Abstract
The focus of the review is on the specific aspects of nickel effect on plants as compared to other heavy metals; their specificity is derived from different physical and chemical properties. The various facets of the physiological role of nickel and its toxic activity in higher plants, its intracellular partition and transport in plant tissues and organ are discussed. The putative mechanisms of nickel hyperaccumulation are considered in several representatives of angiosperm plant families. The existing evidence was used to outline the metabolic changes in plants affected by nickel. The comparison with other heavy metals is used to disclose the general mechanisms that disturb plant mineral nutrition, water regime, photosynthesis, and morphogenesis as well as the common cell responses aimed at detoxification of heavy metals. The numerous nonspecific effects of heavy metals depend on their direct and indirect action; in addition, some effects of nickel are specific. To illustrate, high Ni content in endoderm and pericycle cells blocks cell divisions in the pericycle and results in the inhibition of root branching.
Similar content being viewed by others
References
Metal Ions in Biological Systems, Concepts on Metal Ion Toxicity, vol. 20, Singel, H. and Singel, A., Eds., New York: Marcel Dekker, 1986.
Eskew, D.L., Welch, R.M., and Cary, E.E., Nickel: An Essential Micronutrient for Legumes and Possibly All Higher Plants, Science, 1983, vol. 222, pp. 621–623.
Andreeva, I.V., Govorina, V.V., Vinogradova, S.B., and Yagodin, B.A., Nickel in Plants, Agrokhimiya, 2001, no. 3, pp. 82–94.
Brown, P.H., Welch, R.M., and Cary, E.E., Nickel: A Micronutrient Essential for Higher Plants, Plant Physiol., 1987, vol. 85, pp. 801–803.
Dixon, N.E., Gazzola, C., Blakeley, R.L., and Zemer, B., Jack-Bean Urease (EC 3.5.1.5.3). A Metalloenzyme. A Simple Biological Role for Nickel, J. Am. Chem. Soc., 1975, vol. 97, pp. 4131–4133.
Fishbein, W.N., Smith, M.J., Nagarajan, K., and Scurzi, W., The First Natural Nickel Metalloenzyme: Urease, Fed. Proc. Am. Soc. Exp. Biol., 1976, vol. 35, p. 1680.
Polacco, J.C., Freyermuth, S.K., Gerendas, J., and Cinzio, S., Soybean Genes Involved in Nickel Insertion into Urease, J. Exp. Bot., 1999, vol. 50, pp. 1149–1156.
Sirko, A. and Brodzik, R., Plant Ureases: Roles and Regulation, Acta Biochim. Pol., 2000, vol. 47, pp. 1189–1195.
Welch, R.M., The Biological Significance of Nickel, J. Plant Nutr., 1981, vol. 3, pp. 345–356.
Walker, C.D., Graham, R.D., Madison, J.T., Cary, E.E., and Welch, R.M., Effects of Ni Deficiency on Some Nitrogen Metabolites in Cowpeas (Vigna unguiculata L. Walp.), Plant Physiol., 1985, vol. 79, pp. 474–479.
Zonia, L.E., Stebbins, N.E., and Polacco, J.C., Essential Role of Urease in Germination of Nitrogen-Limited Arabidopsis thaliana Seeds, Plant Physiol., 1995, vol. 107, pp. 1097–1103.
Gerendas, J. and Sattelmacher, B., Significance of Ni Supply for Growth, Urease Activity and the Concentrations of Urea, A mino Acids and Mineral Nutrients of Urea-Grown Plants, Plant Soil, 1997, vol. 190, pp. 153–162.
Gerendas, J. and Sattelmacher, B., Influence of Ni Supply on Growth and Nitrogen Metabolism of Brassica napus L. Grown with NH4NO3 or Urea as N Source, Ann. Bot., 1999, vol. 83, pp. 65–71.
Hirai, M., Kawai-Hirai, R., Hirai, T., and Ueki, T., Structural Change of Jack Bean Urease Induced by Addition of Surfactants Studied with Synchrotron-Radiation Small-Angle X-Ray Scattering, Eur. J. Biochem., 1993, vol. 215, pp. 55–61.
