Glutathione Transferases

The 55 Arabidopsis glutathione transferases (GSTs) are, with one microsomal exception, a monophyletic group of soluble enzymes that can be divided into phi, tau, theta, zeta, lambda, dehydroascorbate reductase (DHAR) and TCHQD classes. The populous phi and tau classes are often highly stress inducible and regularly crop up in proteomic and transcriptomic studies. Despite much study on their xenobiotic-detoxifying activities their natural roles are unclear, although roles in defence-related secondary metabolism are likely. The smaller DHAR and lambda classes are likely glutathione-dependent reductases, the zeta class functions in tyrosine catabolism and the theta class has a putative role in detoxifying oxidised lipids. This review describes the evidence for the functional roles of GSTs and the potential for these enzymes to perform diverse functions that in many cases are not “glutathione transferase” activities. As well as biochemical data, expression data from proteomic and transcriptomic studies are included, along with subcellular localisation experiments and the results of functional genomic studies.

[1]  R. Edwards,et al.  Roles for glutathione transferases in plant secondary metabolism. , 2010, Phytochemistry.

[2]  Robert Schmidt,et al.  PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update , 2009, Nucleic Acids Res..

[3]  D. Leister,et al.  Chloroplast proteins without cleavable transit peptides: rare exceptions or a major constituent of the chloroplast proteome? , 2009, Molecular plant.

[4]  Patricia C. Babbitt,et al.  Glutathione Transferases Are Structural and Functional Outliers in the Thioredoxin Fold† , 2009, Biochemistry.

[5]  P. He,et al.  One for all: the receptor-associated kinase BAK1. , 2009, Trends in plant science.

[6]  A. Varma,et al.  Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. , 2009, Journal of plant physiology.

[7]  R. Edwards,et al.  Selective Binding of Glutathione Conjugates of Fatty Acid Derivatives by Plant Glutathione Transferases* , 2009, The Journal of Biological Chemistry.

[8]  G. Friso,et al.  Large Scale Comparative Proteomics of a Chloroplast Clp Protease Mutant Reveals Folding Stress, Altered Protein Homeostasis, and Feedback Regulation of Metabolism* , 2009, Molecular & Cellular Proteomics.

[9]  Adam J. Carroll,et al.  The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. , 2009, The Plant journal : for cell and molecular biology.

[10]  A. Weber,et al.  In-Depth Proteome Analysis of Arabidopsis Leaf Peroxisomes Combined with in Vivo Subcellular Targeting Verification Indicates Novel Metabolic and Regulatory Functions of Peroxisomes1[W][OA] , 2009, Plant Physiology.

[11]  S. Kim,et al.  Modulations of AtGSTF10 expression induce stress tolerance and BAK1-mediated cell death. , 2009, Biochemical and biophysical research communications.

[12]  Robert Edwards,et al.  Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily , 2009, Journal of experimental botany.

[13]  Qi Sun,et al.  PPDB, the Plant Proteomics Database at Cornell , 2008, Nucleic Acids Res..

[14]  Martin J. Mueller,et al.  Impact of cyclopentenone-oxylipins on the proteome of Arabidopsis thaliana. , 2008, Biochimica et biophysica acta.

[15]  E. Peiter,et al.  Getting the most out of publicly available T-DNA insertion lines. , 2008, The Plant journal : for cell and molecular biology.

[16]  A. Millar,et al.  Novel Proteins, Putative Membrane Transporters, and an Integrated Metabolic Network Are Revealed by Quantitative Proteomic Analysis of Arabidopsis Cell Culture Peroxisomes1[W][OA] , 2008, Plant Physiology.

[17]  O. Emanuelsson,et al.  Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast Proteome , 2008, PloS one.

[18]  M. Kitayama,et al.  Characterization of PAP1-upregulated Glutathione S-transferase genes in Arabidopsis thaliana , 2008 .

[19]  M. Hirai.  A robust omics-based approach for the identification of glucosinolate biosynthetic genes , 2008, Phytochemistry Reviews.

[20]  Wolfram Weckwerth,et al.  Proteome Analysis of Arabidopsis Leaf Peroxisomes Reveals Novel Targeting Peptides, Metabolic Pathways, and Defense Mechanisms[W] , 2007, The Plant Cell Online.

[21]  Karam B. Singh,et al.  Differential Gene Expression and Subcellular Targeting of Arabidopsis Glutathione S-Transferase F8 Is Achieved through Alternative Transcription Start Sites* , 2007, Journal of Biological Chemistry.

[22]  J. Yoon,et al.  Phytotoxicity and phytoremediation of 2,6-dinitrotoluene using a model plant, Arabidopsis thaliana. , 2007, Chemosphere.

