The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress

Plant Journal

Volumn 58, Issue 1, 2009, Pages 53-68

  Sappl, Pia G ^a,b,c   Carroll, Adam J ^a   Clifton, Rachael ^a,d   Lister, Ryan ^a,e   Whelan, James ^a   Harvey Millar, A ^a   Singh, Karam B ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b CSIRO   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY COLLEGE CORK   (Ireland)

^e SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Arabidopsis metabolite profiling; Hydrogen peroxide; Plant detoxification genes; Plant GSTs; Plant stress responses; Salicylic acid

Indexed keywords

ARABIDOPSIS;

1 CHLORO 2,4 DINITROBENZENE; ARABIDOPSIS PROTEIN; GLUTATHIONE; GLUTATHIONE TRANSFERASE P1; HYDROGEN PEROXIDE; PLANT RNA; SALICYLIC ACID DERIVATIVE;

ARABIDOPSIS; ARTICLE; CULTURE TECHNIQUE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; METABOLOMICS; MULTIGENE FAMILY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; SEEDLING; SIGNAL TRANSDUCTION; TIME; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CULTURE TECHNIQUES; DINITROCHLOROBENZENE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GLUTATHIONE; GLUTATHIONE S-TRANSFERASE PI; HYDROGEN PEROXIDE; METABOLOMICS; MULTIGENE FAMILY; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; PRINCIPAL COMPONENT ANALYSIS; RNA, PLANT; SALICYLIC ACIDS; SEEDLING; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 63349110495     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03761.x     Document Type: Article

References (73)

