Heavy Metal-Induced Oxidative Stress in Plants: Response of the Antioxidative System

  • Ivna ŠtolfaEmail author
  • Tanja Žuna Pfeiffer
  • Dubravka Špoljarić
  • Tihana Teklić
  • Zdenko Lončarić


Heavy metals (HMs) are among the most important environmental pollutants, particularly in areas with strong anthropogenic pressure. For plants, high levels of HMs are extremely toxic since they may act in several different modes: by the direct inhibition of plant growth and biosynthetic pathways or through the production of reactive oxygen species (ROS). Certain metals generate ROS due to their involvement in redox reactions like Fenton and/or Haber–Weiss reactions, while metals without redox capacity enhance ROS production by reducing the antioxidant glutathione pool, activating calcium-dependent systems and influencing iron-mediated processes. ROS production affects lipids, proteins, and DNA and consequently leads to cell death. In response, plants are equipped with complex enzymatic and nonenzymatic mechanisms involved in antioxidative defense to neutralize HM toxicity, and the main components of these mechanisms will be reviewed in this chapter.


Heavy metals ROS Antioxidants 


  1. Agrawal SB, Mishra S (2009) Effects of supplemental ultraviolet-B and cadmium on growth, antioxidants and yield of Pisum sativum L. Ecotoxicol Environ Saf 72:610–618PubMedCrossRefGoogle Scholar
  2. Agrawal SB, Agrawal M, Lee EH, Kramer GF, Pillai P (1992) Changes in polyamine and glutathione contents of a green algae, Chlorogonium elongatum (Dang) France exposed to mercur. Environ Exp Bot 32:145–151CrossRefGoogle Scholar
  3. Ahamad ZH, Shuhanija SN (2013) Physiological and biochemical responses of a Malaysian red alga, Gracilaria manilaensis treated with copper, lead and mercury. J Environ Res Dev 7:1246–1253Google Scholar
  4. Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173CrossRefGoogle Scholar
  5. Ahn YO, Kim SH, Lee J, Kim HR, Lee HS, Kwak SS (2012) Three Brassica rapa metallothionein genes are differentially regulated under various stress conditions. Mol Biol Rep 39:2059–2067PubMedCrossRefGoogle Scholar
  6. Akinci IE, Akinci S (2010) Effect of chromium toxicity on germination and early seedling growth in melon (Cucumis melo L.). Afr J Biotechnol 9:4589–4594Google Scholar
  7. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881PubMedCrossRefGoogle Scholar
  8. Alloway BJ (2013) Sources of heavy metals and metalloids in soils. In: Alloway BJ (ed) Heavy metals in soils, trace metals and metalloids in soils and their bioavailability. Springer, LondonGoogle Scholar
  9. Alloway BJ, Steinnes E (1999) Anthropogenic additions of cadmium to soils. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants, Developments in plants and soils sciences. Kluwer, DordrechtGoogle Scholar
  10. Alrawiq N, Khairiah J, Talib ML, Ismail BS, Anizan I (2014) Accumulation and translocation of heavy metals in soil and paddy plant samples collected from rice fields irrigated with recycled and non-recycled water in MADA Kedah, Malaysia. Int J ChemTech Res 6:2347–2356Google Scholar
  11. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341PubMedCrossRefGoogle Scholar
  12. Amin H, Arain BA, Amin F, Surhio MA (2013) Phytotoxicity of chromium on germination, growth and biochemical attributes of Hibiscus esculentus L. Am J Plant Sci 4:2431–2439CrossRefGoogle Scholar
  13. Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC, Pereira E, Ahmad I, Tuteja R, Tuteja N (2014) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 251:1265–1283PubMedCrossRefGoogle Scholar
  14. Aravind P, Prasad MNV (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116PubMedCrossRefGoogle Scholar
  15. Arunakumara KKIU, Zhang X (2007) Effect of Pb2+ on phycobiliprotein content of Spirulina platensis, an edible cyanobacterium. Trop Agric Res 19:150–159Google Scholar
  16. Arunakumara KKIU, Zhang X (2008) Heavy metal bioaccumulation and toxicity with special reference to microalgae. J Ocean Univ Chin 7:25–30Google Scholar
  17. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  18. Baccouch S, Chaoui A, El Ferjani E (1998) Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots. Plant Physiol Biochem 36:689–694CrossRefGoogle Scholar
  19. Bah AM, Dai H, Zhao J, Sun H, Cao F, Zhang G, Wu F (2011) Effects of cadmium, chromium and lead on growth, metal uptake and antioxidative capacity in Typha angustifolia. Biol Trace Elem Res 142:77–92PubMedCrossRefGoogle Scholar
  20. Balakrishnan CP, Narayanan CS (2007) Phytotoxicity of heavy metals nickel and lead on the cyanobacterial pigments. Seaweed Res Util 29:217–226Google Scholar
  21. Barondeau DP, Kassmann CJ, Bruns CK, Tainer JA, Getzoff ED (2004) Nickel superoxide dismutase structure and mechanism. Biochemistry 43:8038–8047PubMedCrossRefGoogle Scholar
  22. Bestwick CS, Al A, Puri N, Mansfield JW (2001) Characterization of lipid peroxidation and changes to pro- and antioxidant enzyme activities during the hypersensitive reaction in lettuce (Lactuca sativa L.). Plant Sci 161:497–506CrossRefGoogle Scholar
  23. Bharwana SA, Ali S, Farooq MA, Abbas F, Iqbal N, Ahmad MSA, Shakoor MB (2013) Influence of lead stress on growth, photosynthesis and lead uptake in the seedlings of cotton. Int J Agron Plant Prod 4:2492–2501Google Scholar
  24. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:1115–1121Google Scholar
  25. Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol 156:205–215CrossRefGoogle Scholar
  26. Brunetti C, Di Ferdinando M, Fini A, Pollastri S, Tattini M (2013) Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. Int J Mol Sci 14:3540–3555PubMedCentralPubMedCrossRefGoogle Scholar