Takishima, K., Suga, T., and Mamiya, G., The Structure of Jack Bean Urease. The Complete Amino Acid Sequence, Limited Proteolysis and Reactive Cysteine Residues, Eur. J. Biochem., 1988, vol. 175, pp. 151–165.
Winkler, R.G., Polacco, J.C., Eskew, D.L., and Welch, R.M., Nickel Is Not Required for Apourease Synthesis in Soybean Seeds, Plant Physiol., 1983, vol. 72, pp. 262–263.
Dalton, D.A., Evans, H.J., and Hanus, F.J., Stimulation by Nickel of Soil Microbial Urease Activity and Urease and Hydrogenase Activities in Soybeans Grown in a Low-Nickel Soil, Plant Soil, 1985, vol. 88, pp. 245–258.
Gerendas, J. and Sattelmacher, B., Significance of N Source (Urea vs. NH4NO3) and Ni Supply for Growth, Urease Activity and Nitrogen Metabolism of Zucchini (Cucurbita pepo convar. giromontiina), Plant Soil, 1997, vol. 196, pp. 217–222.
Krogmeier, M.J., McCarty, G.W., and Bremner, J.M., Phytotoxicity of Foliar-Applied Urea, Proc. Natl. Acad. Sci. USA, 1989, vol. 86, pp. 8189–8191.
Eskew, D.L., Welch, R.M., and Norvell, W.A., Nickel in Higher Plants: Further Evidence for an Essential Role, Plant Physiol., 1984, vol. 76, pp. 691–693.
Das, P.K., Kar, M., and Mishra, D., Nickel Nutrition of Plants: Effect of Nickel on Some Oxidase Activities during Rice (Oryza sativa L.) Seed Germination, Z. Pflanzenphysiol., 1978, vol. 90, pp. 225–233.
Orlov, D.S., Sadovnikova, L.K., and Lozanovskaya, I.N., Ekologiya i okhrana biosfery pri khimicheskom zagryaznenii (Ecology and Protection of Biosphere under Chemical Pollution), Moscow: Vysshaya Shkola, 2002.
Emsley, J., The Elements, Oxford: Clarendon, 1991.
Aschmann, S.G. and Zasoski, R.J., Nickel and Rubidium Uptake by Whole Oat Plants in Solution Culture, Physiol. Plant., 1987, vol. 71, pp. 191–196.
Temp, G.A., Nickel in Plants and Its Toxicity, Ustoichivost’ k tyazhelym metallam dikorastushchikh vidov (Resistance of Wild Species to Heavy Metals), Alekseeva-Popova, N.V. Ed., Leningrad: Lenuprizdat, 1991, pp. 139–146.
Sajwan, K.S., Ornes, W.H., Youngblood, T.V., and Alva, A.K., Uptake of Soil Applied Cadmium, Nickel and Selenium by Bush Beans, Water, Air, Soil Pollut., 1996, vol. 91, pp. 209–217.
Merkusheva, M.G., Ubugunov, V.L., and Lavrent’eva, I.N., Heavy Metals in Soil and Phytomass of Pastures in the West Transbaikal Region, Agrokhimiya, 2001, no. 8, pp. 63–72.
Kukier, U., Peters, C.A., Chaney, R.L., Angle, J.S., and Roseberg, R.J., The Effect of pH on Metal Accumulation in Two Alyssum Species, J. Environ. Qual., 2004, vol. 33, pp. 2090–2102.
Taylor, G.J. and Crowder, A.A., Uptake and Accumulation of Copper, Nickel, and Iron by Typha latifolia Grown in Solution Culture, Can. J. Bot., 1983, vol. 61, pp. 1825–1830.
Boyd, R.S. and Martens, S.N., Nickel Hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): A Constitutive Trait, Am. J. Bot., 1998, vol. 85, pp. 259–265.
Gabbrielli, R. and Pandolfini, T., Effect of Mg2+ and Ca2+ on the Response to Nickel Toxicity in a Serpentine Endemic and Nickel-Accumulating Species, Physiol. Plant., 1984, vol. 62, pp. 540–544.
