Skip to main content
Log in

Combined effect of Cd and Pb spiked field soils on bioaccumulation, DNA damage, and peroxidase activities in Trifolium repens

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The present study was designed to investigate the combined effects of Cd and Pb on accumulation and genotoxic potential in white clover (Trifolium repens). For this purpose, T. repens was exposed to contaminated soils (2.5–20 mg kg−1 cadmium (Cd), 250–2000 mg kg−1 lead (Pb) and a mixture of these two heavy metals) for 3, 10 and 56 days. The resulting bioaccumulation of Cd and Pb, DNA damage (comet assay) and peroxidase activities (APOX and GPOX) were determined. The exposure time is a determinant factor in experiments designed to measure the influence of heavy metal contamination. The accumulation of Cd or Pb resulting from exposure to the two-metal mixture does not appear to depend significantly on whether the white clover is exposed to soil containing one heavy metal or both. However, when T. repens is exposed to a Cd/Pb mixture, the percentage of DNA damage is lower than when the plant is exposed to monometallic Cd. DNA damage is close to that observed in the case of monometallic Pb exposure. Peroxidase activity cannot be associated with DNA damage under these experimental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aina R, Palin L, Citterio S (2006) Molecular evidence for benzo[a]pyrene and naphthalene genotoxicity in Trifolium repens L. Chemosphere 65(4):666–673

    Article  CAS  Google Scholar 

  • Ajmone-Marsan F, Biasoli M (2010) Trace elements in soils of urban areas. Water Air Soil Pollut 213:121–143. doi:10.1007/s11270-010-0372-6

    Article  CAS  Google Scholar 

  • An Y-J, Kim Y-M, Kwon T-I, Jeong S-W (2004) Combined effect of copper, cadmium, and lead upon Cucumis sativus growth and bioaccumulation. Sci Total Environ 326:85–93

    Article  CAS  Google Scholar 

  • Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradere P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71:2187–2192

    Article  CAS  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Bernard F, Brulle F, Dumez S, Lemiere S, Platel A, Nesslany F, Cuny D, Deram A, Vandenbulcke F (2014) Antioxidant responses of Annelids, Brassicaceae and Fabaceae to pollutants: A review. Ecotoxicol Environ Saf, in press

  • Bidar G, Garçon G, Pruvot C, Dewaele D, Cazier F, Douay F, Shirali P (2007) Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147(3):546–553

    Article  CAS  Google Scholar 

  • Bidar G, Pruvot C, Garçon G, Verdin A, Shirali P, Douay F (2009) Seasonal and annual variations of metal uptake, bioaccumulation, and toxicity in Trifolium repens and Lolium perenne growing in a heavy metal-contaminated field. Environ Sci Pollut Res Int 16(1):42–53

    Article  CAS  Google Scholar 

  • Bu-Olayan AH, Thomas BV (2009) Translocation and bioaccumulation of trace metals in desert plants of Kuwait governorates. Res J Environ Sci 3:581–587

    Article  CAS  Google Scholar 

  • Cesarino I, Araújo P, Paes Leme AF, Creste S, Mazzafera P (2013) Suspension cell culture as a tool for the characterization of class III peroxidases in sugarcane. Plant Physiol Biochem 62:1–10

    Article  CAS  Google Scholar 

  • Chen X, Wu C, Tang J, Hu S (2005) Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere 60:665–671

    Article  CAS  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  CAS  Google Scholar 

  • Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36

    Article  CAS  Google Scholar 

  • Dubey RS (2010) Metal toxicity, oxidative stress and antioxidative defense system in plants. In: Gupta SD (ed) Reactive oxygen species and antioxidants in higher plants. Science, USA, pp 177–203

    Chapter  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Ghiani A, Fumagalli P, Van Nguyen T, Gentili R, Citterio S (2014) The combined toxic and genotoxic effects of Cd and As to plant bioindicator Trifolium repens L. PLoS ONE 9(6), e99239. doi:10.1371/journal.pone.0099239

    Article  CAS  Google Scholar 

  • Gichner T, Patková Z, Száková J, Demnerová K (2004) Cadmium induces DNA damage in tobacco roots, but no DNA damage, somatic mutations or homologous recombination in tobacco leaves. Mutat Res 559(1–2):49–57

