Heavy Metal Toxicity and Antioxidative Response in Plants: An Overview

  • Shumailah Ishtiyaq
  • Harsh Kumar
  • Mayank Varun
  • Bhumesh Kumar
  • Manoj S. Paul


Environmental pollution caused by heavy metals has received worldwide attention. The intractable and pertinacious nature of heavy metals leads to severe threat to environment, and affects the life of both plants and animals, causing serious diseases in humans. Heavy metal toxicity in plants cause imbalances in the redox metabolism that leads to oxidative damage which is characterized by enhanced production of reactive oxygen species (ROS). To minimize the deleterious consequences of ROS, plants in general have developed biological detoxification and defense mechanisms that protect the cellular components from being oxidized. Antioxidative defense activity of plants is composed of enzymatic scavengers such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR) and guaiacol peroxidase (GPX) and non-enzymatic components like ascorbic acid (AA), α-tocopherol, carotenoids, flavonoids and proline that plays the most crucial and effective role in detoxifying ROS and the changes in their activity is often used to predict metal tolerance. In this chapter, the current state of knowledge about the role of ROS, defense mechanisms and adaptation strategies of plants with special reference to antioxidative defense system to alleviate heavy metal toxicity is discussed. Recent researches have thrown ample lights on how enzymatic and non-enzymatic machinery of plants can protect, regulate and integrate cell responses to heavy metal stress.


Antioxidant defense Oxidative stress Reactive oxygen species Secondary metabolism Metal chelation Glutathione Phytoremediation 



Financial support from University Grants Commission [UGC-MRP – F. No. 43-100/2014(SR)] is gratefully acknowledged. We gratefully acknowledge the University Grants Commission for providing financial support by sanctioning the Post Doctoral Fellowship (F./PDFSS-2014-15-SC-UTT-8854) to Mayank Varun.


  1. Adriano DC (2003) Trace elements in terrestrial environments: biogeochemistry, bioavailability and risks of metals, 2nd edn. Springer, New York, pp 1–6Google Scholar
  2. Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants location and functional significance. Plant Sci 196:67–76PubMedCrossRefPubMedCentralGoogle Scholar
  3. Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defences. Free Radic Biol Med 23:473–479PubMedCrossRefPubMedCentralGoogle Scholar
  4. Alloway BJ, Ayres DC (1997) Chemical principles of environmental pollution, 2nd edn. CRC Press, London, p 395Google Scholar
  5. Aravind P, Prasad MNV (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L: a free-floating freshwater macrophyte. Plant Physiol Biochem 41:391–397Google Scholar
  6. Arisi ACM, Mocquot B, Mench M, Foyer CH, Jouanian L (2000) Responses to cadmium in leaves of transformed poplars overexpressing γ-glutamylcysteine synthetase. Physiol Plant 109:143–149CrossRefGoogle Scholar
  7. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedCrossRefPubMedCentralGoogle Scholar
  8. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedPubMedCentralCrossRefGoogle Scholar
  9. Axtell NR, Sternberg PKS, Claussen K (2003) Lead and nickel removal using Microspora and Lemna minor. Bioresour Technol 89:41–48PubMedCrossRefPubMedCentralGoogle Scholar
  10. Badiye A, Kapoor N, Khajuria H (2013) Copper toxicity: a comprehensive study. Res J Recent Sci 2:58–67Google Scholar
  11. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements- a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  12. Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Raton, pp 85–108Google Scholar
  13. Balestrasse KB, Gardey L, Gallego SM, Tomaro ML (2001) Response of antioxidant defence system in soybean nodules and roots subjected to cadmium stress. Aust J Plant Physiol 28:497–504Google Scholar
