AJPS  Vol.5 No.26 , December 2014
Possible Application of the Medicinal Plant Hyoscyamus albus in Phytoremediation: Excess Copper Compensates for Iron Deficiency, Depending on the Light Conditions
Abstract: Seedlings of the medicinal plant Hyoscyamus albus were supplied with an excess of Cu to examine the possible application in phytoremediation. The seedlings were cultured in B5 medium supplied with basal 0.1 μM Cu and 200 μM Cu under various light conditions: short day (SD); long day (LD); and continuous light (CL). In addition, the effect of supplying 200 μM Cu under Fe deficiency was determined, in order to elucidate the interaction between Cu and Fe. Interestingly, Fe-deficiency symptoms that developed in plants grown with basic levels of Cu under LD almost disappeared when excess Cu was supplied. Plant growth mainly depended on the photo irradiation period (SD < LD~CL); and 200 μM Cu did not inhibit growth at all when Fe was available, whereas in the absence of Fe, CL caused damage to growth. Analysis of the Cu and Fe contents of the plants revealed that Cu was distributed equally in both the aerial parts and roots, whereas most of the Fe was found in the roots; under Fe deficiency, Cu accumulation in the roots apparently increased. Cu was mainly distributed in the soluble fraction, which included vacuoles and the cell-wall fraction. These results provide evidence indicating that H. albus seedlings are tolerant of Cu present in excess. Furthermore, excess Cu was able to compensate for Fe deficiency, depending on the light conditions. Continuous light inhibited this effect, probably as a result of the induction of Mn deficiency. The possible applications of this newly discovered cuprophyte are discussed.
Cite this paper: Tamari, N. , Mine, A. , Sako, A. , Tamagawa, S. , Tabira, Y. and Kitamura, Y. (2014) Possible Application of the Medicinal Plant Hyoscyamus albus in Phytoremediation: Excess Copper Compensates for Iron Deficiency, Depending on the Light Conditions. American Journal of Plant Sciences, 5, 3812-3822. doi: 10.4236/ajps.2014.526399.

[1]   Evans, W. (1996) Trease and Evans’ Pharmacognosy. WB Saunders Company Ltd., London.

[2]   Higa, A., Miyamoto, E., Rahman, L. and Kitamura, Y. (2008) Root Tip-Dependent, Active Riboflavin Secretion by Hyoscyamus albus Hairy Roots under Iron Deficiency. Plant Physiology and Biochemistry, 46, 452-460.

[3]   Higa, A., Mori, Y. and Kitamura, Y. (2010) Iron Deficiency Induces Changes in Riboflavin Secretion and the Mitochondrial Electron Transport Chain in Hairy Roots of Hyoscyamus albus. Journal of Plant Physiology, 167, 870-878.

[4]   FAO Repository (1998) Lecture Notes on the Major Soils of the World.

[5]   Burkhead, J.L., Reynolds, K.A., Abdel-Ghany, S.E., Cohu, C.M. and Pilon, M. (2009) Copper Homeostasis. New Phytologist, 182, 799-816.

[6]   Masarovicǒvá, E., Králǒvá, K. and Kummerova, M. (2010) Principles of Classification of Medicinal Plants as Hyperaccumulators or Excluders. Acta Physiologiae Plantarum, 32, 7.

[7]   Ravet, K. and Pilon, M. (2013) Copper and Iron Homeostasis in Plants: The Challenges of Oxidative Stress. Antioxidants & Redox Signaling, 19, 919-932.

[8]   Puig, S., Andrés-Colás, N., García-Molina, A. and Peñarrubia, L. (2007) Copper and Iron Homeostasis in Arabidopsis: Responses to Metal Deficiencies, Interactions and Biotechnological Applications. Plant, Cell & Environment, 30, 271-290.

[9]   Waters, B.M. and Armbrust, L.C. (2013) Optimal Copper Supply Is Required for Normal Plant Iron Deficiency Responses. Plant Signaling & Behavior, 8, 1-5.

