Assessment of Antioxidant Potential of Plants in Response to Heavy Metals

  • Namira Arif
  • Vaishali Yadav
  • Shweta Singh
  • Bishwajit Kumar Kushwaha
  • Swati Singh
  • Durgesh Kumar Tripathi
  • Kanchan Vishwakarma
  • Shivesh Sharma
  • N. K. Dubey
  • D. K. ChauhanEmail author


Heavy metals (HMs) are consequential environmental contaminant, and their prodigious bioaccumulation in the surroundings has become an enigma for all living organisms including plants. Heavy metal has the potential to react with various indispensable cellular components like DNA, protein, and enzymes and in turn induce several stress responses in plants like oxidative stress which is the root cause for the progression of cell death in the plant. Stress responses inflicted by oxidative stress include severe morphological, metabolic, and physiological amendments in plants like DNA strand breakage, defragmentation of proteins, and damage of photosynthetic pigment, which may stimulate cell death. In reaction, plants have a range of mechanisms to minimize the heavy metal toxicity. Plants are endowed with antioxidant defense mechanism, which can be divided into two groups such as enzymatic antioxidants and nonenzymatic antioxidants, for instance, SOD, CAT, APX, GPX, GR and AsA, GSH, carotenoids, alkaloids, tocopherols, proline, and phenolic compounds, respectively, that together act as the scavengers for free radicals to mitigate the damaging impacts of heavy metal agglomeration in the cells. These antioxidant potentials could be assessed by different in vivo and in vitro methods such as hydrogen atom transfer and electron transfer through which we can evaluate the ROS detrimental action of antioxidant enzymes. Therefore, the present chapter attempts to provide the contemporary knowledge regarding the metal-influenced antioxidant status in plants and also provides the precise pathway that should follow for the future research in the area of antioxidant potentials.


Antioxidant Oxidative stress Heavy metal Detoxification 


  1. Abeysinghe DC, Wijerathne SMNK, Dharmadasa RM (2014) Secondary metabolites contents and antioxidant capacities of acmella oleraceae grown under different growing systems. World J Agric Res 2(4):163–167CrossRefGoogle Scholar
  2. Agrawal SB, Mishra S (2009) Effects of supplemental ultraviolet-B and cadmium on growth, antioxidants and yield of Pisum sativum L. Ecotoxicol Environ Safe 72:610–618CrossRefGoogle Scholar
  3. Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602PubMedCrossRefGoogle Scholar
  4. Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta Gen Subj 1523:37–48CrossRefGoogle Scholar
  5. Ahmad P, Azooz MM, Prasad MNV (eds) (2012) Ecophysiology and responses of plants under salt stress. Springer Science & Business MediaGoogle Scholar
  6. Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877PubMedCrossRefGoogle Scholar
  7. Alam MN, Bristi NJ, Rafiquzzaman M (2013) Review on in vivo and in vitro methods evaluation of antioxidant activity. Saudi Pharm J 21:143–152PubMedCrossRefGoogle Scholar
  8. Ali AA, Alqurainy F (2006) Activities of antioxidants in plants under environmental stress. The lutein-prevention and treatment for diseases. In: Motohashi N (ed) The lutein prevention and treatment for disease. Kerala, Transworld Research Network, pp 187–256Google Scholar
  9. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233CrossRefGoogle Scholar
  10. Andrianos V, Stoikou V, Tsikrika K, Lamprou D, Stasinos S, Proestos C, Zabetakis I (2016) Carotenoids and antioxidant enzymes as biomarkers of the impact of heavy metals in food chain. Curr Res Nutr Food Sci 4:15–24CrossRefGoogle Scholar
  11. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  12. Arruti A, Fernández-Olmo I, Irabien Á (2010) Evaluation of the contribution of local sources to trace metals levels in urban PM2. 5 and PM10 in the Cantabria region (Northern Spain). J Environ Monit 12:1451–1458PubMedCrossRefGoogle Scholar
  13. Asada K (2000) The water–water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B Biol Sci 355:1419–1431PubMedPubMedCentralCrossRefGoogle Scholar
  14. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedPubMedCentralCrossRefGoogle Scholar
  15. Badarinath AV, Rao KM, Chetty CMS, Ramkanth S, Rajan TVS, Gnanaprakash K (2010) A review on in-vitro antioxidant methods: comparisons, correlations and considerations. Int J PharmTech Res 2:1276–1285Google Scholar
