Toxic Effects of Heavy Metals on Germination and Physiological Processes of Plants

  • Parvaze Ahmad Wani
  • Mohammad Saghir Khan
  • Almas Zaidi


Pollution of the environment by toxic metals in recent years has accelerated dramatically due to rapid industrial progress. Heavy metals when taken up in amounts in excess of the normal concentration produce lethal effects on plants, on microbes, and directly or indirectly on the human health. Deleterious impact of metals on plants includes the reduction in germinability of seeds, inactivation of enzymes, damage to cells by acting as antimetabolites, or formation of precipitates or chelates with essential metabolites. Heavy metals also show unconstructive effects on other physiological processes like photosynthesis, gaseous exchange, water relations, and mineral/nutrient absorption by plants. These adverse effects may be due to the generation of reactive oxygen species which may cause oxidative stress. The impact of heavy metals on germination of legume seeds and different physiological events of plants with special reference to leguminous plants grown in distinct agroecological niches is highlighted.


  1. Agarwala SC, Nautiyal BD, Chatterjee C, Nautiyal N (1995) Variations in copper and zinc supply influence growth and activities of some enzymes in maize. Soil Sci Plant Nutr 41:329–335Google Scholar
  2. AI-Rumaih MM, Rushdy SS, Warsy AS (2001) Effect of cadmium chloride on seed germination and growth characteristics of cowpea (Vigna unguiculata l.) plants in the presence and absence of gibberellic acid. Saudi J Biol Sci 8:41–50Google Scholar
  3. Arora NK, Khare E, Singh S, Maheshwari DK (2010) Effect of Al and heavy metals on enzymes of nitrogen metabolism of fast and slow growing rhizobia under explanta conditions. World J Microbiol Biotechnol 26:811–816Google Scholar
  4. Arun KS, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753Google Scholar
  5. Atici O, Ağar G, Battal P (2005) Changes in phytohormone contents in chickpea seeds germinating under lead or zinc stress. Biol Plant 49:215–222Google Scholar
  6. Atıcı Ö, Agar G, Battal P (2003) Interaction between endogenous plant hormones and α-amylase in germinating chickpea seeds under cadmium exposure. Fresenius Environ Bull 12:781–785Google Scholar
  7. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107Google Scholar
  8. Barcelo J, Poschenriender C, Ruano A, Gunse B (1985) Leaf water potential in Cr(VI) treated bean plants (Phaseolus vulgaris L). Plant Physiol Suppl 77:163–164Google Scholar
  9. Barcelo J, Cabot C, Poschenrieder C (1986) Cadmium induced decrease of water stress resistance in bush bean plants (Phaseolus vulgaris L.). II. Effects of Cd on endogenous abscisic acid levels. Plant Physiol 125:27–34Google Scholar
  10. Berglund AH, Mike F, Quartacci MF, Calucci LC, Navari-Izzo F, Pinzino C, Liljenberg C (2002) Alterations of wheat root plasma membrane lipid composition induced by copper stress result in changed physicochemical properties of plasma membrane lipid vesicles. Biochim Biophys Acta 1564:466–472PubMedGoogle Scholar
  11. Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18Google Scholar
  12. Bibi M, Hussain M (2005) Effect of copper and lead on photosynthesis and plant pigments in black gram (Vigna mungo L.). Bull Environ Contam Toxicol 74:1126–1133PubMedGoogle Scholar
  13. Bouazizi H, Jouili H, Geitmann A, Ferjani EEI (2010) Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. Ecotoxicol Environ Saf 73:1304–1308PubMedGoogle Scholar
  14. Cakmak I, Horst WJ (1991) Effect of aluminum on net efflux of nitrate and potassium from root tips of soybean (Glycine max L.). J Plant Physiol 130:400–403Google Scholar
  15. Cambrolle J, Mateos-Naranjo E, Redondo-Gomez S, Luque T, Figueroa ME (2011) Growth, reproductive and photosynthetic responses to copper in the yellow-horned poppy, Glaucium flavum Crantz. Environ Exp Bot 71:57–64Google Scholar