[10]   Khan, F., Younas, A., Shaheeen, S., Yousaf, Z., Gilani, K., Munawar, M., Sia, Z. K., Ahmad, M. and Zafar, M. (2011) Scavenging Evaluation of Copper and Cadmium during in Vivo and in Vitro Growth of Lycopersicon esculentum Mill. by Atomic Absorption Spectroscopy. Journal of Medicinal Plants Research, 5, 6468-6472.

[11]   Küpper, H., Götz, B., Mijovilovich, A., Küpper, F.C. and Meyer-Klaucke, W. (2009) Complexation and Toxicity of Copper in Higher Plants. I. Characterization of Copper Accumulation, Speciation, and Toxicity in Crassula helmsii as a New Copper Accumulator. Plant Physiology, 151, 702-714.

[12]   Faucon, M.P., Shutcha, M.N. and Meerts, P. (2007) Revisiting Copper and Cobalt Concentrations in Supposed Hyperaccumulators from SC Africa: Influence of Washing and Metal Concentrations in Soil. Plant and Soil, 301, 29-36.

[13]   Murashige, T. and Skoog, F. (1962) A Revised Medium for Rapid Growth and Bioassay with Tobacco Tissue Cultures. Physiologia Plantarum, 15, 473-497.

[14]   Gamborg, O.L., Miller, R.A. and Ojima, K. (1968) Nutrient Requirements of Suspension Cultures of Soybean Root Cells. Experimental Cell Research, 50, 151-158.

[15]   Wang, X., Liu, Y., Zeng, G., Chai, L., Song, X., Min, Z. and Xiao, X. (2008) Subcellular Distribution and Chemical Forms of Cadmium in Bechmeria nivea L. Gaud. Environmental and Experimental Botany, 62, 389-395.

[16]   López-Millán, A.F., Morales, F., Andaluz, S., Gogorcena, Y., Abadía, A., De Las Rivas, J. and Abadía, J. (2000) Responses of Sugar Beet Roots to Iron Deficiency. Changes in Carbon Assimilation and Oxygen Use. Plant Physiology, 124, 885-898.

[17]   Landsberg, E.C. (1986) Function of Rhizodermal Transfer Cells in the Fe Stress Response Mechanism of Capsicum annuum L. Plant Physiology, 82, 511-517.

[18]   Rellán-álvarez, R., El-Jendoubi, H., Wohlgemuth, G., Abadía, A., Fiehn, O., Abadía, J. and álvarez-Fernández, A. (2011) Metabolite Profile Changes in Xylem Sap and Leaf Extracts of Strategy I Plants in Response to Iron Deficiency and Resupply. Frontiers in Plant Science, 2, 18.

[19]   Rombolà, A.D. and Tagliavini, M. (2006) Iron Nutrition of Fruit Tree Crops. In: Barton, L.L. and Abadía, J., Eds., Nutrition in Plants and Rhizospheric Microorganisms, Springer, Berlin, 61-83.

[20]   Martins, L.L. and Mourato, M.P. (2006) Effect of Excess Copper on Tomato Plants: Growth Parameters, Enzyme Activities, Chlorophyll, and Mineral Content. Journal of Plant Nutrition, 29, 2179-2198.

[21]   Pätsikkä, E., Kairavuo, M., Sersen, F., Aro, E.M. and Tyystjärvi, E. (2002) Excess Copper Predisposes Photosystem II to Photoinhibition in Vivo by Outcompeting Iron and Causing Decrease in Leaf Chlorophyll. Plant Physiology, 129, 1359-1367.

[22]   Potters, G., Pasternak, T.P., Guisez, Y., Palme, K.J. and Jansen, M.A. (2007) Stress-Induced Morphogenic Responses: Growing out of Trouble? Trends in Plant Science, 12, 98-105.

[23]   Lequeux, H., Hermans, C., Lutts, S. and Verbruggen, N. (2010) Response to Copper Excess in Arabidopsis thaliana: Impact on the Root System Architecture, Hormone Distribution, Lignin Accumulation and Mineral Profile. Plant Physiology and Biochemistry, 48, 673-682.

[24]   Foyer, C.H. and Noctor, G. (2009) Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications. Antioxidants and Redox Signaling, 11, 861-905.

