Mechanisms of Heavy Metal Toxicity in Plants



Pollution of the environment with the toxic heavy metals has become one of the major causes for worry for human health in both emerging and advanced countries. Metal contamination issues are becoming more and more common in India and elsewhere, with many documented cases of metal toxicity in mining industries, foundries, smelters, coal-burning power plants, and agriculture. As land application becomes one of the foremost waste utilization and disposal practices, soil is increasingly being seen as a major source of metal(loid)s reaching food chain, largely through plant uptake and animal transfer. Heavy metal buildup in soils is of concern in agricultural production due to the adverse effects on food safety and marketability, crop growth due to phytotoxicity, and environmental health of soil organisms. Metal toxicity has high impact and relevance to plants, and consequently, it affects the ecosystem, where the plants form an integral component. A few metals, including copper, manganese, iron, cobalt, zinc, and chromium, are, however, essential to plant metabolism in trace quantities. It is only when metals are present in bioavailable forms and at excessive levels; they have the potential to turn out to be toxic to plants through formation of complex compounds within the cell. Plants growing in metal-contaminated sites exhibit altered metabolism, growth reduction, lower biomass production, and metal accumulation. Various physiological and biochemical processes in plants are affected by metal toxicities. The present-day investigations into toxicity and tolerance in metal-stressed plants are prompted by the growing metal pollution in the environment. This article details the range of heavy metals, toxicity for plants, and mechanisms of plants to cope with metal toxicity.


Heavy Metal Metal Toxicity Heavy Metal Toxicity Nitrate Reductase Activity Heavy Metal Stress 


  1. Aizer RS, Rajagopel CK, Money NS (1975) Available zinc, copper, iron, and manganese status of the acid rice soils of Kuttanad, Kerala State. Agric Res J Kerala 13:15–19Google Scholar
  2. Alcantara E, Romera FJ, Canete M, De La Guardia MD (1994) Effects of heavy metals on both induction and function of root Fe (III) reductase in Fe-deficient cucumber (Cucumis sativus L.) plants. J Exp Bot 45:1893–1898CrossRefGoogle Scholar
  3. Alia Prasad KVSK, Pardha Saradhi P (1995) Effect of zinc on free radical and proline in Brasica juncea and Cajanus cajan. Phytochem 39:45–47CrossRefGoogle Scholar
  4. Ames BA, Shingenaga MK, Park EM (1991) In: Elmsford (ed) Oxidative damage and repair: chemical, biological and medical aspects. Pergamon Press, New York, pp 181–187CrossRefGoogle Scholar
  5. Arduini I, Godbold DL, Onnis A (1995) Influence of copper on root growth and morphology of Pinus pinea L. and Pinus pinaster Ait. seedlings. Tree Physiol 15:411–415PubMedCrossRefGoogle Scholar
  6. Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1338Google Scholar
  7. Aust SD, Marehouse CE, Thomas CE (1985) Role of metals in oxygen radical reactions. J Free Radi Biol Med 1:3–25CrossRefGoogle Scholar
  8. Bachman GR, Miller WB (1995) Iron chelate inducible iron/ manganese toxicity in zonal geranium. J Plant Nutr 18:1917–1929CrossRefGoogle Scholar
  9. Baker WG (1972) Toxicity levels of mercury lead, copper and zinc in tissue culture systems of cauliflowers lettuce potato and carrot. Can J Bot 50:973–976CrossRefGoogle Scholar
  10. Bakkaus E, Gouget B, Gallien JP, Khodja H, Carrot H, Morel JL, Collins R (2005) Concentration and distribution of cobalt in higher plants: the use of micro-PIXE spectroscopy. Nucl Inst Methods B 231:350–356CrossRefGoogle Scholar