  16. Caro A, Puntarulo S (1996) Effect of in vivo iron supplementation on oxygen radical production by soybean roots. Biochim Biophys Acta 1229:245–251Google Scholar
  17. Casano LM, Gomez LD, Lascano HR, Gonzales CA, Trippi VS (1997) Inactivation and degradation of CuZn-SOD by active oxygen species in wheat chloroplasts exposed to photo-oxidative stress. Plant Cell Physiol 38:433–440PubMedGoogle Scholar
  18. Chaoui A, Mazhoudi S, Ghorbal MH, Ferjani EE (1997) Cadmium and Zn induction of lipid peroxidation and effects of antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147Google Scholar
  19. Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74PubMedGoogle Scholar
  20. Cortes OEJ, Barbosa LAD, Kiperstok A (2003) Biological treatment of industrial liquid effluent in copper production industry. Tecbahia Revista Baiana de Tecnologia 18:89–99Google Scholar
  21. Cyplik P, Grajek W, Marecik R, Kroliczak P (2007) Effect of macro/micronutrients and carbon source over the denitrification rate of Haloferax denitrifications archaeon. Enzyme Microb Technol 40:212–220Google Scholar
  22. Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36PubMedGoogle Scholar
  23. de Vries W, Romkens PF, Schutze G (2007) Critical soil concentrations of cadmium, lead, and mercury in view of health effects on humans and animals. Rev Environ Contam Toxicol 191:91–130PubMedGoogle Scholar
  24. Dewar J, Taylor JRN, Berjak P (1998) Changes in selected plant growth regulators during germination in sorghum. Seed Sci Res 8:1–8Google Scholar
  25. Dickinson RE, Cicerone RJ (1986) Future global warming from atmospheric trace gases. Nature 319:109–115Google Scholar
  26. Dixit V, Pandey V, Shyam R (2002) Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum Azad) root mitochondria. Plant Cell Environ 25:687–690Google Scholar
  27. Doelman P, Haanstra L (1984) Short-term and long-term effects of Cd, Cr, Cu, Ni, Pb, and Zn on microbial respiration in relation to abiotic soil factors. Plant Soil 79:317–321Google Scholar
  28. Ernst WHO (1998) Effects of heavy metals in plants at the cellular and organismic level ecotoxicology. In: Gerrit S, Bernd M (eds) Bioaccumulation and biological effects of chemicals. Wiley and Spektrum Akademischer, New York, pp 587–620Google Scholar
  29. Ernst WHO, Verkleij JAC, Schat H (1990) Evolutionary biology of metal resistance in Silene vulgaris. Evol Trends Plants 4:45–51Google Scholar
  30. Ernst WHO, Verkleij JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229–248Google Scholar
  31. Fargasova A (1994) Effect of Pb, Cd, Hg, As and Cr on germination and root growth of Sinapsis alba seeds. Bull Environ Contam Toxicol 52:452–456PubMedGoogle Scholar
  32. Fargašová A (1998) Root growth inhibition, photosynthetic pigments production, and metal accumulation in Synapis alba as the parameters for trace metals effect determination. Bull Environ Contam Toxicol 61:762–769PubMedGoogle Scholar
  33. Ferguson SJ (1998) Nitrogen cycle enzymology. Curr Opin Chem Biol 2:182–193PubMedGoogle Scholar
  34. Fernandes JC, Henriques FS (1991) Biochemical, physiological and structural effects of excess copper in plants. Bot Rev 57:246–273Google Scholar
  35. Fodor E, Szabo-Nagy A, Erdel L (1995) The effects of cadmium on the fluidity and H+ ATPase activity of plasma membrane from sunflower and wheat roots. J Plant Physiol 147:87–92Google Scholar
  36. Fornazier RF, Ferreira RR, Victoria AP, Molina SMG, Lea PJ, Azevedo RA (2002) Effect of cadmium on antioxidant enzyme activities in sugarcane. Biol Plant 45:91–97Google Scholar
  37. Forstner U (1995) Land contamination by metals: global scope and magnitude of problem. In: Allen HE, Huang CP, Bailey GW, Bowers AR (eds) Metal speciation and contamination of soil. CRC, Boca Raton, FL, pp 1–33Google Scholar
