Abstract
Ubiquitously distributed multifunctional superfamily of Glutathione S-transferases (GST) generally constitute a dimeric enzymes and catalyse the conjugation of the thiol group of the glutathione (GSH) to diverse electrophilic centres on lipophilic molecules with the formation of rather less active end products. Besides their well investigated conjugation reaction for the detoxification of endogenous and xenobiotic compounds, they can also be involved in both GSH dependent peroxidation or isomerization reactions, and several other non-catalytic functions, like binding of non-substrate ligands, stress-induced signalling processes and preventing of apoptosis. Plant GSTs have been a focus of attention because of their roles in herbicide detoxification and today seven distinct classes of soluble (cytosolic) GSTs are presented as Phi, Tau, Theta, Zeta, Lambda, Dehydroascorbate reductases (DHARs) and Tetrachlorohydroquinone dehalogenase (TCHQD). While GSTs show overall sequence diversification within and between classes, they retain a high level of three-dimensional structure conservation over long evolutionary periods. In this review mainly the soluble plant GSTs will be considered by giving attention to their structures, subcellular localizations, genomic organizations, catalytic/noncatalytic functions, and comparisons given with respect to their mammalian counterparts where necessary.
Similar content being viewed by others
Literature Cited
Alfenito, M. R., E. Souer, C. D. Goodman, R. Buell, J. Mol, R. Koes & V. Walbot. 1998. Functional complementation of anthocyanin sequestration in the vacuole by widely divergent Glutathione S-transferases. The Plant Cell 10: 1135–1149.
Allocati, N., E. Casalone, M. Masulli, I. Ceccarelli, E. Carletti, M. W. Parker & C. Di Ilio. 1999. Functional analysis of the evolutionarily conserved praline 53 residue in Proteus mirabilis Glutathione S-transferase B1-1. FEBS Lett. 445: 347–350.
Armstrong, R. N. 1991. Glutathione S-transferases: reaction mechanism, structure, and function. Chem. Res. Toxicol. 4: 131–140.
——— 1997. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10: 2–18.
——— 1998. Mechanistic imperatives for the evolution of glutathione S-transferases. Curr. Opin. Chem. Biol. 2: 618–623.
Axarli, I. A., D. J. Rigden & N. E. Labrou. 2004. Characterization of the ligandin site of maize glutathione S-transferase I. Biochem. J. 382: 885–893.
Bartling, D., R. Radzio, U. Steiner, & E. W. Weiler. 1993. A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana Eur. J. Biochem. 216: 579–586.
Bilang, J., & A. Sturm. 1995. Cloning a characterization of a GST that can be photolabelled with 5-azido-indole-3-acetic acid. Plant Physiol. 109: 253–260.
Board, P. G., R. T. Baker, G. Chelvanayagam & L. S. Jermiin. 1997. Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem. J. 238: 929–935.
Boyland, E. & L. F. Chasseaud. 1969. The role of glutathione and glutathione S-transferases in mercapturic acid biosynthesis. Adv. Enzymol. Rel. Areas Mol. Biol. 32: 173–219.
Brown, H. M. 1990. Mode of action, crop selectivity, and soil reactions of the sulfonylurea herbicides. Pestic. Sci. 29: 263–281.
Caccuri, A. M., G. Antonini, M. Nicotra, A. Battistoni, M. Lo Bello, P. G. Board, M. W. Parker & G. Ricci. 1997. Catalytic mechanism and role of hydroxyl residues in the active site of theta class glutathione S-transferases. Investigation of Ser-9 and Tyr-113 in a glutathione S-transferase from the Australian sheep bowfly, Lucilia cuprina. J. Biol. Chem. 272: 29681–29686.
———, G. Antonini, P. Ascenzi, M. Nicotra, M. Nuccetelli, A. P. Mazzetti, G. Federici, M. Lo Bello, & G. Ricci. 1999. Temperature adaptation of glutathione S-transferase P1-1. A case of homotropic regulation of substrate binding. J. Biol. Chem. 274: 19276–19280.
Cheng, W. & K. B. Singh. 1999. The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J. 19: 667–677.
Coleman, J. O. D., M. M. A. Blake-Kalff & T. G. E. Davies. 1997. Detoxification of xenobiotics by plants:chemical modification and vascular compartmentation. Trends. Plant Sci. 2: 144–151.