  11. Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect on cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Func Plant Biol 30:57–64CrossRefGoogle Scholar
  12. Becker M, Asch F (2005) Iron toxicity in rice-conditions and management concepts. J Plant Nutr Soil Sci 168:558–573CrossRefGoogle Scholar
  13. Bishnoi NR, Chugh LK, Sawhney SK (1993a) Effect of chromium on photosynthesis, respiration and nitrogen fixation in pea (Pisum sativum L) seedlings. J Plant Physiol 142:25–30CrossRefGoogle Scholar
  14. Bishnoi NR, Dua A, Gupta VK, Sawhney SK (1993b) Effect of chromium on seed germination, seedling growth and yield of peas. Agric Ecosyst Environ 47:47–57CrossRefGoogle Scholar
  15. Blaylock MJ, Huang JW (2000) Phytoextraction of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals-using plants to clean up the environment. Wiley, New York, pp 53–70Google Scholar
  16. Boonyapookana B, Upatham ES, Kruatrachue M, Pokethitiyook P, Singhakaew S (2002) Phytoaccumulation and phytotoxicity of cadmium and chromium in duckweed Wolffia globosa. Int J Phytoremed 4:87–100CrossRefGoogle Scholar
  17. Cakmak I, Marshner H (1993) Effect of zinc nutritional status on superoxide radical and hydrogen peroxide scavenging enzymes in bean leaves. In: Barrow NJ (ed) Plant nutrition-from genetic engineering field practice. Kluwer, Dordrecht, pp 133–137CrossRefGoogle Scholar
  18. Cargnelutti D, Tabaldi LA, Spanevello RM, Jucoski GO, Battisti V, Redin M, Linares CEB, Dressler VL, Flores MM, Nicoloso FT, Morsch VM, Schetinger MRC (2006) Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65:999–1106PubMedCrossRefGoogle Scholar
  19. Chakravarty B, Srivastava S (1992) Toxicity of some heavy metals in vivo and in vitro in Helianthus annuus. Mutat Res 283:287–294PubMedCrossRefGoogle Scholar
  20. Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74PubMedCrossRefGoogle Scholar
  21. Clarimont KB, Hagar WG, Davis EA (1986) Manganese toxicity to chlorophyll synthesis in tobacco callus. Plant Physiol 80:291–293CrossRefGoogle Scholar
  22. Clements HF, Putnam EW, Suehisa RH, Yee GLN, Wehling ML (1974) Soil toxicities as causes of sugarcane leaf freckle, macadamia leaf chlorosis (Keaau) and Maui sugarcane growth failure. Hawaii Agric Exp Station Tech Bull 88, pp 52Google Scholar
  23. Costa G, Morel JL (1994) Water relations, gas exchange and amino acid content in Cd-treated lettuce. Plant Physiol Biochem 32:561–570Google Scholar
  24. Crawford TW, Stroehlein JL, Kuehl RO (1989) Manganese and rates of growth and mineral accumulation in cucumber. J Am Soc Hortic Sci 114:300–306Google Scholar
  25. Cunningham RP (1997) DNA repair: caretakers of the genome? Curr Biol 7:576–579CrossRefGoogle Scholar
  26. Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36PubMedCrossRefGoogle Scholar
  27. Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr 25:2389–2407CrossRefGoogle Scholar
  28. de Dorlodot S, Lutts S, Bertin P (2005) Effects of ferrous iron toxicity on the growth and mineral composition of an inter specific rice. J Plant Nutr 28:1–20CrossRefGoogle Scholar
  29. De Filippis LF, Ziegler H (1993) Effect of sublethal concentrations of zinc, cadmium and mercury on the photosynthetic carbon reduction cycle of Euglena. J Plant Physiol 142:167–172CrossRefGoogle Scholar
  30. Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Holzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266CrossRefGoogle Scholar
  31. Ebbs SD, Kochian LV (1997) Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J Environ Qual 26:776–781CrossRefGoogle Scholar