Ehlken, S. and Kirchner, G., Environmental Processes Affecting Plant Root Uptake of Radioactive Trace Elements and Variability of Transfer Factor Data: A Review, J. Environ. Rad., 2002, vol. 58, pp. 97–112.
Kochian, L.V., Molecular Physiology of Mineral Nutrient Acquisition, Transport, and Utilization, Biochemistry and Molecular Biology of Plants, Buchanan, B.B., Gruissem, W., and Jones, R.L., Eds., Rockville, 2000, pp. 1204–1249.
Guerinot, M.L., Molecular Mechanisms of Ion Transport in Plant Cells, Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment, Raskin, I. and Ensley, B.D., Eds., New York: John Wiley and Sons, 2000, pp. 271–285.
Li, L., Tutone, A.F., Drummond, R.S.M., Gardner, R.C., and Luan, S., A Novel Family of Magnesium Transport Genes in Arabidopsis, Plant Cell, 2001, vol. 13, pp. 2761–2775.
Seregin, I.V. and Ivanov, V.B., Physiological Aspects of Cadmium and Lead Toxic Effects on Higher Plants, Fiziol. Rast. (Moscow), 2001, vol. 48, pp. 606–630 (Russ. J. Plant Physiol., Engl. Transl., pp. 523–544).
Baker, A.J.M., Accumulators and Excluders-Strategies in Response of Plants to Heavy Metals, J. Plant Nutr., 1981, vol. 3, pp. 643–654.
Antosiewicz, D.M., Adaptation of Plants to an Environment Polluted with Heavy Metals, Byul. Izobr., 1992, vol. 61, pp. 281–299.
Brooks, R.R., Wither, E.D., and Zepemick, B., Cobalt and Nickel in Rinorea Species, Plant Soil, 1977, vol. 47, pp. 707–712.
Phytoremediation of Toxic Metals Using Plants to Clean up the Environment, Raskin, I. and Ensley, B.D., Eds., New York: J. Wiley and Sons, 2000.
Reeves, R.D., Baker, A.J.M., Bornidi, A., and Berazain, R., Nickel Hyperaccumulation in the Serpentine Flora of Cuba, Ann. Bot., 1999, vol. 83, pp. 29–38.
Brooks, R.R., Plants That Hyperaccumulate Heavy Metals (Their Role in Phytoremediation, Microbiology, Archaeology, Mineral Exploration and Phytomining), Wallingford: CAB, 1998.
Davis, M.A., Pritchard, S.G., Boyd, R.S., and Prior, S.A., Developmental and Induced Responses of Nickel-Based and Organic Defenses of the Nickel-Hyperaccumulating Shrub, Psychotria douarrei, New Phytol., 2001, vol. 150, pp. 49–58.
Severne, B.C., Nickel Accumulation by Hybanthus floribundus, Nature, 1974, vol. 248, pp. 807–808.
Sagner, S., Kneer, R., Wanner, G., Cosson, J.-P., Deus-Neumann, B., and Zenk, M.H., Hyperaccumulation, Complexation and Distribution of Nickel in Sebertia acuminata, Phytochemistry, 1998, vol. 47, pp. 339–343.
Davis, M.A. and Boyd, R.S., Dynamics of Ni-Based Defense and Organic Defenses in the Ni Hyperaccumulator, Streptanthus polygaloides (Brassicaceae), New Phytol., 2000, vol. 146, pp. 211–217.
Boyd, R.S., Shaw, J.J., and Martens, S.N., Nickel Hyperaccumulation Defends Streptanthus polygaloides (Brassicaceae) against Pathogens, Am. J. Bot., 1994, vol. 81, pp. 294–300.
Yang, X.E., Baligar, V.C., Foster, J.C., and Martens, D.C., Accumulation and Transport of Nickel in Relation to Organic Acids in Ryegrass and Maize Grown with Different Nickel Levels, Plant Soil, 1997, vol. 196, pp. 271–276.