  27. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Planta 83:463–468CrossRefGoogle Scholar
  28. Cardoso PF, Gratão PL, Gomes-Junior RA, Medici LO, Azevedo RA (2005) Response of Crotalaria juncea to nickel exposure. Braz J Plant Physiol 17:267–272CrossRefGoogle Scholar
  29. Cetin ES, Babalik Z, Hallac-Turk F, Gokturk-Baydar N (2014) The effects of cadmium chloride on secondary metabolite production in Vitis vinifera cv. cell suspension cultures. Biol Res 47:47PubMedCentralPubMedCrossRefGoogle Scholar
  30. Chaudri AM, Allain CM, Barbosa-Jefferson VL, Nicholson FA, Chambers BJ, McGrath SP (2000) A study of the impacts of Zn and Cu on two rhizobial species in soils of a long term field experiment. Plant Soil 22:167–179CrossRefGoogle Scholar
  31. Chen G, Asada K (1992) Inactivation of ascorbate peroxidase by thiols requires hydrogen peroxide. Plant Cell Physiol 33:117–123Google Scholar
  32. Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793PubMedCrossRefGoogle Scholar
  33. Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672PubMedCrossRefGoogle Scholar
  34. Chongpraditnun P, Mori S, Chino M (1992) Excess copper induces a cytosolic Cu, Zn-superoxide dismutase in soybean root. Plant Cell Physiol 33:239–244Google Scholar
  35. Chou TS, Chao YY, Huei Kao C (2012) Involvement of hydrogen peroxide in heat shock- and cadmium-induced expression of ascorbate peroxidase and glutathione reductase in leaves of rice seedlings. J Plant Physiol 169:478–486PubMedCrossRefGoogle Scholar
  36. Ci D, Jiang D, Dai T, Jing Q, Cao W (2009) Effects of cadmium on plant growth and physiological traits in contrast wheat recombinant inbred lines differing in cadmium tolerance. Chemosphere 77:1620–1625PubMedCrossRefGoogle Scholar
  37. Cobbett CS (2000) Phytochelatins and their role in heavy metal detoxification. Plant Physiol 123:825–832PubMedCentralPubMedCrossRefGoogle Scholar
  38. 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
  39. Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459PubMedCrossRefGoogle Scholar
  40. Creissen GP, Mullineaux PM (1995) Cloning and characterization of glutathione reductase cDNAs and identification of two genes encoding the tobacco enzyme. Planta 197:422–425PubMedCrossRefGoogle Scholar
  41. Cuypers A, Vangronsveld J, Clijsters H (2000) Biphasic effect of copper on the ascorbate-glutathione pathway in primary leaves of Phaseolus vulgaris seedlings during the early stages of metal assimilation. Physiol Planta 110:512–517CrossRefGoogle Scholar
  42. Cuypers A, Vangronsveld J, Clijsters H (2001) The redox status of plant cells (AsA and GSH) is sensitive to zinc imposed oxidative stress in roots and primary leaves of Phaseolus vulgaris. Plant Physiol Biochem 39:657–664CrossRefGoogle Scholar
  43. Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Van Sanden S, Van Belleghem F, Guisez Y, Colpaert J, Vangronsveld J (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168:309–316PubMedCrossRefGoogle Scholar
  44. D’Souza RM, Devaraj VR (2012) Induction of oxidative stress and antioxidative mechanisms in Hyacinth bean under zinc stress. Afr Crop Sci J 20:17–29Google Scholar
  45. Dandan L, Dongmei Z, Peng W, Weng Nanyan W, Xiangdong Z (2011) Subcellular Cd distribution and its correlation with antioxidant enzymatic activities in wheat (Triticum aestivum) roots. Ecotoxicol Environ Saf 74:874–881PubMedCrossRefGoogle Scholar
  46. Das PK, Kar M, Mishra D (1978) Nickel nutrition of plants. 1. Effects of nickel on some oxidase activities during rice (Oryza sativa L.) seed germination. Z Pflanzenphysiol 90:225–233CrossRefGoogle Scholar
  47. Daud MK, Mei L, Variath MT, Ali S, Li C, Rafiq MT, Zhu SJ (2014) Chromium (VI) uptake and tolerance potential in cotton cultivars: effect on their root physiology, ultramorphology, and oxidative metabolism. Bio Med Res Int 2014:1–11CrossRefGoogle Scholar
  48. Davletova S, Rizhsky L, Liang H, Shengqiang D, Oliver D, Coutu J, Shulaev V, Schlauch K, Mittler R (2004) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281PubMedCrossRefGoogle Scholar
  49. De Jesus MD, Tabatabai F, Chapman DJ (1989) Taxonomic distribution of copper-zinc superoxide dismutase in green algae and its phylogenetic importance. J Phycol 25:767–772CrossRefGoogle Scholar
  50. Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603PubMedCrossRefGoogle Scholar
  51. del Río LA, Scandalio LM, Corpas FJ, Palma JM, Barroso JM (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes, production, scavenging, and role in cell signaling. Plant Physiol 141:330–335PubMedCentralPubMedCrossRefGoogle Scholar
  52. Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Hölzer-Feller RU (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266CrossRefGoogle Scholar
  53. Devi Chinmayee M, Anu MS, Mahesh B, Mary Sheeba A, Mini I, Swapna TS (2014) A comparative study of heavy metal accumulation and antioxidant responses in Jatropha curcas L. J Environ Sci Toxicol Food Technol 8:58–67Google Scholar
  54. Dietz KJ, Bair M, Kramer U (1999) Free radical and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants from molecules to ecosystems. Springer, BerlinGoogle Scholar
  55. Dinakar N, Nagajyothi PC, Suresh S, Udaykiran Y, Damodharam T (2008) Phytotoxicity of cadmium on protein, proline and antioxidant enzyme activities in growing Arachis hypogaea L. seedlings. J Environ Sci 20:199–206CrossRefGoogle Scholar
  56. Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1119PubMedCrossRefGoogle Scholar
  57. Duman F (2011) Effects of exogenous glycinebetaine and trehalose on lead accumulation in an aquatic plant (Lemna gibba L.). Int J Phytoremediation 13:492–497PubMedCrossRefGoogle Scholar