  38. Fuhrer J (1988) Ethylene biosynthesis and cadmium toxicity in leaf tissue of beans Phaseolus vulgaris L. Plant Physiol 70:162–167Google Scholar
  39. Gajewska E, Skłodowska M, Laba M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50:653–659Google Scholar
  40. Garg N, Bhandari P (2011) Influence of cadmium stress and arbuscular mycorrhizal fungi on nodule senescence in Cajanus cajan (L.) Mill sp. Int J Phytoremed 14:62–74Google Scholar
  41. Giller KE, McGrath SP, Hirsch PR (1989) Absence of nitrogen fixation in clover grown on soil subject to long-term contamination with heavy metals is due to survival of only ineffective Rhizobium. Soil Biol Biochem 21:841–848Google Scholar
  42. Girotti AW (1985) Mechanism of lipid peroxidation. J Free Radic Biol Med 1:87–95PubMedGoogle Scholar
  43. Gonçalves JF, Antes FG, Maldaner J, Pereira LB, Tabaldi LA, Rauber R, Rossato LV, Bisognin DA, Dressler VL, de Moraes Flores EM, Nicoloso FT (2009) Cadmium and mineral nutrient accumulation in potato plantlets grown under cadmium stress in two different experimental culture conditions. Plant Physiol Biochem 47:814–821PubMedGoogle Scholar
  44. Gross R, Auslitz J, Schramel P, Payer HD (1987) Concentrations of lead, cadmium, mercury and other elements in seeds of Lupinus mutabilis and of other legumes. J Environ Pathol Toxicol Oncol 7:59–65PubMedGoogle Scholar
  45. Gwozdz EA, Przymusinski R, Rucinska R, Deckert J (1997) Plant cell responses to heavy metals: molecular and physiological aspects. Acta Physiol Plant 19:459–465Google Scholar
  46. Hamman B, Koning G, Him Lok K (2003) Homeopathically prepared gibberellic acid and barley seed germination. Homeopathy 92:140–144PubMedGoogle Scholar
  47. Hansch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266PubMedGoogle Scholar
  48. Hartley-Whitaker J, Ainsworth G, Meharg AA (2001) Copper and arsenate-induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant Cell Environ 24:713–772Google Scholar
  49. Hemida SK, Omar SA, Abdel-Mallek AY (1997) Microbial populations and enzyme activity in soil treated with heavy metals. Water Air Soil Pollut 95:13–22Google Scholar
  50. Hernandez LE, Cooke DT (1997) Modification of the root plasma membrane lipid composition of Cd treated Pisum sativum. J Exp Bot 48:1375–1381Google Scholar
  51. Holleman AF, Wiberg E (1985) Lehrbuch der Anorganischen Chemie. Walter de Gruyter, Berlin, p 868Google Scholar
  52. Holtan-Hartwig L, Bechmann M, Hoyas TR, Linjordet R, Bakken LR (2002) Heavy metals tolerance of soil denitrifying communities: N2O dynamics. Soil Biol Biochem 34:1181–1190Google Scholar
  53. Hristozkova M, Geneva M, Stancheva I (2006) Response of pea plants (Pisum sativum L.) to reduced supply with molybdenum and copper. Int J Agric Biol 8:218–220Google Scholar
  54. Hsu FR, Chou CH (1992) Inhibitory effects of heavy metals on seed germination and seedling growth of Miscanthus species. Bot Bull Acad Sin 33:335–342Google Scholar
  55. Hsu YT, Kao CH (2003) Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. -. Plant Cell Environ 26:867–874PubMedGoogle Scholar
  56. Hussain M, Ahmad MSA, Kausar A (2006) Effect of lead and chromium on growth, photosynthetic pigments and yield components in mash bean [Vigna mungo (L.) Hepper]. Pak J Bot 38:1389–1396Google Scholar
  57. Imlay JA, Chin SM, Lin S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240:640–642PubMedGoogle Scholar
  58. 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
  59. Jamal SN, Iqbal MZ, Athar M (2006) Effect of aluminum and chromium on the germination and growth of two Vigna species. Int J Environ Sci Technol 3:53–58Google Scholar
  60. Janicka-Russak M, Kabala K, Burzynski M, Kobus G (2008) Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots. J Exp Bot 59:3721–3728PubMedGoogle Scholar