Seregin, I.V., Kozhevnikova, A.D., Kazyumina, E.M., and Ivanov, V.B., Nickel Toxicity and Distribution in Maize Roots, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 793–800 (Russ. J. Plant Physiol., Engl. Transl., pp. 711–718).
Kramer, U., Cotter-Howells, J.D., Charnock, J.M., Baker, A.J.M., and Smith, A.C., Free Histidine as a Metal Chelator in Plants That Accumulate Nickel, Lett. Nature, 1996, vol. 379, pp. 635–638.
Kramer, U., Smith, R.D., Wenzel, W.W., Raskin, I., and Salt, D.E., The Role of Metal Transport and Tolerance in Nickel Hyperaccumulation by Thlaspi goesingense Halacsy, Plant Physiol., 1997, vol. 115, pp. 1641–1650.
Andreeva, I.V., Govorina, V.V., Yagodin, B.A., and Dosimova, O.T., Dynamics of Nickel Accumulation and Distribution in Oat Plants, Agrokhimiya, 2000, no. 4, pp. 68–71.
Ewais, E.A., Effects of Cadmium, Nickel and Lead on Growth, Chlorophyll Content and Proteins of Weeds, Biol. Plant., 1997, vol. 39, pp. 403–410.
Sresty, T.V.S. and Madhava Rao, K.V., Ultrastructural Alterations in Response to Zinc and Nickel Stress in the Root Cells of Pigeonpea, Environ. Exp. Bot., 1999, vol. 41, pp. 3–13.
Stanković, Z., Pajević, S., Vučković, M., and Stojanović, S., Concentrations of Trace Metals in Dominant Aquatic Plants of the Lake Provala (Vojvodina, Yugoslavia), Biol. Plant., 2000, vol. 43, pp. 583–585.
Rubio, M.I., Escrig, I., Martinez-Cortina, C., Lopez-Benet, F.J., and Sanz, A., Cadmium and Nickel Accumulation in Rice Plants. Effects on Mineral Nutrition and Possible Interactions of Abscisic and Gibberellic Acids, Plant Growth Regul., 1994, vol. 14, pp. 151–157.
Reeves, R.D., Brooks, R.R., and Macfarlane, R.M., Nickel Uptake by Californian Streptanthus and Caulanthus with Particular Reference to the Hyperaccumulator S. polygaloides Gray (Brassicaceae), Am. J. Bot., 1981, vol. 68, pp. 708–712.
Kovacević, G., Kastori, R., and Merkulov, L.J., Dry Matter and Leaf Structure in Young Wheat Plants as Affected by Cadmium, Lead, and Nickel, Biol. Plant., 1999, vol. 42, pp. 119–123.
Taylor, G.J. and Crowder, A.A., Copper and Nickel Tolerance in Typha latifolia Clones from Contaminated and Uncontaminated Environments, Can. J. Bot., 1984, vol. 62, pp. 1304–1308.
Heath, S.M., Southworth, D., and D’Allura, J.A., Localization of Nickel in Epidermal Subsidiary Cells of Leaves of Thlaspi montanum var siskiyouense (Brassicaceae) Using Energy-Dispersive X-Ray Microanalysis, Int. J. Plant Sci., 1997, vol. 158, pp. 184–188.
Kupper, H., Lombi, E., Zhao, F.J., Wieshammer, G., and McGrath, S.P., Cellular Compartmentation of Nickel in the Hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense, J. Exp. Bot., 2001, vol. 52, pp. 2291–3000.
Nabais, C., Freitas, H., Hagemeyer, J., and Breckle, S.-W., Radial Distribution of Ni in Stem wood of Quercus ilex L. Trees Grown on Serpentine and Sandy Loam (Umbric Leptosol) Soils of NE-Portugal, Plant Soil, 1996, vol. 183, pp. 181–185.
Psaras, G.K. and Manetas, Y., Nickel Localization in Seeds of the Metal Hyperaccumulator Thlaspi pindicum Hausskn., Ann. Bot., 2001, vol. 88, pp. 513–516.
Broadhurst, C.L., Chaney, R.L., Angle, J.S., Maugel, T.K., Erbe, E.F., and Murphy, C.A., Simultaneous Hyperaccumulation of Nickel, Manganese, and Calcium in Alysum Leaf Trichomes, Environ. Sci. Technol., 2004, vol. 38, pp. 5797–5802.
