland ve D.I. Arnon, The Water-culture Method for Growing Plants without Soil, Univ. Calif. Coll., Agric. Exp. Sta. Circ., 347, 1-32, 1938.
• [34] Y. Okatan, G.M. Kahanak ve L.D. Nooden, Characterization and Kinetics of Soybean Maturation and Monocarpic Senescence, Physiol. Plant., 52, 330-338, 1981.
• [35] T.R. Parsons ve J.D.H. Strickland, Discussion of Spectrophotometric Determination of Marine Pigments, with Revised Equations for Ascerting Chlorophylls and Caretonoids, J Mar. Res., 21, 115-163, 1963.
• [36] M.M. Bradford, A rapid and Sensitive Method for the Quantization of Microgram Quantities of Protein Utilising the Principle of Protein–dye Binding, Anal. Biochem., 72, 248-254, 1976.
• [37] H. Birecka, K.A. Briber ve J.L.Catalfamo, Comparative Studies on Tobacco Pit and Sweet Potato Root Isoperoxidases in Relation to Injury, Indolaceticacid and Ethylene effects, Plant Physiol., 52, 43-49, 1973.
• [38] R.L. Heath ve L. Packer, Photoperoxidation in Isolated Chloroplast. I. Kinetics and Stoichiometry of Fatty Acid Peroxidation, Arch. Biochem. Biophys., 125, 189-198, 1968.
• [39] EPA, Microwave assisted acid digestion of sediments, sludges, soils, and oils. Method 3051, Test Methods for Evaluating Solid Waste, Physical/Chemical Methods, 3rd ed: U.S. Environmental Protection Agency, Office of Solid Waste and Emergency Response. U.S. Government Printing Office: Washington DC, 1986; SW. 846, 1994.
• [40] Ö. Munzuroğlu ve H. Geçkil, Effects of Metals on Seed Germination, Root Elongation and Coleoptile and Hypocotyl Growth in Triticum aestivum and Cucumis sativus, Environ. Cont. and Toxi., 43, 203-213, 2002.
• [41] S. Akıncı ve İ.E. Akıncı, Nikelin Ispanakta (Spinacia oleracea) Çimlenme ve Bazı Fide Büyüme Parametreleri Üzerine Etkisi, Ekoloji, 20, 79, 69-76, 2011.
• [42] W. Li, M.A. Khan, S. Yamaguchi ve Y. Kamiya, Effects of Heavy Metals on Seed Germination and Early Seedling Growth of Arabidopsis thaliana, Plant Growth Regulation, 46, 45-50, 2005.
• [43] I.V. Seregin ve A.D. Kozhevnikova, Distribution of Cadmium, Lead, Nickel, and Strontium in Imbibing Maize Caryopses, Russian Journal of Plant Physiol., 52, 4, 565-569, 2005.
• [44] L. Espen, L. Piroyano, S.M. Cocucci, Effect of Ni During the Early Phases of Radish (Raphanus sativus) Seed Germination, Environmental and Experimental Botany, 38, 187-197, 1997.
• [45] P. Sharma, R. Bhardwaj, N. Arora, H.K. Arora ve A. Kumar, Effects of 28-homobrassinolide on Nickel Uptake, Protein Content and Antioxidative Defence System in Brassica juncea, Biol Plant., 52, 767-770, 2008.
• [46] S. Citterio, A. Santagostino, P. Fumagalli, N. Prato, P. Ranalli, ve S. Sgorbati, Heavy Metal Tolerance and Accumulation of Cd, Cr, and Ni by Cannabis sativa L., Plant and Soil, 256, 243-252, 2003.
• [47] C.D. Jadia ve M.H. Fulekar, Phytoremediation: The Application of Vermicompost to Remove Zinc, Cadmium, Copper, Nickel and Lead by Sunflower Plant, Environ. Engineering and Management Journal, 7(5), 547-558, 2008.
• [48] P.K. Das, M. Kar ve D.Mishra, Nickel Nutrition of Plants: Effect of Nickel on Some Oxidase Activities during Rice (Oryza sativa L.) Seed Germination, Z. Pflanzenphysiol., 90, 225-233, 1978. [49] J.R. Peralta, J.L. Gardea Torresdey, K.J. Tiemann, E. Gomez, S. Arteaga, E. Rascon ve J.G. Parsons, Uptake and Effects of Five Heavy Metals on Seed Germination and Plant Growth in Alfalfa (Medicago sativa) L., Bull. of Environmental Cont. and Toxic., 66(6), 727-734, 2001.
• [50] M.S.A. Ahmad, M. Ashraf, R. Ahmed ve M.Y. Ashraf, Effect of Nickel on Seed Germinability of Some Elite Sunflower (Helianthus annuus L.) Cultivars, Pak. J. Bot., 41, 1871-1882, 2009.
