Phytochelatins and Metallothioneins: Molecular Approaches

Year 2012, Volume: 12 Issue: 1, 1 - 16, 01.04.2012

Mustafa Yıldız Süleyman Cenkci Hakan Terzi

Abstract

Keywords

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Fitoşelatinler ve Metallotiyoneinler: Moleküler Yaklaşımlar (011001) (1-16)

Abstract

Fitoşelatinler (PC’ler) ve metallotiyoneinler (MT’ler), bitkilerde ve diğer organizmalarda bulunan sisteince zengin proteinlerdir. PC’ler enzimatik olarak fitoşelatin sentaz (PCS) ile glutatyondan sentezlenirken, MT’ler ise gen ürünü polipeptitlerdir. Bitkilerde, PC’ler ve MT’lerin metal iyonlarını bağlayabildiklerinden dolayı ağır metal toleransı ve homeostazisinde fonksiyon gördükleri ileri sürülmüştür. PC sentaz enzimi ve MT’leri kodlayan genler bitkilerde ve diğer organizmalarda teşhis edilmiştir. PC'ler ve MT’ler ile ilgili genlerin genetik düzenlenmesi, bitkilerde ağır metal toleransının geliştirilmesi için oldukça önemlidir. Bu derlemede, PC’ler ve MT’lerin biyosentezi ve ağır metal stresi koşullarında ifadesi, düzenlenmesi ve muhtemel fonksiyonları hakkında son gelişmeler tartışılmıştır

Keywords

Bitkiler, Ağır metal stresi, Fitoşelatinler, Metallotiyoneinler, Detoksifikasyon, Tolerans

References

• Ahner, B. and Morel, F.M.M., 1999. Phytochelatins in microalgae. Progress in Phycological Research, 13, 1- 31.
• Arnetoli, M., Vooijs, R., ten Bookum, W., Galardi, F., Gonnelli, C., Gabbrielli, R., Schat, H. and Verkleij, J.A.C., 2008. Arsenate tolerance in Silene paradoxa does sequestration. Environmental Pollution, 152, 585- 591.
• phytochelatin-dependent
• Baker, A.J.M. and Brooks, R.R., 1989. Terrestrial higher plants which hyperaccumulate metallic elements–a review phytochemistry. Biorecovery, 1, 81-126. ecology and
• Bilecen, K., Ozturk, U.H., Duru, A.D., Sutlu, T., Petoukhov, M.V., Svergun, D.I., Koch, M.H., Sezerman, U.O., Cakmak, I. and Sayers, Z., 2005. Triticum durum metallothionein: Isolation of the gene and structural characterization of the protein using solution scattering and molecular modeling. Journal of Biological Chemistry, 280, 13701-13711.
• Blaylock, M.J. and Huang, J.W., 2000. Phytoextraction of Metals. In: Raskin, I. and Ensley, B.D. (eds.), Phytoremediation of Toxic Metals: Using Plants to Clean-up the Environment. Wiley, New York, pp. 53
• Blindauer, C.A., 2008. Metallothioneins with unusual residues: Histidines as modulators of zinc affinity and reactivity. Journal of Inorganic Biochemistry, 102, 507-521.
• Brunetti, P., Zanella, L., Proia, A., De Paolis, A., Falasca, G., Altamura, M.M., di Toppi, L.S., Costantino, P. and Cardarelli, M., 2011. phytochelatin content of Arabidopsis seedlings over- expressing the phytochelatin synthase gene AtPCS1. Journal of Experimental Botany, 62, 5509-5519.
• Chaurasia, N., Mishra, Y. and Rai, L. C., 2008. Cloning expression and analysis of phytochelatin synthase (pcs) gene from Anabaena sp. PCC 7120 offering multiple stress tolerance in Escherichia coli. Biochemical Communications, 376, 225-230. Biophysical Research
• Cherian, G.M. and Chan, H.M., 1993. Biological Functions of Metallothioneins: A Review. In: Suzuki, K.T., Metallothionein III Biological roles and medical implications (Advances in Life Sciences), Birkhäuser Verlag, pp. 87-109. Kimura, M., (Eds.),
• Chiang, H.C., Lo, J.C., and Yeh, K.C., 2006. Genes associated with heavy metal tolerance and accumulation Arabidopsis halleri: A genomic survey with cDNA Microarray. Environmental Science and Technology,
• Clemens, S., Kim, E.J., Neumann, D. and Schroeder, J.I., 1999. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO Journal, 18, 3325-3333.
