Skip to main content
SpringerLink
Log in

Interactive effects of cadmium and copper on metal accumulation, oxidative stress, and mineral composition in Brassica napus

  • Original Paper
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

Heavy metals’ frequent occurrence and toxicity caused considerable concerns in assessing the interactive effects of metals on exposed plants. Therefore, a hydroponic study was conducted to assess the growth response and physio-chemical changes in Brassica napus plants under single and combined stress of two environmentally alarming metals (Cd and Cu). Results showed that 15-day metal exposure to different metal concentrations (0, 50, 200 µM) significantly enhanced Cd accumulation, while lesser extent of Cu was observed in plant tissues. Nonetheless, Cu caused more pronounced oxidative damages and plant growth retardation. Both metals showed similar trend of changes in mineral composition, although Cu proved more damaging effect on K and Mn contents, and Cd on Zn contents. In combined treatments, Cd stimulated Cu uptake, notably at low concentration, while its own uptake was restricted by the presence of Cu. At either level of concentration, combined stress of these metals exacerbated plant growth inhibition and caused further oxidative damages compared to their individual stress. However, metals synergistic effects occurred only in conditions where Cu uptake was enhanced by Cd. A greater synergistic effect was observed in sensitive cultivar Zheda 622 as compared to the tolerant cultivar ZS 758. As to mineral composition, no metals synergistic effects were noted. This study highlighted the ecotoxicological significance of Cd-led Cu uptake in B. napus, which was assumed to drive metals’ synergistic toxicity, and showed that the relationship between Cd-led Cu uptake and plant growth responses could vary with respect to cultivar.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ali S, Zeng FR, Qiu BY, Cai SG, Qiu L, Wu FB, Zhang GP (2011) Interactive effects of aluminum and chromium stresses on the uptake of nutrients and the metals in barley. Soil Sci Plant Nutr 57(1):68–79

    Article  CAS  Google Scholar 

  • Ali B, Huang CR, Qi ZY, Ali S, Daud MK, Geng XX, Liu HB, Zhou WJ (2013a) 5-Aminolevulinic acid ameliorates cadmium-induced morphological, biochemical and ultrastructural changes in seedlings of oilseed rape. Environ Sci Pollut Res 20:7256–7267

    Article  CAS  Google Scholar 

  • Ali B, Tao Q, Zhou Y, Gill RA, Ali S, Rafiq MT, Xu L, Zhou WJ (2013b) 5-Aminolevulinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. Ecotoxicol Environ Saf 92:271–280

    Article  CAS  Google Scholar 

  • Ali B, Qian P, Jin R, Ali S, Khan M, Aziz R, Tian T, Zhou W (2014) Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. Biol Plant 58(1):131–138

    Article  CAS  Google Scholar 

  • Al-Subu MM, Salim R, Douleh A, Atallah A (1993) Combined effects of cadmium, lead and copper on the growth and on metal uptake of broad beans, carrots, radishes and marrow vegetables. Rev Int Contam Ambient 9(1):1–9

    CAS  Google Scholar 

  • An YJ, Kim YM, Kwon TI, Jeong SW (2004) Combined effect of copper, cadmium, and lead upon Cucumis sativus growth and bioaccumulation. Sci Total Environ 326:85–93

    Article  CAS  Google Scholar 

  • Andres-Colas N, Perea-Garcia A, Puig S, Penarrubia L (2010) Deregulated copper transport affects Arabidopsis development especially in the absence of environmental cycles. Plant Physiol 153:170–184

    Article  CAS  Google Scholar 

  • Andresen E, Küpper H (2013) Cadmium toxicity in plants. Met Ions Life Sci 11:395–413

    Article  CAS  Google Scholar 

  • Belimov AA, Safronova VI, Tsyganov VE, Borisov AY, Kozhemyakov AP, Stepanok VV, Martenson AM, Gianinazzi-Pearson V, Tikhonvich IA (2003) Genetic variability in tolerance to cadmium and accumulation of heavy metals in pea (Pisum sativum L.). Euphytica 131:25–35