Cummins, I., D. J. Cole & R. Edwards. 1997. Purification of multiple glutathione transferases involved in herbicide detoxification from wheat (Triticum aestivum L.) treated with the sanefer fenchlorazole-ethyl. Pestic. Biochem. Physiol. 59: 35–49.
———, D. J. Cole & R. Edwards. 1999. A role for glutathione S-transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J. 18: 285–292.
Davies, J. & D. C. Caseley. 1999. Herbicide safeners: a review. Pestic. Sci. 55: 1043–1058.
Dean, J. V. & T. P. Devarenne. 1997. Peroxidase-mediated conjugation of glutathione to unsaturated phenylpropanoids: evidence against glutathione S-transferase involvement. Physiol. Plant 99: 271–278.
DeRidder, B. P., D. P. Dixon, D. J. Beussman, R. Edwards & P. B. Goldsbrough. 2002. Induction of glutathione S-transferases in Arabidopsis by herbicide safeners. Plant Physiol. 130: 1497–1505.
Diesperger, H. & H. Sandermann. 1979. Soluble and microsomal glutathione S-transferase activities in pea seedlings (Pisum sativum L.). Planta 146: 643–648.
Dirr, H., P. Reinemer & R. Huber. 1994. X-ray crystal structures of cytosolic glutathione S-transferases-implications for protein architecture, substrate recognition and catalytic function. Eur. J. Biochem. 220: 645–661.
Dixon, D. P., D. J. Cole & R. Edwards. 1997. Characteristics of multiple GSTs containing the GST I subunit with activities toward herbicide substrates in maize (Zea mays). Pesticide Sci. 50: 72–82.
———, D. J. Cole & R. Edwards. 1998a. Purification, regulation and cloning of a GST from maize resembling the auxin-inducible type-III GSTs. Plant Mol. Biol. 36: 75–87.
———, L. Cummins, D. J. Cole & R. Edwards. 1998b. Glutathione-mediated detoxification systems in plants. Curr. Opin. in Plant Biol. 1: 258–266.
———, D. J. Cole & R. Edwards. 1999. Dimerization of maize GSTs in recombinant bacteria. Plant Mol. Biol. 40: 997–1008.
———, D. J. Cole & R. Edwards. 2000. Characteristics of a zeta class GSTs from Arabidopsis thaliana with a putative role in tyrosine catabolism. Arch. Biochem. Biophys. 384: 407–412.
———, B. G. Davis & R. Edwards. 2002a. Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in A. thaliana. The Journal of Biol. Chem. 277: 30859–30869
———, A. Lapthorn & R. Edwards. 2002b. Plant glutathione transferases. Genome Biology. 3: 3004.1–3004.10.
Droog, F. 1997. Plant glutathione S-transferase, a tale of theta and tau. J. Plant Growth Regul. 16: 95–107.
Eaton, D. L. & T. K. Bammler. 1999. Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol. Sci. 49: 156–164.
Edwards, R. 1996. Characterization of glutathione transferases and glutathione peroxidases in pea (Pisum sativum). Physiol Plant. 98: 594–604.
——— & D. P. Dixon. 2005. Plant glutathione transferases. Methods in Enzymology. 401: 169–186.
———, J. W. Blount & R. Dixon. 1991. Glutathione and elicitation of the phytoalexin response in legume cell cultures. Planta. 184: 403–409.
———, P. D. Dixon & V. Walbot. 2000. Plant glutathione S-tranferases: Enzymes with multiple functions in sickness and health. Trends in Plant Sci. 5: 193–198.
Erhardt, J. & H. W. Dir. 1995. Native dimer stabilizes the subunit tertiary structure of porcine class Pi glutathione S-transferase. Eur. J. Biochem. 230: 614–620.
Eshdat, Y., D. Holland, Z. Faltin, & G. Ben-Hayyim. 1997. Plant glutathione peroxidases. Physiol Plant. 100: 234–240.
Fernandez-Canon, J. M., & M. A. Penalva. 1998. Characterization of a fungal maleylacetoacetate isomerase gene and identification of its human homologue. J. Biol. Chem. 273: 329–337.