  14. Barcelo J, Poschenrieder C, Andreu I, Gunse B (1986) Cadmium induced decrease of water stress resistance in bush bean plants (Phaseolus vulgaris L. cv. Contender) I. Effect of Cd on water potential, relative water content, and cell wall elasticity. J Plant Physiol 125:17–25CrossRefGoogle Scholar
  15. Barnes J, Zheng Y, Lyons T (2002) Plant resistance to zone: the role of ascorbate. In: Omasa KH, Saji S, Youssefian N (eds) Air pollution and plant biotechnology – prospects for phytomonitoring and phytoremediation. Springer, Tokyo, pp 235–252Google Scholar
  16. Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brasica napus) grown on cadmium polluted soil: cause and consequences for photosynthesis and growth. Planta 212:696–709PubMedCrossRefPubMedCentralGoogle Scholar
  17. Baszynski T, Wajda L, Krol M, Wolinska D, Krupa A, Tuken–Dorf (1980) Photosynthetic activities of cadmium–treated tomato plants. Physiol Plant 48:365–370CrossRefGoogle Scholar
  18. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plant. Curr Sci 89:1113–1121Google Scholar
  19. 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
  20. Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31(3):860–865CrossRefGoogle Scholar
  21. Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Plant 138:447–462PubMedCrossRefPubMedCentralGoogle Scholar
  22. Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116CrossRefGoogle Scholar
  23. Cai-lin GE, Yang X, Yang J (2003) Effect of heavy metal stress on different rice varieties of superoxide dismutase. Acta Agric Nucleatae Sin 17(4):286–291Google Scholar
  24. Chaney RL, Angle JS, Li YM, Baker AJM (1999) Method for phytomining of nickel, cobalt and other metals from soil. US Patent 5,944,872, 27 JanGoogle Scholar
  25. Chang TC, You SJ, Yu BS, Chen CM, Chiu YC (2009) Treating high-mercury-containing lamps using fullscale thermal desorption technology. J Hazard Mater 162:967–972PubMedCrossRefPubMedCentralGoogle Scholar
  26. Che D, Meagher R, Heaton ACP, Lima A, Rugh CL, Merkle SA (2003) Expression of mercuric ion reductase in Eastern cottonwood (Populus deltoides) confers mercuric ion reduction and resistance. Plant Biotechnol J 1:311–319PubMedCrossRefPubMedCentralGoogle Scholar
  27. Chen HM, Zeng CR, Tu C, Shen ZG (2000) Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41:229–234PubMedCrossRefPubMedCentralGoogle Scholar
  28. Cho U, Seo N (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120CrossRefGoogle Scholar
  29. Cleland RE, Grace SC (1999) Voltammetric detection of superoxide production by photosystem II. FEBS Lett 457:348–352PubMedCrossRefPubMedCentralGoogle Scholar
  30. Corpas FJ, Barroso JB, del Río LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145–150PubMedCrossRefGoogle Scholar
  31. Cosio C, Martinoia E, Keller C (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiol 134:716–725PubMedPubMedCentralCrossRefGoogle Scholar
  32. D’Souza R, Varun M, Pratas J, Paul MS (2013) Spatial distribution of heavy metals in soil and flora associated with the glass industry in North Central India: implications for phytoremediation. Soil Sediment Contam 22:1–20CrossRefGoogle Scholar
  33. Davis LC, Castro-Diaz S, Zhang Q, Erickson LE (2002) Benefits of vegetation for soils with organic contaminants. Crit Rev Plant Sci 21:457–491CrossRefGoogle Scholar
  34. del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335PubMedPubMedCentralCrossRefGoogle Scholar
  35. Demirevska-Kepova K, Simova-Stoilova L, Stoyanova ZP, Feller U (2006) Cadmium stress in barley: growth, leaf pigment, and protein composition and detoxification of reactive oxygen species. J Plant Nutr 29:451–468CrossRefGoogle Scholar
  36. Djingova R, Kuleff I (2000) Instrumental techniques for trace analysis. In: Vernet JP (ed) Trace elements: their distribution and effects in the environment. Elsevier, LondonGoogle Scholar
  37. Dursun K, Elmastaş M, Ozturk L, Kayır O (2016) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59:813–820CrossRefGoogle Scholar
