Abstract
A facultative halophite Mesembryanthemum crystallinum L. (the common ice plant) was shown to grow successively at the high concentrations of Cu and Zn. Although 25 µM CuSO4 or 800 µM ZnSO4 retarded markedly plant growth, they did not interfere with the completion of plant development and the formation of viable seeds. In such plants, leaves accumulated more than 200 µg of Cu and 1700 µg of Zn per 1 g of dry weight. A damaging effect of heavy metals (HMs) was manifested in a reduced content of water in leaves and proline accumulation in them. As copper is a metal with transient valence, copper salts are more toxic than zinc salts, which was manifested in a stronger inhibition of the chlorophyll synthesis. Both HMs induced oxidative stress, as evident from increased activities of guaiacol peroxidase and lipoxygenase. Moderate Cu and Zn concentrations did not damage cell membranes in leaves, as evident from the absence of their action on electrolyte leakage either under optimum conditions or after heat treatment. A capability of a substantial HM accumulation by the common ice plant and their considerable transport to shoots (up to 50 µg of Cu and 560 µg of Zn per plant) make it possible to consider the common ice plant as a promising phytoremediator.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Abbreviations
- Chl:
-
chlorophyll
- HM:
-
heavy metal
- MDA:
-
malondialdehyde
- ROS:
-
reactive oxygen species
- TBA:
-
thiobarbituric acid
REFERENCES
Il'in, V.B., Tyazhelye metally v sisteme pochva-rastenie (Heavy Metals in the Soil-Plant System), Novosibirsk: Nauka, 1991.
Dan, T., Raj, S.K., and Saxena, P.K., Physiology of Heavy Metal Uptake and Tolerance in Plants, Agro's Annu. Rev. Plant Physiol. (India), 1998–1999, vol. 4, pp. 195–213.
Lombi, E., Zhao, F.J., Dunham, S.J., and McGrath, S.P., Phytoremediation of Heavy Metal-Contaminated Soils: Natural Hyperaccumulation versus Chemically Enhanced Phytoextraction, J. Environ. Qual., 2001, vol. 30, pp. 1919–1926.
Schuetzenduebel, A. and Polle, A., Plant Responses to Abiotic Stresses: Heavy Metal-Induced Oxidative Stress and Protection by Mycorrhization, J. Exp. Bot., 2002, vol. 53, pp. 1351–1365.
De Vos, C.H.R., Schat, H., de Waal, M.A.M., Vooijs, R., and Ernst, W.H.O., Increased Resistance to Copper-Induced Damage of the Root Cell Plasmalemma in Copper Tolerant Silene cucubalus, Physiol. Plant., 1991, vol. 82, pp. 523–528.
Ivanov, V.B., Bystrova, E.I., and Seregin, I.V., Comparative Impacts of Heavy Metals on Root Growth as Related to Their Specificity and Selectivity, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 445–454 (Russ. J. Plant Physiol., Engl. Transl., pp. 398–406).
Lukatkin, A.S., Bashmakov, D.I., and Kipaikina, N.V., Protective Role of Thidiazuron Treatment on Cucumber Seedlings Exposed to Heavy Metals and Chilling, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 346–348 (Russ. J. Plant Physiol., Engl. Transl., pp. 305–307).
Cunningham, S.D. and Ow, D.W., Promises and Prospect of Phytoremediation, Plant Physiol., 1996, vol. 110, pp. 715–719.
Zhulidov, D.A., Robards, R.D., Zhulidov, A.V., Zhulidova, O.V., Markelov, D.A., Rusanov, V.A., and Headley, J.V., Zinc Accumulation by Slime Mold Fuligo septica (L.) Wiggers in the Former Soviet Union and North Korea, J. Environ. Qual., 2002, vol. 31, pp. 1038–1042.
Gleba, D., Borisjuk, N.V., Borisjuk, L.G., Kneer, R., Poulev, A., Skarzhinskaya, M., Dushenkov, S., Logendra, S., Gleba, Y.Y., and Raskin, I., Use of Plant Roots for Phytoremediation and Molecular Farming, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 5973–5977.