• Clemens, S., 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie, 88, 1707-1719.
• Clemens, S. and Peršoh, S., 2009. Multi-tasking phytochelatin synthases. Plant Science, 177, 266- 271.
• Cobbett, C.S., 2000. Phytochelatins and their roles in heavy metal detoxification. Plant Physiology, 123, 825-832.
• Cobbett, C. and Goldsbrough, P.B., 2002. Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annual Reviews of Plant Biology, 53, 159-182.
• Collin-Hansen, C., Pedersen, S.A. and Andersan, R.A., 2007. First report of phytochelatins in a mushroom: Induction of phytochelatins by metal exposure in Boletus edulis. Mycologia, 99, 161-174.
• De Knecht, J.A., Van Dillen, M., Koevoets, P., Schat, H., Verkleij, J. and Ernst, W., 1994. Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris (chain length distribution and sulfide incorporation). Plant Physiology, 104, 255-261.
• Dixon, D.P., Cummins, L., Cole, D.J. and Edwards, R., 1998. Glutathione-mediated detoxification systems in plants. Current Opinions in Plant Biology, 1, 258- 266.
• Diwan, H., Khan, I., Ahmad, A. and Iqbal, M., 2010. Induction of phytochelatins and antioxidant defence system in Brassica juncea and Vigna radiata in response to chromium treatments. Plant Growth Regulation, 61, 97-107.
• Domènech, J., Orihuela, R., Mir, G., Molinas, M., Atrian, S. and Capdevila, M., 2007. The CdII-binding abilities of recombinant Quercus suber metallothionein: Bridging the gap between phytochelatins and metallothioneins. Journal of Biological Inorganic Chemistry, 12, 867-882.
• Duan, G.L., Hu, Y., Liu, W.J., Kneer, R., Zhao, F.J. and Zhu, Y.G., 2011. Evidence for a role of phytochelatins in regulating arsenic accumulation in rice grain. Environmental and Experimental Botany, 71, 416- 421.
• Ebbs, S., Lau, I., Ahner, B. and Kochian, L., 2002. Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J & C. Presl). Planta, 214, 635-640.
• Ernst, W.H., Krauss, G.J., Verkleij, J.A. and Wesenberg, D., 2008. Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell and Environment,
• Foley, R.C., Liang, Z.M. and Singh, K.B., 1997. Analysis of type 1 metallothionein cDNAs in Vicia faba. Plant Molecular Biology, 33, 583-591.
• Foyer, C.H. and Noctor, G., 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 17, 1866-1875.
• Freisinger, E., 2007. Spectroscopic characterization of a fruit-specific metallothionein: M. acuminata MT3. Inorganica Chimica Acta, 360, 369-380.
• Freisinger, E., 2009. Metallothioneins in plants. Metal Ions in Life Sciences, 5, 107-153.
• Gasic, K. and Korban, S.S., 2007. Expression of Arabidopsis phytochelatin synthase in indian mustard (Brassica juncea) plants enhances tolerance for Cd and Zn. Planta, 225, 1277-1285.
• Gisbert, C., Ros, R., De Haro, A., Walker, D.J., Pilar Bernal, M., Serrano, R. and Navarro-Avino, J., 2003. A plant genetically modified that accumulates Pb is especially Biochemical Communications, 303, 440-445. Biophysical Research
• Grill, E., Loffler, S., Winnaker, E.L. and Zenk, M.H., 1989. Phytochelatins, the heavy metal-binding peptides of plants, are synthesized from glutathione by a specific gammaglutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proceedings of the National Academy of Sciences, USA, 86, 6838-9842.
• Grispen, V.M.J., Irtelli, B., Hakvoort, H.W.J., Vooijs, R., Bliek, T., ten Bookum, W.M., Verkleij, J.A.C. and Schat, H., 2009. Expression of the Arabidopsis metallothionein 2b enhances arsenite sensitivity and root Environmental and Experimental Botany, 66, 69-73.