  38. Ebinghaus R, Tripathi RM, Wallschläger LSE (1999) Natural and anthropogenic mercury sources and their impact on the air-surface exchange of mercury on regional and global scales. In: Ebinghaus R, Turner RR, Lacerda LD, Vasiliev O, Salomons W (eds) Mercury contaminated sites: characterization, risk assessment and remediation. Springer, New YorkCrossRefGoogle Scholar
  39. Eick MJ, Peak JD, Brady PV, Pasak JD (1999) Kinetics of lead absorption and desorption on goethite: residence time effect. Soil Sci 164:28–39CrossRefGoogle Scholar
  40. Elinder CG (1985) Cadmium: uses, occurrence, and intake. In: Friberg L, Elinder CG, Kjellstrom T (eds) Cadmium and health: a toxicological and epidemiological appraisal. CRC Press, Boca Raton, pp 24–63Google Scholar
  41. Elstner EF (1991) Mechanism of oxygen activation in different compartments. In: Pell EJ, Steffen KL (eds) Active oxygen/oxidative stress and plant metabolism. American Socienty of Plant Physiologists, Roseville, pp 13–25Google Scholar
  42. EPA (2004) National priorities list for Smalley-Piper. US Environmental Protection Agency, Collierville Google Scholar
  43. Falandysz J, Lipka K, Kawano M, Brzostowski A, Dadej M, Jedrusiak A, Puzyn T (2003) Mercury content and its bioconcentration factors in wild mushrooms at Lukta and Morag, northeastern Poland. J Agric Food Chem 51:2832–2836PubMedCrossRefPubMedCentralGoogle Scholar
  44. Fini A, Brunettii C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress induced Flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6:709–771PubMedPubMedCentralCrossRefGoogle Scholar
  45. Fontes RLF, Cox FR (1995) Effects of sulfur supply on soybean plants exposed to zinc toxicity. J Plant Nutr 18:1893–1906CrossRefGoogle Scholar
  46. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedPubMedCentralCrossRefGoogle Scholar
  47. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254CrossRefGoogle Scholar
  48. Francesconi K, Visoottiviseth P, Sridokchan W, Goessler W (2002) Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic contaminated soils. Sci Total Environ 284:27–35PubMedCrossRefPubMedCentralGoogle Scholar
  49. Gardea-Torresdey JL, Peralta-Videa JR, Rosa GD, Parsons JG (2005) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Environ Health Perspect 249:1797–1810Google Scholar
  50. Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:8–96CrossRefGoogle Scholar
  51. Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  52. Gumaelius L, Lahner B, Salt DE, Banks JA (2004) Arsenic hyperaccumulation in gametophytes of Pteris vittata. A new model system for analysis of arsenic hyperaccumulation. Plant Physiol 36:3198–3208CrossRefGoogle Scholar
  53. Guo T, Zhang G, Zhou M, Wu F, Chen J (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258:241–248CrossRefGoogle Scholar
  54. Gupta AS, Heinen JL, Holaday AS, Burke JJ, Allen RD (1993) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci U S A 90:1629–1633PubMedPubMedCentralCrossRefGoogle Scholar
  55. Haag-Kerwer A, Schafer HJ, Heiss S, Walter C, Rausch T (1999) Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. J Exp Bot 50:1827–1835CrossRefGoogle Scholar
  56. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322PubMedPubMedCentralCrossRefGoogle Scholar
  57. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Clarendon Press, OxfordGoogle Scholar
  58. Hambidge KM, Krebs NF (2007) Zinc deficiency: a special challenge. J Nutr 137:1101–1107PubMedCrossRefPubMedCentralGoogle Scholar
  59. Harinasut P, Poonsopa D, Roengmongkol K, Charoensataporn R (2003) Salinity effects on antioxidant enzymes in mulberry cultivar. Sci Asia 29:109–113CrossRefGoogle Scholar
  60. Hasan SA, Hayat S, Ali B, Ahmad A (2008) 28-homobrassinolide protects chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidants. Environ Pollut 151:60–66PubMedCrossRefPubMedCentralGoogle Scholar
  61. Heyno E, Mary V, Schopfer P, Krieger-Liszkay A (2011) Oxygen activation at the plasma membrane: relation between superoxide and hydroxyl radical production by isolated membranes. Planta 234:35–45PubMedCrossRefPubMedCentralGoogle Scholar