  58. Duman F, Ozturk F (2010) Nickel accumulation and its effect on biomass, protein content and antioxidative enzymes in roots and leaves of watercress (Nasturtium officinale R. Br.). J Environ Sci 22:526–532CrossRefGoogle Scholar
  59. Duman F, Aksoy A, Aydin Z, Temizgul R (2011) Effects of exogenous glycinebetaine and trehalose on cadmium accumulation and biological responses of an aquatic plant (Lemna gibba L.). Water Air Soil Pollut 217:545–556CrossRefGoogle Scholar
  60. Ebbs S, Uchil S (2008) Cadmium and zinc induced chlorosis in Indian mustard [Brassica juncea (L.) Czern] involves preferential loss of chlorophyll b. Photosynthetica 46:49–55CrossRefGoogle Scholar
  61. Ekmekçi Y, Tanyolaç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611PubMedCrossRefGoogle Scholar
  62. Fahr M, Laplaze L, Bendaou N, Hocher V, ElMzibri M, Bogusz D, Smouni A (2013) Effects of lead on root growth. Front Plant Sci 4:175PubMedCentralPubMedCrossRefGoogle Scholar
  63. Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61:1549–1566PubMedCrossRefGoogle Scholar
  64. Farid M, Shakoor MB, Ehsan S, Ali S, Zubair M, Hanif MA (2013) Morphological, physiological and biochemical responses of different plant species to Cd stress. Int J Chem Biochem Sci 3:53–60Google Scholar
  65. Fatima RA, Ahmad M (2005) Certain antioxidant enzymes of Allium cepa as biomarkers for the detection of toxic heavy metals in wastewater. Sci Total Environ 346:256–273PubMedCrossRefGoogle Scholar
  66. Fernàndez-Martínez J, Zacchini M, Fernández-Marín B, García-Plazaola JI, Fleck I (2014) Gas-exchange, photo- and antioxidant protection, and metal accumulation in I-214 and Eridano Populus sp. clones subjected to elevated zinc concentrations. Environ Exp Bot 107:144–153CrossRefGoogle Scholar
  67. Filek M, Keskinen R, Hartikainen H, Szarejko I, Janiak A, Miszalski Z, Golda A (2008) The protective role of selenium in rape seedlings subjected to cadmium stress. J Plant Physiol 165:833–844PubMedCrossRefGoogle Scholar
  68. Florence TM, Stauber JL (1986) Toxicity of copper complexes to the marine diatom Nitzschia closterium. Aquat Toxicol 8:11–26CrossRefGoogle Scholar
  69. Fodor F (2002) Physiological responses of vascular plants to heavy metals. In: Prasad MN, Strzalka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer, DordrechtGoogle Scholar
  70. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts. A proposed role in ascorbic acid metabolism. Planta 133:21–25PubMedCrossRefGoogle Scholar
  71. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  72. Franklin NM, Stauber JL, Markich SJ, Lim RP (2000) pH-dependent toxicity of copper and uranium to a tropical freshwater alga (Chlorella sp.). Aquat Toxicol 48:275–289PubMedCrossRefGoogle Scholar
  73. Franklin NM, Adams MS, Stauber JL, Lim RP (2001) Development of a rapid enzyme inhibition bioassay with marine and freshwater microalgae using flow cytometry. Arch Environ Contam Toxicol 40:469–480PubMedCrossRefGoogle Scholar
  74. Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191PubMedCentralPubMedCrossRefGoogle Scholar
  75. Gajewska E, Skłodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Planta 27:329–339CrossRefGoogle Scholar
  76. Gajewska E, Skłodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36PubMedCrossRefGoogle Scholar
  77. Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159CrossRefGoogle Scholar
  78. Gaur JP, Rai LC (2001) Heavy metal tolerance in algae. In: Rai LC, Gaur JP (eds) Algal adaptation to environmental stresses: physiological, biochemical and molecular mechanisms. Springer, BerlinGoogle Scholar
  79. Gichner T, Znidar I, Száková J (2008) Evaluation of DNA damage and mutagenicity induced by lead in tobacco plants. Mutat Res 652:186–190PubMedCrossRefGoogle Scholar
  80. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefGoogle Scholar
  81. Gill SS, Khana NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120PubMedCrossRefGoogle Scholar
  82. Gill SS, Gill R, Anjum NA (2014) Target osmoprotectants for abiotic stress tolerance in crop plants-glycine betaine and proline. In: Anjum NA, Gill SS, Gill R (eds) Plant adaptation to environmental change: significance of amino acids and their derivatives. CAB, Wallingford, CTGoogle Scholar
  83. Gomes-Júnior RA, Moldes CA, Delite FS, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA (2006a) Nickel elicits a fast antioxidant response in Coffea arabica cells. Plant Physiol Biochem 44:420–429PubMedCrossRefGoogle Scholar
  84. Gomes-Júnior RA, Moldes CA, Delite FS, Pompeu GB, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA (2006b) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65:1330–1337PubMedCrossRefGoogle Scholar
  85. Gouveia C, Kreusch M, Schmidt ÉC, Felix MR, Osorio LK, Pereira DT, dos Santos R, Ouriques LC, Martins Rde P, Latini A, Ramlov F, Carvalho TJ, Chow F, Maraschin M, Bouzon ZL (2013) The effects of lead and copper on the cellular architecture and metabolism of the red alga Gracilaria domingensis. Microsc Microanal 19:513–524PubMedCrossRefGoogle Scholar
  86. Grant CA, Buckley WT, Bailey LD, Selles F (1998) Cadmium accumulation in crops. Can J Plant Sci 78:1–17CrossRefGoogle Scholar
  87. Gratão 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
  88. Gratão PL, Pompeu GB, Cardoso PF, Lea PJ, Azevedo RA (2006) Plant antioxidant responses to toxic elements. Curr Top Biochem Res 8:41–70Google Scholar
  89. Greger M (2004) Metal availability, uptake, transport and accumulation in plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems, 2nd edn. Springer, BerlinGoogle Scholar
  90. Grzesiak M, Filek M, Barbasz A, Kreczmer B, Hartikainen H (2013) Relationships between polyamines, ethylene, osmoprotectants and antioxidant enzymes activities in wheat seedlings after short-term PEG- and NaCl-induced stresses. Plant Growth Regul 69:177–189CrossRefGoogle Scholar