• Grispen, V.M.J., Hakvoort, H.W.J. Bliek, T., Verkleij, J.A.C. and Schat, H., 2011. Combined expression of the Arabidopsis metallothionein mt2b and the heavy metal transporting ATPase HMA4 enhances cadmium tolerance and the root to shoot translocation of cadmium and zinc in tobacco. Environmental and Experimental Botany, 72, 71-76.
• Gueldry, O., Lazard, M., Delort, F., Dauplais, M., Grigoras, I., Blanquet, S. and Plateau, P., 2003. Ycf1p dependent Hg(II) detoxification in Saccharomyces cerevisiae. European Journal of Biochemistry, 270, 2486-2496.
• Guo, W.-J., Bundithya, W. and Goldsbrough, P.B., 2003. Characterization of the Arabidopsis metallothionein gene family: Tissue-specific expression and induction during senescence and in response to copper. New Phytologist, 159, 369-381.
• Guo, J., Dai, X., Xu, W. and Ma, M., 2008. Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere, 72, 1020- 1026.
• Gupta, D.K., Huang, H.G., Yang, X.E., Razafindrabe, B.H.N. and Inouhe, M., 2010. The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. Journal of Hazardous Materials, 177, 437-444.
• Ha, S.B., Smith, A.P., Howden, R., Dietrich, W.M., Bugg, S., O'Connell, M.J., Goldsbrough, P.B. and Cobbett, C.S., 1999. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell, 11, 1153-1163.
• Hammond, J.P., Bowen, H.C., White, P.J., Mills, V., Pyke, K.A., Baker, A.J., Whiting, S.N., May, S.T. and Broadley, M.R., 2006. A comparison of the Thlaspi caerulescens transcriptomes. New Phytologist, 170, 239-260.
• Hassinen, V.H., Tuomainen, M., Peräniemi, S., Schat, H., Kärenlampi, S.O. and Tervahauta, A.I., 2009. Metallothioneins 2 and 3 contribute to metal- adapted phenotype but are not directly linked to Zn accumulation in metal hyperaccumulator, Thlaspi caerulescens. Journal of Experimental Botany, 60, 187-196.
• Hassinen, V.H., Tervahauta, A.I., Schat, H. and Kärenlampi, S.O., 2011. Plant metallothioneins – Metal chelators with ROS scavenging activity? Plant Biology, 13, 225-232.
• Heiss, S., Wachter, A., Bogs, J., Cobbett, C. and Rausch, T., 2003. Phytochelatin synthase (PCS) protein is induced in Brassica juncea leaves after prolonged Cd exposure. Journal of Experimental Botany, 54, 1833- 1839.
• Huang, G.Y. and Wang, Y.S., 2009. Expression analysis of type 2 metallothionein gene in mangrove species (Bruguiera gymnorrhiza) under heavy metal stress. Chemosphere, 77, 1026-1029.
• Huang, G.Y. and Wang, Y.S., 2010. Expression and characterization analysis of type 2 metallothionein from grey mangrove species (Avicennia marina) in response to metal stress. Aquatic Toxicology, 99, 86- 92.
• Huang, G.Y., Wang, Y.S. and Ying, G.G., 2011. Cadmium- inducible BgMT2, a type 2 metallothionein gene from mangrove species (Bruguiera gymnorrhiza), its encoding protein shows metal-binding ability. Journal of Experimental Marine Biology and Ecology,
• Iglesia-Turiño, S., Febrero, A., Jauregui, O., Caldelas, C., Araus, J.L. and Bort, J., 2006. Detection and quantification of unbound phytochelatin 2 in plant extracts of Brassica napus grown with different levels of mercury. Plant Physiology, 142, 742-749.
• Jack, E., Hakvoort, H.W.J., Reumer, A., Verkleij, J.A.C., Schat H. and Ernst W.H.O., 2007. Real-time PCR analysis of metallothionein-2b expression in metallicolous and non-metallicolous populations of Silene vulgaris (Moench) Garcke. Environmental and Experimental Botany, 59, 84-91.