[23]  C. Sieben,et al.  A Plant Homolog of Animal Chloride Intracellular Channels (CLICs) Generates an Ion Conductance in Heterologous Systems* , 2007, Journal of Biological Chemistry.

[24]  R. Edwards,et al.  Enzymes of tyrosine catabolism in Arabidopsis thaliana. , 2006, Plant science : an international journal of experimental plant biology.

[25]  C. Frova.  Glutathione transferases in the genomics era: new insights and perspectives. , 2006, Biomolecular engineering.

[26]  D. Gallie,et al.  Dehydroascorbate Reductase Affects Leaf Growth, Development, and Function1 , 2006, Plant Physiology.

[27]  A. Millar,et al.  Desensitization of GSTF8 Induction by a Prior Chemical Treatment Is Long Lasting and Operates in a Tissue-Dependent Manner1[W] , 2006, Plant Physiology.

[28]  L. De Bellis,et al.  Characterization of two Arabidopsis thaliana glutathione S-transferases , 2006, Plant Cell Reports.

[29]  H. Kamada,et al.  Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. , 2006, Plant & cell physiology.

[30]  Ralf Morgenstern,et al.  Bioinformatic and enzymatic characterization of the MAPEG superfamily , 2005, The FEBS journal.

[31]  R. Edwards,et al.  Differential Induction of Glutathione Transferases and Glucosyltransferases in Wheat, Maize and Arabidopsis thaliana by Herbicide Safeners , 2005, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[32]  R. Edwards,et al.  Stress-Induced Protein S-Glutathionylation in Arabidopsis , 2005 .

[33]  J. Schnoor,et al.  Gene Expression and Microscopic Analysis of Arabidopsis Exposed to Chloroacetanilide Herbicides and Explosive Compounds. A Phytoremediation Approach 1 , 2005 .

[34]  A. Moons.  Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). , 2005, Vitamins and hormones.

[35]  Thomas Girke,et al.  The Vegetative Vacuole Proteome of Arabidopsis thaliana Reveals Predicted and Unexpected Proteinsw⃞ , 2004, The Plant Cell Online.

[36]  B. Miller,et al.  Direct determination of thiol pKa by isothermal titration microcalorimetry. , 2004, Journal of the American Chemical Society.

[37]  F. Regnier,et al.  Proteomic Analysis of Arabidopsis Glutathione S-transferases from Benoxacor- and Copper-treated Seedlings* , 2004, Journal of Biological Chemistry.

[38]  Alexandra M. E. Jones,et al.  Specific changes in the Arabidopsis proteome in response to bacterial challenge: differentiating basal and R-gene mediated resistance. , 2004, Phytochemistry.

[39]  Klaus F. X. Mayer,et al.  Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism , 2004, Plant Molecular Biology.

[40]  W. Kim,et al.  A proteomic analysis identifies glutathione S-transferase isoforms whose abundance is differentially regulated by ethylene during the formation of early root epidermis in Arabidopsis seedlings. , 2004, Biochimica et biophysica acta.

[41]  Julian Tonti-Filippini,et al.  Experimental Analysis of the Arabidopsis Mitochondrial Proteome Highlights Signaling and Regulatory Components, Provides Assessment of Targeting Prediction Programs, and Indicates Plant-Specific Mitochondrial Proteins Online version contains Web-only data. Article, publication date, and citation inf , 2004, The Plant Cell Online.

[42]  Ulrich Wagner,et al.  Probing the Diversity of the Arabidopsis glutathione S-Transferase Gene Family , 2002, Plant Molecular Biology.

[43]  P. Goldsbrough,et al.  An Arabidopsis gene with homology to glutathione S-transferases is regulated by ethylene , 1993, Plant Molecular Biology.

[44]  A. Millar,et al.  Proteomic Analysis of Glutathione S-Transferases of Arabidopsis thaliana Reveals Differential Salicylic Acid-Induced Expression of the Plant-Specific Phi and Tau Classes , 2004, Plant Molecular Biology.

[45]  L. Holuigue,et al.  NPR1-independent activation of immediate early salicylic acid-responsive genes in Arabidopsis. , 2004, Molecular plant-microbe interactions : MPMI.

[46]  S. Kitamura,et al.  TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[47]  Karam B. Singh,et al.  Early induction of the Arabidopsis GSTF8 promoter by specific strains of the fungal pathogen Rhizoctonia solani. , 2004, Molecular plant-microbe interactions : MPMI.

[48]  Haibiao Gong,et al.  Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro , 2004, Plant Molecular Biology.