  62. Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. J Plant Growth Regul 42:227–238CrossRefGoogle Scholar
  63. Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147:806–816PubMedCrossRefPubMedCentralGoogle Scholar
  64. Jackson C, Dench J, Moore AL, Halliwell B, Foyer CH, Hall DO (1978) Subcellular localisation and identification of superoxide dismutase in the leaves of higher plants. Eur J Biochem 91:339–344PubMedCrossRefPubMedCentralGoogle Scholar
  65. Jadia CD, Fulekar MH (1999) Phytoremediation of heavy metals: recent techniques. Afr J Biotechnol l8:921–928Google Scholar
  66. Janas KM, Amarowicz R, Zielinska-Tomaszewska J, Kosinśka A, Posmyk MM (2009) Induction of phenolic compounds in two dark-grown lentil cultivars with different tolerance to copper ions. Acta Physiol Plant 31:587–595CrossRefGoogle Scholar
  67. Kabata-Pendias A (2001) Trace elements in soils and plants. CRC Press, Boca RatonGoogle Scholar
  68. Kacabova P, Natr L (1986) Effect of Pb on growth characteristics and chlorophyll content in barley seedlings. Phosynthetica 20:411–417Google Scholar
  69. Kahle H (1993) Response of roots of trees to heavy metals. Environ Exp Bot 33:99–119CrossRefGoogle Scholar
  70. Kamal-Eldin A, Appelqvist LA (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31:671–701PubMedCrossRefPubMedCentralGoogle Scholar
  71. Karuppanapandian T, Moon JC, Kim C, Manoharan K, Kim W (2011) Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust J Crop Sci 5:709–725Google Scholar
  72. Kerkeb L, Kramer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724PubMedPubMedCentralCrossRefGoogle Scholar
  73. Khan NA, Samiullah, Singh S, Naza R (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci 193:435–444CrossRefGoogle Scholar
  74. Khurana N, Chatterjee C (2001) Influence of variable zinc on yield, seed oil content, and physiology of sunflower. Soil Sci Plant Ann 32:3023–3030CrossRefGoogle Scholar
  75. Krieger-Liszkay (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346PubMedCrossRefPubMedCentralGoogle Scholar
  76. Leon AM, Palma JM, Corpas FJ, Gomez M, Romero-Puertas MC, Chatterjee D, Mateos RM, del Rio LA, Sandalio LM (2002) Antioxidant enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40:813–820CrossRefGoogle Scholar
  77. Li Y, Song Y, Shi G, Wang J, Hou X (2009) Response of antioxidant activity to excess copper in two cultivars of Brassica campestris ssp. chinensis Makino. Acta Physiol Plant 31:55–162CrossRefGoogle Scholar
  78. Liao S, Chang N (2004) Heavy metal phytoremediation by water hyacinth at constructed wetlands in Taiwan. J Aquat Plant Manag 42:60–68Google Scholar
  79. Lösch R (2004) Plant mitochondrial respiration under the influence of heavy metals. In: Prasad MNV (ed) Heavy metal stress in plants from biomolecules to ecosystems, 2nd edn. Springer, Berlin, pp 182–200CrossRefGoogle Scholar
  80. Marschner H (1995) Mineral nutrition of higher plants. Academic, London, pp 24–28Google Scholar
  81. Massa N, Andreucci F, Poli M, Aceto M, Barbato R, Berta G (2010) Screening for heavy metal accumulators amongst autochthonous plants in a polluted site in Italy. Ecotoxicol Environ Saf 73:1988–1997PubMedCrossRefPubMedCentralGoogle Scholar
  82. McArthur J, Ravenscroft P, Safiulla S, Thirlwall MF (2001) Arsenic in groundwater: testing pollution mechanisms for sedimentary aquifers in Bangladesh. Water Resour Res 37:109–117CrossRefGoogle Scholar
  83. McIntyre T (2003) Phytoremediation of heavy metals from soils. Adv Biochem Eng Biotechnol 78:97–123PubMedPubMedCentralGoogle Scholar
  84. Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178PubMedPubMedCentralGoogle Scholar
  85. Minnich MM, McBride MB, Chaney RL (1987) Copper activity in soil solution. II. Relation to copper accumulation in young snap beans. Soil Sci Soc Am J 51:573–578CrossRefGoogle Scholar
  86. Mitchell RL, Burchett MD, Pulkownik A, McCluskey L (1988) Effects of environmentally hazardous chemicals on the emergence and early growth of selected Australian native plants. Plant Soil 112:195–199CrossRefGoogle Scholar