• [51] G.R. Rout, S. Samantary ve P. Das, Effects of Chromium and Nickel on Germination and Growth in Tolerant and Non-Tolerant Populations of Echinochloa colona, Chemosphere, 40, 855-859, 2000.
• [52] F. Kırbağ-Zengin ve Ö. Munzuroğlu, Effects of Lead and Copper on the Growth of Root, Shoot and Leaf of Bean (Phaseolus vulgaris L.) Seedlings, G.Ü. Fen Bilimleri Dergisi, 17(3), 1-10, 2004.
• [53] P.C. Lolkema, M.H. Donker, A.J. Schouten ve W.H.O. Ernst, The Possible Role of Metallothioneins in Copper Tolerance of Silene cucubalus, Planta, 162, 174-179, 1984.
• [54] J.C. Fernandes ve F.S. Henriques, Biochemical, Physiological and Structural Effect of Excess Copper in Plants, The Bot. Revi., 57, 246-273, 1991.
• [55] C. Gonnelli, F. Galardi, R. Gabbrıelli, Nikel and Copper Tolerance and Toxicity in Three Tuscan Populations of Silene paradoxa, Physiologia Plantarum, 113, 507-514, 2001.
• [56] I.V. Seregin, A.D. Kozhevnikova, E.M. Kazyumina ve V.B.Ivanov, Nikel Toxicity and Distribution in Maize Roots, Russian Journal of Plant Physiology, 50(5), 711-717, 2003.
• [57] S.R. Lavado, A.C. Porcelli ve R. Alvarez, Nutrient and Heavy Metal Concentration and Distribution in Corn, Soybean and Wheat as Affected by Different Tillage Systems in the Argentina Pamps, Soil and Tillage Research, 62, 55-60, 2001.
• [58] X. Yang, V.C.Baligar, D.C. Martens ve R.B. Clark, Plant Tolerance to Nickel Toxicity: II. Nickel Effects on Influx and Transport of Mineral Nutrients in Four Plant Species, J. Plant Nutr., 19, 265-279, 1996.
• [59] B.U.Z. Rahmatullah, M. Salim ve K. Hussin, Influences of Ni Supply on Tomato Growth and N Uptake, International Journal of Agriculture and Biology, 3(2), 320-323, 2001.
• [60] H. Kupper, E. Lombi, F.J. Zhao, G. Wieshammer ve S.P. Mcgrath, Cellular Compartmentation of Nickel in the Hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense, J. Exp. Bot., 52, 2291-2300, 2001.
• [61] S. Clemens, M.G. Palmgren ve U. Kramer, A Long Way a Head: Understanding and Engineering Plant Metal Accumulation, Trends Plant Sci.,7, 309, 2002.
• [62] E. Gajewska, M. Skłodowska, M. Słaba ve J. Mazur, Effect of Nickel on Antioxidative Enzyme Activities, Proline and Chlorophyll Contents in Wheat Shoots, Biol. Plant., 50, 653-659, 2006.
• [63] C.M. Luna, C.A. Gonzalez ve V.S.Trippi, Oxidative Damage Caused by Excess of Copper in Oat Leaves, Plant Cell Physiol., 35, 11-15, 1994.
• [64] A. Cuypers, K.M. Koistinen, H. Kokko, S. Kärenlampi, S. Auriola ve J. Vangronsveld, Analysis of Bean (Phaseolus vulgaris L.) Proteins Affected by Copper Stress, Journal of Plant Physiology, 162, 383-392, 2005.
• [65] R. Athar ve M. Ahmad, Heavy Metal Toxicity: Effect on Plant Growth and Metal Uptake by Wheat, and on Free Living Azotobacter, Water Air Soil Pollut., 138, 165-180, 2002.
• [66] H. Rahman, S. Sabreen, S. Alam ve S. Kawai, Effects of Nickel on Growth and Composition of Metal Micronutrients in Barley Plants Grown in Nutrient Solution, J. Plant Nutr., 28, 393-404, 2005.
• [67] P.H. Brown, R.M. Welch, E.E. Cary ve R.T. Checkai, Beneficial Effects of Nickel on Plant Growth, Journal of Plant Nutrition, 10, 2125-2135, 1987.
• [68] B. Mocquot, J. Vangronsveld, H. Clijestres ve M. Mench, Copper Toxicity in Young Maize (Zea mays L.) Plants: Effects on Growth, Mineral and Chlorophyll Contents and Enzyme Activities, Plant Soil, 182, 287-300, 1996.
• [69] P. Vijayarengan ve D. Dhanavel, Effects of Nickel on Chlorophyll Content of Black Gram Cultivars, Adv. Plant Sci., 18, 253, 2005.