  91. Guan LM, Scandalios JG (2000) Hydrogen peroxide-mediated catalase gene expression in response to wounding. Free Radic Biol Med 28:1182–1190PubMedCrossRefGoogle Scholar
  92. Guan LM, Scandalios JG (2002) Catalase gene expression in response to auxin-mediated developmental signals. Physiol Planta 114:288–295CrossRefGoogle Scholar
  93. Guo TR, Zhang GP, Zhang YH (2007) Physiological changes in barley plants under combined toxicity of aluminum, copper and cadmium. Colloids Surf B Biointerfaces 57:182–188PubMedCrossRefGoogle Scholar
  94. Gupta M, Cuypers A, Vangronsveld J, Clijsters H (1999) Copper affects the enzymes of the ascorbate-glutathione cycle and its related metabolites in the roots of Phaseolus vulgaris. Physiol Planta 106:262–267CrossRefGoogle Scholar
  95. Gupta DK, Nicoloso FT, Schetinger M, Rossato L, Pereira LB, Castro G, Srivastava S, Tripathi RD (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172:479–484PubMedCrossRefGoogle Scholar
  96. Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177:437–444PubMedCrossRefGoogle Scholar
  97. Gupta DK, Vandenhove H, Inouhe M (2013) Role of phytochelatins in heavy metal stress and detoxification mechanisms in plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, BerlinCrossRefGoogle Scholar
  98. Gururani MA, Upadhyaya CP, Strasser RJ, Yu JW, Park SW (2013) Evaluation of abiotic stress tolerance in transgenic potato plants with reduced expression of PSII manganese stabilizing protein. Plant Sci 198:7–16PubMedCrossRefGoogle Scholar
  99. Hajimahmoodi M, Ali Faramarzi M, Mohammadi N, Soltani N, Oveisi R, Nastaran M, Nafissi-Varcheh N (2009) Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. J Appl Phycol 22:43–50CrossRefGoogle Scholar
  100. Hao F, Wang X, Chen J (2006) Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci 170:151–158CrossRefGoogle Scholar
  101. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulations in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  102. Hassinen VH, Tervahauta AI, Schat H, Karenlampi SO (2011) Plant metallothioneins—metal chelators with ROS scavenging activity? Plant Biol 13:225–232PubMedCrossRefGoogle Scholar
  103. Hédiji H, Djebali W, Cabasson C, Maucourt M, Baldet P, Bertrand A, Zoghlami LB, Deborde C, Moing A, Brouquisse R, Chaïbi W, Gallusci P (2010) Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotoxicol Environ Saf 73:1965–1974PubMedCrossRefGoogle Scholar
  104. Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093PubMedCrossRefGoogle Scholar
  105. Heidari M, Saran S (2011) Effects of lead and cadmium on seed germination, seedling growth and antioxidant enzymes activities of mustard (Sinapis arvensis L.). J Agric Biol Sci 6:6–11Google Scholar
  106. Hirata T, Tanaka M, Ooike M, Tsunomura T, Sakaguchi M (1999) Radical scavenging activities of phycocyanobilin prepared from a cyanobacterium, Spirulina platensis. Fish Sci 65:971–972Google Scholar
  107. Hirata T, Tanaka M, Ooike M, Tsunomura T, Sakaguchi M (2000) Antioxidant activities of phycocyanobilin prepared from Spirulina platensis. J App Phycol 12:435–439CrossRefGoogle Scholar
  108. Hong Z, Lakkineni K, Zhang Z, Verma DP (2000) Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136PubMedCentralPubMedCrossRefGoogle Scholar
  109. Hou W, Chen X, Song G, Wang Q, Chang CC (2007) Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor). Plant Physiol Biochem 45:62–69PubMedCrossRefGoogle Scholar
  110. Ikenaka Y, Nakayama SMM, Muzandu K, Choongo K, Teraoka H, Mizuno N, Ishizuka M (2010) Heavy metal contamination of soil and sediment in Zambia. Afr J Environ Sci Technol 4:729–739Google Scholar
  111. Ip PF, Chen F (2005) Employment of reactive oxygen species to enhance astaxanthin formation in Chlorella zofingiensis in heterotrophic culture. Process Biochem 40:3491–3496CrossRefGoogle Scholar
  112. Islam MM, Hoque A, Okuma E, Banu NA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycine betaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597PubMedCrossRefGoogle Scholar
  113. Jain RS, Srivastava S, Solomon S, Shrivastava AK, Chandra A (2010) Impact of excess zinc on growth parameters, cell division, nutrient accumulation, photosynthetic pigments and oxidative stress of sugarcane (Saccharum spp.). Acta Physiol Plant 32:979–986CrossRefGoogle Scholar
  114. Janicka-Russak M, Kabala K, Burzyński M, Klobus G (2008) Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots. J Exp Bot 59:3721–3728PubMedCentralPubMedCrossRefGoogle Scholar
  115. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657PubMedCrossRefGoogle Scholar
  116. Karuppanapandian T, Sinha PB, Haniya AMK, Manoharan K (2006) Differential antioxidative responses of ascorbate-glutathione cycle enzymes metabolites to chromium stress in greengram (Vigna radiata L. Wilczek) leaves. J Plant Biol 49:440–447CrossRefGoogle Scholar
  117. Keilig K, Ludwig-Müller J (2009) Effect of flavonoids on heavy metal tolerance in Arabidopsis thaliana seedlings. Bot Stud 50:311–318Google Scholar
  118. Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 12:6894–6918PubMedCentralPubMedCrossRefGoogle Scholar
  119. Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R (2010) Transcriptional control of gene expression by microRNAs. Cell 140:111–122PubMedCrossRefGoogle Scholar
  120. Kováčik J, Babula P, Hedbavny J, Kryštofová O, Provaznik I (2015) Physiology and methodology of chromium toxicity using alga Scenedesmus quadricauda as model object. Chemosphere 120:23–30PubMedCrossRefGoogle Scholar
  121. Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith AC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638CrossRefGoogle Scholar