Lasat, M.M., Phytoextraction of Toxic Metals: A Review of Biological Mechanisms, J. Environ. Qual., 2002, vol. 31, pp. 109–120.
Kuznetsov, Vl.V., Neto, D.S., Borisova, N.N., Dam, Z.B., Rakitin, V.Yu., Aleksandrova, S.N., and Kholodova, V.P., Stress-Induced CAM Development and the Limit of Adaptation Potential in Mesembryanthemum crystallinum Plants under Extreme Conditions, Fiziol. Rast. (Moscow), 2000, vol. 47, pp. 190–198 (Russ. J. Plant Physiol., Engl. Transl., pp. 168–175).
Shevyakova, N.I., Netronina, I.A., Aronova, E.E., and Kuznetsov, Vl.V., Compartmentation of Cadmium and Iron in Mesembryanthemum crystallinum Plants during the Adaptation to Cadmium Stress, Fiziol. Rast. 2003, vol. 50, pp. 756–763 (Russ. J. Plant Physiol., Engl. Transl., pp. 678–685).
Thomas, J.C., Malik, F.K., Endreszl, C., Davis, E.C., and Murray, K.S., Distinct Responses to Copper Stress in the Halophyte Mesembryanthemum crystallinum, Physiol. Plant., 1998, vol. 102, pp. 360–368.
Winter, K., Zum Problem der Ausbildung des Crassula-ceensaurestoffwechsels bei Mesembryanthemum crystallinum unter NaCl-Einfluss, Planta, 1973, vol. 109, pp. 135–145.
Golubkina, N.A., Fluorimetry for Selenium Analysis, Zh. Anal. Khim., 1995, vol. 50, pp. 492–497.
Shlyk, A.A., Determination of Chlorophylls and Carotenoids in Extracts from Green Leaves, Biokhimicheskie metody v fiziologii rastenii (Biochemical Methods in Plant Physiology), Pavlinova, O.A., Ed., Moscow: Nauka, 1971.
Bates, L.S., Waldren, R.P., and Teare, I.D., Rapid Determination of Free Proline for Water-Stress Studies, Plant Soil, 1973, vol. 39, pp. 205–207.
Heath, R.L. and Packer, L., Photoperoxidation in Isolated Chloroplasts. Kinetics and Stoichiometry of Fatty Acid Peroxidation, Arch. Biochem. Biophys., 1968, vol. 125, pp. 189–198.
Ridge, I. and Osborne, D.J., Role of Peroxidase when Hydroxyproline-Rich Protein in Plant Cell Wall Is Increased by Ethylene, Nature (New Biol.), 1971, vol. 229, pp. 205–208.
Bradford, M.M., A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Proteins Utilizing the Principle of Protein-Dye Binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.
Dospekhov, B.A., Metodika polevogo opyta s osnovami statisticheskoi obrabotki rezul'tatov issledovanii (Methods of Field Experiments with Basics of Statistical Processing of Results), Moscow: Agropromizdat, 1985.
Kuznetsov, Vl.V. and Shevyakova, N.I., Proline under Stress: Biological Role, Metabolism, and Regulation, Fiziol. Rast. (Moscow), 1999, vol. 46, pp. 305–320 (Russ. J. Plant Physiol., Engl. Transl., pp. 274–289).
Cuypers, A., Vangronsveld, J., and Clijsters, H., Peroxidases in Roots and Primary Leaves of Phaseolus vulgaris. Copper and Zinc Phytotoxicity: A Comparison, J. Plant Physiol., 2002, vol. 159, pp. 869–876.
Mahalingam, R. and Federoff, N., Stress Response, Cell Death and Signaling: The Many Faces of Reactive Oxygen Species, Physiol. Plant., 2003, vol. 119, pp. 56–68.
Maksymiec, W., Effect of Copper on Cellular Processes in Higher Plants, Photosynthetica, 1997, vol. 34, pp. 321–342.