  16. Baier M, Dietz KJ (2005) Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 56:1449–1462PubMedCrossRefGoogle Scholar
  17. Bansal M, Kaushal N (2014) Oxidative stress mechanisms and their modulation. Springer, New DelhiCrossRefGoogle Scholar
  18. Baratta MT, Dorman HJ, Deans SG, Figueiredo AC, Barroso JG, Ruberto G (1998) Antimicrobial and antioxidant properties of some commercial essential oils. Flavour Frag J 13:235–244CrossRefGoogle Scholar
  19. Begović L, Mlinarić S, Dunić JA, Katanić Z, Lončarić Z, Lepeduš H, Cesar V (2016) Response of Lemna minor L. to short-term cobalt exposure: the effect on photosynthetic electron transport chain and induction of oxidative damage. Aquat Toxicol 175:117–126PubMedCrossRefGoogle Scholar
  20. Britton G, Liaaen-Jensen S, Pfander H (eds) (2009) Carotenoids volume 5: nutrition and health (Vol. 5) SSBMGoogle Scholar
  21. Cannon RE, White JA, Scandalios JG (1987) Cloning of cDNA for maize superoxide dismutase 2 (SOD2). Proc Nalt Acad Sci 84:179–183CrossRefGoogle Scholar
  22. Campos C, Guzmán R, López-Fernández E, Casado Á (2009) Evaluation of the copper (II) reduction assay using bathocuproinedisulfonic acid disodium salt for the total antioxidant capacity assessment: The CUPRAC–BCS assay. Anal Biochem 392(1):37–44PubMedCrossRefGoogle Scholar
  23. Caregnato FF, Koller CE, MacFarlane GR, Moreira JC (2008) The glutathione antioxidant system as a biomarker suite for the assessment of heavy metal exposure and effect in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 56:1119–1127PubMedCrossRefGoogle Scholar
  24. Cargnelutti D, Tabaldi LA, Spanevello RM, de Oliveira JG, Battisti V, Redin M, Morsch VM (2006) Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65:999–1006PubMedCrossRefGoogle Scholar
  25. Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019PubMedPubMedCentralCrossRefGoogle Scholar
  26. Çekiç SD, Avan AN, Uzunboy S, Apak R (2015) A colourimetric sensor for the simultaneous determination of oxidative status and antioxidant activity on the same membrane: N, N-Dimethyl-p-phenylene diamine (DMPD) on Nafion. Anal Chim Acta 865:60–70PubMedCrossRefGoogle Scholar
  27. Cheeseman JM (2006) Hydrogen peroxide concentrations in leaves under natural conditions. J Exp Bot 57:2435–2444PubMedCrossRefGoogle Scholar
  28. Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chugh V, Kaur N, Gupta AK (2011) Evaluation of oxidative stress tolerance in maize (Zea mays L.) seedlings in response to drought. Indian J Biochem Biophys 48:47–53PubMedGoogle Scholar
  30. Collin VC, Eymery F, Genty B, Rey P, Havaux M (2008) Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal induced oxidative stress. Plant Cell Environ 31:244–257PubMedGoogle Scholar
  31. Dai HP, Shan CJ, Zhao H, Li JC, Jia GL, Jiang H, Wang Q (2015) The difference in antioxidant capacity of four alfalfa cultivars in response to Zn. Ecotoxicol Environ Safe 114:312–317CrossRefGoogle Scholar
  32. Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53CrossRefGoogle Scholar
  33. Ding S, Lei M, Lu Q, Zhang A, Yin Y, Wen X, Lu C (2012) Enhanced sensitivity and characterization of photosystem II in transgenic tobacco plants with decreased chloroplast glutathione reductase under chilling stress. BBA Bioenerg 1817:1979–1991CrossRefGoogle Scholar
  34. Dixit G, Singh AP, Kumar A, Mishra S, Dwivedi S, Kumar S, Tripathi RD (2016) Reduced arsenic accumulation in rice (Oryza sativaL.) shoot involves sulfur mediated improved thiol metabolism, antioxidant system and altered arsenic transporters. Plant Physiol Biochem 99:86–96Google Scholar
  35. Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. Biometals 17:379–387PubMedCrossRefGoogle Scholar
  36. 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
  37. Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255–1264PubMedCrossRefGoogle Scholar
  38. Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015 Article ID 756120: 18Google Scholar
  39. Eshagberi GO (2012) Toxic effects of heavy metal on crop plants. Multidiscip J Emp Res 10:1–10Google Scholar
  40. Fariduddin Q, Yusuf M, Hayat S, Ahmad A (2009) Effect of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ Exp Bot 66:418–424Google Scholar
  41. Fatima RA, Ahmad M (2005) Certain antioxidant enzymes of Allium cepaas biomarkers for the detection of toxic heavy metals in wastewater. Sci Total Environ 346:256–273Google Scholar