  61. Jayakumar K, Jaleel CA, Azooz MM (2008) Impact of cobalt on germination and seedling growth of Eleusine coracana L. and Oryza sativa L. under hydroponic culture. Global J Mol Sci 3:18–20Google Scholar
  62. Kappus H (1985) Lipid peroxidation: mechanisms. In: Sites H (ed) Analysis enzymology and biological relevance of oxidative stress. Academic, London, pp 273–310Google Scholar
  63. Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5754PubMedGoogle Scholar
  64. Korashy HM, El-Kadi AOS (2008) Modulation of TCDD-mediated induction of cytochrome P450 1A1 by mercury, lead, and copper in human HepG2 cell line. Toxicol In Vitro 22:154–158PubMedGoogle Scholar
  65. Krupa Z (1999) Cadmium against higher plant photosynthesis- a variety of effects and where do they possibly come from. Z Naturforsch 54c:723–729Google Scholar
  66. Lagisz M, Laskowski R (2008) Evidence for between-generation effects in carabids exposed to heavy metals pollution. Ecotoxicology 17:59–66PubMedGoogle Scholar
  67. Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Biol 51:71–79Google Scholar
  68. Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682PubMedGoogle Scholar
  69. Letham DS (1994) Cytokinins as phytohormones-sites of biosynthesis, translocation and function of translocated cytokinins. In: Mok DWS, Mok MC (eds) Cytokinins: chemistry, activity and function. CRC, Boca Raton, FL, pp 57–80Google Scholar
  70. Letham DS, Palni LMS (1983) The biosynthesis and metabolism of cytokinins. Annu Rev Plant Physiol 34:163–197Google Scholar
  71. Li Y, Trush MA (1993a) DNA damage resulting from the oxidation of hydroquinone by copper: role for a Cu(II)/Cu/I) redox cycle and reactive oxygen generation. Carcinogenes 7:1303–1311Google Scholar
  72. Li Y, Trush MA (1993b) Oxidation of hydroquinone by copper: chemical mechanism and biological effects. Biochem Biophys Acta 300:346–355Google Scholar
  73. 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
  74. Lund BO, Miller BM, Woods JS (1993) Studies on Hg(II)-induced H2O2 formation and oxidative stress in vivo and in vitro in rat kidney mitochondria. Biochem Biopharmacol 45:2017–2024Google Scholar
  75. Macfarlane GR, Burchett MD (2001) Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 42:233–240PubMedGoogle Scholar
  76. Mahieu S, Frérot H, Vidal C, Galiana A, Heulin K, Maure L, Brunel B, Lefèbvre C, Escarré J, Cleyet-Marel JC (2011) Anthyllis vulneraria/Mesorhizobium metallidurans, an efficient symbiotic nitrogen fixing association able to grow in mine tailings highly contaminated by Zn, Pb and Cd. Plant Soil 342:405–417Google Scholar
  77. Maksymiec W, Bednara J, Baszynski T (1995) Response of runner bean plants to excess copper as a function of plant growth stages: effects on morphology and structure of primary leaves and their chloroplast ultrastructure. Photosynthetica 31:427–435Google Scholar
  78. Manivasagaperumal R, Vijayarengan P, Balamurugan S, Thiyagarajan G (2011) Effect of copper on growth, dry matter yield and nutrient content of vigna radiata (l.) wilczek. J Phytol 3:53–62Google Scholar
  79. Mateos-Naranjo E, Redondo-Gomez S, Cambrolle J, Figueroa ME (2008) Growth and photosynthetic responses to copper stress of an invasive cordgrass, Spartina densiflora. Mar Environ Res 66:459–465PubMedGoogle Scholar
  80. Matraszek R (2008) Nitrate reductase activity of two leafy vegetables as affected by nickel and different nitrogen forms. Acta Physiol Plant 30:361–370Google Scholar
  81. Mazhoudi S, Chaoui A, Ghorbal MH, El Ferjani E (1997) Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum, Mill). Plant Sci 127:129–137Google Scholar
  82. McGrath SP, Chaudri AM, Giller KE (1995) Long-term effects of metals in sewage sludge on soils, microorganisms and plants. J Ind Microbiol 14:94–104PubMedGoogle Scholar
  83. Mcllveen WD, Nagusanti JJ (1994) Nickel in the terrestrial environment. Sci Total Environ 148:109–138Google Scholar