  87. Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610PubMedCrossRefPubMedCentralGoogle Scholar
  88. Molina AS, Nievas C, Chaca MVP, 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 56:285–295CrossRefGoogle Scholar
  89. Navrot N, Rouhier N, Gelhaye E, Jaquot JP (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant 129:185–195CrossRefGoogle Scholar
  90. Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850PubMedPubMedCentralCrossRefGoogle Scholar
  91. Noctor G, Paepe RD, Foyer CH (2006) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134CrossRefGoogle Scholar
  92. Nouet C, Motte P, Hanikenne M (2011) Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci 16(7):395–404PubMedCrossRefPubMedCentralGoogle Scholar
  93. O’Sullivan JN, Asher CJ, Blamey FPC (1997) Nutrient disorders of sweet potato, ACIAR monograph no. 48. Australian Centre for International Agricultural Research, CanberraGoogle Scholar
  94. Ottabbong E (1989) Chemistry of Cr in some Swedish soil: 2. Fate and impact of added Cr on pH and status of soluble Mn in four soils. Acta Agric Scand 39:131–138CrossRefGoogle Scholar
  95. Paivoke H (1983) The short term effect of Zn on the growth anatomy and acid phosphate activity of pea seedlings. Ann Bot 20:307–309Google Scholar
  96. Palma JM, Corpas FJ, del Rio LA (2009) Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics 9:2301–2312PubMedCrossRefPubMedCentralGoogle Scholar
  97. 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 For Res 13:233–238CrossRefGoogle Scholar
  98. Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographic area. New Phytol 159:421–430CrossRefGoogle Scholar
  99. Pekker I, Tel-or E, Mittler R (2002) Reactive oxygen intermediates and glutathione regulate the expression of cytosolic ascorbate peroxidase during iron mediated oxidative stress in bean. Plant Mol Biol 49:429–438PubMedCrossRefPubMedCentralGoogle Scholar
  100. Pence NS, Larsen PB, Ebbs SD, Letham DL, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960Google Scholar
  101. Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41PubMedCrossRefPubMedCentralGoogle Scholar
  102. Phillips DA (1981) Chemistry and biochemistry of trace metals in biological systems. In: Lepp NW (ed) Effect of heavy metal pollution on plants, vol 1. Applied Science Publishers, LondonGoogle Scholar
  103. Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. Plant Physiol 133:829–837PubMedPubMedCentralCrossRefGoogle Scholar
  104. Poskuta JW, Parys E, Romanovska E (1987) Effects of lead on the gaseous exchange and photosynthetic carbon metabolism of pea seedlings. Acta Bot Soc Poland 57:149–155CrossRefGoogle Scholar
  105. Pulford I, Watson C, McGregor SD (2001) Uptake of chromium by trees: prospects for phytoremediation. Environ Geochem Health 23:307–311CrossRefGoogle Scholar
  106. Racchi ML, Bagnoli F, Balla I, Danti S (2001) Differential activity of catalase and superoxide dismutase in seedlings and in vitro micropropagated oak (Quercus robur L.). Plant Cell Rep 20:169–174CrossRefGoogle Scholar
  107. Radotic K, Ducic T, Mutavdzic D (2000) Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium. Environ Exp Bot 44:105–113PubMedCrossRefPubMedCentralGoogle Scholar
  108. Rasmusson G, Geisler DA, Møller IM (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8:47–60PubMedCrossRefPubMedCentralGoogle Scholar
  109. Ren F, Liu T, Liu H, Hu B (1993) Influence of zinc on the growth, distribution of elements, and metabolism of one-year old American ginseng plants. J Plant Nutr 16:393–405CrossRefGoogle Scholar
  110. Romero MC, Corpas FJ, Rodrıguez-Serrano M, Gomez M, del Rio LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357CrossRefGoogle Scholar
  111. Sahi SV, Bryant NL, Sharma NC, Singh SR (2002) Characterization of a lead hyperaccumulator shrub, Sesbania drummondii. Environ Sci Technol 36:4676–4680PubMedCrossRefPubMedCentralGoogle Scholar