  42. FAO (2009) Press release, 19 June 2009.
  43. Fernández LG, Fernández-Pascual M, Mañero FJG, García JAL (2015) Phytoremediation of contaminated waters to improve water quality. In: Phytoremediation. Springer International Publishing, pp 11–26Google Scholar
  44. Ferrat L, Pergent-Martini C, Roméo M (2003) Assessment of the use of biomarkers in aquatic plants for the evaluation of environmental quality: application to seagrasses. Aquat Toxicol 65:187–204PubMedCrossRefGoogle Scholar
  45. Filippenko V, Frenette M, Scaiano JC (2009) Solvent-independent antioxidant activity from thermally generated carbon-centered radical antioxidants. Org Lett 11:3634–3637PubMedCrossRefGoogle Scholar
  46. Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6:709–711PubMedPubMedCentralCrossRefGoogle Scholar
  47. Flora SJ (2009) Structural, chemical and biological aspects of antioxidants for strategies against metal and metalloid exposure. Oxid Med Cell Longev 2:191–206PubMedPubMedCentralCrossRefGoogle Scholar
  48. 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
  49. Fritioff Å, Greger M (2003) Aquatic and terrestrial plant species with potential to remove heavy metals from stormwater. Int J Phytorem 5:211–224CrossRefGoogle Scholar
  50. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705PubMedCrossRefGoogle Scholar
  51. 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
  52. Gill SS, Khan NA, Anjum NA, Tuteja N (2011) Amelioration of cadmium stress in crop plants by nutrients management: morphological, physiological and biochemical aspects. Plant Stress 5:1–23Google Scholar
  53. Gliszczyńska-Świgło A (2006) Antioxidant activity of water soluble vitamins in the TEAC (trolox equivalent antioxidant capacity) and the FRAP (ferric reducing antioxidant power) assays. Food Chem 96:131–136CrossRefGoogle Scholar
  54. Gout E, Boisson AM, Aubert S, Douce R, Bligny R (2001) Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells. Carbon-13 and phosphorous-31 nuclear magnetic resonance studies. Plant Physiol 125:912–925PubMedPubMedCentralCrossRefGoogle Scholar
  55. Grassmann J, Hippeli S, Elstner EF (2002) Plant’s defence and its benefits for animals and medicine: role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol Biochem 40:471–478CrossRefGoogle Scholar
  56. Gutteridge J, Halliwell B (2000) Free radicals and antioxidants in the year 2000: a historical look to the future. Ann N Y Acad Sci 899:136–147PubMedCrossRefGoogle Scholar
  57. Hajar EWI, Sulaiman AZB, Sakinah AM (2014) Assessment of heavy metals tolerance in leaves, stems and flowers of Stevia rebaudiana plant. Proc Environ Sci 20:386–393CrossRefGoogle Scholar
  58. Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97:1634–1658PubMedCrossRefGoogle Scholar
  59. Han D, Xiong S, Tu S, Liu J, Chen C (2015) Interactive effects of selenium and arsenic on growth, antioxidant system, arsenic and selenium species of Nicotiana tabacum L. Environ Exp Bot 117:12–19CrossRefGoogle Scholar
  60. Hartmann A, Nieβ AM, Grünert-Fuchs M, Poch B, Speit G (1995) Vitamin E prevents exercise-induced DNA damage. Mut Res Lett 346:195–202CrossRefGoogle Scholar
  61. Haytowitz DB, Bhagwat S (2010) USDA database for the oxygen radical absorbance capacity (ORAC) of selected foods, Release 2. US Department of AgricultureGoogle Scholar
  62. He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140PubMedCrossRefGoogle Scholar
  63. Hernández I, Alegre L, Van Breusegem F, Munné-Bosch S (2009) How relevant are flavonoids as antioxidants in plants? Trends Plant Sci 14:125–132PubMedCrossRefGoogle Scholar
  64. Iannone MF, Groppa MD, Benavides MP (2015) Cadmium induces different biochemical responses in wild type and catalase-deficient tobacco plants. Environ Exp Bot 109:201–211CrossRefGoogle Scholar
  65. Igamberdiev AU, Mikkelsen TN, Ambus P, Bauwe H, Lea PJ, Gardeström P (2004) Photorespiration contributes to stomatal regulation and carbon isotope fractionation: a study with barley, potato and Arabidopsis plants deficient in glycine decarboxylase. Photosynth Res 81:139–152CrossRefGoogle Scholar