  32. Elamin OM, Wilcox GE (1986a) Effect of magnesium and manganese nutrition on muskmelon growth and manganese toxicity. J Am Soc Hortic Sci 111:582–587Google Scholar
  33. Elamin OM, Wilcox GE (1986b) Effect of magnesium and manganese nutrition on watermelon growth and manganese toxicity. J Am Soc Hortic Sci 111:588–593Google Scholar
  34. El‐Jaoual T, Cox DA (1998) Manganese toxicity in plants. J Plant Nutr 21:353–386. doi: 10.1080/01904169809365409 CrossRefGoogle Scholar
  35. Epstein E (1961) Mineral metabolism of halophytes. In: Rorison IH (ed) Ecological aspects of the mineral nutrition of plants. Blackwell Publishers, Oxford, pp 345–353Google Scholar
  36. Fodor A, Szabo-Nagy A, Erdei L (1995) The effects of cadmium on the fluidity and H-ATPase activity of plasma membrane from sunflower and wheat roots. J Plant Physiol 14:787–792Google Scholar
  37. Fontes RLS, Cox FR (1998) Zinc toxicity in soybean grown at high iron concentration in nutrient solution. J Plant Nutr 21:1723–1730CrossRefGoogle Scholar
  38. Foy CD (1978) The physiology of metal toxicity in plants. Ann Rev Plant Physiol 29:511–566CrossRefGoogle Scholar
  39. Foy CD, Weil RR, Coradetti CA (1995) Differential manganese tolerances of cotton genotypes in nutrient solution. J Plant Nutr 18:685–706CrossRefGoogle Scholar
  40. Gajewska E, Sklodowska M, Slaba M, Mazur J (2006) Effect of nickel on antioxidative enzymes activities, proline and chlorophyll contents in wheat shoots. Biol Planta 50:653–659CrossRefGoogle Scholar
  41. Garg N, Singla P (2011) Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ Chem Lett 9:303–321CrossRefGoogle Scholar
  42. Gimeno-Garcia E, Andreu V, Boluda R (1996) Heavy metals incidence in the application of inorganic fertilizers and pesticides to rice farming soils. Environ Pollut 92:19–25PubMedCrossRefGoogle Scholar
  43. Goldbold DJ, Hutterman A (1986) The uptake and toxicity of mercury and lead to spruce (Picea abies) seedlings. Water Air Soil Pollut 31:509–515CrossRefGoogle Scholar
  44. Goldstein S, Czapski C (1986) The role and mechanism of metal ions and their complexes in enhancing damage in biological systems or in protecting these systems from the toxicity of O2 . J Free Radic Biol Med 2(1):3–11PubMedCrossRefGoogle Scholar
  45. Gonnelli C, Galardi F, Gabbrielli R (2001) Nickel and copper tolerance in three Tuscan populations of Silene paradoxa. Physiol Planta 113:507–514CrossRefGoogle Scholar
  46. Gopal R, Dube BK, Sinha P, Chatterjee C (2003) Cobalt toxicity effects on growth and metabolism of tomato. Commun Soil Sci Plant Anal 34:619–628. doi: 10.1081/CSS-120018963 CrossRefGoogle Scholar
  47. Gruenhage L, Jager IIJ (1985) Effect of heavy metals on growth and heavy metals content of Allium Porrum and Pisum sativum. Angew Bot 59:11–28Google Scholar
  48. Guo J, Dai X, Xu W, Ma M (2008) Over expressing GSHI and AsPCSI simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026PubMedCrossRefGoogle Scholar
  49. Halliwell B, Cutteridge JMC (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186:1–85PubMedCrossRefGoogle Scholar
  50. Han FX, Su Y, Monts DL, Waggoner AC, Plodinec JM (2006) Binding distribution, and plant uptake of mercury in a soil from Oak Ridge, Tennessee, USA. Sci Total Environ 368:753–768PubMedCrossRefGoogle Scholar
  51. Hawkes JS (1997) Heavy metals. J Chem Educ 74:1369–1374CrossRefGoogle Scholar
  52. Hegedus A, Erdei S, Horvath G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedings under cadmium stress. Plant Sci 160:1085–1093PubMedCrossRefGoogle Scholar
  53. Hernandez LE, Carpena-Ruiz R, Garate A (1996) Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J Plant Nutr 19:1581–1598CrossRefGoogle Scholar