    Article  CAS  Google Scholar 

  • Burkhead J, Reynolds K, Abdel-Ghany S, Cohu C, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    Article  CAS  Google Scholar 

  • Burton KW, Morgan E, Roig A (1986) Interactive effects of cadmium, copper and nickel on the growth of sikta spruce and studies of metal uptake from nutrient solutions. New Phytol 108:549–557

    Article  Google Scholar 

  • 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 168:309–316

    Article  CAS  Google Scholar 

  • Cuypers A, Keunen E, Bohler S, Jozefczak M, Opdenakker K, Gielen H, Vercampt H, Bielen A, Schellingen K, Vangronsveld J, Remans T (2012) Cadmium and copper stress induce a cellular oxidative challenge leading to damage versus signalling. In: Gupta DK, Sandalio LM (eds) Metal toxicity in plants: perception, signaling and remediation. Springer, Berlin, pp 65–90

    Chapter  Google Scholar 

  • Davis RD, Becker PHT (1978) Upper critical levels of toxic elements in plants: II. Critical levels of copper in young barley, wheat, rape, lettuce and rye grass, and of nickel and zinc in young barley and rye grass. New Phytol 80:23–32

    Article  CAS  Google Scholar 

  • de López-Camelo GL, de Miguez RS, Marbán L (1997) Heavy metals input with phosphate fertilizers used in Argentina. Sci Total Environ 204(3):245–250

    Article  Google Scholar 

  • Farooq MA, Li L, Ali B, Gill RA, Wang J, Ali S, Gill MB, Zhou WJ (2015) Oxidative injury and antioxidant enzymes regulation in arsenic–exposed seedlings of four Brassica napus L. cultivars. Environ Sci Pollut Res 22:10699–10712

    Article  CAS  Google Scholar 

  • Franklin NM, Stauber JL, Lim RP, Petocz P (2002) Toxicity of metal mixtures to a tropical freshwater alga (Chlorella sp.): the effect of interactions between copper, cadmium, and zinc on metal cell binding and uptake. Environ Toxicol Chem 21:2412–2422

    Article  CAS  Google Scholar 

  • Ghasemi R, Ghaderian SM, Krämer U (2009) Interference of nickel with copper and iron homeostasis contributes to metal toxicity symptoms in the nickel hyperaccumulator plant Alyssum inflatum. New Phytol 184:566–580

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  Google Scholar 

  • Gill RA, Zang LL, Ali B, Farooq MA, Cui P, Yang S, Ali S, Zhou WJ (2015) Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 120:154–164

    Article  CAS  Google Scholar 

  • Gisi U (1996) Synergistic interaction of fungicides in mixtures. Phytopathology 86:1273–1279

    CAS  Google Scholar 

  • Gondar D, López R, Fiol S, Antelo JM, Arce F (2006) Cadmium, lead, and copper binding to humic acid and fulvic acid extracted from an ombrotrophic peat bog. Geoderma 135:196–203

    Article  CAS  Google Scholar 

  • Guo T, Zhang GP, Zhou M, Wu F, Chen JX (2004) Influence of aluminum and cadmium stresses on mineral nutrition and root exudates in two barley cultivars. Pedosphere 17(4):505–512

    Article  Google Scholar 

  • Guo TR, Zhang GP, Zhang YH (2007) Physiological changes in barley plants under combined toxicity of aluminum, copper and cadmium. Colloid Surface B 57(2):182–188

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Huang Y, Hu Y, Liu Y (2009) Combined toxicity of copper and cadmium to six rice genotypes (Oryza sativa L.). J Environ Sci 21:647–653

    Article  CAS  Google Scholar 

  • Islam MK, Khanam S, Lee SY, Waghmode TR, Alam I, Huh MR (2015) Interactive effects of arsenic and chromium stresses on mineral and metal uptake in jute (Corchorus olitorius L.). POJ 8(3):220–231

    Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2011) Trace elements in soils and plants, 4th edn. CRC Press, Boca Raton

    Google Scholar 

  • Kikuchi T, Okazaki M, Toyota K, Motobayashi T, Kato M (2007) The input–output balance of cadmium in a paddy field of Tokyo. Chemosphere 67:920–927

    Article  CAS  Google Scholar 

  • Kuboi T, Noguchi A, Yazaki J (1987) Relationship between tolerance and accumulation characteristics of cadmium in higher plants. Plant Soil 104:275–280

    Article  CAS  Google Scholar 

  • Lachman J, Dudjak J, Miholova D, Kolihova D, Pivec V (2004) Effect of cadmium stress on the uptake and distribution of microelements copper and zinc in plants parts of barley (Horderum sativum L.). SAB 35(3):81–86

    Google Scholar 

  • Lichtenthaler H, Wellburn A (1983) Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Lidon FC, Henriques FS (1992) Copper toxicity in rice: a diagnostic criteria and its effect on Mn and Fe contents. Soil Sci 154(2):130–135

    Article  CAS  Google Scholar 

  • Lin Y-F, Aarts GM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206

    Article  CAS  Google Scholar 

  • Lin S-L, Wu L (1994) Effects of copper concentration on mineral nutrient uptake and copper accumulation in protein of copper-tolerant and nontolerant Lotus purshianus L. Ecotoxicol Environ Saf 29(2):214–228

    Article  CAS  Google Scholar 

  • Liu Y, Vijver MG, Qiu H, Baas J, Peijnenburg W (2015) Statistically significant deviations from additivity: What do they mean in assessing toxicity of mixtures? Ecotoxicol Environ Saf 122:37–44

    Article  CAS  Google Scholar 

  • Momoh E, Zhou W (2001) Growth and yield responses to plant density and stage of transplanting in winter oilseed rape (Brassica napus L.). J Agron Crop Sci 186:253–259

    Article  Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    Article  CAS  Google Scholar 

  • Nishizono H, Ichikawa H, Suziki S, Ishii F (1987) The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense. Plant Soil 101:15–20

    Article  CAS  Google Scholar 

  • Oliveira LM, Ma LQ, Santos JA, Guilherme LR, Lessl JT (2014) Effects of arsenate, chromate, and sulfate on arsenic and chromium uptake and translocation by arsenic hyperaccumulator Pteris vittata L. Environ Pollut 184:187–192

    Article  Google Scholar 

  • Qian H, Li J, Pan X, Sun L, Lu T, Ran H, Fu Z (2009) Combined effect of copper and cadmium on heavy metals ions accumulation and antioxidative induction in Chlorella vulgaris. Bull Environ Contam Toxicol 87:512–516

    Article  Google Scholar 

  • Ravet K, Pilon M (2013) Copper and iron homeostasis in plants: the challenges of oxidative stress. Antioxid Redox Signal 19:919–932

    Article  CAS  Google Scholar 

  • Smith SR (2009) A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge: Review article. Environ Int 35:142–156

    Article  CAS  Google Scholar 

  • Spurgeon DJ, Jones MAH, Dorne J-L, Svendsen C, Swain S, Stürzenbaum SR (2010) Systems toxicology approaches for understanding the joint effects of environmental chemical mixtures. Sci Total Environ 408:3725–3734

    Article  CAS  Google Scholar 

  • Teisseire H, Couderchet M, Vernet G (1999) Phytotoxicity of diuron alone and in combination with copper or folpet on duckweed (Lemna minor). Environ Pollut 106:39–45

    Article  CAS  Google Scholar 

  • Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  CAS  Google Scholar 

  • Velikova V, Edreva A, Loreto F (2004) Endogenous isoprene protects Phragmites australis leaves against singlet oxygen. Physiol Plant 122:219–225

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:1–9

    Article  Google Scholar 

  • Wei B, Yang L (2010) A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchem J 9:99–107