  66. Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 755Google Scholar
  67. Islam F, Yasmeen T, Riaz M, Arif MS, Ali S, Raza SH (2014) Proteus mirabilis alleviates zinc toxicity by preventing oxidative stress in maize (Zea mays) plants. Ecotoxical Environ Safe 110:143–152CrossRefGoogle Scholar
  68. Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65:591–598PubMedCrossRefGoogle Scholar
  69. Jaleel CA, Jayakumar K, Chang-Xing Z, Azooz MM (2009) Antioxidant potentials protect Vigna radiata (L.) Wilczek plants from soil cobalt stress and improve growth and pigment composition. Plant Omics 2:120Google Scholar
  70. Jayakumar K, Vijayarengan P, Changxing Z, Gomathinayagam M, Jaleel CA (2008) Soil applied cobalt alters the nodulation, leg-haemoglobin content and antioxidant status of glycine max (L.). Merr Collid Surf B 67:272–275CrossRefGoogle Scholar
  71. Johnston JW, Dussert S, Gale S, Nadarajan J, Harding K, Benson EE (2006) Optimisation of the azinobis-3-ethyl-benzothiazoline-6-sulphonic acid radical scavenging assay for physiological studies of total antioxidant activity in woody plant germplasm. Plant Physiol Biochem 44:193–201PubMedCrossRefGoogle Scholar
  72. Kabata A, Pendias H (2001) Trace elements in soils and plants. CRC, WashingtonGoogle Scholar
  73. Kabata-Pendias A (2004) Soil–plant transfer of trace elements—an environmental issue. Geoderma 122:143–149CrossRefGoogle Scholar
  74. Kafel A, Nadgórska-Socha A, Gospodarek J, Babczyńska A, Skowronek M, Kandziora M, Rozpędek K (2010) The effects of Aphis fabae infestation on the antioxidant response and heavy metal content in field grown Philadelphus coronarius plants. Sci Total Environ 408:1111–1119PubMedCrossRefGoogle Scholar
  75. Kähkönen MP, Heinonen M (2003) Antioxidant activity of anthocyanins and their aglycons. J Agric Food Chem 51:628–633PubMedCrossRefGoogle Scholar
  76. Karadag A, Ozcelik B, Saner S (2009) Review of methods to determine antioxidant capacities. Food Anal Method 2:41–60CrossRefGoogle Scholar
  77. Karuppanapandian T, Manoharan K (2008) Uptake and translocation of tri- and hexa-valent chromium and their effects on black gram (Vigna mungo L. Hepper cv. Co4) roots. J Plant Biol 51:192–201CrossRefGoogle Scholar
  78. Karuppanapandian T, Sinha PB, Haniya AMK, Mamoharan K (2006) Differential antioxidative responses of ascorbate-glutathione cycle enzymes and metabolites to chromium stress in green gram (Vigna radiata L. Wilczek) leaves. J Plant Biol 49:440–447CrossRefGoogle Scholar
  79. 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 709Google Scholar
  80. Kasote DM, Katyare SS, Hegde MV, Bae H (2015) Significance of antioxidant potential of plants and its relevance to therapeutic applications. Int J Biol Sci 982Google Scholar
  81. Kazemi N, Khavari-Nejad RA, Fahimi H, Saadatmand S, Nejad-Sattari T (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic –Amsterdam 126:402–407Google Scholar
  82. Keilig K, Ludwig-Müller J (2009) Effect of flavonoids on heavy metal tolerance in Arabidopsis thaliana seedlings. Bot Stud 50:311–318Google Scholar
  83. Khatun S, Ali MB, Hahn EJ, Paek KY (2008) Copper toxicity in Withania somnifera: growth and antioxidant enzymes responses of in vitro grown plants. Environ Exp Bot 64:279–285CrossRefGoogle Scholar
  84. Kiffin R, Bandyopadhyay U, Cuervo AM (2006) Oxidative stress and autophagy. Antioxid Redox Signal 8:152–162PubMedCrossRefGoogle Scholar
  85. Kliebenstein DJ, Osbourn A (2012) Making new molecules–evolution of pathways for novel metabolites in plants. Curr Opin Plant Biol 15:415–423PubMedCrossRefGoogle Scholar
  86. Koji Y, Shiro M, Michio K, Mitsutaka T, Hiroshi M (2009) Antioxidant capacity and damages caused by salinity stress in apical and basal regions of rice leaf. Plant Prod Sci 12:319–326CrossRefGoogle Scholar
  87. Korkina LG (2007) Phenylpropanoids as naturally occurring antioxidants: from plant defense to human health. Cell Mol Biol 53:15–25PubMedGoogle Scholar