  54. Hewilt EJ (1953) Metal inter-relationships in plant nutrition. J Exp Bot 4:59–64CrossRefGoogle Scholar
  55. Horiguchi T (1988) Mechanism of manganese toxicity and tolerance of plants. IV. Effects of silicon on alleviation of manganese toxicity of rice plants. Soil Sci Plant Nutr 34:65–73CrossRefGoogle Scholar
  56. Horst J (1988a) Beschreibung der Gleichgewichtslage des ionenaustauschs an schwach saoren harzen mit hilfe eines models der oberflachenkomplexbildung, doctoral thesis, University of Karlsruhe, Kfk report, 4464Google Scholar
  57. Horst WJ (1988b) The physiology of Mn toxicity. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in soils and plants. Kluwer Academic Publishers, Dordrecht, pp 175–188CrossRefGoogle Scholar
  58. Hossain MA, Piyatida P, Jaime A, da Silva T, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot vol 2012, Article ID 872875, 37 pp. doi:  10.1155/2012/872875
  59. Huang CV, Bazzaz FA, Venderhoef LN (1974) The inhibition of soya bean metabolism by cadmium and lead. Plant Physiol 34:122–124CrossRefGoogle Scholar
  60. Huffman EWD Jr, Allaway HW (1973a) Chromium in plants: distribution in tissues, organelles, and extracts and availability of bean leaf Cr to animals. J Agric Food Chem 21:982–986PubMedCrossRefGoogle Scholar
  61. Huffman EWD Jr, Allaway WH (1973b) Growth of plants in solution culture containing low levels of chromium. Plant Physiol 52:72–75PubMedPubMedCentralCrossRefGoogle Scholar
  62. Illan YA, Crapski C, Meisel D (1976) The one-electron transfer redox potentials of free radicals. 1. The oxygen/superoxide system. Biochim Biophys Acta 430:209–224CrossRefGoogle Scholar
  63. Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65:591–598PubMedCrossRefGoogle Scholar
  64. Izosimova A (2005) Modelling the interaction between calcium and nickel in the soil-plant system. FAL Agric Res Spec Issue 288:99Google Scholar
  65. Jain R, Srivastava S, Madan VK, Jain R (2000) Influence of chromium on growth and cell division of sugarcane. Indian J Plant Physiol 5:228–231Google Scholar
  66. Juwarkar AS, Shende GB (1986) Interaction of Cd-Pb effect on growth yield and content of Cd, Pb in barley. Indian J Environ Health 28:235–243Google Scholar
  67. Kaji T, Suzuki M, Yamamoto C, Mishima A, Sakamoto M, Kozuka H (1995) Severe damage of cultured vascular endothelial cell monolayer after simultaneous exposure to cadmium and lead. Arch Environ Contam Toxicol 28:168–172PubMedCrossRefGoogle Scholar
  68. Kamal M, Ghalya AE, Mahmouda N, Cote R (2004) Phytoaccumulation of heavy metals by aquatic plants. Environ Int 29:1029–1039PubMedCrossRefGoogle Scholar
  69. Kasprzak KS (1995) Possible role of oxidative damage in metal induced carcinogenesis. Cancer Invest 13:411–430PubMedCrossRefGoogle Scholar
  70. Khan S, Khan NN (1983) Influence of lead and cadmium on growth and nutrient concentration of tomato (Lycopersicum esculentum) and egg plant (Solanum melongena). Plant Soil 74:387–394CrossRefGoogle Scholar
  71. Kitao M, Lei TT, Koike T (1997a) Effects of manganese toxicity on photosynthesis of white birch (Betula platyphylla var. japonica) seedlings. Physiol Plant 101:249–256CrossRefGoogle Scholar
  72. Kitao M, Lei TT, Koike T (1997b) Effects of manganese in solution culture on the growth of five deciduous broad-leaved tree species with different successional characters from northern Japan. Photosynthesis 36:31–40CrossRefGoogle Scholar
  73. Kumar G, Singh RP, Sushila (1992) Nitrate assimilation and biomass production in Seasamum indicum (L.) seedlings in lead enriched environment. Water Soil Pollut 215:124–215Google Scholar
