Plant Molecular Biology

, Volume 49, Issue 5, pp 515–532 | Cite as

Probing the Diversity of the Arabidopsis glutathione S-Transferase Gene Family

  • Ulrich Wagner
  • Robert Edwards
  • David P. Dixon
  • Felix Mauch
Article

Abstract

Glutathione S-transferases (GSTs) appear to be ubiquitous in plants and have defined roles in herbicide detoxification. In contrast, little is known about their roles in normal plant physiology and during responses to biotic and abiotic stress. Forty-seven members of the GST super-family were identified in the Arabidopsis genome, grouped into four classes, with amino acid sequence identity between classes being below 25%. The two small zeta (GSTZ) and theta (GSTT) classes have related GSTs in animals while the large phi (GSTF) and tau (GSTU) classes are plant specific. As a first step to functionally characterize this diverse super-family, 10 cDNAs representing all GST classes were cloned by RT-PCR and used to study AtGST expression in response to treatment with phytohormones, herbicides, oxidative stress and inoculation with virulent and avirulent strains of the downy mildew pathogen Peronospora parasitica. The abundance of transcripts encoding AtGSTF9, AtGSTF10, AtGSTU5, AtGSTU13 and AtGSTT1 were unaffected by any of the treatments. In contrast, AtGSTF6 was upregulated by all treatments while AtGSTF2, AtGSTF8, AtGSTU19 and AtGSTZ1 each showed a selective spectrum of inducibility to the different stresses indicating that regulation of gene expression in this super-family is controlled by multiple mechanisms. The respective cDNAs were over expressed in E. coli. All GSTs except AtGSTF10 formed soluble proteins which catalysed a specific range of glutathione conjugation or glutathione peroxidase activities. Our results give further insights into the complex regulation and enzymic functions of this plant gene super-family.

