Skip to main content
SpringerLink
Log in

Lipid peroxidation and antioxidative response in Arabidopsis thaliana exposed to cadmium and copper

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Formation of lipid hydroperoxides, malondialdehyde (MDA) and hydroxyalkenals (HAEs), membrane damages and antioxidative response of plants expressed as changes in glutathione S-transferase activity (GST) and anthocyanin accumulation were studied in Arabidopsis thaliana (L.) Heynh cv. Columbia plants treated for 7 days with various concentrations: 5, 25, 50, 100 μM Cd and Cu. Increased lipid hydroperoxide content was metal concentration-dependent. The level of MDA + HAE was elevated in Cd- and Cu- treated plants, but it was metal concentration-dependent under Cu stress. Electrolyte leakage measurements showed a larger membrane damage under Cu- than Cd-treatment. In Cu-stressed plants, GST activity was always enhanced in comparison with control, while in plants exposed to Cd it dropped slightly at lower metal concentrations; but at 100 μM Cd it was even higher than in plants treated with the same Cu concentration. Anthocyanin accumulation was considerably higher under Cu than Cd stress. Both lipid peroxidation and antioxidative response was stronger in Cu- than Cd-treated Arabidopsis thaliana plants. Various mechanisms of defense against the lipid peroxidation products, depending on the metal type, are discussed.

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

Abbreviations

BHT:

2(6)-Di-tert-butyl-p-cresol

CDNB:

1-Chloro-2,4-dinitrobenzene

GST:

Glutathione S-transferase

HAEs:

Hydroxyalkenals

MDA:

Malondialdehyde

LOX:

Lipoxygenase

References

  • Alfenito MR, Souer E, Goodman CD, Buell R, Mol J, Koes R, Walbot V (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 10:1135–1149

    Article  CAS  PubMed  Google Scholar 

  • Ålin P, Danielson H, Mannervik B (1985) 4-Hydroxyalk-2-enals are substrates for glutathione transferase. FEBS Lett 179:267–270

    Article  PubMed  Google Scholar 

  • Bartosz G (1997) Oxidative stress in plants. Acta Physiol Plant 19:47–64

    Article  CAS  Google Scholar 

  • Bert V, Bonnin I, Saumitou-Laprade P, de Laguérie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57

    Article  CAS  Google Scholar 

  • Bette A, Kutschera U (1996) Pigment accumulation and photosynthesis in developing rye coleoptiles. Bot Acta 109:194–198

    CAS  Google Scholar 

  • Cadenas E (1989) Biochemistry of oxygen toxicity. Annu Rev Biochem 58:79–110

    Article  CAS  PubMed  Google Scholar 

  • Cho U-H, Park J-O (2000) Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156:1–9

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Hölzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266

    Article  CAS  Google Scholar 

  • 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 52:1101–1109

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA, Steele CL (1999) Flavonoids and isoflavonoids—a gold mine for metabolic engineering. Trends Plant Sci 4:394–400

    Article  PubMed  Google Scholar 

  • Djebali W, Zarrouk M, Brouquisse R, El Kahoui S, Limam F, Ghorbel MH, Chaibi W (2005) Ultrastructure and lipid alteration induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol 7:358–368

    Article  CAS  PubMed  Google Scholar 

  • Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2003) Response of the ascorbate-glutathione cycle to excess cooper in Arabidopsis thaliana (L.). Plant Sci 164:195–202

    Article  Google Scholar 

  • Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2004) Symptoms of copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana (L.). BioMetals 17:379–387

  • Duthie G, Crozier A (2000) Plant-derived phenolic antioxidants. Curr Opinion Lipid 11:43–47

    Article  CAS  Google Scholar 

  • Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198

    Article  CAS  PubMed  Google Scholar 

  • Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves; evidence for involvement of oxidative stress. Plant Sci 121:151–159

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Meth Enzymol 186:1–85

    Article  CAS  PubMed  Google Scholar 

  • Iannelli MA, Pietrini F, Fiore L, Petrilli L, Massacci A (2002) Antioxidant response to cadmium in Phragmites australis plants. Plant Physiol Biochem 40:977–982

    Article  CAS  Google Scholar 

  • Kappus H (1985) Lipid peroxidation: mechanism, analysis, enzymology and biological relevance. In: Sies H (ed) Oxidative stress. Academic Press, London, pp 273–310

    Google Scholar 

  • Kondo T, Yoshida K, Nakagawa A, Kawai T, Tamura H, Goto T (1992) Structural basis of blue-colour development in flower petals from Commelina communis. Nature 358:515–518

    Article  CAS  Google Scholar 

  • Krupa Z (1999) Cadmium against higher plant photosynthesis—a variety of effects and where do they possibly come from? Z Naturforsch 53c:723–729

    Google Scholar 

  • Krupa Z, Baranowska M, Orzeł D (1996) Can anthocyanins be considered as heavy metal stress indicator in higher plants? Acta Physiol Plant 18:147–151

    CAS  Google Scholar 

  • Lane TW, Morel FMM (2000) A biological function for cadmium in marine diatoms. Proc Nat Acad Sci USA 97:4627–4631

    Article  CAS  PubMed  Google Scholar 

  • Lange H, Shropshire W, Mohr H (1971) An analysis of phytochrome-mediated anthocyanin synthesis. Plant Physiol 47:649–655

