NaCl protects against Cd and Cu-induced toxicity in the halophyte Atriplex halimus

Insaf Bankaji, Noomene Sleimi, Aurelio Gómez-Cadenas, Rosa M. Pérez-Clemente


The objective of the present work was to evaluate the extent of Cd- and Cu-induced oxidative stress and the antioxidant response triggered in the halophyte species Atriplex halimus after metallic trace elements exposure. Plants were treated for one month with Cd2+ or Cu2+ (400 µM) in the absence or presence of 200 mM NaCl in the irrigation solution. The interaction between salinity and heavy metal stress was analyzed in relation to plant growth, tissue ion contents (Na+, K+ and Mg2+), oxidative damage and antioxidative metabolism. Data indicate that shoot and root weight significantly decreased as a consequence of Cd2+- or Cu2+-induced stress. Metallic stress leads to unbalanced nutrient uptake by reducing the translocation of K+ and Mg2+ from the root to the shoot. The levels of malondialdehyde increased in root tissue when Cd, and especially Cu, were added to the irrigation solution, indicating that oxidative damage occurred. Results showed that NaCl gave a partial protection against Cd and Cu induced toxicity, although these contaminants had distinct influence on plant physiology. It can be concluded that salinity drastically modified heavy metal absorption and improved plant growth. Salinity also decreased oxidative damage, but differently in plants exposed to Cd or Cu stress.


Atriplex halimus; oxidative damage; trace element toxicity; salinity

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Aebi H, 1984. Catalase in vitro. Method Enzymol 105: 121-126.

Anderson ME, 1985. Determination of glutathione and glutathione disulfide in biological samples. Method Enzymol 113: 548-555.

Arbona V, Gómez-Cadenas A, 2008. Hormonal modulation of citrus responses to flooding. J Plant Growth Regul 27: 241-250.

Arbona V, Hossain Z, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A, 2008. Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132: 452-466.

Bankaji I, Sleimi N, López-Climent MF, Perez-Clemente RM, Gomez-Cadenas A, 2014. Effects of combined abiotic stresses on growth, trace element accumulation, and phytohormone regulation in two halophytic species. J Plant Growth Regul 33: 632-643.

Barthwal J, Nair S, Kakkar P, 2008. Heavy metal accumulation in medicinal plants collected from environmentally different sites. Biomed Environ Sci 4: 319-324.

Clemens S, Aarts MGM, Thomine S, Verbruggen N, 2013. Plant science: The key to preventing slow cadmium poisoning. Trends Plant Sci 18: 92-99.

Clemente R, Walkerb DJ, Pardo T, Martínez-Fernández D, Bernala MP, 2012. The use of a halophytic plant species and organic amendments for the remediation of a trace elements-contaminated soil under semi-arid conditions. J Hazard Mater 223-224: 63-71.

da Silva CTB, Souza VK, Da Silva APF, Lyra Lemos RP, Conserva LM, 2010. Determination of the phenolic content and antioxidant potential of crude extracts and isolated compounds from leaves of Cordia multispicata and Tournefortia bicolor. Pharm Biol 48: 63-69.

de Vos CHR, Vonk MJ, Vooijs R, Schat H, 1992. Glutathione depletion due to copper induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98: 853-885.

Fielding JL, Hall JL, 1978. A biolchemical and cytochemical study of peroxidase activity in roots of Pisum sativum: I. A comparison of dab-peroxidase and guaiacol-peroxidase with particular emphasis on the properties of cell wall activity. J Exp Bot 4: 969-981.

Foyer CH, Noctor G, 2005. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 7: 1866-1875.

Gattward JN, Almeida AAF, Souza JO, Gomes FP, Kronzucker HJ, 2012. Sodium-potassium synergism in Theobroma cacao: Stimulation of photosynthesis, water-use efficiency and mineral nutrition. Physiol Plant 146: 350-362.

Gomes-Junior RA, Moldes CA, Delite FS, Pompeu GB, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA, 2006. Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65: 1330-1337.

Han RM, Lefèvre I, Ruan CJ, Qin P, Lutts S, 2012. NaCl differently interferes with Cd and Zn toxicities in the wetland halophyte species Kosteletzkya virginica (L.) Presl. Plant Growth Regul 68: 97-109.

Hewitt EJ, 1966. Sand and water culture methods used in the study of plant nutrition. Technical Communication No. 22, 2nd ed. Com. Bur. of HortiCul. and Plant Crops East Malling. Maidstore, Kent.

Hirata K, Tsuji N, Miyamoto K, 2005. Biosynthetic regulation of phytochelatins, heavy metal-binding peptides. J Biosci Bioeng 100: 593-599.

Hodges DM, DeLong JM, Forney CF, Prange RK, 1999. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604-611.

