Abstract
Short-term responses of Sedum alfredii roots to Cd exposure was compared in Cd hyperaccumulator (HE) and nonhyperaccumulating ecotype (NHE). Cadmium exposure significantly inhibited root elongation and induced loss of plasma membrane integrity and lipid peroxidation of roots tips in the NHE, whereas these effects were much less pronounced in the HE plants. A strong accumulation of reactive oxygen species with increasing Cd concentration was noted in the NHE root tips, but not in HE. After Cd exposure, a dose-dependent decrease in oxidized glutathione and marked increase in reduced glutathione and non-protein thiols were observed in root tips of HE, but were not seen in the NHE plants. These results suggest that the HE tolerates high Cd in the environment through the differential adaptations against Cd-induced oxidative stress.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Abbreviations
- CAT:
-
catalase
- DHE:
-
dihydroethidium
- DTNB:
-
5,5′-dithiobis-2-nitrobenzoic acid
- GSH:
-
reduced glutathione
- GSSG:
-
oxidized glutathione
- MDA:
-
malondialdehyde
- NPT:
-
non-protein thiols
- ROS:
-
reactive oxygen species
- TBARS:
-
thiobarbituric acid reactive substances
- TCA:
-
trichloroacetic acid
- TMP:
-
2,2,6,6-tetramethyl-4-(methylsulfonyloxy)-1-piperidinooxy
References
Bertin, G., Averbeck, D.: Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences. — Biochemistry 88: 1549–1559, 2006.
Bidwell, S.D., Crawford, S.A., Woodrow, I.E., Sommer-Knudsen, J., Marshall, A.T.: Sub-cellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. — Plant Cell Environ. 27: 705–716, 2004.
Boominathan, R., Doran, P.M.: Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. — New Phytol. 156: 205–215, 2002.
Boominathan, R., Doran, P.M.: Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. — Biotechnol. Bioeng. 83: 158–167, 2003.
Clemens, S.: Molecular mechanisms of plant metal tolerance and homeostasis. — Planta 212: 475–486, 2001.
Das, P., Samantaray, S., Rout, G.R.: Studies on cadmium toxicity in plants: a review. — Environ. Pollut. 98: 29–36, 1997.
De Vos, C.H.R., Vonk, M.J., Vooijs, R., Schat, H.: Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. — Plant Physiol. 98: 853–858, 1992.
Dixit, V., Pandey, V., Shyam, R.: Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). — J. exp. Bot. 52: 1101–1109, 2001.
Dunand, C., Crevecoeur, M., Penel, C.: Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. — New Phytol. 174: 332–341, 2007.
Foreman, J., Demidchik, V., Bothwell, J.H.F., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D.G., Davies, J.M., Dolan, L.: Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. — Nature 422: 442–446, 2003.
Freeman, J.L., Persans, M.W., Nieman, K., Albrecht, C., Peer, W., Pickering, I.J., Salt, D.E.: Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. — Plant Cell 16: 2176–2191, 2004.
Gechev, T.S., Hille, J.: Hydrogen peroxide as a signal controlling plant programmed cell death. — J. cell. Biol. 168: 17–20, 2005.
Hall, J.L.: Cellular mechanisms for heavy metal detoxification and tolerance. — J. exp. Bot. 53: 1–11, 2002.
Han, Y., Zhang, J., Chen, X.Y., Gao, Z.Z., Xuan, W., Xu, S., Ding, X., Shen, W.B.: Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. — New Phytol. 177: 155–166, 2008.
Huang, H.G., Li, T.X., Tian, S.K., Gupta, D.K., Zhang, X.Z., Yang, X.E.: Role of EDTA in alleviating lead toxicity in accumulator species of Sedum alfredii H. — Bioresour. Technol. 99: 6088–6096, 2008.
Jin, X.F., Yang, X., Mahmood, Q., Islam, E., Liu, D., Li, H.: Response of antioxidant enzymes, ascorbate and glutathione metabolism towards cadmium in hyperaccumulator and nonhyperaccumulator ecotypes of Sedum alfredii H. — Environ. Toxicol. 23: 517–529, 2008a.
Jin, X.F., Yang, X.O., Islam, E., Liu, D., Mahmood, Q.: Effects of cadmium on ultrastructure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredii Hance. — J. Hazard. Materials 156: 387–397, 2008b.
Kramer, U., Cotter Howells, J.D., Charnock, J.M., Baker, A.J.M., Smith, J.A.C.: Free histidine as a metal chelator in plants that accumulate nickel. — Nature 379: 635–638, 1996.
Li, W.C., Ye, Z.H., Wong, M.H.: Effects of bacteria an enhanced metal uptake of the Cd/Zn-hyperaccumulating plant, Sedum alfredii. — J. exp. Bot. 58: 4173–4182, 2007.