    Article  PubMed  Google Scholar 

  • Liu D, Jiang W, Gao X (2003) Effects of cadmium on root growth, cell division and nucleoli in root tip cells of garlic. Biol Plant 47:79–83

    Article  CAS  Google Scholar 

  • Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20

    Article  CAS  Google Scholar 

  • Lozano-Rodriguez E, Hernandez LE, Bonay P, Carpena-Ruiz RO (1997) Distribution of cadmium in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 48:123–128

    Article  CAS  Google Scholar 

  • Maksymiec W (1997) Effect of copper on cellular processes in higher plants. Photosynthetica 34:321–342

    Article  CAS  Google Scholar 

  • Mannervik B, Guthenberg C (1981) Glutathione transferase. Meth Enzymol 77:231–235

    Article  CAS  PubMed  Google Scholar 

  • Mazhoudi S, Chaoui A, Ghorbal MH, El Ferjani E (1997) Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum Mill). Plant Sci 127:129–137

    Article  CAS  Google Scholar 

  • Metwally A, Safronova VI, Belimov AA, Dietz K-J (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178

    CAS  PubMed  Google Scholar 

  • Milosevic N, Slusarenko AJ (1996) Active oxygen metabolism and lignification in the hypersensitive response in bean. Physiol Mol Plant Pathol 49:148–158

    Article  Google Scholar 

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  CAS  PubMed  Google Scholar 

  • Rangel Z, Kordan HA (1987) Effect of growth regulators on light-dependent anthocyanins production in Zea mays seedlings. Physiol Plant 69:511–516

    Article  Google Scholar 

  • Rice-Evans C, Miller NJ, Papanga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–158

    Article  Google Scholar 

  • Romero-Puertas MC, Palma JM, Gómez M, del Rio LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686

    Article  CAS  Google Scholar 

  • Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Schröder P (2001) The role glutathione and glutathione S-transferases in plant reaction and adaptation to xenobiotics. In: Grill D, Tausz M, De Kok LJ (eds) Significance of glutathione in plant adaptation to the environment. Kluwer, Dordrecht, pp 185–206

    Google Scholar 

  • Shah K, Kumar RG, 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 161:1135–1144

    Article  CAS  Google Scholar 

  • Shewfelt RL, Purvis AC (1995) Toward a comprehensive model for lipid peroxidation in plant tissue disorders. HortScience 30:213–218

    CAS  Google Scholar 

  • Siedlecka A, Tukendorf A, Skórzyńska-Polit E, Maksymiec W, Wójcik M, Baszyński T, Krupa Z (2001) Angiosperms (Astraceae, Convolvulaceae, Fabaceae and Poaceae; other than Brassicaceae). In: Prasad MNV (ed) Metals in the environment: analysis by biodiversity. Marcel Dekker, Inc, New York, pp 171–217

    Google Scholar 

  • Skórzyńska-Polit E, Krupa Z (2003) Activity of lipoxygenase in Arabidopsis thaliana—a preliminary study. Cell Mol Biol Lett 8:79–284

    Google Scholar 

  • Skórzyńska-Polit E, Drążkiewicz M, Krupa Z (2003) The activity of the antioxidative system in cadmium-treated Arabidopsis thaliana. Biol Plant 47:71–78

    Article  Google Scholar 

  • Skórzyńska-Polit E, Pawlikowska-Pawlęga B, Szczuka E, Drążkiewicz M, Krupa Z (2006) The activity and localization of lipoxygenases in Arabidopsis thaliana under cadmium and copper stresses. Plant Growth Reg 48:29–39

    Article  Google Scholar 

  • Spiteller G (1996) Enzymatic lipid peroxidation—a consequence of cell injury? Free Radical Biol Med 21:1003–1009

    Article  CAS  Google Scholar 

  • Spiteller G (2003) The relationship between changes in the cell wall, lipid peroxidation, proliferation, senescence and cell death. Physiol Plant 119:5–18

    Article  CAS  Google Scholar 

  • Tsuda T, Shiga K, Ohshima K, Kawakishi S, Osawa T (1996) Inhibition of lipid peroxidation and the active oxygen radical scavenging effect of anthocyanin pigments isolated from Phaseolus vulgaris L. Biochem Pharm 52:1033–1039

    Article  CAS  PubMed  Google Scholar 

  • Uchida K (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 42:318–343

    Article  CAS  PubMed  Google Scholar 

  • Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Ewa Skórzyńska-Polit

    Present address: Department of Plant Physiology and Biotechnology, The John Paul II Catholic University of Lublin, Konstantynow1H, 20-708, Lublin, Poland

Authors and Affiliations

  1. Department of Plant Physiology, Maria Curie-Skłodowska University, Akademicka 19, 20-033, Lublin, Poland

    Maria Drążkiewicz & Zbigniew Krupa

Authors
  1. Ewa Skórzyńska-Polit
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Drążkiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zbigniew Krupa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ewa Skórzyńska-Polit.

Additional information

Communicated by M. N. V. Prasad.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Skórzyńska-Polit, E., Drążkiewicz, M. & Krupa, Z. Lipid peroxidation and antioxidative response in Arabidopsis thaliana exposed to cadmium and copper. Acta Physiol Plant 32, 169–175 (2010). https://doi.org/10.1007/s11738-009-0393-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-009-0393-1

Keywords

Search

Navigation