Arabidopsis glutathione S-transferase multigen family regulation substrates 

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References

  1. Alfenito, M.R., Souer, E., Goodman, C.D., Buell, R., Mol, J., Koes, R. and Walbot, V. 1998. Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 10: 1135–1149.Google Scholar
  2. Alvarez, M.E., Pennell, R.I., Meijer, P.-J., Ishikawa, A., Dixon, R.A. and Lamb, C. 1998. Reactive oxygen species intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773–784.Google Scholar
  3. Armstrong, R.N. 1997. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10: 2–18.Google Scholar
  4. Bartling, D.B., Radzio, R., Steiner, U. and Weiler, E.W. 1993. A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. Eur. J. Biochem. 216: 579–586.Google Scholar
  5. Bilang, J. and Sturm, A. 1995. Cloning and characterization of a glutathione S-transferase that can be photolabeled with 5–azidoindole-acetic acid. Plant Physiol. 109: 253–260.Google Scholar
  6. Board, P.G., Coggan, M., Chelvanayagam, G., Easteal, S., Jermiin, L.S., Schulte, G.K., Danley, D.E., Hoth, L.R., Griffor, M.C., Kamath, A.V., Rosner, M.H., Chrunyk, B.A., Perregaux, D.E., Gabel, C.A., Geoghegan, K.F. and Pandit J. 2000. Identification, characterization, and crystal structure of the omega class glutathione transferases. J. Biol. Chem. 275: 24798–24806.Google Scholar
  7. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.Google Scholar
  8. Chen, W.Q., Chao, G. and Singh, K.B. 1996. The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF-and OBP1–binding sites. Plant J. 10: 955–966.Google Scholar
  9. Chen, W.Q. and Singh, K.B. 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.Google Scholar
  10. Cummins, I., Cole, D.J. and Edwards, R. 1997. Purification of multiple glutathione transferases involved in herbicide detoxification from wheat (Triticum aestivum L.) treated with the safener fenchlorazole-ethyl. Pesticide Biochem. Physiol. 59: 35–49.Google Scholar
  11. Cummins, I., Cole, J.D. and Edwards, R. 1999. A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18: 285–292.Google Scholar
  12. Dixon, D.P., Cummins, I., Cole, D.J. and Edwards, R. 1998a. Glutathione mediated detoxification systems in plants. Current Opinion in Plant Biology 1: 258–266.Google Scholar
  13. Dixon, D.P., Cole, D.J. and Edwards, R. 1998b. Purification, regulation and cloning of a glutathione transferase from maize resembling the auxin-inducible type-III GSTs. Plant Mol. Biol. 36: 75–87.Google Scholar
  14. Dixon, D.P., Cole, D.J. and Edwards, R. 1999. Identification and cloning of AtGST 10 (Accession Nos. AJ131580 and AJ132398), members of a novel type of plant glutathione transferases. Plant Physiol. 119: 1568.Google Scholar
  15. Dixon, D.P., Cole, D.J. and Edwards, R. 2000. Characterisation of a zeta class glutathione transferase from Arabidopsis thaliana with a putative role in tyrosine catabolism. Arch. Biochem. Biophys. 384: 407–412.Google Scholar
  16. Droog, F. (1997). Plant glutathione S-transferases, a tale of theta and tau. Journal of Plant Growth Regulation 16: 95–107.Google Scholar
  17. Dudler, R., Hertig, C., Rebmann, G., Bull, J. and Mauch, F. 1991. A pathogen-induced wheat gene encodes a protein homologous to glutathione-S-transferases. Mol. Plant-Microbe Interact. 4: 14–18.Google Scholar
  18. Edwards, R., Dixon, D.P. and Walbot, V. 2000. Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends in Plant Science 5: 193–198.Google Scholar
  19. Fernández-Cañón, J.M. and Peñalva, M.A. 1998. Characterization of a fungal maleylacetoacetate isomerase gene and identification of its human homologue. J. Biol. Chem. 273: 329–337.Google Scholar
  20. Gonneau, J., Mornet. R. and Laloue, M. 1998. A Nicotiana plumbaginifolia protein labeled with an azido cytokinin agonist is a glutathione S-transferase. Physiologia Plantarum 103: 114–124.Google Scholar
  21. Greenberg, J.T., Guo, A.L., Klessig, D.F. and Ausubel, F.M. 1994. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551–563.Google Scholar
  22. Habig, W.H., Pabst, M.J. and Jakoby, W.B. 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249: 7130–7139.Google Scholar
  23. Hayes, J.D. and McLellan, L.I. 1999. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 31: 273–300.Google Scholar
  24. Hogge, L.R., Reed, D.W., Underhill, E.W. and Haughn, G.W. 1988. HPLC separation of glucosinolates from leaves and seeds of Arabidopsis thaliana and their identification using thermospray liquid chromatography/mass spectrometry. J. Chromatogr. Sci. 26: 551–556.Google Scholar