  122. Kruk J, Holländer-Czytko H, Oettmeier W, Trebst A (2005) Tocopherol as singlet oxygen scavenger in photosystem II. J Plant Physiol 162:749–757PubMedCrossRefGoogle Scholar
  123. Kubiś J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. J Plant Physiol 165:397–406PubMedCrossRefGoogle Scholar
  124. Kumar H, Sharma D, Kumar V (2012) Nickel-induced oxidative stress and role of antioxidant defence in barley roots and leaves. Int J Environ Biol 2:121–128Google Scholar
  125. Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2013) Modulation of antioxidant machinery in α-tocopherol-enriched transgenic Brassica juncea plants tolerant to abiotic stress conditions. Protoplasma 250:1079–1089PubMedCrossRefGoogle Scholar
  126. Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM (2005) A cadmium enzyme from a marine diatom. Nature 435:42PubMedCrossRefGoogle Scholar
  127. Lang M, Zhang Y, Chai T (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158CrossRefGoogle Scholar
  128. Larkum AWD (2003) Light harvesting systems in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, DordrechtCrossRefGoogle Scholar
  129. Lee MY, Shin HW (2003) Cadmium-induced changes in antioxidant enzymes from the marine alga Nannochloropsis oculata. J Appl Phycol 15:13–19CrossRefGoogle Scholar
  130. Leszczyszyn OI, Imam HT, Blindauer CA (2013) Diversity and distribution of plant metallothioneins: a review of structure, properties and functions. Metallomics 5:1146–1169PubMedCrossRefGoogle Scholar
  131. Li D, Zhou D, Wang P, Weng N, Zhu X (2011) Subcellular Cd distribution and its correlation with antioxidant enzymatic activities in wheat (Triticum aestivum) roots. Ecotoxicol Environ Saf 74:874–881CrossRefGoogle Scholar
  132. Li X, Yang Y, Jia L, Chen H, Wei X (2013) Zinc-induced oxidative damage, antioxidant enzyme response and proline metabolism in roots and leaves of wheat plants. Ecotoxicol Environ Saf 89:150–157PubMedCrossRefGoogle Scholar
  133. Liu D, Zou J, Wang M, Jiang W (2008) Hexavalent chromium uptake and its effects on mineral uptake, antioxidant defence system and photosynthesis in Amaranthus viridis L. Bioresour Technol 99:2628–2636PubMedCrossRefGoogle Scholar
  134. Lopez-Millan A, Sagardoy R, Solanas M, Abadia A, Abadia J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. J Environ Exp Bot 65:376–385CrossRefGoogle Scholar
  135. Ma M, Zhu W, Wang Z, Witkaamp GJ (2003) Accumulation, assimilation and growth inhibition of copper on fresh-water alga (Scenedesmus subspicatus 86.81 SAG) in the presence of EDTA and fulvic acid. Aquat Toxicol 63:221–228PubMedCrossRefGoogle Scholar
  136. Malar S, Vikram SS, Favas PJC, Perumal V (2014) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud 55:54CrossRefGoogle Scholar
  137. Malešev D, Kuntić V (2007) Investigation of metal-flavonoid chelates and the determination of flavonoids via metal-flavonoid complexing reactions. J Serb Chem Soc 72:921–939CrossRefGoogle Scholar
  138. Mallick N (2004) Copper-induced oxidative stress in the chlorophycean microalga Chlorella vulgaris: response of the antioxidant system. J Plant Physiol 161:591–597PubMedCrossRefGoogle Scholar
  139. Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193CrossRefGoogle Scholar
  140. Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55:64–69PubMedCrossRefGoogle Scholar
  141. Mallory AC, Bouché N (2008) MicroRNA-directed regulation: to cleave or not to cleave. Trends Plant Sci 13:359–367PubMedCrossRefGoogle Scholar
  142. Mano J (2002) Early events in environmental stresses in plants: induction mechanisms of oxidative stress. In: Inzé D (ed) Oxidative stress in plants. Taylor and Francis, LondonGoogle Scholar
  143. Marques AP, Rangel AO, Castro PM (2007) Zinc accumulation in plant species indigenous to a Portuguese polluted site: relation with soil contamination. J Environ Qual 36:646–653PubMedCrossRefGoogle Scholar
  144. Matringe M, Ksas B, Rey P, Havaux M (2008) Tocotrienols, the unsaturated forms of vitamin E, can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiol 147:764–778PubMedCentralPubMedCrossRefGoogle Scholar
  145. Mehta SK, Gaur JP (1999) Heavy metal induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Phytol 143:253–259CrossRefGoogle Scholar
  146. Mijovilovich A, Leitenmaier B, Meyer-Klaucke W, Kroneck PMH, Gotz B, Kupper H (2009) Complexation and toxicity of copper in higher plants. II. Different mechanisms for copper versus cadmium detoxification in the copper-sensitive cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype). Plant Physiol 151:715–731PubMedCentralPubMedCrossRefGoogle Scholar
  147. Millar AH, Mittova V, Kiddle G, Heazlewood L, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443–447PubMedCentralPubMedCrossRefGoogle Scholar
  148. Miranda MS, Sato S, Mancini-Filho J (2001) Antioxidant activity of the microalga Chlorella vulgaris cultured on special conditions. Boll Chim Farm 140:165–168PubMedGoogle Scholar
  149. Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039PubMedCrossRefGoogle Scholar
  150. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  151. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  152. Mohan BS, Hosetti BB (1997) Potential phytotoxicity of lead and cadmium to Lemna minor grown in sewage stabilization ponds. Environ Pollut 98:233–238CrossRefGoogle Scholar
  153. Morelli E, Scarano G (2004) Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutum. Plant Sci 167:289–296CrossRefGoogle Scholar
  154. Moura DJ, Péres VF, Jacques RA, Saffi J (2012) Heavy metal toxicity: oxidative stress parameters and DNA repair. In: Gupta DK, Sandalio LM (eds) Metal toxicity in plants: perception, signaling and remediation. Springer, HeidelbergGoogle Scholar