Fernandez-Canon, J. M., M. W. Baetscher, M. Finegold, T. Burlingame, K. M. Gibson, & M. Grompe. 2002. Maleylacetoacetate isomerase (MAAI/GSTZ)-deficient mice reveal a glutathione-dependent nonenzymatic bypass in tyrosine catabolism. Mol Cell Biol 22: 4943–4951.
Flury, T., E. Wagner & K. Kreuz. 1996. An inducible glutathione S-transferase in soybean hypocotyls is localized in the apoplast. Plant Physiol. 112: 1185–1190.
Frear, D. S., & H. R. Swanson. 1970. Biosynthesis of S-(4-ethylamino-6-isopropylamino-2-s-triazine) glutathione: Partial purification and properties of glutathione S-transferase from corn. Phytochemistry. 9: 2123–2132.
Frova, C. 2006. Glutathione transferases in the genomic era: New insights and perspectives. Biomolecular Engineering. 23: 149–169.
Gonneau, M., R. Mornet & M. Laloue. 1998. A Nicotiana plumbaginifolia protein labelled with an azido cytokinin agonist is a glutathione S-transferase. Physiol Plant. 103: 114–124.
Graminski, G. F., P. Zhang, M. A. Sesay, H. L. Ammon & R. N. Armstrong. 1989. Formation of 1-(S-glutathionyl)-2,4,6-trinitrocyclohexadienate anion at the active site of glutathione S-transferase: Evidence for enzymic stabilization of s-complex intermediates in nucleophilic aromatic substitution reactions. Biochemistry. 28: 6252–6258.
Gronwald, J. W. & K. L. Plaisance. 1998. Isolation and characterisation of glutathione S-transferase isozymes from sorghum. Plant Physiol. 117: 877–892.
Habig, W. H., M. J. Pabst & W. B. Jakoby. 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249: 7130–7139.
Harris, J. M., D. J. Meyer, B. Coles & B. Ketterer. 1991. A novel glutathione transferase (13–13) isolated from the matrix of rat liver mitochondria having structural similarity to class theta enzymes. Biochem. J. 278: 137–141.
Hayes, J. D., & D. J. Pulford. 1995. The glutathione S-transferase supergene family: Regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. CRC CritRev. Biochem. Mol. Biol. 30: 445–600.
——— & L. I. Mc Lennan. 1999. Glutathione and glutathione-dependent enzymes represent a coordinately regulated defense against oxidative stress. Free Radic. Res. 31: 273–300
Hegazy, U. M., B. Mannervik & G. Stenberg. 2004. Functional role of the lock and key motif at the subunit interface of glutathione transferase P1–1. J. Biol. Chem. 279: 9586–9596.
Henderson, C. J., A. G. Smith, J. Ure, K. Brown, E. J. Bacon & C. R. Wolf. 1998. Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc. Natl. Acad. Sci. USA. 95: 5275–5280.
Hussey, A. J. & J. D. Hayes. 1992. Characterization of a human class theta glutathione S-transferase with activity towards 1-menaphthyl sulphate. Biochem. J. 286: 929–935.
Ishikawa, T., C. D. Wright & H. Ishizuka. 1994. GS-X pump is functionally overexpressed in cis-diamminedichloroplatinum (II)-resistant human leukemia HL-60 cells and down-regulated by cell differentiation. J. Biol. Chem. 269: 29085–29093.
Ji, X., P. Zhang, R. N. Armstrong & G. L. Gilliland. 1992. The three-dimensional structure of a glutathione S-transferase from the Mu gene class. Structural analysis of the binary complex of isoenzyme 3–3 and glutathione at 2.2 A resolution. Biochemistry. 31: 10169–10184.
Ji, X., E. C. von Rosenvinge, W. W. Johnson, R. N. Armstrong & G. L. Gilliland. 1996. Location of a potential transport binding site in a sigma class glutathione transferase by x-ray crystallography. Proc. Natl. Acad. Sci. USA. 93: 8208–8213.
Jones, A. M. 1994. Auxin-binding proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 393–420.
Kampranis, S. C., R. Damianova, M. Atallah, G. Toby, G. Kondi, P. N. Tsichlis & A. M. Makris. 2000. A novel plant glutathione S-transferase/peroxidase suppresses Bax lethality in yeast. J. Biol. Chem. 275: 29207–29216.