  25. Itzhaki, H. and Woodson, W.R. 1993. Characterization of an ethylene-responsive glutathione S-transferase gene cluster in carnation. Plant Mol. Biol. 22: 43–58.Google Scholar
  26. Itzhaki, H., Maxson, J.M. and Woodson, W.R. 1994. An ethylene-responsive enhancer element is involved in the senescence-related expression of the carnation glutathione S-transferase (GST1) gene. Proc. Natl. Acad. Sci. USA 91: 8925–8929.Google Scholar
  27. Kampranis, S.C., Damianova, R., Atallah, M., Toby, G., Kondi, G., Tsichlis, P.N. and Makris, A.M. 2000. A novel plant glutathione S-transferase/peroxidase suppresses Bax lethality in yeast. J. Biol. Chem. 275: 29207–29216.Google Scholar
  28. Kim, C.-S., Kwak, J.-M., Nam, H.-G., Kim, K.-C. and Cho, B.-H. 1994. Isolation and characterization of two cDNA clones that are rapidly induced during the wound response of Arabidopsis thaliana. Plant Cell Rep. 13: 340–343.Google Scholar
  29. Kiyosue, T., Yamaguchi-Shinozaki, K. and Shinozaki, K. 1993. Characterization of two cDNAs (ERD11) and (ERD13) for dehydration-inducible genes that encode putative glutathione S-transferases in Arabidopsis thaliana L. FEBS Lett. 335: 189–192.Google Scholar
  30. Kliebenstein, D.J., Dietrich, R.A., Martin, A.C., Last, R.L. and Dangl, J.L. 1999. LSD1 regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Molec Plant Microbe Interact. 12: 1022–1026.Google Scholar
  31. Kodym, R., Calkins, P. and Story, M. 1999. The cloning and characterization of a new stress response protein. J Biol Chem 274: 5131–5137.Google Scholar
  32. Lamoureux, G.L. and Rusness, D.G. 1993. Glutathione in the metabolism and detoxification of xenobiotics in plants. In: De Kok L.J., et al. (Eds.) Sulfur Nutrition and Assimilation in Higher Plants, SPB Academic Publishing, pp. 221–237.Google Scholar
  33. Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593.Google Scholar
  34. Li, Z.-S., Alfentino, M., Rea, P.A., Walbot, V. and Dixon, R.A. 1997. Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. Phytochemistry 45: 689–693.Google Scholar
  35. Litwack, G., Ketterer, B. and Arias, I.M. 1971. Ligandin: A hepatic protein which binds steroid, bilirubin, carcinogens and a number of exogenous organic anions. Nature 234: 466–467.Google Scholar
  36. Loyall, L., Uchida, K., Braun, S., Furuya, M. and Frohnmeyer, H. 2000. Glutathione and a UV light-induced glutathione S-transferase are involved in signaling to chalcone synthase in cell cultures. Plant Cell 12: 1939–1950.Google Scholar
  37. Lu, Y.-P., Li, Z.-S. and Rea, P.A. 1997. AtMRP1 gene of Arabidopsis encodes a glutathione S-conjguate pump: Isolation and functional definition of a plant ATP-binding cassette transporter gene. Proc. Natl. Acad. Sci. USA 94: 8243–8248.Google Scholar
  38. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K.A., Dangl, J.L. and Dietrich, R.A. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genet. 26: 403–410.Google Scholar
  39. Mannervik, B. and Guthenberg, C. 1981. Glutathione transferase (human placenta). Methods Enzymol 77: 231–235.Google Scholar
  40. Marrs, K.A., Alfenito, M.R., Lloyd, A.M. and Walbot, V. 1995. A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375: 397–400.Google Scholar
  41. Marrs, K.A. 1996. The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 127–158.Google Scholar
  42. Marrs, K.A. and Walbot, V. 1997. Expression and RNA splicing of the maize glutathione S-transferase Bronze-2 gene is regulated by cadmium and other stresses. Plant Physiol. 113: 93–102.Google Scholar
  43. Martinoia, E., Grill, E., Tommasini, R., Kreuz, K. and Amrhein, N. 1993. ATP-dependent glutathione S-conjugate 'export' pump in the vacuolar membrane of plants. Nature 364: 247–249.Google Scholar
  44. Mauch, F. and Dudler, R. 1993. Differential induction of distinct glutathione S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol. 102: 1193–1201.Google Scholar
  45. Mauch-Mani, B. and Slusarenko, A.J. 1994. Systemic acquired resistance in Arabidopsis thaliana induced by a predisposing infection with a pathogenic isolate of Fusarium oxysporum. Molec Plant-Microbe Interact. 7: 378–383.Google Scholar
  46. Maxson, J.M. and Woodson,W.R. 1996. Cloning of a DNA-binding protein that interacts with the ethylene-responsive enhancer element of the carnation GST1 gene. Plant Mol. Biol. 31: 751–759.Google Scholar
  47. McGonigle, B., Keeler, S.J., Lau, S.-L.C., Koeppe, M.K. and O'Keefe, D.P. 2000. A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol. 124: 1105–1120.Google Scholar