  155. Nadgórska-Socha A, Kafel A, Kandziora-Ciupa M, Gospodarek J, Zawisza-Raszka A (2013) Accumulation of heavy metals and antioxidant responses in Vicia faba plants grown on monometallic contaminated soil. Environ Sci Pollut Res Int 20:1124–1134PubMedCentralPubMedCrossRefGoogle Scholar
  156. Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299PubMedCrossRefGoogle Scholar
  157. Naser AH (2013) Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review. Mar Pollut Bull 72:6–13PubMedCrossRefGoogle Scholar
  158. Navari-Izzo F, Quartacci MF, Sgherri C (2002) Lipoic acid: a unique anti-oxidant in the detoxification of activated oxygen species. Plant Physiol Biochem 40:463–470CrossRefGoogle Scholar
  159. Neill JS, Desikan R, Clarke A, Hurst RD, Hanckok JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247PubMedCrossRefGoogle Scholar
  160. Nematshahi N, Lahouti M, Ganjeali A (2012) Accumulation of chromium and its effect on growth of (Allium cepa cv. Hybrid). Eur J Exp Biol 2:969–974Google Scholar
  161. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279PubMedCrossRefGoogle Scholar
  162. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304PubMedCrossRefGoogle Scholar
  163. Oancea S, Foca N, Airinei A (2005) Effects of heavy metals on plant growth and photosynthetic activity. Analele Univ. “Al. I. Cuza”, Tom I, s, Biofizica, Fizica medicala si fizica mediului, pp 107–110Google Scholar
  164. Obroucheva NV, Bystrova EI, Ivanov VB, Antipova OV, Seregin IV (1998) Root growth responses to lead in young maize seedlings. Plant Soil 200:55–61CrossRefGoogle Scholar
  165. Okamoto OK, Colepicolo P (1998) Response of superoxide dismutase to pollutant metal stress in the marine dinoflagellate Gonyaulax polyedra. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 119:67–73PubMedCrossRefGoogle Scholar
  166. Panda SK, Chaudhury I, Khan MH (2003) Heavy metals induce lipid peroxidation and affect antioxidants in wheat leaves. Biol Plant 46:289–294CrossRefGoogle Scholar
  167. 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
  168. Papadakis AK, Roubelakis-Angelakis KA (2005) Polyamines inhibit NADPH oxidase-mediated superoxide generation and putrescine prevents programmed cell death induced by polyamine oxidase-generated hydrogen peroxide. Planta 220:826–837PubMedCrossRefGoogle Scholar
  169. Parida BK, Chhibba IM, Nayyar VK (2003) Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition. Sci Hortic 98:113–119CrossRefGoogle Scholar
  170. Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45CrossRefGoogle Scholar
  171. Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigene family in rice and its evolution in land plants. Phytochemistry 65:1879–1893PubMedCrossRefGoogle Scholar
  172. Pawlik-Skowrońska B (2001) Phytochelatin production in freshwater algae Stigeoclonium in response to heavy metals contained in mining water; effects of some environmental factors. Aquat Toxicol 52:241–249PubMedCrossRefGoogle Scholar
  173. Perl-Treves R, Perl A (2002) Oxidative stress: an Introduction. In: Inzé D (ed) Oxidative stress in plants. Taylor and Francis, LondonGoogle Scholar
  174. Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018CrossRefGoogle Scholar
  175. Poniedziałek M, Sękara A, Ciura J, Jędrszczyk E (2005) Nickel and manganese accumulation and distribution in organs of nine crops. Folia Hortic 17:11–22Google Scholar
  176. Prasad TK, Anderson MD, Martin BA, Steward CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74PubMedCentralPubMedCrossRefGoogle Scholar
  177. Pumas C, Vacharapiyasophon P, Peerapornpisal Y, Leelapornpisid P, Boonchum W, Ishii M, Khanongnuch C (2011) Thermostability of phycobiliproteins and antioxidant activity from four thermotolerant cyanobacteria. Phycol Res 59:166–174CrossRefGoogle Scholar
  178. 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 44:105–113PubMedCrossRefGoogle Scholar
  179. Rafati M, Khorasani N, Moattar F, Shirvany A, Moraghebi F, Hosseinzadeh S (2011) Phytoremediation potential of Populus alba and Morus alba for cadmium, chromium and nickel absorption from polluted soil. Int J Environ Res 5:961–970Google Scholar
  180. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181PubMedCrossRefGoogle Scholar
  181. Rijstenbil JW, Derksen JWM, Gerringa LJA, Poortvliet TCW, Sandee A, Van den Berg M, Van Drie J, Wijnholds JA (1994) Oxidative stress induced by copper: defense and damage in the marine planktonic diatom Ditylum brightwellii (Grunow) West, grown in continuous cultures with high and low zinc levels. Mar Biol 119:583–590CrossRefGoogle Scholar
  182. Rivelli AR, De Maria S, Puschenreiter M, Gherbin P (2012) Accumulation of cadmium, zinc, and copper by Helianthus annuus L.: impact on plant growth and uptake of nutritional elements. Int J Phytoremediation 14:320–334PubMedCrossRefGoogle Scholar
  183. Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544PubMedCrossRefGoogle Scholar
  184. Romero-Puertas MC, Rodríguez-Serrano M, Corpas F, Gomez M, del Rio L, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2 •− and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134CrossRefGoogle Scholar
  185. Romero-Puertas MC, Corpas F, Rodríguez-Serrano M, Gómez M, del Rio L, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by Cd in pea plants. J Plant Physiol 164:1346–1357PubMedCrossRefGoogle Scholar
  186. Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars—metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393PubMedCentralPubMedCrossRefGoogle Scholar
  187. Sabatini SE, Juarez AB, Eppis MR, Bianchi L, Luquet CM, Rios de Molina MC (2009) Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicol Environ Saf 72:1200–1206PubMedCrossRefGoogle Scholar
  188. Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126PubMedGoogle Scholar