Hossain MA, Hasanuzzaman M, Fujita M, 2011. Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean. Front Agric in China 5: 1-14.

Kachout SS, Mansoura AB, Leclerc JC, Jaffel K, Rejeb MN, Ouerghi Z, 2009. Effects of heavy metals on antioxidant activities of: Atriplex hortensis and Atriplex rosea. J Appl Bot Food Qual 83: 37-43.

Lee S, Moon JS, Ko TS, Petros D, Goldsbrough PB, Korban SS, 2003. Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131: 656-663.

Lefévre I, Marchal G, Meerts, P, Corréal E, Lutts S, 2009. Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65: 142-152.

Leitenmaier B, Küpper H, 2013. Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Scie 4 (20): 374.

Lopez-Chuken UJ, Young SD, 2005. Plant screening of halophyte species for cadmium phytoremediation. Z Naturforsch C 3: 236-243.

López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A, 2011. Effects of cadmium on gas exchange and phytohormone contents in citrus. Biol Plant 55: 187-190.

López-Climent MF, Arbona V, Pérez-Clemente RM, Zandalinas SI, Gómez-Cadenas A, 2014. Effect of cadmium and calcium treatments on phytochelatin and glutathione levels in citrus plants. Plant Biol 16: 79-87.

Lutts S, Lefevre I, Delpérée, Kivits S, Dechamps C, Robledo A, Correal E, 2004. Heavy metal accumulation by the halophyte species Mediterranean saltbush. J Environ Qual 33: 1271-1279.

Manousaki E, Kalogerakis N, 2009. Phytoextraction of Pb and Cd by the Mediterranean saltbuss (Atriplex halimus L.): metal uptake in relation to salinity. Environ Sci Pollut Res 16: 844-854.

Mendoza-Cózatl DG, Moreno-Sánchez R, 2006. Control of glutathione and phytochelatin synthesis under cadmium stress. Pathway modeling for plants J Theor Biol 238: 919-936.

Mourato M, Reis R, Martins LL, 2012. Characterization of plant antioxidative system in response to abiotic stresses: a focus on heavy metal toxicity. In: Advances in selected plant physiology aspects; Montanaro G (ed.). pp: 23-44. InTech, Croatia.

Nagarani N, JanakiDevi V, YokeshBabu M, Kumaraguru AK, 2012. Protective effect of Kappaphycus alvarezii (Rhodophyta) extract against DNA damage induced by mercury chloride in marine fish. Toxicol Environ Chem 94: 1401-1410.

Nakano Y, Asada K, 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Phys 22: 867-880.

Pan X, Yang J, Zhang D, Chen X, Mu S, 2011. Cu(II) complexation of high molecular weight (HMW) fluorescent substances in root exudates from a wetland halophyte (Salicornia europaea L.). J Biosci Bioeng 111: 193-197.

Panda SK, Matsumoto H, 2010. Changes in antioxidant gene expression and induction of oxidative stress in pea (Pisum sativum L.) under Al stress. Biometals 23: 753-762.

Romero‐Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gomez M, Del Rio LA, 1999. Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radical Research 31: 25-31.

Rosa SB, Caverzan A, Teixeira FK, Lazzarotto F, Silveira JAG, Ferreira-Silva SL Abreu-Neto J, Margis R, Margis-Pinheiro M, 2010. Cytosolic APx knockdown indicates an ambiguous redox responses in rice. Phytochemistry 71: 548-558.

Sbartai H, Djebar MR, Sbartai I, Berrabbah H, 2012. Bioaccumulation of cadmium and zinc in tomato (Lycopersicon esculentum L.) C R Biol 335: 585-593.

Stolt JP, Sneller FEC, Brynelsson T, Lundborg T, Schat H, 2003. Phytochelatin and cadmium accumulation in wheat. Environ Exp Bot 49: 21-28.

Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F, 2004. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39: 45-58.

Vranová E, Inzé D, Van Breusegem F, 2002. Signal transduction during oxidative stress. J Exp Bot 53: 1227-1236.

Walker DJ, Lutts S, Sánchez-García M, Correal E, 2014. Atriplex halimus L.: Its biology and uses. J Arid Environ 100-101: 111-121.

Watanabe ME, 1997. Phytoremediation on the brink of commercialisation. Environ Sci Tech 31: 182-186.

Xu J, Yin H, Liu X, Li X, 2010. Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231: 449-459.

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.

Zu Y, Li YT, Chen J, Chen H, Qin L, Schvartz C, 2005. Hyperaccumulation of Pb, Zn and Cd in herbaceous grown on lead-zinc mining area in Yunnan, China. Environ Int 31: 755-762.

DOI: 10.5424/sjar/2016144-10117