1. Alfenito, M.R., Souer, E., Goodman, C.D., Buell, R., Mol, J., Koes, R. Walbot, V. (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell, 10, 1135 1149.
2. Amirsadeghi, S., Robson, C.A., McDonald, A.E. Vanlerberghe, G.C. (2006) Changes in plant mitochondrial electron transport alter cellular levels of reactive oxygen species and susceptibility to cell death signaling molecules. Plant Cell Physiol. 47, 1509 1519.
3. Baxter, C.J., Redestig, H., Schauer, N., Repsilber, D., Patil, K., Nielsen, J., Selbig, J., Liu, J., Fernie, A.R. Sweetlove, L.J. (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol. 143, 312 325.
4. Bianchi, M.W., Roux, C. Vartanian, N. (2002) Drought regulation of GST8, encoding the Arabidopsis homologue of ParC/Nt107 glutathione transferase/peroxidase. Physiol. Plant. 116, 96 105.
5. Bilang, J. Sturm, A. (1995) Cloning and characterization of a glutathione S-transferase that can be photolabeled with 5-azido-indole-3-acetic acid. Plant Physiol. 109, 253 260.
6. Borsani, O., Valpuesta, V. Botella, M.A. (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 126, 1024 1030.
7. Capell, T., Bassie, L. Christou, P. (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Natl Acad. Sci. USA, 101, 9909 9914.
8. Chalfun-Junior, A., Franken, J., Mes, J.J., Marsch-Martinez, N., Pereira, A. Angenent, G.C. (2005) ASYMMETRIC LEAVES2-LIKE1 gene, a member of the AS2/LOB family, controls proximal-distal patterning in Arabidopsis petals. Plant Mol. Biol. 57, 559 575.
9. Chen, W. (1999) Regulation of glutathione S-transferase gene expression in Arabidopsis. In Department of Molecular, Cell and Developmental Biology. Los Angeles : University of California, pp. 144.
10. Chen, W. 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.
11. 2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J. 10, 955 966.
12. Clifton, R., Lister, R., Parker, K.L., Sappl, P.G., Elhafez, D., Millar, A.H., Day, D.A. Whelan, J. (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58, 193 212.
13. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
14. Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M. Jacobsen, S.E. (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature, 452, 215 219.
15. Coleman, J., Blake-Kalff, M. Davies, E. (1997) Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends Plant Sci. 2, 144 151.
16. Dempsey, D., Shah, J. Klessig, D. (1999) Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18, 547 575.
17. Desikan, R., Neill, S.J. Hancock, J.T. (2000) Hydrogen peroxide-induced gene expression in Arabidopsis thaliana. Free. Rad. Biol. Med. 28, 773 778.
18. Desikan, R., Mackerness, S.A.H., Hancock, J.T. Neill, S.J. (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159 172.
19. Dixon, D.P., Lapthorn, A. Edwards, R. (2002a) Plant glutathione transferases. Genome Biol. 3, reviews 3004.1 3004.10.
20. Dixon, D.P., Davis, B.G. Edwards, R. (2002b) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J. Biol. Chem. 277, 30859 30869.
21. Droog, F. (1997) Plant glutathione S-transferases, a tale of theta and tau. J. Plant Growth Regul. 16, 95 107.
22. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., Foyer, C.H. De Paepe, R. (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell, 15, 1212 1226.
23. Edwards, R. Dixon, D.P. (2000) The role of glutathione transferases in herbicide metabolism. In Herbicides and Their Mechanisms of Action (Cobb, A.H. Kirkwood, R.C., eds). Sheffield : Sheffield Academic Press Ltd, pp. 38 71.
24. Edwards, R. Dixon, D.P. (2005) Plant glutathione transferases. In Glutathione Transferases and Gamma-Glutamyl Transpeptidases (Sies, H. Packer, L., eds). San Diego, CA : Elsevier Academic Press Inc, pp. 169 186.
25. Edwards, R., Dixon, D.P. Walbot, V. (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5, 193 198.
26. Enns, L.C., Kanaoka, M.M., Torii, K.U., Comai, L., Okada, K. Cleland, R.E. (2005) Two callose synthases, GSL1 and GSLS, play an essential and resundant role in plant and pollen development and in fertility. Plant Mol. Biol. 58, 333 349.
27. Foley, R.C., Sappl, P.G., Perl-Treves, R., Millar, A.H. Singh, K.B. (2006) Desensitization of GSTF8 induction by a prior chemical treatment is long lasting and operates in a tissue dependent manner. Plant Physiol. 142, 245 253.
28. Foyer, C.H. Noctor, G. (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 17, 1866 1875.
29. Glombitza, S., Dubuis, P.H., Thulke, O. et al. (2004) Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant Mol. Biol. 54, 817 835.
30. Gonneau, M., Pagant, S., Brun, F. Laloue, M. (2001) Photoaffinity labelling with the cytokinin agonist azido-CPPU of a 34 kDa peptide of the intracellular pathogenesis-related protein family in the moss Physcomitrella patens. Plant Mol. Biol. 46, 539 548.
31. Gronwald, J.W. Plaisance, K.L. (1998) Isolation and characterisation of glutathione S-transferase isozymes from sorghum. Plant Physiol. 117, 877 892.
32. Habig, W.H., Pabst, M.J. Jakoby, W.B. (1974) The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130 7139.
33. Helliwell, C.A. Waterhouse, P.M. (2003) Constructs and methods for high-througput gene silencing in plants. Methods 30, 289 295.
34. Helliwell, C.A., Chin-Atkins, A.N., Wilson, I.W., Chapple, R., Dennis, E.S. Chaudhury, A. (2001) The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell, 13, 2115 2125.