• [70] D. Mishra ve M. Kar, Nickel in Plant Growth and Metabolism, Bot. Rev., 40, 395-452, 1974.
• [71] E.A. Ewais, Effects of Cadmium, Nickel and Lead on Growth, Chlorophyll Content and Proteins of Weeds, Biol. Plant., 39, 403-410, 1997.
• [72] S. Monni, C. Uhlig, E. Hansen ve E. Magel, Ecophysiological Responses of Empetrum nigrum to Heavy Metal Pollution, Environ. Pollut., 112, 121-129, 2001.
• [73] H. Helmy-Latif, The Influence of Nickel Sulphate on Some Physiological Aspects of Two Cultivares of Raphanus sativus L. Arch., Biol. Sci. Belgrade, 62(3), 683-691, 2010.
• [74] D.D.K. Prasad ve A.R.K. Prasad, Effect of Lead and Mercury on Chlorophyll Synthesis in Mung Bean Seedlings, Phytochemistry, 26, 881, 1987.
• [75] M. Rizwan, M.G. Mostofa, M.Z. Ahmad, Y. Zhou, M. Adeel, S. Mehmood, M.A. Ahmad, R. Javed, M. Imtiaz ve O. Aziz, Hydrogen Sulfide Enhances Rice Tolerance to Nickel through the Prevention of Chloroplast Damage and the Improvement of Nitrogen Metabolism under Excessive Nickel, Plant Physiol. Biochem., 138, 100-111, 2019.
• [76] A.J.M. Baker, Accumulators and Excluders, Strategies in the Response of Plants to Heavy Metals, Journal of Plant Nutr., 3, 643-654, 1981.
• [77] W. Maksymiec, R. Russa, T. Urbanik-Sypniewska ve T. Baszynskı, Effect of Excess Cu on the Photosynthetic Apparatus of Runner Bean Leaves Treated at Two Different Growth Stages, Physiologia Plantarum, 91, 715-721, 1994.
• [78] M. Ciscato, R. Valcke, K. Van Loven, H. Clijsters ve F. Navarı-Izzo, Effects of in Vivo Copper Treatment on the Photosynthetic Apparatus of Two Triticum durum Cultivars with Different Stress Sensitivity, Physiol. Plant., 100, 901-908, 1997.
• [79] A.K. Tripati, T. Sadhna ve S. Tripathi, Changes in Some Physiological and Biochemical Characters in Albizia lebbek as Bio-indicators of Heavy Metal Toxicity, J. Environ Biol., 20, 93-98, 1999.
• [80] V.K. Kashin, Physiological Role of Nickel in Living Organisms, Mikroelem. Sib., 6, 78-87, 1968.
• [81] V.G. Lapa, , G.M. Prilutskii, , M.Z. Skuratovskaya ve N.K. Tribel, Effect of Trace Elements Copper, Zinc, Nickel and Cobalt on Biosythesis in Potatoes and Harvest Qualities of Tubers, Nauch. Tr. Zhitomir. Sel’skokhoz. Inst., 16, 120-123, 1969.
• [82] G.E. Bartley ve P.A. Scolnık, Plant Carotenoids: Pigments for Photoprotection, Visual Attraction and Human Health, The Plant Cell, 7, 1027-1038, 1995.
• [83] D. Mishra ve B. Samal, Interaction of Benezimidazole and Nickel in Delaying the Senescence of Detached Rice Leaves, Z. Naturforsch, 26, 1377-1380, 1971.
• [84] J.M. Palma, L.M. Sandalino, F.J. Corpas, M.C. Romero-Puertas, I. McCarthy ve L.A. Del Rio, Plant Proteases, Protein Degradation and Oxidative Stress: Role of Peroxisomes, Plant Physiol. Biochem., 40, 521-530, 2002.
• [85] S. Sagner, R. Kneer, G. Wanner, J.P. Cosson, B. Deus-Neumann ve M.H. Zenk, Hyperaccumulation, Complexation and Distribution of Nickel in Sebertia acuminate, Phytochemistry, 47, 339-347, 1998.
• [86] R.R. Brooks, S. Shaw ve A.A. MARFIL, The Chemical Form and Physiological Function of Nickel in Some Iberian Alyssum species, Physiol. Plant., 51, 167-170, 1981.
• [87] S. Hayat, B. Ali, H.S. Aiman ve A. Ahmad, Brassinosteroids enhanced antioxidants under cadmium stress in Brassica juncea, Environ. Exp. Bot., 60, 33-41, 2007.
• [88] D.A. Priestley, Seed Aging, Cornell University Press, London, 1986.