Liszkay, A., Van der Zalm, E., Schopfer, P.: Production of reactive oxygen intermediates (O2 ·−, H2O2, and OH·) by maize roots and their role in wall loosening and elongation growth. — Plant Physiol. 136: 3114–3123, 2004.
Lu, L.L., Tian, S.K., Yang, X.E., Wang, X.C., Brown, P., Li, T.Q., He, Z.L.: Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. — J. exp. Bot. 59: 3203–3213, 2008.
Metwally, A., Safronova, V.I., Belimov, A.A., Dietz, K.J.: Genotypic variation of the response to cadmium toxicity in Pisum sativum. — J. exp. Bot. 56: 167–178, 2005.
Nedelkoska, T.V., Doran, P.M.: Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. — Biotechnol. Bioeng. 67: 607–615, 2000.
Pietrini, F., Iannelli, M.A., Pasqualini, S., Massacci, A.: Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. — Plant Physiol. 133: 829–837, 2003.
Rodriguez-Serrano, M., Romero-Puertas, M.C., Zabalza, A., Corpas, F.J., Gomez, M., Del Rio, L.A., Sandalio, L.M.: Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. — Plant Cell Environ. 29: 1532–1544, 2006.
Salt, D.E., Prince, R.C., Baker, A.J.M., Raskin, I., Pickering, I.J.: Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. — Environ. Sci. Technol. 33: 713–717, 1999.
Sandalio, L.M., Dalurzo, H.C., Gomez, M., Romero-Puertas, M.C., Del Rio, L.A.: Cadmium-induced changes in the growth and oxidative metabolism of pea plants. — J. exp. Bot. 52: 2115–2126, 2001.
Schutzendubel, A., Schwanz, P., Teichmann, T., Gross, K., Langenfeld-Heyser, R., Godbold, D.L., Polle, A.: Cadmiuminduced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. — Plant Physiol. 127: 887–898, 2001.
Sun, Q., Ye, Z.H., Wang, X.R., Wong, M.H.: Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. J. Plant Physiol. 164: 1489–1498, 2007.
Tian, S.K., Lu, L.L., Yang, X.E., Labavitch, J.M., Huang, Y.Y., Brown, P.: Stem and leaf sequestration of zinc at the cellular level in the hyperaccumulator Sedum alfredii. — New Phytol. 182: 116–126, 2009.
Ueno, D., Ma, J.F., Iwashita, T., Zhao, F.J., McGrath, S.P.: Identification of the form of Cd in the leaves of a superior Cd-accumulating ecotype of Thlaspi caerulescens using Cd-113-NMR. — Planta 221: 928–936, 2005.
Wojcik, M., Tukiendorf, A.: Glutathione in adaptation of Arabidopsis thaliana to cadmium stress. — Biol. Plant. 55: 125–132, 2011.
Xiong, Y.H., Yang, X.E., Ye, Z.Q., He, Z.L.: Characteristics of cadmium uptake and accumulation by two contrasting ecotypes of Sedum alfredii Hance. — J. Environ. Sci. 39: 2925–2940, 2004.
Yamamoto, Y., Kobayashi, Y., Devi, S.R., Rikiishi, S., Matsumoto, H.: Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. — Plant Physiol. 128: 63–72, 2002.
Yamamoto, Y., Kobayashi, Y., Matsumoto, H.: Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. — Plant Physiol. 125: 199–208, 2001.
Yang, X.E., Long, X.X., Ye, H.B., He, Z.L., Calvert, D.V., Stoffella, P.J.: Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). — Plant Soil 259: 181–189, 2004.
Zhu, Y.L., Pilon-Smits, E.A.H., Jouanin, L., Terry, N.: Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. — Plant Physiol. 119: 73–79, 1999a.
Zhu, Y.L., Pilon-Smits, E.A.H., Tarun, A.S., Weber, S.U., Jouanin, L., Terry, N.: Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing gammaglutamylcysteine synthetase. — Plant Physiol. 121: 1169–1177, 1999b.
Acknowledgements
This work was supported by Project from the National Natural Science Foundation of China (31000935), Key Project from Ministry of Environmental Protection of China (2011467057), “863” Target Goal Project from Ministry of Science of China (2009AA06Z316), and Project from Department of Education of Zhejiang Province (Y200909812). We thank Mr. Jianguo Zhao, Le Zhang and Huijuan Yang for their great assistance in our experiments.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Tian, S.K., Lu, L.L., Yang, X.E. et al. Root adaptations to cadmium-induced oxidative stress contribute to Cd tolerance in the hyperaccumulator Sedum alfredii . Biol Plant 56, 344–350 (2012). https://doi.org/10.1007/s10535-012-0096-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-012-0096-0