Liu, D. and Kottke, I., Subcellular Localization of Chromium and Nickel in Root Cells of Allium cepa by EELS and ESI, Cell Biol. Toxicol., 2003, vol. 19, pp. 299–311.
Cataldo, D.A., McFadden, K.M., Garland, T.R., and Wildung, R.E., Organic Constituents and Complexation of Nickel (II), Iron (III), Cadmium (II) and Plutonium (IV) in Soybean Xylem Exudates, Plant Physiol., 1988, vol. 86, pp. 734–739.
Zeller, S. and Feller, U., Redistribution of Cobalt and Nickel in Detached Wheat Shoots: Effects of Steam-Girdling and of Cobalt and Nickel Supply, Biol. Plant., 1998, vol. 41, pp. 427–434.
Lee, J., Reeves, R.D., Brooks, R.R., and Jaffre, T., Isolation and Identification of a Citrate-Complex of Nickel from Nickel-Accumulating Plants, Phytochemistry, 1977, vol. 16, pp. 1503–1505.
Kersten, W.J., Brooks, R.R., Reeves, R.D., and Jaffre, T., Nature of Nickel Complexes in Psychotria douarrei and Other Nickel-Accumulating Plants, Phytochemistry, 1980, vol. 19, pp. 1963–1965.
Homer, F.A., Reeves, R.D., Brooks, R.R., and Baker, A.J.M., Characterization of the Nickel-Rich Extract from the Nickel Hyperaccumulator Dichapetalum gelonioides, Phytochemistry, 1991, vol. 30, pp. 2141–2145.
Persans, M.W., Yan, X., Patnoe, J.M., Kramer, U., and Salt, D.E., Molecular Dissection of the Role of Histidine in Nickel Hyperaccumulation in Thlaspi goesingense (Halacsy), Plant Physiol., 1999, vol. 121, pp. 1117–1126.
Kerkeb, L. and Kramer, U., The Role of Free Histidine in Xylem Loading of Nickel in Alyssum lesbiacum and Brassica juncea, Plant Physiol., 2003, vol. 131, pp. 716–724.
Brooks, R.R., Shaw, S., and Marfil, A.A., The Chemical Form and Physiological Function of Nickel in Some Iberian Alyssum Species, Physiol. Plant., 1981, vol. 51, pp. 167–170.
Kramer, U., Pickering, I.J., Prince, R.C., Raskin, I., and Salt, D.E., Subcellular Localization and Speciation of Nickel in Hyperaccumulator and Non-Accumulator Thlaspi Species, Plant Physiol., 2000, vol. 122, pp. 1343–1353.
Rudakova, E.V., Karakis, K.D., and Sidorshina, E.I., The Role of Plant Cell Walls in Absorption and Accumulation of Metal Ions, Fiziol. Biokh. Kul’t. Rast., 1988, vol. 20, pp. 3–12.
Merce, A.L.R., Landaluze, J.S., Mangrich, A.S., Szpoganicz, B., and Sierakowski, M.R., Complexes of Arabinogalactan of Pereskia aculeate and Co2+, Cu2+, Mn2+, and Ni2+, Biores. Technol., 2001, vol. 76, pp. 29–37.
Persans, M.W., Nieman, K., and Salt, D.E., Functional Activity and Role of Cation-Efflux Family Members in Ni Hyperaccumulation in Thlaspi goesingense, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 9995–10000.
Salt, D.E. and Wagner, G.J., Cadmium Transport across Tonoplast of Vesicles from Oat Roots. Evidence for a Cd2+/H+ Antiport Activity, J. Biol. Chem., 1993, vol. 268, pp. 12297–12302.
Gries, G.E. and Wagner, G.J., Association of Nickel versus Transport of Cadmium and Calcium in Tonoplast Vesicles of Oat Roots, Planta, 1998, vol. 204, pp. 390–396.