  88. Kotapati KV, Palaka BK, Kandukuri A, Reddy R (2014) Response of antioxidative enzymes and lipoxygenase to drought stress in finger millet leaves (Eleusine Coracana (L.) Gaertn)Google Scholar
  89. Krishnaiah D, Sarbatly R, Nithyanandam R (2011) A review of the antioxidant potential of medicinal plant species. Food Bioprod Process 89:217–233CrossRefGoogle Scholar
  90. Kuiper C, Vissers MC (2013) Ascorbate as a co-factor for Fe-and 2-oxoglutarate dependent dioxygenases: physiological activity in tumor growth and progression. Front Oncol 4:359–359Google Scholar
  91. Kumar JN, Soni H, Kumar RN, Bhatt I (2008) Assessing heavy metal hyper-accumulation and mobility in selected vegetable crops: a case study of organic farm, Gujarat, India. Nat Environ Pollut Technol 7(2):203–210Google Scholar
  92. Kumar RR, Goswami S, SinghK GK, Rai GK, Rai RD (2013) Modulation of redox signal transduction in plant system through induction of free radical/ROS scavenging redox-sensitive enzymes and metabolites. Aust J Crop Sci 1744Google Scholar
  93. Kusvuran S (2012) Influence of drought stress on growth, ion accumulation and antioxidative enzymes in okra genotypes. Int J Agric Biol 14:401–406Google Scholar
  94. Kuźniak E, Głowacki R, Chwatko G, Kopczewski T, Wielanek M, Gajewska E, Skłodowska M (2014) Involvement of ascorbate, glutathione, protein S-thiolation and salicylic acid in benzothiadiazole-inducible defence response of cucumber against Pseudomonas syringae pv lachrymans. Physiol Mol Plant 86:89–97CrossRefGoogle Scholar
  95. Lasat MM (2000) Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. J Hazard Sub Res 2:1–25Google Scholar
  96. Lenntech Water Treatment and Air Purification (2004) Water treatment. Lenntech, Rotterdamseweg, Netherlands (
  97. Leterrier M, Corpas FJ, Barroso JB, Sandalio LM, Luis A (2005) Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 138:2111–2123PubMedPubMedCentralCrossRefGoogle Scholar
  98. Li Z, Keasling JD, Niyogi KK (2012) Overlapping photoprotective function of vitamin E and carotenoids in Chlamydomonas. Plant Physiol 158:313–323PubMedCrossRefGoogle Scholar
  99. 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
  100. Lomonte C, Sgherri C, Baker AJ, Kolev SD, Navari-Izzo F (2010) Antioxidative response of Atriplex codonocarpa to mercury. Environ Exp Bot 69:9–16CrossRefGoogle Scholar
  101. Lopez‐Huertas E, Charlton WL, Johnson B, Graham IA, Baker A (2000) Stress induces peroxisome biogenesis genes. EMBO J 19:6770–6777PubMedPubMedCentralCrossRefGoogle Scholar
  102. Løvdal T, Olsen KM, Slimestad R, Verheul M, Lillo C (2010) Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 71:605–613PubMedCrossRefGoogle Scholar
  103. Malar S, Vikram SS, Favas PJ, Perumal V (2014) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud 54Google Scholar
  104. Malik JA, Goel S, Kaur N, Sharma S, Singh I, Nayyar H (2012) Selenium antagonises the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environ Exp Bot 77:242–248CrossRefGoogle Scholar
  105. Mangabeira PA, Gavrilov KL, De Almeida AAF, Oliveira AH, Severo MI, Rosa TS, Mielke MS (2006) Chromium localization in plant tissues of Lycopersicum esculentum Mill using ICP-MS and ion microscopy (SIMS). Appl Surf Sci 252:3488–3501CrossRefGoogle Scholar
  106. Mazid M, Khan TA, Mohammad F (2011) Role of secondary metabolites in defense mechanisms of plants. Biol Med 3:232–249Google Scholar
  107. 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
  108. Minkov IN, Jahoubjan GT, Denev ID, Toneva VT (1999) Photooxidative stress in higher plants. Handb Plant Crop Stress 2:499–525Google Scholar
  109. Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. Febs Lett 566:1–5PubMedCrossRefGoogle Scholar
  110. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  111. 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 164:601–610PubMedCrossRefGoogle Scholar
  112. Myburgh KH (2014) Polyphenol supplementation: benefits for exercise performance or oxidative stress? Sports Med 44:57–70PubMedCentralCrossRefGoogle Scholar
  113. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216CrossRefGoogle Scholar