• Kamiya, T. and Fujiwara, T., 2011. A novel allele of the Arabidopsis conferring high sensitivity to arsenic and antimony. Soil Science and Plant Nutrition, 57, 272-278. gene
• Kim, D.Y., Bovet, L., Kushnir, S., Noh, E.W., Martinoia, E. and Lee, Y., 2006. AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiology, 140, 922
• Kohler, A., Blaudez, D., Chalot, M. and Martin, F., 2004. Cloning and expression of multiple metallothioneins from hybrid poplar. New Phytologist, 164, 83-93.
• Lane, B., Kajioka, R. and Kennedy, T., 1987. The Wheat- Germ-Ec Protein is a zinc containing metallothionein. Biochemistry and Cell Biology-Biochimie Et Biologie Cellulaire, 65, 1001-1005.
• Lee, S., Moon, J.S., Ko, T.S., Petros, D., Goldsbrough, P.B. and Korban, S.S., 2003. Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiology, 131, 656-663.
• Li, Z.S., Lu, Y.P., Zhen, R.G., Szczypka, M., Thiele, D.J. and Rea, P.A. 1997. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed bis(glutathionato)cadmium. Proceedings of the National Academy of Sciences, 94, 42-47. of
• Li, Y., Dhankher, O.M., Carreira, L., Lee, D., Chen, A., Schroeder, J.I., Balish, R.S. and Meagher, R.B., 2004. Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant and Cell Physiology, 45, 1787-1797.
• Li, J.C, Guo, J.B. Xu, W.Z. and Ma, M. 2007. RNA interference-mediated silencing of phytochelatin synthase gene reduce cadmium accumulation in rice seeds. Journal of Integrative Biology, 49, 1032-1037.
• Li, H., Shi, W.Y., Shao, H.B. and Shao, M.A., 2009. The remediation of the lead-polluted garden soil by natural zeolite. Journal of Hazardous Materials, 169, 1106-1111.
• Liang, G., Lia, X., Du, G. and Chen, J., 2009. A new strategy to enhance glutathione production by multiple H2O2-induced oxidative stresses in Candida utilis. Bioresource Technology, 100, 350-355.
• Liu, W.J., Wood, B.A., Raab, A., McGrath, S.P., Zhao, F.J. and Feldmann, J., 2010. Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis. Plant Physiology, 152, 2211-2221.
• Liu, G.Y., Zhang, Y.X. and Chai, T.Y., 2011. Phytochelatin sSynthase of Thlaspi caerulescens enhanced tolerance and accumulation of heavy metals when expressed in yeast and tobacco. Plant Cell Reports, 30, 1067-1076.
• Maier, T., Yu, C., Küllertz, G. and Clemens, S., 1993. Localization and functional characterization of metal- binding sites in phytochelatin synthases. Planta, 218, 300-308.
• Martinez, M., Bernal, P., Almela, C., Velez, D., Garcia- Agustin, P., Serrano, R. and Navarro-Avino, J., 2006. An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils. Chemosphere, 64, 478-485.
• Mendoza-Cozatl, D., Loza-Tavera, H., Hernández- Navarro, A. and Moreno-Sánchez, R., 2005. Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiology Reviews, 29, 653-671.
• Mendoza-Cozatl, D.G., Moreno, A.Q. and Zapata-Perez, O., 2007. Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, Avicennia germinans, exposed to cadmium and copper. Aquatic Toxicology, 83, 306- 314.
• Mendoza-Cozatl, D.G., Butko, E., Springer, F., Torpey, J.W., Komives, E.A., Kehr, J. and Schroeder, J.I., 2008. Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol–peptides in the long- distance transport of cadmium and the effect of cadmium on iron translocation. Plant Journal, 54, 249-259.
• Mendoza-Cozatl, D.G., Zhai, Z., Jobe, T.O., Akmakjian, G.Z., Song, W.Y., Limbo, O., Russell, M.R., Kozlovskyy, V.I., Martinoia, E., Vatamaniuk, O.K., Russell, P. and Schroeder J.I., 2010. Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance. Journal of Biological Chemistry, 285, 40416-40426.