  48. Meyer, R.C., Goldsbrough, P.B. and Woodson, W.R. 1991. An ethylene-responsive flower senescence-related gene from carnation encodes a protein homologous to glutathione S-transferases. Plant Mol. Biol. 17: 277–281.Google Scholar
  49. Muller, M., Meijer, C., Zaman, G.J.R., Borst, P., Scheper, R.J., Mulder, N.H., de Vries, E.G.E. and Jansen, P.L.M. 1994. Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc. Natl. Acad. Sci. USA 91: 13033–13037.Google Scholar
  50. Mueller, L.A., Goodman, C.D., Silady, R.A. and Walbot, V. 2000. AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiol. 123: 1561–1570.Google Scholar
  51. Neuefeind, T., Huber, R., Dasenbrock, H., Prade, L. and Bieseler, B. 1997. Crystal structure of herbicide-detoxifying maize glutathione S-transferase-I in complex with lactoylglutathione: evidence for an induced-fit mechanism. J. Mol. Biol. 274: 446–453.Google Scholar
  52. Neuefeind, T., Huber, R., Reinemer, P., Knäblein, J., Prade, L., Mann, K. and Bieseler, B. 1997. 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.Google Scholar
  53. Paine, K. and Flower, D.R. 2000. The lipocalin website. Biochim. Biophys. Acta 1482: 351–352.Google Scholar
  54. Ranson, H., Collins, F. and Hemingway, J. 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.Google Scholar
  55. Rea, P.A., Li, Z.-S., Lu, Y.-P., Drozdowicz, Y.M. and Martinoia, E. 1998. From vacuolar GS-X pumps to multispecific ABC transporters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 727–760.Google Scholar
  56. Reinemer, P., Prade, L., Hof, P., Neuefeind, T., Huber, R., Zettl, R., Palme, K., Schell, J., Koelln, I., Bartunik, H.D. and Bieseler, B. 1996. Three-dimensional structure of glutathione S-transferase from Arabidopsis thaliana at 2.2 Å resolution: structural characterization of herbicide-conjugating plant glutathione S-transferases and a novel active site architecture. J. Mol. Biol. 255: 289–309.Google Scholar
  57. Reuber, T.L., Plotnikova, J.M., Dewdney, J., Rogers, E.E., Wood, W. and Ausubel, F.M. 1998. Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16: 473–485.Google Scholar
  58. Reymond, P., Weber, H., Damond, M. and Farmer, E.E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707–719.Google Scholar
  59. Roxas, V.P., Smith, R.K., Allen, E.R. and Allen, R.D. 1997. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nature Biotechnology 15: 988–991.Google Scholar
  60. Sharma, Y.K., Leon, J., Raskin, I. and Davies, K.R. 1996. Ozoneinduced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc. Natl. Acad. Sci. USA 93: 5099–5104.Google Scholar
  61. Tenhaken, R., Levine, A., Brisson, L.F., Dixon, R.A. and Lamb, C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Acad. Natl. Sci. USA 92: 4158–4163.Google Scholar
  62. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin. F. and Higgins, D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882.Google Scholar
  63. Ulmasov, T., Ohmiya, A., Hagen, G. and Guilfoyle, T. 1995. The soybean GH2/4 gene that encodes a glutathione S-transferase has a promoter that is activated by a wide range of chemical agents. Plant Physiol. 108: 919–927.Google Scholar
  64. van der Kop, D.A.M., Schuyer, M., Scheres, B., van der Zaal, B.J. and Hooykaas, P.J.J. 1996. Isolation and characterization of an auxin-inducible glutathione S-transferase gene of Arabidopsis thaliana. Plant Mol. Biol. 30: 839–844.Google Scholar
  65. Vollenweider, S., Weber, H., Stolz, S., Chételat, A. and Farmer, E.E. 2000. Fatty acid ketodienes and fatty acid ketotrienes: Michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves. Plant J. 24: 467–476.Google Scholar
  66. Wilce, M.C.J. and Parker, M.W. 1994. Structure and function of glutathione S-transferases. Biochim. Biophys. Acta 1205: 1–18.Google Scholar
  67. Yang, K.-Y., Kim, E.-Y., Kim, C.-S., Guh, J.-O., Kim, K.-C. and Cho, B.-H. 1998. Characterization of a glutathione S-transferase gene AtGST1 in Arabidopsis thaliana. Plant Cell Rep. 17: 700–704.Google Scholar
  68. Zettl, R., Schell, J. and Palme, K. 1994. Photoaffinity labeling of Arabidopsis thaliana 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.Google Scholar
  69. Zhou, J. and Goldsbrough, P.B. 1993. An Arabidopsis gene with homology to glutathione S-transferases is regulated by ethylene. Plant Mol. Biol. 22: 517–523.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Ulrich Wagner
    • 1
    • 2
  • Robert Edwards
    • 1
    • 2
  • David P. Dixon
    • 1
  • Felix Mauch
    • 1
    • 2
  1. 1.Department of BiologyUniversity of FribourgFribourgSwitzerland
  2. 2.Department of Biological SciencesUniversity of DurhamDurhamUK

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