  114. Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Safe 126:245–255CrossRefGoogle Scholar
  115. Namdjoyan S, Kermanian H (2013) Exogenous nitric oxide (as sodium nitroprusside) ameliorates arsenic-induced oxidative stress in watercress (Nasturtium officinale R. Br.) plants. Sci Hortic-Amsterdam 350–356Google Scholar
  116. Noctor G, Foyer CH (1998) Simultaneous measurement of foliar glutathione, γ-glutamylcysteine, and amino acids by high-performance liquid chromatography: comparison with two other assay methods for glutathione. Anal Biochem 264:98–110PubMedCrossRefGoogle Scholar
  117. Nowicka B, Pluciński B, Kuczyńska P, Kruk J (2016) Prenyllipid antioxidants participate in response to acute stress induced by heavy metals in green microalga Chlamydomonas reinhardtii. Environ Exp Bot 123:98–107CrossRefGoogle Scholar
  118. Ordoudi SA, Tsimidou MZ (2006) Crocin bleaching assay step by step: observations and suggestions for an alternative validated protocol. J Agric Food Chem 54:1663–1671PubMedCrossRefGoogle Scholar
  119. Ou B, Huang D, Hampsch-Woodill M, Flanagan JA, Deemer EK (2002) Analysis of antioxidant activities of common vegetables employing oxygen radical absorbance capacity (ORAC) and ferric reducing antioxidant power (FRAP) assays: a comparative study. J Agric Food Chem 50:3122–3128PubMedCrossRefGoogle Scholar
  120. Ozgen M, Reese RN, Tulio AZ, Scheerens JC, Miller AR (2006) Modified 2, 2-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2, 2′-diphenyl-1-picrylhydrazyl (DPPH) methods. J Agric Food Chem 54:1151–1157PubMedCrossRefGoogle Scholar
  121. Padh H (1990) Cellular functions of ascorbic acid. Biochem Cell Biol 68:1166–1173PubMedCrossRefGoogle Scholar
  122. Palozza P, Krinsky NI (1992) β-Carotene and α-tocopherol are synergistic antioxidants. Arch Biochem Biophys 297:184–187PubMedCrossRefGoogle Scholar
  123. Parlak KU (2016) Effect of nickel on growth and biochemical characteristics of wheat (Triticum aestivum L.) seedlings. NJAS-Wagen J Life Sci 76:1–5CrossRefGoogle Scholar
  124. Parvaiz A, Satyawati S (2008) Salt stress and phyto-biochemical responses of plants-a review. Plant Soil Environ 54(3):89–99Google Scholar
  125. Peijnenburg WJGM, Jager T (2003) Monitoring approaches to assess bioaccessibility and bioavailability of metals: matrix issues. Ecotoxicol Environ Safe 56:63–77CrossRefGoogle Scholar
  126. Phang C, Leung DW, Taylor HH, Burritt DJ (2011) The protective effect of sodium nitroprusside (SNP) treatment on Arabidopsis thalianaseedlings exposed to toxic level of Pb is not linked to avoidance of Pb uptake. Ecotoxicol Environ Safe 74:1310–1315Google Scholar
  127. Pinto E, Sigaud-kutner T, Leitao MA, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal–induced oxidative stress in algae1. J Phycol 39:1008–1018CrossRefGoogle Scholar
  128. Posmyk MM, Kontek R, Janas KM (2009) Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Safe 72:596–602CrossRefGoogle Scholar
  129. Prakash D, Sharma G (eds) (2014) Phytochemicals of nutraceutical importance. CABIGoogle Scholar
  130. Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302PubMedCrossRefGoogle Scholar
  131. Rabi T, Bishayee A (2009) Terpenoids and breast cancer chemoprevention. Breast Cancer Res Treat 115:223–239PubMedCrossRefGoogle Scholar
  132. Ragavendran P, Sophia D, Arul Raj C, Starlin T, Gopalakrishnan VK (2012) Phytochemical screening, antioxidant activity of Aerva lanata (L)–an in vitro study. Asian J Pharm Clin Res 5:77–81Google Scholar
  133. Rahman K (2007) Studies on free radicals, antioxidants, and co-factors. Clin Interv Aging 219Google Scholar
  134. Rao KM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128CrossRefGoogle Scholar
  135. Regelsberger G, Atzenhofer W, Rüker F, Peschek GA, Jakopitsch C, Paumann M, Obinger C (2002) Biochemical characterization of a membrane-bound manganese-containing superoxide dismutase from the cyanobacterium Anabaena PCC 7120. J Biol Chem 277:43615–43622PubMedCrossRefGoogle Scholar