  189. Sarma AD, Sreelakshimi Y, Sharma R (1997) Antioxidant ability of anthocyanins against ascorbic acid oxidation. Phytochemistry 45:671–674CrossRefGoogle Scholar
  190. Schat H, Sharma SS, Vooijs R (1997) Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiol Planta 101:477–482CrossRefGoogle Scholar
  191. Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392PubMedCrossRefGoogle Scholar
  192. Scheidegger C, Sigg L, Behra R (2011) Characterization of lead induced metal–phytochelatin complexes in Chlamydomonas reinhardtii. Environ Toxicol Chem 30:2546–2552PubMedCrossRefGoogle Scholar
  193. Schreck E, Foucault Y, Sarret G, Sobanska S, Cécillon L, Castrec-Rouelle M, Uzu G, Dumat C (2012) Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: mechanisms involved for lead. Sci Tot Environ 427–428:253–262CrossRefGoogle Scholar
  194. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedCrossRefGoogle Scholar
  195. Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898PubMedCentralPubMedCrossRefGoogle Scholar
  196. Semane B, Cuypers A, Smeets K, Van Belleghem F, Horemans N, Schat H, Vangronsveld J (2007) Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Physiol Planta 129:519–528CrossRefGoogle Scholar
  197. Senden MHMN, van der Meer AJGM, Verburg TG, Wolterbeek HT (1995) Citric acid in tomato plant roots and its effect on cadmium uptake and distribution. Plant Soil 17:333–339CrossRefGoogle Scholar
  198. Shah KH, Ritambhara GK, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144CrossRefGoogle Scholar
  199. Shahid M, Pinelli E, Pourrut B, Silvestre J, Dumat C (2011) Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol Environ Saf 74:78–84PubMedCrossRefGoogle Scholar
  200. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726PubMedCrossRefGoogle Scholar
  201. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50PubMedCrossRefGoogle Scholar
  202. Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52CrossRefGoogle Scholar
  203. Sharma SS, Schat H, Vooijs R (1998) In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry 49:15311–15535Google Scholar
  204. Sheldon AR, Menzies NW (2005) The effect of copper toxicity on the growth and root morphology of Rhodes grass (Chloris gayana Knuth.) in resin buffered solution culture. Plant Soil 278:341–349CrossRefGoogle Scholar
  205. Shu X, Yan Yin L, Fa Zhang Q, Bo Wang W (2011) Effect of Pb toxicity on leaf growth, antioxidant enzyme activities, and photosynthesis in cuttings and seedlings of Jatropha curcas L. Environ Sci Pollut Res 19:893–902CrossRefGoogle Scholar
  206. Shukla UC, Murthy RC, Kakkar P (2008) Combined effect of ultraviolet-B radiation and cadmium contamination on nutrient uptake and photosynthetic pigments in Brassica campestris L. seedlings. Environ Toxicol 23:712–719PubMedCrossRefGoogle Scholar
  207. Siedlecka A, Krupa Z (1999) Cd/Fe interactions in higher plants - Its consequences for the photosynthetic apparatus. Photosynth Res 36:321–331CrossRefGoogle Scholar
  208. Singh VP (2005) Metal toxicity and tolerance in plants and animals. Sarup, New DelhiGoogle Scholar
  209. Skowroński T, De Knecht JA, Simons J, Verkleji JAC (1998) Phytochelatin synthesis in response to cadmium uptake in Vaucheria (Xanthophyceae). Eur J Phycol 33:87–91CrossRefGoogle Scholar
  210. Ślesak I, Libik M, Karpinska B, Karpinski S, Miszalski Z (2007) The role of hydrogen peroxide in regulation of plant metabolism and cellular signaling in response to environmental stresses. Acta Biochim Pol 54:39–50PubMedGoogle Scholar
  211. Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden S, Vangronsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8CrossRefGoogle Scholar
  212. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35:291–314PubMedCrossRefGoogle Scholar
  213. Stroiński A, Kozłowska M (1997) Cadmium induced oxidative stress in potato tuber. Acta Soc Bot Pol 66:189–195CrossRefGoogle Scholar
  214. Su C, LiQin J, WenJun Z (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skep Crit 3:24–38Google Scholar
  215. Sun Q, Ye 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 164:1489–1498PubMedCrossRefGoogle Scholar
  216. Surosz W, Palinska KA (2005) Effects of heavy-metal stress on cyanobacterium Anabaena flos-aquae. Arch Environ Contam Toxicol 48:40–48PubMedCrossRefGoogle Scholar
  217. Tahara S (2007) A journey of twenty-five years through the ecological biochemistry of flavonoids. Biosci Biotechnol Biochem 71:1387–1404PubMedCrossRefGoogle Scholar
  218. Taiz L, Zeiger E (2002) Plant physiology. Sinauer, Sunderland, MAGoogle Scholar
  219. Tamás L, Dudíková J, Ďurčeková K, Halušková L, Huttová J, Mistrík I, Olle M (2008) Alterations of the gene expression, lipid peroxidation, proline and thiol content along the barley root exposed to cadmium. J Plant Physiol 165:1193–1203PubMedCrossRefGoogle Scholar
  220. Tang YL, Ren WW, Zhang L, Tang KX (2011) Molecular cloning and characterization of gene coding for γ-tocopherol methyltransferase from lettuce (Lactuca sativa). Genet Mol Res 10:320–412Google Scholar
  221. Teklić T, Engler M, Cesar V, Lepeduš H, Parađiković N, Lončarić Z, Štolfa I, Marotti T, Mikac N, Žarković N (2008a) Influence of excess copper on lettuce (Lactuca sativa L.) grown in soil and nutrient solution. J Food Agric Environ 6:439–444Google Scholar
  222. Teklić T, Hancock JT, Engler M, Parađiković N, Cesar V, Lepeduš H, Štolfa I, Bešlo D (2008b) Antioxidative responses in radish (Raphanus sativus L.) plants stressed by copper and lead in nutrient solution and soil. Acta Biol Cracov Bot 50:79–86Google Scholar
  223. Tian S, Lu L, Yang X, Huang H, Wang K, Brown P (2011) Root adaptations to cadmium-induced oxidative stress contribute to Cd tolerance in the hyperaccumulator Sedum alfredii. Biol Plant 56:344–350CrossRefGoogle Scholar