[49]  C. Frova.  The plant glutathione transferase gene family: genomic structure, functions, expression and evolution , 2003 .

[50]  James Whelan,et al.  Molecular Definition of the Ascorbate-Glutathione Cycle in Arabidopsis Mitochondria Reveals Dual Targeting of Antioxidant Defenses in Plants* , 2003, Journal of Biological Chemistry.

[51]  P. Goldsbrough,et al.  Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids. , 2003, The Plant journal : for cell and molecular biology.

[52]  Ulrich Wagner,et al.  The rapid induction of glutathione S-transferases AtGSTF2 and AtGSTF6 by avirulent Pseudomonas syringae is the result of combined salicylic acid and ethylene signaling. , 2003, Plant & cell physiology.

[53]  P. Goldsbrough,et al.  Induction of Glutathione S-Transferases in Arabidopsis by Herbicide Safeners1 , 2002, Plant Physiology.

[54]  M. Bianchi,et al.  Drought regulation of GST8, encoding the Arabidopsis homologue of ParC/Nt107 glutathione transferase/peroxidase. , 2002, Physiologia plantarum.

[55]  B. G. Davis,et al.  Functional Divergence in the Glutathione Transferase Superfamily in Plants , 2002, The Journal of Biological Chemistry.

[56]  M. Parker,et al.  From glutathione transferase to pore in a CLIC , 2002, European Biophysics Journal.

[57]  Robert Edwards,et al.  Structure of a tau class glutathione S-transferase from wheat active in herbicide detoxification. , 2002, Biochemistry.

[58]  A. Lapthorn,et al.  Plant glutathione transferases , 2002, Genome Biology.

[59]  A. Lapthorn,et al.  The structure of a zeta class glutathione S-transferase from Arabidopsis thaliana: characterisation of a GST with novel active-site architecture and a putative role in tyrosine catabolism. , 2001, Journal of molecular biology.

[60]  R. Edwards,et al.  Characterisation of a zeta class glutathione transferase from Arabidopsis thaliana with a putative role in tyrosine catabolism. , 2000, Archives of biochemistry and biophysics.

[61]  A. Yokota,et al.  Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. , 2000, Plant & cell physiology.

[62]  V. Walbot,et al.  AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. , 2000, Plant physiology.

[63]  Kunisuke Tanaka,et al.  Molecular cloning and characterization of a rice dehydroascorbate reductase , 2000, FEBS letters.

[64]  V. Walbot,et al.  AN 9 , a Petunia Glutathione S-Transferase Required for Anthocyanin Sequestration , Is a Flavonoid-Binding Protein 1 , 2000 .

[65]  B. Persson,et al.  Common structural features of mapeg—a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism , 2008, Protein science : a publication of the Protein Society.

[66]  K B Singh,et al.  The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. , 1999, The Plant journal : for cell and molecular biology.

[67]  R. Huber,et al.  Structures of herbicides in complex with their detoxifying enzyme glutathione S-transferase - explanations for the selectivity of the enzyme in plants. , 1998, Structure.

[68]  C. Foyer,et al.  ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. , 1998, Annual review of plant physiology and plant molecular biology.

[69]  P. Mullineaux,et al.  The presence of dehydroascorbate and dehydroascorbate reductase in plant tissues , 1998, FEBS letters.

[70]  M. Peñalva,et al.  Characterization of a Fungal Maleylacetoacetate Isomerase Gene and Identification of Its Human Homologue* , 1998, The Journal of Biological Chemistry.

[71]  H. Follmann,et al.  Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants , 1997, FEBS letters.

[72]  L. Prade,et al.  Dimer interface of glutathione S-transferase from Arabidopsis thaliana: influence of the G-site architecture on the dimer interface and implications for classification. , 1997, Biological chemistry.

[73]  K. Marrs.  THE FUNCTIONS AND REGULATION OF GLUTATHIONE S-TRANSFERASES IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[74]  P. Board,et al.  Purification and characterization of a recombinant human Theta-class glutathione transferase (GSTT2-2). , 1996, The Biochemical journal.

[75]  R. Huber,et al.  Three-dimensional structure of glutathione S-transferase from Arabidopsis thaliana at 2.2 A resolution: structural characterization of herbicide-conjugating plant glutathione S-transferases and a novel active site architecture. , 1996, Journal of molecular biology.

[76]  B. J. van der Zaal,et al.  2,4-Dichlorophenoxyacetic Acid and Related Chlorinated Compounds Inhibit Two Auxin-Regulated Type-III Tobacco Glutathione S-Transferases , 1995, Plant physiology.

[77]  T. Mantle,et al.  Glutathione S-transferases. , 1990, Biochemical Society transactions.