  74. L’Huillier L, d’Auzac J, Durand M, Michaud-Ferriere N (1996) Nickel effects on two maize (Zea mays) cultivars: growth, structure, Ni concentration, and localization. Can J Bot 74:1547–1554CrossRefGoogle Scholar
  75. Lee YW, Klein CB, Kargacin B, Salnikow K, Kitahara J, Dowjat K, Zhitkovich A, Christie NT, Costa M (1995) Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens. Mol Cell Biol 15:2547–2557PubMedPubMedCentralCrossRefGoogle Scholar
  76. Lee CW, Choi JM, Pak CH (1996) Micronutrient toxicity in seed geranium (Pelargonium x hortorum Bailey). J Am Soc Hortic Sci 121:77–82Google Scholar
  77. Lenntech Water Treatment and Air Purification (2004) Water treatment. Lenntech, Rotterdamseweg, Google Scholar
  78. Lewis S, Donkin ME, Depledge MH (2001) Hsp 70 expression in Enteromorpha intestinalis (Chlorophyta) exposed to environmental stressors. Aquat Toxicol 51:277–291PubMedCrossRefGoogle Scholar
  79. Li Z, McLaren RG, Metherell AK (2004) The availability of native and applied soil cobalt to ryegrass in relation to soil cobalt and manganese status and other soil properties. N Z J Agric Res 47:33–43CrossRefGoogle Scholar
  80. Li HF, Gray C, Mico C, Zhao FJ, McGrath SP (2009) Phytotoxicity and bioavailability of cobalt to plants in a range of soils. Chemosphere 75:979–986PubMedCrossRefGoogle Scholar
  81. Luna CM, Gonzalez CA, Trippi VS (1994) Oxidative damage caused by an excess of copper in oat leaves. Plant Cell Physiol 35:11–15Google Scholar
  82. Luo Y, Han Z, Chin SM, Linn S (1994) Three chemically distinct types of oxidants formed by iron mediated Fenton reactions in the presence of DNA. Proc Natl Acad Sci U S A 91:12438–12442PubMedPubMedCentralCrossRefGoogle Scholar
  83. Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plants and heavy metals. Springer Briefs in Biometals. doi:  10.1007/978-94-007-4441
  84. Marschner H (1986) Mineral nutrition of higher plants. Academic, London, p 674Google Scholar
  85. Mathys W (1975) Enzymes of heavy metal-resistant and non-resistant populations of Silene cucubalus and their interactions with some heavy metals in vitro and in vivo. Physiol Plant 33:161–165CrossRefGoogle Scholar
  86. Meharg AA (1994) Integrated tolerance mechanisms-constitutive and adaptive plant-response to elevated metal concentrations in the environment. Plant Cell Environ 17:989–993CrossRefGoogle Scholar
  87. Meharg AA, Macnair MR (1992) Suppression of the high affinity phosphate uptake system; a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43:519–524CrossRefGoogle Scholar
  88. Mildvan AS (1970) Metal in enzymes catalysis. In: Boyer DD (ed) The enzymes, vol 11. Academic, London, pp 445–536Google Scholar
  89. Miller JE, Hassete JJ, Koppe DE (1975) Interaction of lead and cadmium of electron energy transfer reaction in corn mitochondria. Physiol Plant 28:166–171CrossRefGoogle Scholar
  90. Mohanpuria P, Rana NK, Yadav SK (2007) Cadmium induced oxidative stress influence on glutathione metabolic genes of Camellia sinensis (L.). O Kuntze. Environ Toxicol 22:368–374PubMedCrossRefGoogle Scholar
  91. Monni S, Salemma M, Millar N (2000) The tolerance of Empetrum nigrum to copper and nickel. Environ Pollut 109:221–229PubMedCrossRefGoogle Scholar
  92. Moreno-Caselles J, Moral R, Pera-Espinosa A, Marcia MD (2000) Cadmium accumulation and distribution in cucumber plants. J Plant Nutr 23:243–250CrossRefGoogle Scholar
  93. Morzck E Jr, Funicclli NA (1982) Effect of lead and on germination of Spartina alterniflora Loisel seeds at various salinities. Environ Exp Bot 22:23–32CrossRefGoogle Scholar
  94. Mukherji S, Maitra P (1976) Toxic effects of lead growth and metabolism of germinating rice (Oryza sativa L.) seeds mitosis of onion (Allium cepa) root tip cells. Ind J Exp Biol 14:519–521Google Scholar