  224. Tomašević M, Aničić M (2010) Trace element content in urban tree leaves and sem-edax characterization of deposited particles. FU Phys Chem Technol 8:1–13CrossRefGoogle Scholar
  225. Trebst A, Depka B, Holländer-Czytko H (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett 516:156–160PubMedCrossRefGoogle Scholar
  226. Tripathi BN, Gaur JP (2006) Physiological behavior of Scenedesmus sp. during exposure to elevated levels of Cu and Zn and after withdrawal of metal stress. Protoplasma 229:1–9PubMedCrossRefGoogle Scholar
  227. Tripathi BN, Mehta SK, Amar A, Gaur JP (2006) Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+. Chemosphere 62:538–544PubMedCrossRefGoogle Scholar
  228. Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633PubMedCentralPubMedCrossRefGoogle Scholar
  229. Tsuji N, Hirayanagi N, Okada M, Miyasaka H, Hirata K, Zenk MH, Miyamoto K (2002) Enhancement of tolerance to heavy metals and oxidative stress in Dunaliella tertiolecta by Zn-induced phytochelatin synthesis. Biochem Biophys Res Commun 293:653–659PubMedCrossRefGoogle Scholar
  230. Van Assche F, Clijsters H (1990) Effect of metal on enzyme activity on plants. Plant Cell Environ 13:195–206CrossRefGoogle Scholar
  231. Van Assche F, Put C, Clijsters HMM (1986) Heavy metals induce specific isozyme patterns of peroxidase in Phaseolus vulgaris L. Arch Int Physiol Biochim 94:60Google Scholar
  232. Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60:9–18PubMedCrossRefGoogle Scholar
  233. 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
  234. Viehweger K (2014) How plants cope with heavy metals. Bot Stud 55:35CrossRefGoogle Scholar
  235. Volland S, Lütz C, Michalkec B, Lütz-Meindl U (2012) Intracellular chromium localization and cell physiological response in the unicellular alga Micrasterias. Aquat Toxicol 109:59–69PubMedCentralPubMedCrossRefGoogle Scholar
  236. Wada N, Sakamoto T, Matsugo S (2013) Multiple roles of photosynthetic and sunscreen pigments in cyanobacteria focusing on the oxidative stress. Metabolites 3:463–483PubMedCentralPubMedCrossRefGoogle Scholar
  237. Wang Y, Fang J, Leonard SS, Murali Krishna Rao K (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443PubMedCrossRefGoogle Scholar
  238. Wang R, Gao F, Guo BQ, Huang JC, Wang L, Zhou YJ (2013) Short term chromium stress induced alterations in the maize leaf proteome. Int J Mol Sci 14:11125–11144PubMedCentralPubMedCrossRefGoogle Scholar
  239. Weckx EJ, Clijsters H (1996) Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol Plant 96:506–512CrossRefGoogle Scholar
  240. Willkenes H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816CrossRefGoogle Scholar
  241. Wu TM, Hsu YT, Lee TM (2009) Effects of cadmium on the regulation of antioxidant enzyme activity, gene expression, and antioxidant defences in the marine macroalga Ulva fasciata. Bot Stud 50:25–34Google Scholar
  242. Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550PubMedCentralPubMedCrossRefGoogle Scholar
  243. Xiong ZT (1998) Lead uptake and effects on seed germination and plant growth in a Pb hyperaccumulator Brassica pekinensis Rupr. Bull Environ Contam Toxicol 60:285–291PubMedCrossRefGoogle Scholar
  244. Xue T, Li X, Zhu W, Wu C, Yang G, Zheng C (2009) Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. J Exp Bot 60:339–349PubMedCentralPubMedCrossRefGoogle Scholar
  245. Yamamoto HY, Bassi R (1996) Carotenoids: localization and function. In: Ort DR, Yocum CF (eds) Oxygenic photosynthesis: the light reactions. Kluwer, DordrechtGoogle Scholar
  246. Yan R, Gao S, Yang W, Cao M, Wang S, Chen F (2008) Nickel toxicity induced antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. cotyledons. Plant Soil Environ 54:294–300Google Scholar
  247. Yang Y, Wei X, Lu J, You J, Wang W, Shi R (2010) Lead-induced phytotoxicity mechanism involved in seed germination and seedling growth of wheat (Triticum aestivum L.). Ecotoxicol Environ Saf 73:1982–1987PubMedCrossRefGoogle Scholar
  248. Yannarelli GG, Fernández-Alvarez AJ, Santa-Cruz DM, Tomaro ML (2007) Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress. Phytochemistry 68:505–512PubMedCrossRefGoogle Scholar
  249. Yilmaz DD, Parlak KU (2011) Antioxidative parameters in the opposite-leaved pondweed (Gronlendia densa) in response to nickel stress. Chem Spec Bioavail 23:71–79CrossRefGoogle Scholar
  250. Yusuf MA, Sarin NB (2007) Antioxidant value addition in human diets: genetic transformation of Brassica juncea with γ-TMT gene for increased α-tocopherol content. Transgenic Res 16:109–113PubMedCrossRefGoogle Scholar
  251. Zengin F (2013) Physiological behaviour of bean (Phaseolus vulgaris L.) seedlings under metal stress. Biol Res 46:79–85PubMedCrossRefGoogle Scholar
  252. Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Ser Bot 47:157–164Google Scholar
  253. Zhou ZP, Liu LN, Chen XL, Wang JX, Chen M, Zheng YZ, Zhou BC (2005) Factors that affect antioxidant activity of c-phycocyanins from Spirulina platensis. J Food Biochem 29:313–322CrossRefGoogle Scholar
  254. Zou J, Yu K, Zhang Z, Jiang W, Liu D (2009) Antioxidant response system and chlorophyll fluorescence in chromium (VI)-treated Zea mays (L.) seedlings. Acta Biol Cracov Bot 51:23–33Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Ivna Štolfa
    • 1
    Email author
  • Tanja Žuna Pfeiffer
    • 1
  • Dubravka Špoljarić
    • 1
  • Tihana Teklić
    • 2
  • Zdenko Lončarić
    • 2
  1. 1.Department of BiologyJosip Juraj Strossmayer University of OsijekOsijekCroatia
  2. 2.Faculty of Agriculture in OsijekJosip Juraj Strossmayer University of OsijekOsijekCroatia

Personalised recommendations