    Article  Google Scholar 

  • Wong MK, Chuah GK, Ang KP, Koh LL (1986) Interactive effects of lead, cadmium and copper combinations in the uptake of metals and growth of Brassica chinensis. Environ Exp Bot 26(4):331–339

    Article  CAS  Google Scholar 

  • Wu FB, Zhang GP (2002) Genotypic differences in effect of Cd on growth and mineral concentrations in barley seedlings. Bull Environ Contam Toxicol 69:219–227

    Article  CAS  Google Scholar 

  • Wu J, Mo LY, Qin LT, Zhu ZQ, Zhu YN (2014) Research advancement of the joint toxicity of heavy metals mixture. Appl Mech Mater 522–524:532–536

    Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Int Sch Res Netw ISRN Ecol. doi:10.5402/2011/402647

    Google Scholar 

  • 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 76:167–179

    Article  CAS  Google Scholar 

  • Yadav S, Srivastava J (2014) Phytoremediation of cadmium toxicity by Brassica spp.: a review. Int. J Biol Sci 3(5):47–52

    Google Scholar 

  • Yu RL, Ji J, Yuan X, Song Y, Wang C (2012) Accumulation and translocation of heavy metals in the canola (Brassica napus L.) soil system in Yangtze river delta, China. Plant Soil 353:33–45

    Article  CAS  Google Scholar 

  • Žaltauskaitė J, Šliumpaitė I (2013) Single and combined toxicity of copper and cadmium to Horderum vulgare growth and heavy metal bioaccumulation. In: E3S Web of conferences, vol 1, p 15013. doi:10.1051/e3sconf/20130115013

  • Zeng F, Qiu B, Wu X, Niu S, Wu FB, Zhang GP (2012) Glutathione-mediated alleviation of chromium toxicity in rice plants. Biol Trace Elem Res 148:255–263

    Article  CAS  Google Scholar 

  • Zhou WJ (2001) Oilseed rape. In: Zhang GP, Zhou WJ (eds) Crop production. Zhejiang University Press, Hangzhou, pp 153–178

    Google Scholar 

  • Zhou Z, Zhou J, Li R, Wang H, Wang J (2007) Effect of exogenous amino acids on Cu uptake and translocation in maize seedlings. Plant Soil 292:105–117

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the National High Technology Research and Development Program of China (2013AA103007), Jiangsu Collaborative Innovation Center for Modern Crop Production, Special Fund for Agro-scientific Research in the Public Interest (201303022), National Natural Science Foundation of China (31570434), the Science and Technology Department of Zhejiang Province (2012C12902-1), and China Postdoctoral Science Foundation (2015M570512).

Author information

Authors and Affiliations

  1. Institute of Crop Science and Zhejiang Key Laboratory of Crop Germplasm, Zhejiang University, Hangzhou, 310058, China

    T. M. Mwamba, S. Ali, B. Ali, J. L. Lwalaba, M. A. Farooq & W. Zhou

  2. Department of Crop Science, Faculty of Agriculture, University of Lubumbashi, P.O. Box 1825, Lubumbashi, Democratic Republic of the Congo

    T. M. Mwamba & J. L. Lwalaba

  3. College of Agriculture and Food Science, Zhejiang A & F University, Lin’an, 311300, China

    H. Liu

  4. Zhuji Municipal Agro-Tech Extension Center, Zhuji, 311800, China

    J. Shou

Authors
  1. T. M. Mwamba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. L. Lwalaba
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. A. Farooq
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Shou
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. W. Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to H. Liu or W. Zhou.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mwamba, T.M., Ali, S., Ali, B. et al. Interactive effects of cadmium and copper on metal accumulation, oxidative stress, and mineral composition in Brassica napus . Int. J. Environ. Sci. Technol. 13, 2163–2174 (2016). https://doi.org/10.1007/s13762-016-1040-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-016-1040-1

Keywords

Search

Navigation