  84. Mehrag AA (1993) The role of plasmalemma in metal tolerance in angiosperms. Physiol Plant 88:191–198Google Scholar
  85. Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178PubMedGoogle Scholar
  86. Moffat AS (1999) Engineering plants to cope with metals. Science 285:369–370PubMedGoogle Scholar
  87. Molina AS, Nievas C, Pérez Chaca MV, Garibotto F, González U, Marsá SM, Luna C, Giménez MS, Zirulnik F (2008) Cadmium-induced oxidative damage and antioxidative defense mechanisms in Vigna mungo L. Plant Growth Regul 56:285–295Google Scholar
  88. Monni S, Salemaa M, Millar N (2000) The tolerance of Empetrum nigrum to copper and nickel. Environ Pollut 109:221–229PubMedGoogle Scholar
  89. Monni S, Uhlig C, Hansen E, Magel E (2001) Ecophysiological responses of Empetrum nigrum to heavy metal pollution. Environ Pollut 112:121–129PubMedGoogle Scholar
  90. Moussa HR (2004) Effect of cadmium on growth and oxidative metabolism of faba bean plants. Acta Agron Hung 52:269–276Google Scholar
  91. Mysliwa-Kurdziel B, Strzatka K (2002) Influences of metals on biosynthesis of photosynthetic pigments. In: Prasad MNV, Strzatka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer, Dortrecht, pp 201–227Google Scholar
  92. Nasim SA, Dhir B (2010) Heavy metals alter the potency of medicinal plants. Rev Environ Contam Toxicol 203:139–149PubMedGoogle Scholar
  93. Navarro MC, Perez-Sirvent C, Martinez-Sanchez MJ, Vidal J, Tovar PJ, Bech J (2008) Abandoned mine sites as a source of contamination by heavy metals: a case study in a semi-arid zone. J Geochem Explor 96:183–193Google Scholar
  94. Nieboer E, Richardson DHS (1980) The replacement of the nodescript term heavy metal by a biologically significant and chemically significant classification of metal ions. Environ Pollut B1:3–26Google Scholar
  95. Ortega-Villasante C, Rellán-Álvarez R, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56:2239–2251PubMedGoogle Scholar
  96. Ouzounidou G, Eleftheriou EP, Karataglis S (1992) Ecophysiological and ultrastructural effects of copper in Thlaspi ochroleucum (Cruciferae). Can J Bot 70:947–957Google Scholar
  97. Panda SK, Choudhary S (2005) Chromium stress in plants. Braz J Plant Physiol 17:19–102Google Scholar
  98. Panda SK, Patra HK (2000) Nitrate and ammonium ions effect on the chromium toxicity in developing wheat seedlings. Proc Natl Acad Sci India B 70:75–80Google Scholar
  99. Pandey J, Pandey U (2009) Accumulation of heavy metals in dietary vegetables and cultivated soil horizon in organic farming system in relation to atmospheric deposition in a seasonally dry tropical region of India. Environ Monit Assess 148:61–74PubMedGoogle Scholar
  100. Parmar G, Chanda V (2005) Effects of mercury and chromium on peroxidase and IAA oxidase enzymes in the seedlings of Phaseolus vulgaris. Turk J Biol 29:15–21Google Scholar
  101. 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 66:727–34PubMedGoogle Scholar
  102. Philippot L, Højberg O (1999) Dissimilatory nitrate reductase in bacteria. Biochim Biophys Acta 1446(1–2):1–23PubMedGoogle Scholar
  103. Polle A (1997) Defense against photo-oxidative damage in plants. In: Scandalos JG (ed) Oxidative stress and the molecular biology of antioxidant defences. Cold Spring Harbor Laboratory Press, New York, pp 623–666Google Scholar
  104. Poschenreider CR, Gunse B, Barcelo L (1989) Influence of cadmium on water relations, stomatal resistance and abscisic acid content in expanding bean leaves. Plant Physiol 90:1365–1371Google Scholar
  105. Pospíšilová J (2003) Participation of phytohormones in the stomatal regulation of gas exchange during water stress. Biol Plant 46:491–506Google Scholar
  106. Price AH, Hendry GAF (1991) Iron catalyzed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ 14:477–484Google Scholar