  112. Salim RM, Isa MM, Subu AL, Sayrafi SA, Sayrafi O (1995) Effect of irrigation with lead and cadmium on the growth and metal uptake of cauliflower, spinach and parsley. J Environ Sci Health Part A 30:831–849Google Scholar
  113. Sas-Nowosielska A, Galimska-Stypa R, Kucharski R, Zielonka U, Małkowski E, Gray L (2008) Remediation aspect of microbial changes of plant rhizosphere in mercury contaminated soil. Environ Monit Assess 137:101–109PubMedCrossRefPubMedCentralGoogle Scholar
  114. Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defences. Braz J Med Biol Res 38:995–1014PubMedCrossRefPubMedCentralGoogle Scholar
  115. Senger R, Gautam S, Garg SK, Senger K, Chaudhary R (2009) Lead stress effects on physiobiochemical activities of higher plants. Rev Environ Contam Toxicol 196:1–21Google Scholar
  116. Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753PubMedCrossRefPubMedCentralGoogle Scholar
  117. Sharma S, Adholeya A (2011) Detoxification and accumulation of chromium from tannery effluent and spent chrome effluent by Paecilomyceslilacinus fungi. Int Biodeterior Biodegrad 65:309–317CrossRefGoogle Scholar
  118. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50PubMedCrossRefGoogle Scholar
  119. Sharma P, Dubey RS (2004) Ascorbate peroxidase from rice seedlings properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167:541–550CrossRefGoogle Scholar
  120. Sharma P, Jha AB, Dubey RS (2010) Oxidative stress and antioxidative defense system in plants growing under abiotic stresses. In: Pessarakli M (ed) Handbook of plant and crop stress. CRC Press, Boca Raton, pp 89–138Google Scholar
  121. Sharma P, Ha ABJ, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:217037. CrossRefGoogle Scholar
  122. Shuangxia J, Daniell H (2014) Expression of γ-tocopherol methyltransferase in chloroplasts results in massive proliferation of the inner envelope membrane and decreases susceptibility to salt and metal-induced oxidative stress by reducing reactive oxygen species. Plant Biotechnol J 12:1274–1285CrossRefGoogle Scholar
  123. Shukla V, Dhankar M, Prakash J, Sastry KV (2007) Bioaccumulation of Zn, Cu and Cd in Channa punctatus. J Environ Biol 28:395–397PubMedPubMedCentralGoogle Scholar
  124. Singh S, Khan NA, Nazar R, Anjum NA (2008) Photosynthetic traits and activities of antioxidant enzymes in blackgram (Vigna mungo L. Hepper) under cadmium stress. J Plant Physiol 3:25–32CrossRefGoogle Scholar
  125. Skorzynska PE, Drazkiewicz M, Krupa Z (2004) The activity of the antioxidative system in cadmium-treated Arabidopsis thaliana. Biol Plant 47:71–78CrossRefGoogle Scholar
  126. Skovsen E, Snyder JW, Lambert JD, Ogilby PR (2005) Lifetime and diffusion of singlet oxygen in a cell. J Phys Chem B 109:8570–8573PubMedCrossRefPubMedCentralGoogle Scholar
  127. Srivastava PC, Gupta UC (1996) Trace elements in crop production. Science Publishers, LebanonGoogle Scholar
  128. Srivastava AK, Bhargava P, RaiL C (2005) Salinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolum. World J Microb Biotechnol 22:1291–1298CrossRefGoogle Scholar
  129. Sujatha P, Gupta A (1996) Tannery effluent characteristics and its effects on agriculture. J Ecotoxicol Environ Monit 6:45–48Google Scholar
  130. Sun Q, Yec ZH, Wang XR, Wong MH (2007) Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. J Plant Physiol 164:1489–1498PubMedCrossRefPubMedCentralGoogle Scholar
  131. Tan YF, O'Toole N, Taylor NL, Millar AH (2010) Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol 152:747–761PubMedPubMedCentralCrossRefGoogle Scholar
  132. Tomiyasu T, Kodamatani H, Imura R, Matsuyama A, Miyamoto J, Akagi H, Kocman D, Kotnik J, Fajon V, Horvat M (2017) The dynamics of mercury near Idrija mercury mine, Slovenia: horizontal and vertical distributions of total, methyl, and ethyl mercury concentrations in soils. Chemosphere 184:244–252PubMedCrossRefPubMedCentralGoogle Scholar
  133. Triantaphylids C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968CrossRefGoogle Scholar
  134. Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rend Lincei 19:325–346CrossRefGoogle Scholar