• Mendoza-Cozatl, D.G., Jobe, T.O., Hauser, F. and Schroeder, J.I., 2011. Long-distance transport, vacuolar transcriptional responses induced by cadmium and arsenic. Current Opinion in Plant Biology, 14, 554- 562. tolerance, and
• Merrifield, M.E., Chaseley, J., Kille, P. and Stillman, M.J., 2006. stoichiometry in Fucus vesiculosus metallothionein. Chemical Research in Toxicology, 19, 365-375. cluster
• Mir, G., Domenech, J., Huguet, G., Guo, W.J., Goldsbrough, P., Atrian, S. and Molinas, M., 2004. A plant type 2 mt from cork tissue responds to oxidative stress. Journal of Experimental Botany, 55, 2483-2493.
• Murphy, A. and Zhou, J., 1997. Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana. Plant Physiology, 113, 1293-1301.
• Navabpour, S., Morris, K., Allen, R., Harrison, E.A.H., Mackerness, S. and Buchanan-Wollaston, V., 2003. Expression of senescence-enhanced genes in response to oxidative stress. Journal of Experimental Botany, 54, 2285-2292.
• Noctor, G. and Foyer, C., 1998. Ascorbate and glutathione: Keeping active oxygen under control. Annual Reviews of Plant Physiology and Plant Molecular Biology, 49, 249-279.
• Obertello, M., Wall, L., Laplaze, L., Nicole, M., Auguy, F., Gherbi, H., Bogusz, D. and Franche, C., 2007. Functional Analysis of the metallothionein gene cgMT1 isolated from the actinorhizal tree Casuarina glauca. Molecular Plant–Microbe Interactions, 20, 1231-1240.
• Ortiz, D.F., Ruscitti, T., McCue, K.F. and Ow, D.W., 1995. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. Journal of Biological Chemistry, 270, 4721-4728.
• Park, J., Song, W.Y., Ko, D., Eom, Y., Hansen, T.H., Schiller, M., Lee, T.G., Martinoia, E. and Lee, Y., 2012. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. The Plant Journal, 69, 278-288.
• Peroza, E.A., Schmucki, R., Güntert, P., Freisinger, E. and Zerbe, O., 2009. The metallothionein: A metalbinding domain with a distinctive structure. Journal of Molecular Biology,
• Pomponi, M., Censi, V., Di Girolamo, V., De Paolis, A., Di Toppi, L.S., Aromolo, R., Costantino, P. and Cardarelli, M., 2006. Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd(2+) tolerance and accumulation but not translocation to the shoot. Planta, 223, 180-190.
• Preveral, S., Gayet, L., Moldes, C., Hoffmann, J., Mounicou, S., Gruet, A., Reynaud, F., Lobinski, R., Verbavatz, J.M., Vavasseur, A. and Forestier, C., 2009. A common highly conserved cadmium detoxification mechanism from bacteria to humans: Heavy metal tolerance conferred by the ATP-binding cassette (ABC) transporter SpHMT1 requires glutathione but not metal-chelating phytochelatin peptides. Journal Biological Chemistry, 284, 4936- 4943.
• Rauser, W.E., 1999. Structure and function of metal chelators produced by plants the case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochemistry and Biophysics, 31, 19-48.
• Rea, P.A., 2007. Plant ATP-binding cassette transporters. Annual Reviews of Plant Biology, 58, 347-375.
• Robinson, N.J., Tommey, A.M., Kuske, C. and Jackson, P.J., 1993. Plant metallothioneins. Biochemistry Journal, 295, 1-10.
• Rodríguez-Llorente, I.D., Pérez-Palacios, P., Doukkali, B., Caviedes, M.A. and Pajuelo, E., 2010. Expression of the seed-specific metallothionein mt4a in plant vegetative tissues increases Cu and Zn tolerance. Plant Science, 178, 327-332.
• Roosens, N.H., Bernard, C., Leplae, R. and Verbruggen, N., 2004. Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Letters, 577, 9-16.
• Roosens, N.H., Leplae, R., Bernard, C. and Verbruggen, N., 2005. Variations in plant metallothioneins: The heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta, 222, 716-729.
• Ruiz, O.N., Alvarez, D., Torres, C., Roman, L. and Daniell, H. 2011. Metallothionein expression in chloroplasts enhances phytoremediation capability. Plant Biotechnology Journal, 9, 609-617. accumulation and
• Salt, D.E. and Rauser, W.E., 1995. MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiology, 107, 1293-1301.