  107. Quartacci MF, Cosi E, Navari-Izzo F (2001) Lipid and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 52:77–84PubMedGoogle Scholar
  108. Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C (2005) Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere 60:97–104PubMedGoogle Scholar
  109. Sakadevan K, Zheng H, Bavor HJ (1999) Impact of heavy metals on denitrification in surface wetland sediments receiving wastewater. Water Sci Technol 40:349–355Google Scholar
  110. Salisbury FB, Ross CW (1992) Plant physiology, 2nd edn. Wadsworth, BelmontGoogle Scholar
  111. Salt DE, Prince RC, Pickering IJ, Raskin I (1995a) Mechanisms of Cd mobility and accumulation in Indian mustard. Plant Physiol 109:427–433Google Scholar
  112. Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley BD, Chet I, Raskin I (1995b) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474PubMedGoogle Scholar
  113. Samantaray S, Rout GR, Das P (1999) Studies on differential tolerance of mungbean cultivars to metalliferous mine wastes. Agribiol Res 52:193–201Google Scholar
  114. Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants—a review. Environ Exp Bot 41:105–130Google Scholar
  115. Seregin L, Kozhevnikova A (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277Google Scholar
  116. Seuntjens P, Nowack B, Schulin R (2004) Root-zone modeling of heavy metal uptake and leaching in the presence of organic ligands. Plant Soil 265:61–73Google Scholar
  117. Shainberg O, Rubin B, Rabinowitch HD, Tel-Or E (2001) Loading beans with sublethal levels of copper enhances conditioning to oxidative stress. J Plant Physiol 158:1415–1421Google Scholar
  118. Shalaby AM, Al-Wakeel SAM (1995) Changes in nitrogen metabolism enzyme activities of Vicia faba in response to aluminum and cadmium. Biol Plant 37:101–106Google Scholar
  119. Shamsi IH, Wei K, Zhang GP, Jilani GH, Hassan MJ (2008) Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean. Biol Plant 52:165–169Google Scholar
  120. Shanker AK (2003) Physiological, biochemical and molecular aspects of chromium toxicity and tolerance in selected crops and tree species. Ph.D. Thesis, Tamil Nadu Agricultural University, Coimbatore, IndiaGoogle Scholar
  121. Shanker AK, Sudhagar R, Pathmanabhan G (2003) 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 Delhi, IndiaGoogle Scholar
  122. Sharma DC, Sharma CP (2003) Chromium uptake and toxicity effects on growth and metabolic activities in wheat, Triticum aestivum. Indian J Exp Biol 34:689–691Google Scholar
  123. Sharma J, Subhadra AV (2010) The effect of mercury on nitrate reductase activity in bean leaf segments (Phaseolus vulgaris) and its chelation by phytochelatin synthesis. Life Sci Med Res 2010: 1–8, LSMR-13. E-ISSN: 19487886.
  124. Shaw BP, Rout NP (2002) Mercury and cadmium induced changes in the level of praline and the activity of praline biosynthesizing enzymes in Phaseolus aureus Roxb. and Triticum aestivum L. Biol Plant 45:267–271Google Scholar
  125. Sheoran IS, Aggarwala N, Singh R (1990) Effect of cadmium and nickel on in vitro carbon dioxide exchange rate of pigeon pea (Cajanus cajan L.). Plant Soil 129:243–249Google Scholar
  126. Shewfelt RI, Erickson MC (1991) Role of lipid peroxidation in the mechanism of membrane associated disorders in edible plant tissue. Trends Food Sci Technol 2:152–154Google Scholar
  127. Smiri M (2011) Effect of cadmium on germination, growth, redox and oxidative properties in Pisum sativum seeds. J Environ Chem Ecotoxicol 3:52–59Google Scholar
  128. Sobolev D, Begonia MFT (2008) Effects of heavy metal contamination upon soil microbes: lead-induced changes in general and denitrifying microbial communities as evidenced by molecular markers. Int J Environ Res Public Health 5:450–456PubMedGoogle Scholar