Chardonnens, A.N., van de Laar, T., Koevoets, P.L.M., Kuijper, L.D.J., and Verkleij, J.A.C., Some Notes on Vacuolar Compartmentalization of Cadmium Tolerance in Silene vulgaris, The Role of Vacuolar Compartmentalization in the Mechanism of Naturally Selected Zinc and Cadmium Tolerance, Chardonnens, A.N., Ed., Amsterdam: Vrije Univ., 1999, pp. 31–41.
Ingle, R.A., Fricker, M.D., and Smith, J.A.C., Evidence for Ni-Proton Antiport Activity at the Vacuolar Membrane of the Hyperaccumulator Alyssum lesbiacum, Proc. 9th New Phytol. Symp. Heavy Metals and Plants from Ecosystems to Biomolecules, Philadelphia: Univ. Philadelphia, 2002, p. 31.
Van Assche, F. and Glijsters, H., Effects of Metals on Enzyme Activity in Plants, Plant, Cell Environ., 1990, vol. 13, pp. 195–206.
Kositsin, A.V., Interaction of Metals and Enzymes, Ustoichivost’ k tyazhelym metallam dikorastushchikh vidov (Resistance of Wild Species to Heavy Metals), Alekseeva-Popova, N.V., Ed., Leningrad: Lenuprizdat, 1991, pp. 15–22.
Sheoran, I.S., Singal, H.R., and Singh, R., Effect of Cadmium and Nickel on Photosynthesis and the Enzymes of the Photosynthetic Carbon Reduction Cycle in Pigeonpea (Cajanus cajan L.), Photosynth. Res., 1990, vol. 23, pp. 345–351.
Kevresan, S., Petrović, N., Popović, M., and Kandrac, J., Effect of Heavy Metals on Nitrate and Protein Metabolism in Sugar Beet, Biol. Plant., 1998, vol. 41, pp. 235–240.
Ros, R., Cooke, D.T., Burden, R.S., and James, C.S., Effects of the Herbicide MCPA, and the Heavy Metals, Cadmium and Nickel on the Lipid Composition, Mg2+-ATPase Activity and Fluidity of Plasma Membranes from Rice, Oryza sativa (cv. Bahia) Shoots, J. Exp. Bot., 1990, vol. 41, pp. 457–462.
El-Shintinawy, F., El-Ansary, A., Differential Effect of Cd2+ and Ni2+ on Amino Acid Metabolism in Soybean Seedlings, Biol. Plant., 2000, vol. 43, pp. 79–84.
Schickler, H. and Caspi, H., Response of Antioxidative Enzymes to Nickel and Cadmium Stress in Hyperaccumulator Plants of Genus, Alyssum, Physiol. Plant., 1999, vol. 105, pp. 39–44.
Pandolfini, T., Gabbrielli, R., and Comparini, C., Nickel Toxicity and Peroxidase Activity in Seedlings of Triticum aestivum L., Plant Cell Environ., 1992, vol. 15, pp. 719–725.
Ivanov, V.B., Bystrova, E.I., and Seregin, I.V., Comparative Impacts of Heavy Metals on Root Growth as Related to Their Specificity and Selectivity, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 445–454 (Russ. J. Plant Physiol., Engl. Transl., pp. 398–406).
Ros, R., Morales, A., Segura, J., and Picazo, I., In Vivo and In Vitro Effects of Nickel and Cadmium on the Plasmalemma ATPase from Rice (Oryza sativa L.) Shoots and Roots, Plant Sci., 1992, vol. 83, pp. 1–6.
Piccini, D.F. and Malavolta, E., Effect of Nickel on Two Common Bean Cultivars, J. Plant Nutr., 1992, vol. 15, pp. 2343–2350.
Khalid, B.Y. and Tinsley, J., Some Effects of Nickel Toxicity on Rye Grass, Plant Soil, 1980, vol. 55, pp. 139–144.
Barsukova, V.S. and Gamzikova, O.I., Effects of Nickel Surplus on the Element Content in Wheat Varieties Contrasting in Ni Resistance, Agrokhimiya, 1999, no. 1, pp. 80–85.