  136. Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodríguez-Serrano M, Del Río LA, Palma JM (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170:43–52PubMedCrossRefGoogle Scholar
  137. Salido AL, Hasty KL, Lim JM, Butcher DJ (2003) Phytoremediation of arsenic and lead in contaminated soil using Chinese brake ferns (Pteris vittata) and Indian mustard (Brassica juncea). Int J Phytorem 5:89–103CrossRefGoogle Scholar
  138. Sánchez-Pardo B, Fernández-Pascual M, Zornoza P (2012) Copper microlocalisation, ultrastructural alterations and antioxidant responses in the nodules of white lupin and soybean plants grown under conditions of copper excess. Environ Exp Bot 84:52–60CrossRefGoogle Scholar
  139. Sbartai H, Djebar MR, Sbartai I, Berrabbah H (2012) Bioaccumulation of cadmium and zinc in tomato (Lycopersicon esculentum L.). C R Biol 335:585–593PubMedCrossRefGoogle Scholar
  140. Schardl CL, Panaccione DG, Tudzynski P (2006) Ergot alkaloids–biology and molecular biology. Alkaloids Chem Boil 63:45–86CrossRefGoogle Scholar
  141. Schrader M, Fahimi HD (2006) Peroxisomes and oxidative stress. Biochim Biophys Acta Mol Cell Res 1763:1755–1766CrossRefGoogle Scholar
  142. 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
  143. Shahid M, Pinelli E, Pourrut B, Dumat C (2014) Effect of organic ligands on lead-induced oxidative damage and enhanced antioxidant defense in the leaves of Vicia faba plants. J Geochem Explor 144:282–289CrossRefGoogle Scholar
  144. Shalaby E, Shanab S (2013) Antioxidant compounds, assays of determination and mode of action. Afr J Pharm Pharmacol 7:528–539CrossRefGoogle Scholar
  145. 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 52:165–169CrossRefGoogle Scholar
  146. Shanker AK, Djanaguiraman M, Sudhagar R, Chandrashekar CN, Pathmanabhan G (2004) Differential antioxidative response of ascorbate glutathione pathway enzymes and metabolites to chromium speciation stress in green gram (Vigna radiata (L.) R. Wilczek. cv CO 4) roots. Plant Sci 166:1035–1043CrossRefGoogle Scholar
  147. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012: Article ID 217037, 26 pagesGoogle Scholar
  148. Sharma P, Kumar A, Bhardwaj R (2016) Plant steroidal hormone epibrassinolide regulate–Heavy metal stress tolerance in Oryza sativa L. by modulating antioxidant defense expression. Environ Exp Bot 1–9Google Scholar
  149. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319PubMedCrossRefGoogle Scholar
  150. Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295PubMedCrossRefGoogle Scholar
  151. Sies H (2007) Total antioxidant capacity: appraisal of a concept. J Nutr 137:1493–1495PubMedGoogle Scholar
  152. Sinha RK, Herat S, Tandon PK (2007) Phytoremediation: role of plants in contaminated site management. In: Environmental Bioremediation Technologies, pp 315–330Google Scholar
  153. Singh S, Srivastava PK, Kumar D, Tripathi DK, Chauhan DK, Prasad SM (2015) Morpho-anatomical and biochemical adapting strategies of maize (Zea mays L.) seedlings against lead and chromium stresses. Biocatal Agric Biotechnol 4(3):286–295Google Scholar
  154. Smirnoff N (2005) Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. Antioxidants and Reactive Oxygen Species in Plants 53–86Google Scholar
  155. Srivastava NK, Srivastava AK (2010) Influence of some heavy metals on growth, alkaloid content and composition in Catharanthus roseus L. Indian J Pharm Sci 775Google Scholar
  156. Sun RL, Zhou QX, Sun FH, Jin CX (2007) Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot 60:468–476CrossRefGoogle Scholar
  157. Takeda T, Yoshimura K, Ishikawa T, Shigeoka S (1998) Purification and characterization of ascorbate peroxidase in Chlorella vulgaris. Biochimie 80:295–301PubMedCrossRefGoogle Scholar
  158. Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011: Article ID 939161, 31 pagesGoogle Scholar
  159. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Molecular, clinical and environmental toxicology, pp 133–164 EXS. 101:133–164Google Scholar
  160. Traber MG, Stevens JF (2011) Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med 51(5):1000–1013PubMedPubMedCentralCrossRefGoogle Scholar