  129. Solanki R, Dhankhar R (2011) Biochemical changes and adaptive strategies of plants under heavy metal stress. Biologia 66:195–204Google Scholar
  130. Stimpfl E, Aichner M, Cassar A, Thaler C, Andreaus O, Matteazzi A (2006) The state of fruit orchard soils in South Tyrol (Italy). Laimburg J 3:74–134Google Scholar
  131. Stobrawa K, Lorenc-Plucińska G (2008) Thresholds of heavy-metal toxicity in cuttings of European black poplar (Populus nigra L.) determined according to antioxidant status of fine roots and morphometrical disorders. Sci Total Environ 390:86–96PubMedGoogle Scholar
  132. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336PubMedGoogle Scholar
  133. Suciu I, Cosma C, Todica M, Bolboaca SD, Jantschi L (2008) Analysis of soil heavy metal pollution and pattern in Central Transylvania. Int J Mol Sci 9:434–453PubMedGoogle Scholar
  134. Talanova VV, Titov AF, Boeva NP (2000) Effect of increasing concentrations of lead and cadmium on cucumber seedlings. Biol Plant 43:441–444Google Scholar
  135. Talukdar D (2011) Effect of arsenic-induced toxicity on morphological traits of Trigonella foenum-graecum L. and Lathyrus sativus L. during germination and early seedling growth. Curr Res J Biol Sci 3:116–123Google Scholar
  136. Thomas DJ, Avenson TJ, Thomas JB, Herbert SK (1998) A cyanobacterium lacking iron superoxide dismutase is sensitized to oxidative stress induced with methyl viologen but not sensitized to oxidative stress induced with norflurazon. Plant Physiol 116:1593–1602PubMedGoogle Scholar
  137. Tripathi AK, Sadhna T, Tripathi S (1999) Changes in some physiological and biochemical characters in Albizia lebbek as bio-indicators of heavy metal toxicity. J Environ Biol 20:93–98Google Scholar
  138. Tyler G, Pahlsson AM, Bengtsson G, Baath E, Tranvik L (1989) Heavy metal ecology and terrestrial plants, microorganisms and invertebrates: a review. Water Air Soil Pollut 47:189–215Google Scholar
  139. Upadhyay RK, Panda SK (2009) Copper-induced growth inhibition, oxidative stress and ultrastructural alterations in freshly grown water lettuce (Pistia stratiotes L.). CR Biol 332:623–632Google Scholar
  140. Ureta A, Imperial J, Ruiz-Argueso T, Palacios JM (2005) Rhizobium leguminosarum Biovar viciae symbiotic hydrogenase activity and processing are limited by the level of nickel in agricultural soils. Appl Environ Microbiol 71:7603–7606PubMedGoogle Scholar
  141. Vaalgamaa S, Conley DJ (2008) Detecting environmental change in estuaries: nutrient and heavy metal distributions in sediment cores in estuaries from the Gulf of Finland, Baltic Sea. Estuar Coast Shelf Sci 76(1):45–56Google Scholar
  142. Vajpayee P, Sharma SC, Tripathi RD, Rai UN, Yunus M (1999) Bioaccumulation of chromium and toxicity to photosynthetic pigments, nitrate reductase activity and protein content of Nelumbo nucifera Gaertn. Chemosphere 39:2159–2169Google Scholar
  143. Vajpayee P, Tripathi RD, Rai UN, Ali MB, Singh SN (2000) Chromium (VI) accumulation reduces chlorophyll biosynthesis, nitrate reductase activity and protein content in Nymphaea alba L. Chemosphere 41:1075–1082PubMedGoogle Scholar
  144. Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206Google Scholar
  145. Van Staden J, Davey J, Brown NAC (1982) Endogenous cytokinins in seed development and germination. In: Khan AA (ed) The physiology and biochemistry of seed development, dormancy and germination. Elsevier Biomed, Amsterdam, pp 137–156Google Scholar
  146. Vassilev A, Berova M, Zlatev Z (1998) Influence of Cd on growth, chlorophyll content and water relations in young barley plants. BioI Plant 41:601–606Google Scholar
  147. Vazques MD, Poschenrieder CH, Barcelo J (1987) Chromium (VI) induced structural changes in bush bean plants. Ann Bot 59:427–38Google Scholar
  148. Verkleij JAC, Schat H (1990) Mechanisms of metal tolerance in higher plants. In: Shaw J (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC, Boca Raton, pp 179–193Google Scholar