Karam, D. 1998. Glutathione S-transferase: an enzyme for chemical defense in plants. http://www.colostate.edu/Depts/Entomology/courses/en570/papers_1998/karam.htm. Cited 24 April 2007
Katti, S. K., D. M. LeMaster & H. Eklund. 1990. Crystal structure of thioredoxin from Escherichia coli at 1.68 A resolution. J. Mol. Biol. 212: 167–184.
Ketley, J. N., W. H. Habig & W. B. Jacoby. 1975. Binding of nonsubstrate ligands to the glutathione S-transferases. J. Biol. Chem. 250: 8670–8673.
Labrau, N. E., L. V. Mello & Y. D. Clonis. 2001. Functional and structural roles of the glutathione-binding residues in maize (Zea mays) glutathione S-transferase I. Biochem. J. 358: 101–110.
Lamoureux, G. L. & D. G. Rusness. 1986. Xenobiotic conjugation in higher plants. In: Paulson, G. D., Caldwell, J., Hutson, D. H., and Menn, J. J. (eds). Xenobiotic conjugation chemistry. Am. Chem. Soc. Washington DC. 299: 62–105.
——— & D. G. Rusness. 1993. Glutathione in the metabolism and detoxification of xenobiotics in plants. In: Sulfur nutrition and assimilation in higher plants. De Kok et al (eds), The Hague, SPB Acad. Publ. 221–237.
Li, Z.-S., M. Alfenito, P. A. Rea, V. Walbot & R. A. Dixon. 1997. Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. Phytochemistry. 45: 689–693.
Lim, C. E., K. I. Matthaei, A. C. Blackburn, R. P. Davis, J. E. Dahlstrom, M. E. Koina, M. W. Anders, & P. G. Board. 2004. Mice deficient in glutathione transferase zeta/maleylacetoacetate isomerase exhibit a range of pathological changes and elevated expression of alpha, mu and pi class glutathione transferases. Am. J. Pathol. 165: 679–693.
Listowsky, I., M. Abramovitz, H. Homma & Y. Niitsu. 1988. Intracellular binding and transport of hormones and xenobiotics by glutathione S-transferases. Drug Met. Rev. 19: 305–318.
Litwack, G., B. Ketterer & I. M. Arias. 1971. Ligandin; a hepatic protein which binds steroids, bilirubin, carcinogens, and a number of exogenous organic anions. Nature. 234: 466–467.
Loyall, L., K. Uchida, S. Braun, M. Furuya & H. Frohnmeyer. 2000. Glutathione and a UV light induced GST are involved in signalling to chalcone synthase in cell cultures. Plant Cell. 12: 1939–1950.
Mannervik, B. & U. H. Danielson. 1988. Glutathione transferases- Structure and catalytic activity. CRC Crit. Rev. Biochem. Mol. Biol. 23: 283–337.
Marrs, K. A. 1996. The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 127–158.
Marrs, K. A., M. R. Alfenito, A. M. Lloyd & V. Walbot. 1995. Glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375: 397–400.
Martin, J. L. 1995. Thioredoxin—a fold for all reasons. Structure 3: 245–250.
Matern, U., C. Reichenbach & W. Heller. 1986. Efficient uptake of flavonoids into parsley (Petroselinum hortense) vacuoles requires acylated glycosides. Planta. 167: 183–189.
Maxon, J. M. & W. R. Woodson. 1998. Ethylene-responsive gene expression during carnation flower senescenze. Acta Horticulture. 464: 135–140.
McGonigle, B., S. J. Keeler, S.-M. C. Lau, M. K. Koeppe, D. P. O’Keefe. 2000. A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol. 124: 1105–1120.
McTigue, M. A., D. R. Williams & J. A. Tainer. 1995. Crystal structures of a schistosomal drug and vaccine target: glutathione S-transferase from Schistosoma japonica and its complex with the leading antischistosomal drug praziquantel. J. Mol. Biol. 246: 21–27.
Meyer, D. J., B. Coles, S. E. Pemble, K. S. Gilmore, G. M. Fraser & B. Ketterer. 1991b. Theta, a new class of glutathione transferases purified from rat and man. Biochem. J. 274: 409–414.
Morel, F., C. Rauch, B. Coles, E. Le Ferrac & A. Guillouzo. 2002. The human glutathione transferase alpha locus: genomic organisation of gene cluster and functional characterisation of the genetic polymorphysm in the hGSTA1 promoter. Pharmacogenetics. 12: 277–286.