• Samardžíc, J.T., Nikolíc, D.B., Timotijevíc, G.S., Jovanovíc, Z.S., Milisavljevíc, M.G. and Maksimovíc, V.R., 2010. Tissue expression analysis of FeMT3, a drought and oxidative stress related metallothionein gene from buckwheat (Fagopyrum esculentum). Journal of Plant Physiology, 167, 1407-1411.
• Sánchez-Fernández, R., Davies, T.G., Coleman, J. O. and Rea, P.A., 2001. The Arabidopsis thaliana ABC protein superfamily, a complete inventory. Journal of Biological Chemistry, 276, 30231-30244.
• Sauge-Merle, S., Cuine, S., Carrier, P., Lecomte-Pradines, C., Luu, D.T. and Peltier, G., 2003. Enhanced toxic metal accumulation in engineered bacterial cells expressing Arabidopsis thaliana phytochelatin synthase. Applied and Environmental Microbiology, 69, 490-494.
• Schat, H., Llugany, M., Vooijs, R., Hartley-Whitaker, J. and Bleeker, P.M., 2002. The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. Journal of Experimental Botany, 53, 2381-2392.
• Schicht, O. and Freisinger, E., 2009. Spectroscopic characterization of Cicer arietinum metallothionein 1. Inorganica Chimica Acta, 362, 714-724.
• Schor-Fumbarov, T., Goldsbrough, P.B., Adam, Z. and Tel-Or, E., 2005. Characterization and expression of a metallothionein gene in the aquatic fern Azolla filiculoides under heavy metal stress. Planta, 223, 69- 76.
• Singh, S., Lee, W., Dasilva, N.A., Mulchandani, A. ve Chen, W., 2008. Enhanced arsenic accumulation by engineered yeast cells expressing Arabidopsis thaliana phytochelatin synthase. Biotechnology and Bioengineering, 99, 333-340.
• Song, W.Y., Park, J., Mendoza-Cozatl, D.G., Suter- Grotemeyer, M., Shim, D., Hortensteiner, S., Geisler, M., Weder, B., Rea, P.A., Rentsch, D., Schroederc, J.I., Lee, Y. and Martinoia, E., 2010. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proceedings of the National Academy of Sciences, USA, 107, 21187- 21192.
• Sooksa-Nguan, T., Yakubov, B., Kozlovskyy, V.I., Barkume, C.M., Howe, K.J.H., Thannhauser, T.W., Rutzke, M.A., Hart, J.J., Kochian, L.V., Rea, P.A. and Vatamaniuk, O.K., 2009. Drosophila ABC transporter, DmHMT-1, confers tolerance to cadmium. DmHMT-1 and its yeast homolog, SpHMT-1, are not essential for vacuolar phytochelatin sequestration. Journal of Biological Chemistry, 284, 354-362.
• Sun, Q., Ye, Z.H., Wang, X.R. and Wong, M.H., 2007. Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. Journal of Plant Physiology, 164, 1489-1498.
• Tennstedt, P., Peisker, D., Bottcher, C., Trampczynska, A. and Clemens, S., 2009. Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiology, 149, 938-948.
• Tsai, S.L., Singh, S., DaSilva, N.A. and Chen, W., 2011. Co- expression of Arabidopsis thaliana phytochelatin synthase and Treponema denticola cysteine desulfhydrase for enhanced arsenic accumulation. Biotechnology and Bioengineering, 109, 605-608.
• Usha, B., Prashanth, S.R. and Parida, A., 2007. Differential expression of two metallothionein encoding genes during heavy metal stress in the mangrove species, Avicennia marina (Forsk.) Vierh. Current Science, 93, 1215-1219.
• Usha, B., Venkataraman, G. and Parida, A., 2009. Heavy metal and abiotic stress inducible metallothionein isoforms from Prosopis juliflora (SW) D.C. show differences in binding to heavy metals in vitro. Molecular Genetics and Genomics, 281, 99-108.
• Xiang, C. and Oliver, D., 1998. Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell, 10, 1539- 1550.
• Xue, T., Li, X., Zhu, W., Wu, C., Yang, G. and Zheng, C., 2009. Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. Journal of Experimental Botany, 60, 339-349.