  149. Vijayaragavan M, Prabhahar C, Sureshkumar J, Natarajan A, Vijayarengan P, Sharavanan S (2011) Toxic effect of cadmium on seed germination, growth and biochemical contents of cowpea (Vigna unguiculata L.) plants. Int Multidisciplinary Res J 1(5):01–06Google Scholar
  150. Wang QR, Liu XM, Cui YS, Dong YT, Christie P (2002) Responses of legume and non-legume crop species to heavy metals in soils with multiple metal contamination. J Environ Sci Health A Tox Hazard Subst Environ Eng 37:611–621PubMedGoogle Scholar
  151. Wani PA, Khan MS, Zaidi A (2008a) Effect of heavy metal toxicity on growth, symbiosis, seed yield and metal uptake in pea grown in metal amended soil. Bull Environ Contam Toxicol 81:152–158PubMedGoogle Scholar
  152. Wani PA, Khan MS, Zaidi A (2008b) Effect of metal tolerant plant growth promoting Rhizobium on the performance of pea grown in metal amended soil. Arch Environ Contam Toxicol 55:33–42PubMedGoogle Scholar
  153. Weckx JEJ, Clijsters HMM (1996) Oxidative damage and defense mechanisms in primary leaves of Phasolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol Plant 96:506–512Google Scholar
  154. Weigel HJ (1985) Inhibition of photosynthetic reactions of isolated intact chloroplast by cadmium. J Plant Physiol 119:179–189Google Scholar
  155. Wierzbicka M, Obidzinska J (1998) The effect of lead on seed imbibition and germination in different plant species. Plant Sci 137:155–171Google Scholar
  156. Wozny A, Zatorska BF, Mlodzianowski F (1982) Influence of lead on the development of lupin seedlings and ultrastructural localization of this metal in the roots. Acta Soc Bot Pol 51:345–351Google Scholar
  157. Xiong ZT (1997) Bioaccumulation and physiological effects of excess lead in a roadside pioneer species Sonchus oleraceus L. Environ Pollut 97:275–279PubMedGoogle Scholar
  158. Xiong ZT (1998) Lead uptake and effects on seed germination and plant growth in a Pb hyperaccumulator Brassica pekinensis Rupr. Bull Environ Contam Toxicol 60:285–291PubMedGoogle Scholar
  159. Yang MG, Lin XY, Yang XE (1998) Effect of Cd on growth and nutrient accumulation of different plant species. Chin J Appl Ecol 19:89–94Google Scholar
  160. Yang Y, Chen YX, Tian GM, Zhang ZJ (2005) Microbial activity related to N cycling in the rhizosphere of maize stressed by heavy metals. J Environ Sci (China) 17:448–451Google Scholar
  161. Yangye C (2005) Effects of heavy metals on ammonification, nitrification and denitrification in maize rhizosphere. Pedosphere 11:115–122Google Scholar
  162. Yurekli F, Porgali ZB (2006) The effects of excessive exposure to copper in bean plants. Acta Biol Cracoviensia Ser Bot 48(2):7–13Google Scholar
  163. Zaccheo P, Genevini PL, Cocucci S (1982) Chromium ions toxicity on the membrane transport mechanism in segments of maize seedling roots. J Plant Nutr 5:1217–1227Google Scholar
  164. Zaccheo P, Cocucci M, Cocucci S (1985) Effects of Cr on proton extrusion, potassium uptake and transmembrane electric potential in maize root segments. Plant Cell Environ 8:721–726Google Scholar
  165. Zeid IM (2001) Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol Plant 44:111–115Google Scholar
  166. Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50PubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2012

Authors and Affiliations

  • Parvaze Ahmad Wani
    • 1
  • Mohammad Saghir Khan
    • 2
  • Almas Zaidi
    • 3
  1. 1.Department of Biological Sciences, College of Natural and Applied SciencesCrescent UniversityAbeokutaNigeria
  2. 2.Department of Agricultural Microbiology, Faculty of Agricultural SciencesAligarh Muslim UniversityAligarhIndia
  3. 3.Department of Agricultural Microbiology, Faculty of Agricultural SciencesAligarh Muslim UniversityAligarhIndia

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