Mueller, L. A., C. D. Goodman, R. A. Silady & V. Walbot. 2000. AN9, a petunia GST required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiol. 123: 1561–1570.
Nebert, D. W. & M. Z. Dieter. 2000. The evolution of drug metabolism. Pharmacology. 61: 124–135.
Neuefeind, T., R. Huber, H. Dasenbrock, L. Prade & B. Bieseler. 1997a. Crystal structure of herbicide-detoxifiying maize glutathione S-transferase-I in complex with lactolglutathione: evidence for an induced-fit mechanism. J. Mol. Biol. 274: 446–453.
———, R. Huber, P. Reinemer, J. Knablein, L. Prade, K. Mann & B. Bieseler. 1997b. Cloning, sequencing, crystallization and X-ray structure of glutathione S-transferase-III from Zea mays var. mutin: a leading enzyme in detoxification of maize herbicides. J. Mol. Biol. 274: 577–587.
Pearson, W. R. 2005. Phylogenies of glutathione transferase families. Methods in Enzymology. 401: 186–204.
Pemble, S. E. & J. B. Taylor. 1992. An evolutionary perspective on glutathione transferases inferred from class theta glutathione transferase cDNA. Biochem. J. 287: 957–963.
Pemble, S. E., A. F. Wordle & J. B. Taylor. 1996. Glutathione S-transferase Kappa: characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem. J. 319: 349–754.
Prade, L., P. Hof, & B. Bieseler. 1997. Dimer interface of glutathione S-transferase from A.thaliana: influence of the G-site architecture on the dimmer interface and implications for classification. Biol. Chem. 378: 312–320.
Ranson, H., F. Collins & J. Hemingway. 1998. The role of alternative mRNA splicing in generating heterogeneity within the Anopheles gambiae class I glutathione S-transferase family. Proc. Natl. Acad. Sci. USA. 95: 14284–14289.
Rea, P. A. 1999. MRP subfamily ABC transporters from plants and yeast. J Exp. Bot. 50: 895–913.
Rossjohn, J., P. G. Board, M. W. Parker & M. C. J. Wilce. 1996. A structurally-derived consensus pattern for theta class GSTs. Protein Eng. 9: 327–332.
———, W. J. Mc Kinstry, A. J. Oakley, D. Verger, J. Flanagan, G. Chelvanayagam, K. L. Tan, P. G. Board & M. W. Parker. 1998. Human theta class glutathione transferase: the crystal structure reveals a sulfate-binding pocket within a buried active site. Structure 6: 309–322.
Roxas, V. P., R. K. Smith, E. R. Allen & R. D. Allen. 1997. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat. Biotechnol. 15: 988–991.
Reinemer, P., H. W. Dirr, R. Ladenstein, J. Schaffer, O. Gallay & R. Huber. 1991. The three-dimensional structure of class p glutathione S-transferase in complex with glutathione sulfonate at 2.3 A resolution. EMBO J. 10: 1997–2005.
———, L. Prade, P. Hof, T. Neuefiend, R. Huber, R. Zettl, K. Palme, J. Schell, I. Koelln, H. D. Bartunik & B. Bieseler. 1996. Three-dimensional structure of GST from A.thaliana at 2.2 A resolution: Structural characterization of herbicide-conjugating plant GSTs and a novel active site architecture. J. Mol. Biol. 255: 289–309.
Sandermann, H. 1992. Plant metabolism of xenobiotics. TIBS. 17: 82–84.
Sandermann, H. 1994. Higher plant metabolism of xenobiotics: the ‘green liver’ concept. Pharmacogenetics. 4: 225–241.
Sari-Gorla, M., S. Ferrario, L. Rossini, C. Frova &M. Villa. 1993. Developmental expression of glutathione S-transferase in maize and it is possible connection with herbicide tolerance. Euphytica. 67: 221–230.
Scalla, R. & A. Roulet. 2002. Cloning and characterisation of a glutathione S-transferase induced by a herbicide safener in barley (Hordeum vulgare). Physiol Plant. 116: 336–344.