Bishnoi, N.R., Sheoran, I.S., and Singh, R., Influence of Cadmium and Nickel on Photosynthesis and Water Relations in Wheat Leaves of Different Insertion Level, Photosynthetica, 1993, vol. 28, pp. 473–479.
Molas, J., 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, 1997, vol. 34, pp. 513–522.
Breckle, S.-W., Growth under Stress: Heavy Metals, Plant Roots: The Hidden Half, Waisel, Y., Eshel, A., and Kafkafi, U., Eds., New York: Marcel Dekker, 1991, pp. 351–373.
Veeranjaneyulu, K. and Das, V.S.R., Intrachloroplast Localization of 65Zn and 63Ni in a Zn-Tolerant Plant, Ocimum basilicum Benth, J. Exp. Bot., 1982, vol. 33, pp. 1161–1165.
Mohanty, N., Vaas, I., and Demeter, S., Impairment of Photosystem 2 Activity at the Level of Secondary Quinone Electron Acceptor in Chloroplasts Treated with Cobalt, Nickel and Zinc Ions, Physiol. Plant., 1989, vol. 76, pp. 386–390.
Krupa, Z. and Baszynski, T., Some Aspects of Heavy Metals Toxicity towards Photosynthetic Apparatus — Direct and Indirect Effects on Light and Dark Reactions, Acta Physiol. Plant., 1995, vol. 17, pp. 177–190.
Maksymiec, W., Effect of Copper on Cellular Processes in Higher Plants, Photosynthetica, 1997, vol. 34, pp. 321–342.
Malkin, R. and Niyogi, K., Photosynthesis, Biochemistry and Molecular Biology of Plants, Buchanan, B.B., Gruissem, W., and Jones, R.L., Eds., Rockville, 2000, pp. 568–628.
Taylor, R.W. and Allinson, D.W., Influence of Lead, Cadmium, and Nickel on the Growth of Medicago sativa (L.), Plant Soil, 1981, vol. 60, pp. 223–236.
Wong, M.H. and Bradshaw, A.D., A Comparison of the Toxicity of Heavy Metals, Using Root Elongation of Rye Grass, Lolium perrene, New Phytol., 1982, vol. 91, pp. 255–261.
Wang, W., Root Elongation Method for Toxicity Testing of Organic and Inorganic Pollutants, Environ. Toxicol. Chem., 1987, vol. 6, pp. 409–414.
Samantaray, S., Rout, G.R., and Das, P., Tolerance of Rice to Nickel in Nutrient Solution, Biol. Plant., 1997, vol. 40, pp. 295–298.
Neiboer, E. and Richardson, D.H.S., The Replacement of the Non-Descriptive Term “Heavy Metals” by a Biologically and Chemically Significant Classification of Metal Ions, Environ. Pollut., 1980, vol. 1, pp. 3–26.
Karataglis, S.S., McNeilly, T., and Bradshaw, A.D., Lead and Zink Tolerance of Agrostis capillaris L. and Festuca rubra L. across a Mine Pasture Boundary at Minera, North Wales, Phyton, 1986, vol. 26, pp. 65–72.
Ivanov, V.B., Root Growth Responses to Chemicals, Sov. Sci. Rev. Ser. D, 1994, pp. 1–70.
Seregin, I.V. and Ivanov, V.B., Is the Endodermal Barrier the Only Factor Preventing the Inhibition of Root Branching by Heavy Metal Salts? Fiziol. Rast. (Moscow), 1997, vol. 44, pp. 922–925 (Russ. J. Plant Physiol., Engl. Transl., pp. 797–800).
Seregin, I.V. and Ivanov, V.B., The Transport of Cadmium and Lead Ions through Root Tissues, Fiziol. Rast. (Moscow), 1998, vol. 45, pp. 899–905 (Russ. J. Plant Physiol., Engl. Transl., pp. 780–785).
Seregin, I.V. and Kozhevnikova, A.D., Distribution of Cadmium, Lead, Nickel, and Strontium in Imbibing Maize Caryopses, Fiziol. Rast. (Moscow), 2005, vol. 52, pp. 635–640 (Russ. J. Plant Physiol., Engl. Transl., pp. 565–569).