  95. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216CrossRefGoogle Scholar
  96. Nakos G (1979) Lead pollution: fate of lead in soil and its effects on Pinus haplenis. Plant Soil 50:159–161Google Scholar
  97. Neelima P, Reddy KJ (2002) Interaction of copper and cadmium with seedlings growth and biochemical responses in Solanum melongena. Envin Pollut Technol 1:285–290Google Scholar
  98. Nieboer E, Richardson DHS (1980) The replacement of the nondescript term heavy metals by a biologically and chemistry significant classification of metal ions. Environ Pollut B 1:3–26CrossRefGoogle Scholar
  99. Ouzounidou G (1994) Change in chlorophyll fluorescence as a result of copper treatment: dose response relations in Silene and Thlaspi. Photosynthetica 29:455–462Google Scholar
  100. Paivoke H (1983) The short term effect of zinc on growth anatomy and acid phosphate activity of pea seedlings. Ann Bot 20:307–309Google Scholar
  101. Panda SK, Patra HK (2000) Does chromium (III) produce oxidative stress in excised wheat leaves? J Plant Biol 27:105–110Google Scholar
  102. Pandey N, Sharma CP (2002) Effect of heavy metals Co2+, Ni2+, and Cd2+ on growth and metabolism of cabbage. Plant Sci 163:753–758CrossRefGoogle Scholar
  103. Pandolfini T, Gabbrielli R, Comparini C (1992) Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell Environ 15:719–725CrossRefGoogle Scholar
  104. Parr PD, Taylor FG Jr (1982) Germination and growth effects of hexavalent chromium in Orocol TL (a corrosion inhibitor) on Phaseolus vulgaris. Environ Int 7:197–202CrossRefGoogle Scholar
  105. Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422CrossRefGoogle Scholar
  106. Patterson W, Olson JJ (1983) Effects of heavy metals on radicle growth of selected woody species germinated on filter paper, mineral and organic soil substrates. Can J Forest Res 13:233–238CrossRefGoogle Scholar
  107. Peralta JR, Gardea Torresdey JL, Tiemann KJ, Gomez E, Arteaga S, Rascon E (2001) Uptake and effects of five heavy metals on seed germination and plant growth in alfalfa (Medicago sativa) L. Bull Environ Contam Toxicol 66(6):727–734PubMedGoogle Scholar
  108. Porter JR, Cheridan RP (1981) Inhibition of nitrogen fixation in alfalfa by arsenate, heavy metals, fluoride and simulated acid rain. Plant Physiol 68:143–148PubMedPubMedCentralCrossRefGoogle Scholar
  109. Porter EK, Peterson PJ (1975) Arsenic accumulation by plants on mine waste (United Kingdom). Environ Pollut 4:365–371Google Scholar
  110. Prasad MNV, Hagmeyer J (1999) Heavy metal stress in plants. Springer, Berlin, pp 16–20CrossRefGoogle Scholar
  111. Prasad MNV, Greger M, Landberg T (2001) Acacia nilotica L. bark removes toxic elements from solution: corroboration from toxicity bioassay using Salix viminalis L. in hydroponic system. Int J Phytoremed 3:289–300CrossRefGoogle Scholar
  112. Pryor WA (1988) Why is the hydroxyl radical the only radical that commonly adds to DNA? Hypothesis: it is a rare combination of high electrophilicity, high thermo chemical reactivity, and a mode of production that occurs near DNA. Free Radic Biol Med 4:219–223PubMedCrossRefGoogle Scholar
  113. Rahman H, Sabreen S, Alam S, Kawai S (2005) Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J Plant Nutr 28:393–404CrossRefGoogle Scholar
  114. Reddy AM, Kumar SG, Jyotsnakumari G, Thimmanayak S, Sudhakar C (2005) Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere 60:97–104PubMedCrossRefGoogle Scholar
  115. Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229Google Scholar