  161. Tripathi DK, Singh VP, Prasad SM, Chauhan DK, Dubey NK (2015) Silicon nanoparticles (SiNp) alleviate chromium (VI) phytotoxicity in Pisum sativum (L.) seedlings. Plant Physiol Biochem 96:189–198PubMedCrossRefGoogle Scholar
  162. Tripathi A, Tripathi DK, Chauhan DK, Kumar N (2016) Chromium (VI)-induced phytotoxicity in river catchment agriculture: evidence from physiological, biochemical and anatomical alterations in Cucumis sativus (L.) used as model species. Chem Ecol 32(1):12–33CrossRefGoogle Scholar
  163. Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633PubMedPubMedCentralCrossRefGoogle Scholar
  164. Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiol 154:444–448PubMedPubMedCentralCrossRefGoogle Scholar
  165. 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
  166. Viehweger K (2014) How plants cope with heavy metals. Bot Stud 35Google Scholar
  167. Vitória AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710PubMedCrossRefGoogle Scholar
  168. Wang X, Quinn PJ (2000) The location and function of vitamin E in membranes (Review). Mol Membr Biol 17:143–156PubMedCrossRefGoogle Scholar
  169. Weihong XU, Wenyi LI, Jianping HE, Singh B, Xiong Z (2009) Effects of insoluble Zn, Cd, and EDTA on the growth, activities of antioxidant enzymes and uptake of Zn and Cd in Vetiveria zizanioides. J Environ Sci 21:186–192CrossRefGoogle Scholar
  170. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223PubMedCrossRefGoogle Scholar
  171. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179CrossRefGoogle Scholar
  172. Yoon HS, Lee H, Lee IA, Kim KY, Jo J (2004) Molecular cloning of the monodehydroascorbate reductase gene from Brassica campestris and analysis of its mRNA level in response to oxidative stress. BBA Bioenerg 1658:181–186CrossRefGoogle Scholar
  173. Young AJ, Lowe GM (2001) Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 385:20–27PubMedCrossRefGoogle Scholar
  174. Yusuf M, Khan TA, Fariduddin Q (2016) Interaction of epibrassinolide and selenium ameliorates the excess copper inBrassica juncea through altered proline metabolism and antioxidants. Ecotoxical Environ Safe 129:25–34Google Scholar
  175. Zamocky M, Furtmüller PG, Obinger C (2008) Evolution of catalases from bacteria to humans. Antioxid Redox Signal 10:1527–1548PubMedPubMedCentralCrossRefGoogle Scholar
  176. 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 Bot 47:157–164Google Scholar
  177. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333PubMedCrossRefGoogle Scholar
  178. Zhou ZS, Wang SJ, Yang ZM (2008) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70:1500–1509PubMedCrossRefGoogle Scholar
  179. Ziegler J, Facchini PJ (2008) Alkaloid biosynthesis: metabolism and trafficking. Annu Rev Plant Biol 59:735–769PubMedCrossRefGoogle Scholar
  180. Zitka O, Skalickova S, Gumulec J, Masarik M, Adam V, Hubalek J, Kizek R (2012) Redox status expressed as GSH: GSSG ratio as a marker for oxidative stress in paediatric tumour patients. Oncol Lett 4:1247–1253PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2016

Authors and Affiliations

  • Namira Arif
    • 1
  • Vaishali Yadav
    • 1
  • Shweta Singh
    • 1
  • Bishwajit Kumar Kushwaha
    • 1
  • Swati Singh
    • 1
  • Durgesh Kumar Tripathi
    • 2
    • 3
  • Kanchan Vishwakarma
    • 4
  • Shivesh Sharma
    • 4
    • 5
  • N. K. Dubey
    • 6
  • D. K. Chauhan
    • 1
    Email author
  1. 1.D D Pant Interdisciplinary Research Laboratory, Department of BotanyUniversity of AllahabadAllahabadIndia
  2. 2.Centre of Advanced Study in BotanyBanaras Hindu UniversityVaranasiIndia
  3. 3.Centre for Medical Diagnostic and ResearchMotilal Nehru National Institute of TechnologyAllahabadIndia
  4. 4.Department of BiotechnologyMotilal Nehru National Institute of TechnologyAllahabadIndia
  5. 5.Centre for Medical Diagnostic and ResearchMotilal Nehru National Institute of TechnologyAllahabadIndia
  6. 6.Centre of Advanced Study in BotanyBanaras Hindu UniversityVaranasiIndia

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