Robertson, A.I. and Meakin, M.E.R., The Effect of Nickel on Cell Division and Growth of Brachystegia spiciformis Seedlings, J. Bot. Zimbabwe, 1980, vol. 12, pp. 115–125.
L’Huillier, L., d’Auzac, J., Durand, M., and Michaud-Ferriere, N., Nickel Effects on Two Maize (Zea mays) Cultivars: Growth, Structure, Ni Concentration, and Localization, Can. J. Bot., 1996, vol. 74, pp. 1547–1554.
Knasmuller, S., Gottmann, E., Steinkellner, H., Fomin, A., Pickl, C., Paschke, A., God, R., and Kundi, M., Detection of Genotoxic Effects of Heavy Metal Contaminated Soils with Plant Bioassays, Mutat. Res., 1998, vol. 420, pp. 37–48.
Amosova, N.V., Tazina, I.A., and Synzynys, B.I., Effect of Phytotoxicity and Genotoxicity of Iron, Cobalt, and Nickel Ions on Physiological Parameters in plants of Different Species, S.-kh. Biol., 2003, no. 5, pp. 49–54.
Demchenko, N.P., Kalimova, I.B., and Demchenko, K.N., Effect of Nickel on Growth, proliferation, and Differentiation of Root Cells in Triticum aestivum Seedlings, Fiziol. Rast. (Moscow), 2005, vol. 52, pp. 250–258 (Russ. J. Plant Physiol., Engl. Transl., pp. 220–228).
Liu, D., Jiang, W., Wang, W., and Zhai, L., Evaluation of Metal Ion Toxicity on Root Tip Cells by the Allium Test, Israel J. Plant Sci., 1995, vol. 43, pp. 125–133.
Rauser, W.E., Phytochelatins and Related Peptides: Structure, Biosynthesis and Function, Plant Physiol., 1995, vol. 109, pp. 1141–1149.
Zenk, M.H., Heavy Metal Detoxification in Higher Plants — a Review, Gene, 1996, vol. 179, pp. 21–30.
Ernst, W.H.O., Effects of Heavy Metals in Plants at the Cellular and Organismic Level, Ecotoxicology. Ecological Fundamentals, Chemical Exposure and Biological Effects, Schuurmann, G. and Markert, B., Eds., Heidelberg: Wiley, 1998, pp. 587–620.
Cobbett, C.S., Phytochelatins and Their Roles in Heavy Metal Detoxification, Plant Physiol., 2000, vol. 123, pp. 825–832.
Seregin, I.V., Phytochelatins and Their Role in Cadmium Detoxification in Higher Plants (A Review), Usp. Biol. Khim., 2001, vol. 41, pp. 283–300.
Hall, J.L., Cellular Mechanisms for Heavy Metal Detoxification and Tolerance, J. Exp. Bot., 2002, vol. 53, pp. 1–11.
Schat, H., Llugany, M., Vooijs, R., Hartley-Whitaker, J., and Bleeker, P.M., The Role of Phytochelatins in Constitutive and Adaptive Heavy Metal Tolerances in Hyperaccumulator and Non-Hyperaccumulator Metallophytes, J. Exp. Bot., 2002, vol. 53, pp. 2381–2392.
Robinson, N.J., Tommey, A.M., Kuske, C., and Jackson, P.J., Plant Metallothioneins, Biochem. J., 1993, vol. 295, pp. 1–10.
Zhou, J. and Goldsbrough, P.B., Structure, Organization and Expression of the Metallothionein Gene Family in Arabidopsis, Mol. Gen. Genet., 1995, vol. 248, pp. 318–328.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © I.V. Seregin, A.D. Kozhevnikova, 2006, published in Fiziologiya Rastenii, 2006, Vol. 53, No. 2, pp. 285–308.
Rights and permissions
About this article
Cite this article
Seregin, I.V., Kozhevnikova, A.D. Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53, 257–277 (2006). https://doi.org/10.1134/S1021443706020178
Received:
Issue Date:
DOI: https://doi.org/10.1134/S1021443706020178