  116. Romero-Puertas MC, Rodriquez-Serrano M, Corpas FJ, Gomez M, Del Rio LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2 and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134CrossRefGoogle Scholar
  117. Ros R, Cook DT, Martinez-Cortina C, Picazo I (1992) Nickel and cadmium-related changes in growth, plasma membrane lipid composition, ATPase hydrolytic activity and proton pumping of rice (Oryza sativa L. cv. Bahia) shoots. J Exp Bot 43:1475–1481CrossRefGoogle Scholar
  118. Roseman IE, Levine RL (1987) Purification of a protease from Escherichia coli with specificity for oxidized glutamine synthetase. J Biol Chem 262(5):2101–2110PubMedGoogle Scholar
  119. Rout GR, Sanghamitra S, Das P (2000) Effects of chromium and nickel on germination and growth in tolerant and non-tolerant populations of Echinochloa colona (L). Chemosphere 40:855–859PubMedCrossRefGoogle Scholar
  120. Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley D, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474PubMedCrossRefGoogle Scholar
  121. Schmfger MEV (2001) Phytochelatins: complexation of metals and metalloids, studies on the phytochelatin synthase. PhD Thesis, Munich University of Technology (TUM), MunichGoogle Scholar
  122. Scholz RW, Graham KS, Wynn MK (1990) Interaction of glutathione and a-tocopherol in the inhibition of lipid peroxidation of rat liver microsomes. In: Eddy CC, Hamilton GA, Madyastha KM (eds) Biological oxidation systems. Academic, San Diego, pp 841–867CrossRefGoogle Scholar
  123. Shah K, Dubey RS (1998) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol Plant 40:121–130CrossRefGoogle Scholar
  124. Shanker AK, Sudhagar R, Pathmanabhan G (2003a) Growth phytochelatin SH and antioxidative response of sunflower as affected by chromium speciation. In: 2nd international congress of plant physiology on sustainable plant productivity under changing environment, New DelhiGoogle Scholar
  125. Shanker AK, Djanaguiraman M, Pathmanabhan G, Sudhagar R, Avudainayagam S (2003b) Uptake and phytoaccumulation of chromium by selected tree species. In: Proceedings of the international conference on water and environment held in Bhopal, IndiaGoogle Scholar
  126. Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52CrossRefGoogle Scholar
  127. Singh PK, Tewari SK (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–117PubMedGoogle Scholar
  128. Sinha SK, Srinivastava HS, Mishra SN (1988a) Nitrate assimilation in intact and excised maize leaves in the presence of lead. Bull Environ Contam Toxicol 41:419–422PubMedCrossRefGoogle Scholar
  129. Sinha SK, Srinivastava HS, Mishra SN (1988b) Effect of lead on nitrate reductase activity and nitrate assimilation in pea leaves. Bot Pollut 57:457–463Google Scholar
  130. Sinha S, Guptha M, Chandra P (1997) Oxidative stress induced by iron in Hydrilla verticillata (i.f) royle: response of antioxidants. Ecotoxicol Environ Safe 38:286–291CrossRefGoogle Scholar
  131. Somasekharaiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxidase in chlorophyll degradation. Physiol Plant 85:85–89CrossRefGoogle Scholar
  132. Stadtman ER (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalysed reactions. Annu Rev Biochem 62:797–821PubMedCrossRefGoogle Scholar
  133. Stadtman ER, Oliver CN (1991) Metal-catalyzed oxidation of proteins. Physiological consequences. J Biol Chem 266:2005–2008PubMedGoogle Scholar
  134. Stiborova M, Pitrichova M, Brezinova A (1987) Effect of heavy metal ions in growth and biochemical characteristic of photosynthesis of barley and maize seedlings. Biol Plant 29:453–467CrossRefGoogle Scholar
  135. Sudhakar C, Symalabai L, Veeranjaveyuler K (1992) Lead tolerance of certain legume species grown on lead or tailing. Agric Ecosyst Environ 41:253–261CrossRefGoogle Scholar