Schuphan, I., D. Westpal, A. Hague & W. Ebing. 1981. Biological and chemical behavior of perhalogenmethylmercapto fungicides: Metabolism and in vitro reactions of dichlofluanid in comparison with captan sulfur. In: Rosen, J.D., Magee, P.S., and Casida, J.E., (eds), Pesticide Action and Metabolism. Am. Chem. Soc. Washington DC. 158: 65–85.
Sheehan, D., G. Meade, V. M. Foley,& C. A. Dowd. 2001. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of ancient enzyme superfamily. Biochem. J. 360: 1–16.
Sinning, I., G. J. Kleywegt, S. W. Cowan, P. Reinemer, H. W. Dirr, R. Huber, G. L. Gilliland, R. N. Armstrong, X. Ji, P. G. Board, B. Olin, B. Mannervik & T. A. Jones. 1993. Structure determination and refinement of human alpha class glutathione transferase A1-1, and a comparison with the mu and pi class enzymes. J. Mol. Biol. 232: 192–212.
Skipsey, M., C. J. Andrews, J. K. Townson, I. Jepson & R. Edwards. 1997. Substrate and thiol specificity of a stress-inducible GST from soybean. FEBS Lett. 409: 370–374.
Soranzo, N., M. Sari Gorla, L. Mizzi, G. De Toma, C. Frova. 2004. Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol. Gen. Genomics. 271: 511–521.
Tan, K. L., G. Chelvanayagam, M. W. Parker & P. G. Board. 1996. Mutagenesis of the active site of the human Theta-class glutathione transferase GSTT2–2: catalysis with different substrates involves different residues. Biochem. J. 319: 315–321.
Thom, R., D. P. Dixon, R. Edwards, D. J. Cole & A. Lapthorn. 2001. The structure of a zeta class glutathione S-transferase from A. thaliana: characterization of a GST with novel active site architecture and a putative role in tyrosine catabolism. J. Mol. Biol. 308: 949–962.
Thom, R., I. Cummins, D. P. Dixon, R. Edwards, D. J. Cole & A. J. Lapthorn. 2002. Structure of a tau class glutathione S-transferase from wheat active in herbicide detoxification. Biochemistry. 41: 7008–7020.
Ulmasov, T., G. Hagen & T. Guilfoyle. 1994. The ocs element in the soybean GH2/4 promoter is activated by both active and inactive auxin and salicylic acid analogues. Plant Mol. Biol. 26: 1055–1064.
Urano, J., T. Nakagawa, Y. Maki, T. Masumara, K. Tanaka, N. Murata, T. Ushimaru. 2000. Molecular cloning and characterization of a rice dehydroascorbate reductase. FEBS Lett. 466: 107–111.
Wagner, U., R. Edwards, D. P. Dixon & F. Mauch. 2002. Probing the diversity of the Arabidopsis GST gene family. Plant Mol. Biol. 49: 515–532.
Wilce, M. C. J. & M. W. Parker. 1994. Structure and function of glutathione S-transferases. Biochim. Biophys. Acta. 1205: 1–18.
Wolf, A. E., K. J. Dietz & P. Schröder. 1996. Degredation of GST conjugates by a carboxypeptidase in the plant vacuole. FEBS Lett. 384: 31–34.
Wolfe, K. H., M. Gouy, Y.-W. Yang, P. M. Sharp & W.-H. Li. 1989. Date of monocot–dicot divergence estimated from chloroplast DNA sequence data. Proc. Natl. Acad. Sci. USA. 86: 6201–6205.
Zhang, B., & K. B. Singh. 1994. Ocs element promoter sequences are activated by auxin and salicylic acid in Arabidopsis. Proc. Natl. Acad. Sci. USA. 91: 2507–2511.
Zeng, Q.-Y., H. Lu & X.-R. Wang. 2005. Molecular characterization of a glutathione transferase from Pinus tabulaeformis (Pinaceae). Biochimie 87: 445–455.
Zettl, R., J. Schell & K. Plame. 1994. Photoaffinity labeling of Arabidopsis plasma membrane vesicles by 5-azido[7–3H]indole-3-acetic acid: Identification of a glutathione S-transferase. Proc. Natl. Acad. Sci. USA. 91: 689–693
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Öztetik, E. A Tale of Plant Glutathione S-Transferases: Since 1970. Bot. Rev 74, 419–437 (2008). https://doi.org/10.1007/s12229-008-9013-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12229-008-9013-9