[25]   Zappala, M.N., Ellzey, J.T., Bader, J., Peralta-Videa, J.R. and Gardea-Torresdey, J. (2013) Prosopis pubescens (Screw Bean Mesquite) Seedlings Are Hyperaccumulators of Copper. Archives of Environmental Contamination and Toxicology, 65, 212-223.

[26]   Valderrama, A., Tapia, J., Peñailillo, P. and Carvajal, D.E. (2013) Water Phytoremediation of Cadmium and Copper Using Azolla filiculoides Lam. in a Hydroponic System. Water and Environment Journal, 27, 293-300.

[27]   Dhir, B. and Srivastava, S. (2013) Heavy Metal Tolerance in Metal Hyperaccumulator Plant, Salvinia natans. Bulletin of Environmental Contamination and Toxicology, 90, 720-724.

[28]   Yang, M.J., Yang, X.E. and Römheld, V. (2002) Growth and Nutrient Composition of Elsholtzia splendens Nakai under Copper Toxicity. Journal of Plant Nutrition, 25, 1359-1375.

[29]   Khurana, N., Singh, M.V. and Chatterjee, C. (2006) Copper Stress Alters Physiology and Deteriorates Seed Quality of Rapeseed. Journal of Plant Nutrition, 29, 93-101.

[30]   Oliva, S.R., Mingorance, M.D., Valdés, B. and Leidi, E.O. (2010) Uptake, Localisation and Physiological Changes in Response to Copper Excess in Erica andevalensis. Plant and Soil, 328, 411-420.

[31]   Ke, W., Xiong, Z., Xie, M. and Luo, Q. (2007) Accumulation, Subcellular Localization and Ecophysiological Responses to Copper Stress in two Daucus carota L. Populations. Plant and Soil, 292, 291-304.

[32]   Wang, X.W. and Liu, Z.F. (2013) The Subcellular Distributions of Cadmium, Chromium, Copper, Plumbum and Zinc in Hyperaccumulator and Accumulator. Advanced Materials Research, 726-731, 2434-2437.

[33]   Bernal, M., Ramiro, M.V., Casesb, R., Picorel, R. and Yruela, I. (2006) Excess Copper Effect on Growth, Chloroplast Ultrastructure, Oxygen-Evolution Activity and Chlorophyll Fluorescence in Glycine max Cell Suspensions. Physiologia Plantarum, 127, 312-325.

[34]   Shi, J., Yuan, X., Chen, X., Wu, B., Huang, Y. and Chen, Y. (2011) Copper Uptake and Its Effect on Metal Distribution in Root Growth Zones of Commelina communis Revealed by SRXRF. Biological Trace Element Research, 141, 294-304.

[35]   Jiang, L.Y., Yang, X.E., Shi, W.Y., Ye, Z.Q. and He, Z.L. (2004) Copper Uptake and Tolerance in Two Contrasting Ecotypes of Elsholtzia argyi. Journal of Plant Nutrition, 27, 2067-2083.

[36]   Seigler, D.S. (2002) Plant Secondary Metabolism. Kluwer Academic Publishers, Dordrecht.

[37]   Chipeng, F.K., Hermans, C., Colinet, G., Faucon, M.P., Ngongo, M., Meerts, P. and Verbruggen, N. (2010) Copper Tolerance in the Cuprophyte Haumaniastrum katangense (S. Moore) P.A. Duvign. & Plancke. Plant and Soil, 328, 235-244.

[38]   Ghaderian, S.M. and Ravandi, A.A.G. (2012) Accumulation of Copper and Other Heavy Metals by Plants Growing on Sarcheshmeh Copper Mining Area, Iran. Journal of Geochemical Exploration, 123, 25-32.

[39]   Song, J., Zhao, F.J., Luo, Y.M., McGrath, S.P. and Zhang, H. (2004) Copper Uptake by Elsholtzia splendens and Silene vulgaris and Assessment of Copper Phytoavailability in Contaminated Soils. Environmental Pollution, 128, 307- 315.

[40]   Wink, M. (1993) Allelochemical Properties or the Raison D’être of Alkaloids. The Alkaloids, 43, 1-118.

[41]   Somers, E. (1963) The Uptake of Copper by Fungal Cells. Annals of Applied Biology, 51, 425-437.