  136. Tang SR, Wilke BM, Brooks RR, Tang SR (2001) Heavy-metal uptake by metal tolerant Elsholtzia haichowensis and Commelina communis from China. Commun Soil Sci Plant Anal 32:895–905CrossRefGoogle Scholar
  137. Thomas F, Malick C, Endreszl EC, Davies KS (1998) Distinct responses to copper stress in the halophyte, Mesembryanthemum crystallinum. Physiol Plant 102:360–368CrossRefGoogle Scholar
  138. Van Assche F, Clijsters H (1983) Multiple effects of heavy metals on photosynthesis. In: Marcelle R (ed) Effects of stress on photosynthesis, vol 7. Nijhoff/Junk, The Hague, pp 371–382CrossRefGoogle Scholar
  139. Van Assche F, Clijsters H (1987) Enzymes analysis in plants as a tool for assessing phytotoxicity on heavy metal polluted soils. Med Fac Landouw Rijiksuniv Gent 52:1819–1824Google Scholar
  140. Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206CrossRefGoogle Scholar
  141. Varalakshmi LR, Ganeshamurthy AN (2009) Effect of cadmium on plant biomass and cadmium accumulation in amaranthus (Amaranthus tricolor) cultivars. Indian J Agric Sci 79(1):861–864Google Scholar
  142. Varalakshmi LR, Ganeshamurthy AN (2012) Heavy metal contamination of water bodies, soils and vegetables in peri-urban areas: a case study in Bengaluru. J Hortic Sci 7(1):62–67Google Scholar
  143. Varalakshmi LR, Ganeshamurthy AN (2013) Phytotoxicity of cadmium in radish and its effects on growth, yield and cadmium uptake. Commun Soil Sci Plant Anal 44:1444–1456CrossRefGoogle Scholar
  144. Vazques MD, Poschenrieder C, Barcelo J (1987) Chromium (VI) induced structural changes in bush bean plants. Ann Bot 59:427–438Google Scholar
  145. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  146. Warne MS, Heemsbergen D, Stevens D, McLaughlin M, Cozens G, Whatmuff M, Broos K, Barry G, Bell M, Nash D, Pritchard D, Penney N (2008) Modeling the toxicity of copper and zinc salts to wheat in 14 soils. Environ Toxicol Chem 27:786–792PubMedCrossRefGoogle Scholar
  147. Weckex JEJ, Clijsters HMM (1997) Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol Biochem 35:405–410Google Scholar
  148. Winterhalder EK (1963) Differential resistance of two species of eucalyptus to toxic soil manganese levels. Aust J Sci 25:363–364Google Scholar
  149. Wintz H, Fox T, Vulpe C (2002) Responses of plants to iron, zinc and copper deficiencies. Biochem Soc Trans 30:766–768PubMedCrossRefGoogle Scholar
  150. Wu S (1994) Effect of manganese excess on the soybean plant cultivated under various growth conditions. J Plant Nutr 17:993–1003Google Scholar
  151. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179CrossRefGoogle Scholar
  152. Zeid IM (2001) Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol Plant 44:111–115CrossRefGoogle Scholar
  153. Zhang WH, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120:849–857PubMedPubMedCentralCrossRefGoogle Scholar
  154. Zhou ZS, Huang SQ, Guo K, Mehta SK, Zhang PC, Yang ZM (2007) Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J Inorg Biochem 101:1–9PubMedCrossRefGoogle Scholar
  155. Zhu B, Alva AK (1993) Effect of pH on growth and uptake of copper by Swingle citrumelo seedlings. J Plant Nutr 16:1837–1845CrossRefGoogle Scholar
  156. Zingg JM, Jones PA (1997) Genetic and epigenetic aspects of DNA methylation on genome expression, evolution, mutation and carcinogenesis. Carcinogenesis 18:869–882PubMedCrossRefGoogle Scholar

Copyright information

© Springer India 2016

Authors and Affiliations

  1. 1.Division of Soil Science and Agricultural ChemistryICAR-Indian Institute of Horticultural ResearchBengaluruIndia

Personalised recommendations