  135. USEPA (2000) A guide to developing and documenting cost estimates during the feasibility study (EPA 540-R-00-002).
  136. Valavanidis A, Vlachogianni T (2010) Metal pollution in ecosystems: ecotoxicology studies and risk assessment in the marine environment. Sci Adv Environ Toxicol Ecotoxicol Issues 1–14Google Scholar
  137. Varun M, D’Souza R, Pratas J, Paul MS (2012) Metal contamination of soils and plants associated with the glass industry in North Central India: prospects of phytoremediation. Environ Sci Pollut Res 19:269–281CrossRefGoogle Scholar
  138. Varun M, Jaggi D, D’Souza R, Paul M, Kumar B (2015) Abutilon indicum L.: a prospective weed for phytoremediation. Environ Monit Assess 187(8):527. CrossRefPubMedPubMedCentralGoogle Scholar
  139. Vogel-Mikus K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242PubMedCrossRefPubMedCentralGoogle Scholar
  140. Wang J, Zhao F, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561PubMedPubMedCentralCrossRefGoogle Scholar
  141. Wei CY, Chen TB (2006) Arsenic accumulation by two brake ferns growing on an arsenic mine and their potential in phytoremediation. Chemosphere 63:1048–1053PubMedCrossRefPubMedCentralGoogle Scholar
  142. Xie F, Wang H, Wang H (2009) Effects of arsenic on activities of antioxidant enzymes in the fronds of plants with different abilities to accumulate arsenic. J Agro-Environ Sci 28(7):1379–1385Google Scholar
  143. Yan Y, Jian-Ping L, Xue-Hong Z (2008) Response of hyperaccumulator Leersia hexandra Swartz. to chromium-induced oxidative stress. Ecol Environ 17(4):1476–1482Google Scholar
  144. Yan L, Liuke-Hui, Yu F (2011) Effects of manganesee on enzymatic and non-enzymatic antioxidative defenses of the hyperaccumulate Ploygonum pubescens Blume. J Agro-Environ Sci 30:2422–2427Google Scholar
  145. Yang XE, Long XX, Ni WZ, Ye ZQ, He ZL, Stoffella PJ, Calvert D (2002) Assessing copper thresholds for phytotoxicity and potential dietary toxicity in selected vegetable crops. J Environ Sci Health 37:625–635CrossRefGoogle Scholar
  146. Yang G, Liang M, Zhou P (2010) Antioxidative defense system differences among four plants under combined Pb and Cd stress. Chin J Eco-Agric 18(4):836–842CrossRefGoogle Scholar
  147. Zavoda J, Cutright T, Szpak J, Fallon E (2001) Uptake, selectivity, and inhibition of hydroponic treatment of contaminants. J Environ Eng 127:502–508CrossRefGoogle Scholar
  148. Zhao F, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514CrossRefGoogle Scholar
  149. 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
  150. Zhu Q, Xia H (2012) Effects of lead stress on antioxidant enzyme system and chlorophyll content of Pteris vittata. Guizhou Agric Sci 40:56–58Google Scholar
  151. Zhu YL, Zayed AM, Quian JH, D’souza M, Terry N (1999) Phytoaccumulation of trace elements by wetland plants: II. Water hyacinth. J Environ Qual 28:339–344CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Shumailah Ishtiyaq
    • 1
  • Harsh Kumar
    • 1
  • Mayank Varun
    • 1
  • Bhumesh Kumar
    • 2
  • Manoj S. Paul
    • 1
  1. 1.Department of BotanySt. John’s CollegeAgraIndia
  2. 2.ICAR - Indian Institute of Wheat and Barley ResearchKarnalIndia

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