• Vatamaniuk, O.K., Mari, S., Lu, Y.P. and Rea, P.A., 2000. Mechanism of heavy metal ion activation of phytochelatin (PC) synthase-blocked thiols are sufficient for pc synthase-catalyzed transpeptidation of glutathione and related thiol peptides. Journal of Biological Chemistry, 275, 31451-31459.
• Verbruggen, N., Hermans, C. and Schat, H., 2009. Mechanisms to cope with arsenic or cd excess in plants. current opinion in plant biology, 12, 364-372.
• Wachter, A., Wolf, S., Steininger, H., Bogs, J. and Rausch, T., 2005. Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications glutathione biosynthesis in the Brassicaceae. Plant Journal, 41, 15-30.
• compartmentation of
• Wan, X. and Freisinger, E., 2009. The plant metallothionein 2 from Cicer arietinum forms a single metal-thiolate cluster. Metallomics, 1, 489- 500.
• Wang, X., Song, Y., Mac, Y., Zhuo, R. and Jin, L., 2011. Screening of Cd tolerant genotypes and isolation of metallothionein genes in alfalfa (Medicago sativa L.). Environmental Pollution, 159, 3627-3633.
• Wojas, S., Clemens, S., Hennig, J., Skodowska, A., Kopera, E., Schat, H., Bal, W. and Antosiewicz, D.M., 2008. Overexpression of phytochelatin synthase in tobacco: Distinctive effects of AtPCS1 and CePCS genes on plant response to cadmium. Journal of Experimental Botany, 59, 2205-2219.
• Wong, H.L., Sakamoto, T., Kawasaki, T., Umemura, K. and Shimamoto, K., 2004. Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiology, 135, 1447-1456.
• Wu, G., Kang, H.B., Zhang, X.Y., Shao, H.B., Chu, L.Y. and Ruan, C.J., 2010. A critical review on the bio-removal of hazardous heavy metals from contaminated soils: Issues, progress, eco-environmental concerns and opportunities. Journal of Hazardous Materials, 174, 1-8.
• Yadav, S.K., 2010. Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South African Journal of Botany, 76, 167-179.
• Yang, P.G., Mao, R.Z., Shao, H.B. and Gao, Y.F., 2009a. An investigation on the distribution of eight hazardous heavy metals in the suburban farmland of China. Journal of Hazardous Materials, 167, 1246- 1251.
• Yang, Z., Wu, Y., Li, Y., Ling, H.Q. and Chu, C., 2009b. OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice. Plant Molecular Biology, 70, 219-229.
• Yang, J.L., Wang, Y.C., Liu, G.F., Yang, C.P. and Li, C.H., 2011. Tamarix hispida metallothionein-like ThMT3, a reactive oxygen species scavenger, increases tolerance against Cd2+, Zn2+, Cu2+, and NaCl in transgenic yeast. Molecular Biology Reports, 38, 1567-1574.
• Zhang, Y.W., Tam, N.F.Y. and Wong, Y.S., 2004. Cloning and characterization of type 2 metallothionein-like gene from a wetland plant Typha latifolia. Plant Science, 167, 869-877.
• Zhang, H., Xu, W., Guo, J., He, Z. and Ma, M., 2005. Coordinated responses of phytochelatins and metallothioneins to heavy metals in garlic seedlings. Plant Science, 169, 1059-1065.
• Zhang, Z.C., Chen, B.X. and Qiu, B.S., 2010. Phytochelatin synthesis plays a similar role in shoots of the cadmium hyperaccumulator Sedum alfredii as in non-resistant plants. Plant, Cell and Environment, 33, 1248-1255.
• Zhigang, A., Cuijie, L., Yuangang, Z., Yejie, D., Wachter, A., Gromes, R. and Rausch, T., 2006. Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. Journal of Experimental Botany, 57, 3575-3582.
• Zhou, J. and Goldsbrough, P.B., 1994. Functional homologs of fungal metallothionein genes from Arabidopsis. The Plant Cell, 6, 875-884.
• Zimeri, A.M., Dhankher, O.P., McCaig, B. and Meagher R.B., 2005. The plant MT1 metallothioneins are stabilized by binding cadmium and are required for cadmium tolerance and accumulation. Plant Molecular Biology, 58, 839-955.