• [89] T. Gaspar, C. Penel, D. Hagege ve H. Greppin, Peroxidases in Plant Growth, Differentiation, and Development Processes, In: Łobarzewski, J., Greppin, H., Penel, C., Gaspar, T. (ed.), Biochemical, Molecular and Physiological Aspects of Plant Peroxidases, Pp. 249-280, University M. Curie-Skłodowska, Lublin, 1991.
• [90] A. Riquelme ve L. Cardemil, Peroxidases in the Cell Walls of Seed , Seedlings of Araucaria araucana, Phytochemistry, 32, 15-20, 1993.
• [91] R.J. Bruce ve C.A. West, Elicitation of Lignin Biosynthesis, Isoperoxidase Activity by Pectic Fragments in Suspension Culture of Castor Bean, Plant Physiol., 91, 889-897, 1989.
• [92] D.F. Cippolini, Jr., The Induction of Soluble Peroxidase Activity in Bean Leaves by Wind-Induced Mechanical Perturbation, American Journal of Botany, 85, 1586-1591, 1998.
• [93] J. Diaz, A. Bernal, F. Pomar ve F. Merino, Induction of Shikimate Dehydrogenase and Peroxidase in Pepper (Capsicum annuum L.) Seedlings in Response to Copper Stress and its Relation to Lignification, Plant Sci., 161, 179-188, 2001.
• [94] R.K. Tewari, P. Kumar, P.N. Sharma, S.S. Bisht, Modulation of oxidative stress responsive enzymes by excess cobalt, Plant Sci., 162, 381-388, 2002.
• [95] R. Gabbrielli, , T. Pandolfini, , L. Espen, ve M.R. Palandri, Growth, Peroxidase Activity and Cytological Modifications in Pisum sativum Seedlings Exposed to Ni2+ Toxicity, J. Plant Physiol., 155, 639-645, 1999.
• [96] Y. Ekmekçi ve S. Terzioğlu, Effects of Oxidative Stress Induced by Paraquat on Wild Cultivated Wheats, Pesticide Biochemistry Physiology, 83, 69-81, 2005.
• [97] C.A. Placer, L.L. Cushman ve B.C. Johnson, Estimation of Product of Lipid Peroxidation (Malondy Dialdehyde) in Biochemical Systems, Anal. Biochem., 16, 259-264, 1990.
• [98] U. Mercan, Toksikolojide Serbest Radikallerin Önemi, YYU Vet. Fak. Derg., 15(1-2), 91-96, 2004.
• [99] J.E.J. Weckx ve H.M.M. Clijsters, Zn Phytotoxicity Induces Oxidative Stress in Primary Leaves of Phaseolus vulgaris, Plant Physiol. Biochem., 35(5), 405-410, 1997.
• [100] N. Candan ve L. Tarhan, Changes in Chlorophyll-carotenoid Contents, Antioxidant Enzyme Activities and Lipid Peroxidation Levels in Zn-stressed Mentha pulegium, Turk J. Chem., 27, 21-30, 2003.
• [101] K.V. Madhava Rao ve T.V. Sresty, Antioxidative Parameters in the Seedlings of Pigeonpea (Cajanus cajan L. Millspaugh) in Response to Zn and Ni Stresses, Plant Sci., 157, 113-128, 2000.
• [102] I. Nouairi, W.B. Ammar, N.B. Youssef, D.D.B. MILED, M.H. Ghorbal ve M. Zarrouk, Antioxidant Defense System in Leaves of Indian Mustard (Brassica juncea), Rape (Brassica napus) under Cadmium Stress, Acta Physiol Plant, 31, 237-247, 2009. [103] M. Tester, ve R.A. Leigh, Partitioning of Nutrient Transport Processes in Roots, J. Exp. Bot., 52, 445-457, 2001.
• [104] S. Verma ve R.S. Dubey, Lead Toxicity Induces Lipid Peroxidation and Alters the Activities of Antioxidant Enzymes in Growing Rice Plants, Plant Sci., 164, 645-655, 2003.
• [105] E.O. Uthus ve R.A. Poellot, Dietary Folate Affects the Response of Rats to Nickel Deprivation, Biol. Trace Elem. Res., 52, 23, 1996.
• [106] D.G. Barceloux, Nickel, Clin. Toxicol., 37, 239, 1999.
• [107] G.D. Clayton ve F.E. Clayton, Patty’s Industrial Hygiene Toxicology, 4th ed.; A Wiley-Interscience Publication: New York, pp 2157-2173, 1994.
• [108] P.H. Collery, A.J. Corbell, J.L. Domingo, J.C. Etienne, J. Uobet, Metal Ions in Biology and Medicine, vol 4; John Libbey Eurotext: Paris, pp 172-174, 1996.
• [109] W.H.O., World Health Organization, Quality directive of potable water, WHO 2nd ed.,197, 1994.