    Article  CAS  Google Scholar 

  • Gichner T, Žnidar I, Száková J (2008) Evaluation of DNA damage and mutagenicity induced by lead in tobacco plants. Mutat Res 652:186–190

    Article  CAS  Google Scholar 

  • Gupta DK, Huang HG, Corpas FJ (2013) Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res 20:2150–2161

    Article  CAS  Google Scholar 

  • Hevesy G (1923) the absorption and the translocation of lead by plants: a contribution to the application of the method of radioactive indicators in the investigation of the change of substance in plants. Biochem J 17:439–445

    Article  CAS  Google Scholar 

  • Irfan M, Hayat S, Ahmad A, Alyemeni MN (2013) Soil cadmium enrichment: allocation and plant physiological manifestations. Saudi J Biol Sci 20:1–10

    Article  CAS  Google Scholar 

  • Jonker MJ, Svendsen C, Bedaux JJM, Bongers M, Kammenga JE (2005) Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose response analysis. Environ Toxicol Chem 24:2701–2713

    Article  CAS  Google Scholar 

  • Kabata-Pendias A, Piotrowska M, Dudka M (1993) Trace elements in legumes and monocotyledons and the suitability for the assessment of soil Contamination. In: Markert B (ed) Plants are biomonitors for heavy metal in the terrestrial environment. Wheinheim, VCF 485–494

  • Koppen G, Verschaeve L (1996) The alkaline Comet test on plant cells: a new genotoxicity test for DNA strand breaks in Vicia faba root cells. Mutat Res 360:193–200

    Article  CAS  Google Scholar 

  • Koppen G, Toncelli LM, Triest L, Verschaeve L (1999) The comet assay: a tool to study alteration of DNA integrity in developing plant leaves. Mech Ageing Dev 110(1–2):13–24

    Article  CAS  Google Scholar 

  • Kreuzer L, Bonkowski M, Langel R, Scheu S (2004) Decomposer animals (Lumbricidae, Collembola) and organic matter distribution affect the performance of Lolium perenne (Poaceae) and Trifolium repens (Fabaceae). Soil Biol Biochem 36(12):2005–2011

    Article  CAS  Google Scholar 

  • Kumar PBAN, Dushenkov V, Motto H, Raskin (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–38. doi:10.1021/es00005a014

    Article  CAS  Google Scholar 

  • Kumar A, Prasad MNV, Sytar O (2012) Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere 89:1056–1065

    Article  CAS  Google Scholar 

  • Kumaravel TS, Jha AN (2006) Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutat Res 605:7–16

    Article  CAS  Google Scholar 

  • Liu JN, Zhoub QX, Sun T, Ma LQ, Wang S (2008) Growth responses of three ornamental plants to Cd and Cd–Pb stress and their metal accumulation characteristics. J Hazard Mater 151:261–267

    Article  CAS  Google Scholar 

  • Manier N, Deram A, Broos K, Denayer FO, Van Haluwyn C (2009) White Clover nodulation index in heavy metal contaminated soils a potential bioindicator. J Environ Qual 38:685–692

    Article  CAS  Google Scholar 

  • Manier N, Brulle F, Le Curieux F, Vandenbulcke F, Deram A (2012) Biomarker measurements in Trifolium repens and Eisenia fetida to assess the toxicity of soil contaminated with landfill leachate: a microcosm study. Ecotoxicol Environ Saf 80(1):339–348

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulae V, Van Breusegem F (2011) ROS signalling: the new wave? Trends Plant Sci 16(6):300–309

    Article  CAS  Google Scholar 

  • Mohsin Bhat T, Ansari MYK, Choudhary S, Aslam R, Alka (2011) Synergistic cytotoxic stress and DNA damage in Clover (Trifolium repens) exposed to heavy metal soil from automobile refining shops in Kashmir-Himalaya. ISRN Toxicol. doi:10.5402/2011/109092

    Google Scholar 

  • Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32:73–86

    Article  CAS  Google Scholar 

  • Panagos P, Van Liedekerke M, Yigini Y, Montanarella L (2013) Contaminated sites in Europe: review of the current situation based on data collected through a European network. J Environ Public Health Article ID 158764

  • Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. EEB 52:199–223

    Article  CAS  Google Scholar 

  • Pourrut B, Jean S, Silvestre J, Pinelli E (2011a) Lead-induced DNA damage in Vicia faba root cells: potential involvement of oxidative stress. Mutagen Res 726:123–128

    CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011b) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136. doi:10.1007/978-1-4419-9860-6_4

    CAS  Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Rodriguez-Serrano M, Gómez M, del Río LA, Sandalioa LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357

    Article  CAS  Google Scholar 

  • Rucińska R, Sobkowiak R, Gwóźdź EA (2004) Genotoxicity of Pb in lupin root cells as evaluated by the comet assay. Cell Mol Biol Lett 9(3):519–528

    Google Scholar 

  • Salazar MJ, Pignata ML (2014) Lead accumulation in plants grown in polluted soils: screening of native species for phytoremediation. J Geochem Explor 137:29–36

    Article  CAS  Google Scholar 

  • Sarwar N, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937

    CAS  Google Scholar 

  • Seregin IV, Ivanov VB (2001) Physiological aspects of cadmium and lead toxic effects on higher plants (review). Russ J Plant Physiol 48:523–544

    Article  CAS  Google Scholar 

  • Sharma RK, Agrawal M (2006) Single and combined effects of cadmium and zinc on carrots: uptake and bioaccumulation. J Plant Nutr 29:1791–1804

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175(1):184–191

    Article  CAS  Google Scholar 

  • Srivastava RK, Pandey P, Rajpoot R, Rani A, Dubey RS (2014) Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma 251:1047–1065

    Article  CAS  Google Scholar 

  • Sterckeman T, Douay F, Proix F, Fourrier H, Perdrix E (2002) Assessment of the contamination of cultivated soils by eighteen trace elements around smelters in the North of France. Water Air Soil Pollut 135:173–194

    Article  CAS  Google Scholar 

  • Symeonidis L, Karataglis S (1992) Interactive effects of cadmium, lead and zinc on root growth of two metal tolerant genotypes of Holcus lanatus L. Biometals 5:173–178

    Article  CAS  Google Scholar 

  • Taylor GJ (1989) Multiple metal stress in Triticum aestivum. Differentiation between additive, multiplicative, antagonistic, and synergistic effects. Can J Bot 67:2272–2276

    Article  CAS  Google Scholar 

  • Tkalec M, Štefanić PP, Cvjetko P, Šikić S, Pavlica M, Balen B (2014) The effects of cadmium-zinc interactions on biochemical responses in tobacco seedlings and adult plants. PLoS ONE 9(1), e87582. doi:10.1371/journal.pone.008758

    Article  CAS  Google Scholar 

  • White PA, Claxton LD (2004) Mutagens in contaminated soil: a review. Mutagen Res 567:227–345

    CAS  Google Scholar 

  • Wierzbicka MH, Przedpełska E, Ruzik R, Ouerdane L, Połeć-Pawlak K, Jarosz M, Szpunar J, Szakiel A (2007) Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma 231:99–111

    Article  CAS  Google Scholar 

  • Woźniak K, Blasiak J (2003) In vitro genotoxicity of lead acetate: induction of single and double DNA strand breaks and DNA-protein cross-links. Mutagen Res 535:127–139

    Google Scholar 

  • Zaidi A, Wani PA, Khan MS (2012) Toxicity of heavy metals to legumes and bioremediation. Edn. Springer, Wien, Austria, 245 p. ISBN 978-3-7091-0729-4

  • Zeng XB, Li LF, Mei XR (2008) Heavy metal content in Chinese vegetable plantation land soils and related source analysis. Agric Sci China 7:1115–1112

    Article  Google Scholar 

Download references

Acknowledgments

The present study was supported by a grant from ADEME (Agence De l’Environnement et de la Maîtrise de l’Energie) and Anses (Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail). Fabien Bernard was supported by a doctoral fellowship from ADEME, IRENI (Institut de Recherche en ENvironnement Industriel) and RégionNord/Pas-de-Calais. The authors gratefully thank Dr Franck Marot from ADEME (Agence De l’Environnement et de la Maitrise de l’Energie) for his financial support and helpful discussions.

Conflict of interest

The authors declare that there are no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Lanier.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lanier, C., Bernard, F., Dumez, S. et al. Combined effect of Cd and Pb spiked field soils on bioaccumulation, DNA damage, and peroxidase activities in Trifolium repens . Environ Sci Pollut Res 23, 1755–1767 (2016). https://doi.org/10.1007/s11356-015-5414-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5414-6

Keywords

Navigation