Ramesh, S.A., Shin, R., Eide, D.J., and Schachman, D.P., Differential Metal Selectivity and Gene Expression of Two Zinc Transporters from Rice, Plant Physiol., 2003, vol. 133, pp. 126–134.
Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L.D., Lasat, M.M., Garvin, D.F., Eide, D., and Kochian, L.V., The Molecular Physiology of Heavy Metal Transport in the Zn/Cd Hyperaccumulator Thlaspi caerulescens, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 4956–4960.
Patsikka, E., Kairavuo, M., Sersen, F., Aro, E.-M., and Tyystjarvi, E., Excess Copper Predisposes Photosystem II to Photoinhibition In Vivo by Outcompeting Iron and Causing Decrease in Leaf Chlorophyll, Plant Physiol., 2002, vol. 129, pp. 1359–1367.
Chaney, R.L., Malik, M., Li, Y.M., Brown, S.L., Brewer, E.P., Angle, J.S., and Baker, A.J.M., Phytoremediation of Soil Metals, Curr. Opin. Biotechnol., 1997, vol. 8, pp. 279–284.
Frerot, H., Petit, C., Lefebvre, C., Gruber, W., Collin, C., and Escarre, L., Zinc and Cadmium Accumulation in Controlled Crosses between Metallicolous and Nonmetallicolous of Thlaspi caerulescens, New Phytol., 2002, vol. 157, pp. 643–648.
Ellis, D.R., Lypez-Millon, A.F., and Grusak, M.A., Metal Physiology and Accumulation in a Medicago truncatula Mutant Exhibiting an Elevated Requirement for Zinc, New Phytol., 2003, vol. 158, pp. 207–218.
Malaisse, F., Gregoire, J., Brooks, R.R., Morrisson, R.S., and Reeves, R.D., Aeollanthus biformifolius De Wild.: A Hyperaccumulator of Copper in Zaire, Science, 1978, vol. 199, pp. 887–888.
Patsikka, E., Aro, E.-M., and Tyystjarvi, E., Increase in the Quantum Yield of Photoinhibition Contributes to Copper Toxicity In Vivo, Plant Physiol., 1998, vol. 117, pp. 619–627.
Quartacci, M.F., Pinzino, C., Sgherri, C.L.M., Vecchia, F.D., and Navari-Izzo, F., Growth in Excess Copper Induces Changes in the Lipid Composition and Fluidity of PSII-Enriched Membranes in Wheat, Physiol. Plant., 2000, vol. 108, pp. 87–93.
Hall, J.L., Cellular Mechanisms for Heavy Metal Detoxification and Tolerance, J. Exp. Bot., 2002, vol. 53, pp. 1–11.
Murphy, A. and Taiz, L., Comparison of Metallothionein Gene Expression and Nonprotein Thiols in Ten Arabidopsis Ecotypes, Plant Physiol., 1995, vol. 109, pp. 945–954.
Brkljacic, J.M., Samardzic, J.T., Timotijevic, G.S., and Maksimovic, V.R., Expression Analysis of Buckwheat (Fagopyrum esculentum Moench) Metallothionein-Like Gene (MT3) under Different Stress and Physiological Conditions, J. Plant Physiol., 2004, vol. 161, pp. 741–746.
Author information
Authors and Affiliations
Additional information
__________
Translated from Fiziologiya Rastenii, Vol. 52, No. 6, 2005, pp. 848–858.
Original Russian Text Copyright © 2005 by Kholodova, Volkov, Kuznetsov.
Rights and permissions
About this article
Cite this article
Kholodova, V.P., Volkov, K.S. & Kuznetsov, V.V. Adaptation of the Common Ice Plant to High Copper and Zinc Concentrations and Their Potential Using for Phytoremediation. Russ J Plant Physiol 52, 748–757 (2005). https://doi.org/10.1007/s11183-005-0111-9
Received:
Issue Date:
DOI: https://doi.org/10.1007/s11183-005-0111-9