35. Kasukabe, Y., He, L., Nada, K., Misawa, S., Ihara, I. Tachibana, S. (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol. 45, 712 722.
36. Kitamura, S., Shikazono, N. Tanaka, A. (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J. 37, 104 114.
37. Kiyosue, T., Yamaguchi-Shinozaki, K. 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.
38. Kurepa, J., Smalle, J., Van Montagu, M. Inzé, D. (1998) Polyamines and paraquat toxicity in Arabidopsis thaliana. Plant Cell Physiol. 39, 987 992.
39. Lederer, B. Boger, P. (2003) Binding and protection of porphyrins by glutathione S-transferases of Zea mays L. Biochim. Biophys. Acta, 1621, 226 233.
40. Lederer, B. Boger, P. (2005) A ligand function of glutathione S-transferase. Z. Naturforsch.[C], 60, 166 171.
41. Light, G.G., Mahan, J.R., Roxas, V.P. Allen, R.D. (2005) Transgenic cotton (Gossypium hirsutum L.) seedlings expressing a tobacco glutathione S-transferase fail to provide increased stress tolerance. Planta, 222, 346 354.
42. Lister, R., O'Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H. Ecker, J.R. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell, 133, 523 536.
43. Marrs, K.A. (1996) The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 127 158.
44. Marrs, K.A., Alfenito, M.R., Lloyd, A.M. Walbot, V. (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature, 375, 397 400.
45. Mauch, F. Dudler, R. (1993) Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol. 102, 1193 1201.
46. McGonigle, B., Keeler, S.J., Cindy Lau, S.M., Koeppe, M.K. 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.
47. Meyers, B.C., Lee, D.K., Vu, T.H., Tej, S.S., Edberg, S.B., Matvienko, M. Tindell, L.D. (2004) Arabidopsis MPSS. An online resource for quantitative expression analysis. Plant Physiol. 135, 801 813.
48. Moons, A. (2003) Osgstu3 and osgtu4, encoding tau class glutathione S-transferases, are heavy metal- and hypoxic stress-induced and differentially salt stress-responsive in rice roots. FEBS Lett. 553, 427 432.
49. Moons, A. (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitam. Horm. 72, 155 202.
50. Mueller, L.A., Goodman, C.D., Silady, R.A. Walbot, V. (2000) AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiol. 123, 1561 1570.
51. Nakamura, Y., Yuki, K., Park, S.Y. Ohya, T. (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol. 30, 833 839.
52. Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T. Jones, J.D. (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113 1128.
53. Noctor, G. Foyer, C.H. (1998) Simultaneous measurement of foliar glutathione, gamma-glutamylcysteine, and amino acids by high-performance liquid chromatography: comparison with two other assay methods for glutathione. Anal. Biochem. 264, 98 110.
54. Norman, C., Howell, K.A., Millar, A.H., Whelan, J. Day, D.A. (2004) Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. Plant Physiol. 134, 492 501.
55. Roessner-Tunali, U., Urbanczyk-Wochniak, E., Czechowski, T., Kolbe, A., Willmitzer, L. Fernie, A.R. (2003) De novo amino acid biosynthesis in potato tubers is regulated by sucrose levels. Plant Physiol. 133, 683 692.
56. Roxas, V.P., Smith, R.K. Jr., Allen, E.R. Allen, R.D. (1997a) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nature Biotechnol. 15, 988 991.
57. Roxas, V.P., Wang, J., Lodhi, S.A. Allen, R.D. (1997b) Engineering stress tolerance in transgenic plants. Acta Physiol. Plant, 19, 591 594.
58. Roxas, V.P., Lodhi, S.A., Garrett, D.K., Mahan, J.R. Allen, R.D. (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol. 41, 1229 1234.
59. Sappl, P.G., Heazlewood, J. Millar, A.H. (2004a) Untangling multi-gene families in plants by integrating proteomics into functional genomics. Phytochemistry, 65, 1517 1530.
60. Sappl, P.G., Onate-Sanchez, L., Singh, K.B. Millar, A.H. (2004b) Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Mol. Biol. 54, 205 219.
61. Senaratna, T., Touchell, D., Bunn, E. Dixon, K. (2000) Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul. 30, 157 161.
62. Seppanen, M.M., Cardi, T., Hyokki, M.B. Pehu, E. (2000) Characterisation and expression of cold-induced gluathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids. Plant Sci. 153, 125 133.
63. Sharma, Y.K., Leon, J., Raskin, I. Davis, K.R. (1996) Ozone-induced 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.
64. Smith, A.P., Nourizadeh, S.D., Peer, W.A., Xu, J., Bandyopadhyay, A., Murphy, A.S. Goldsbrough, P.B. (2003) Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids. Plant J. 36, 433 442.
65. Tantikanjana, T., Mikkelsen, M.D., Hussain, M., Halkier, B.A. Sundaresan, V. (2004) Functional analysis of the tandem-duplicated p450 genes SPS/BUS/CYP79F1 and CYP79F2 in glucosinolate biosynthesis and plant development by Ds transposition-generated double mutants. Plant Physiol. 135, 840 848.
66. Taylor, N.L., Heazlewood, J.L., Day, D.A. Millar, A.H. (2005) Differential impact of environmental stresses on the pea mitochondrial proteome. Mol. Cell. Proteomics, 4, 1122 1133.
67. Vollenweider, S., Weber, H., Stolz, S., Chetelat, A. 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.
68. Wagner, U., Edwards, R., Dixon, D.P. Mauch, F. (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515 532.
69. Ye, B., Muller, H.H., Zhang, J. Gressel, J. (1997) Constitutively elevated levels of putrescine and putrescine-generating enzymes correlated with oxidant stress resistance in Conyza bonariensis and wheat. Plant Physiol. 115, 1443 1451.
70. Yu, T., Li, Y.S., Chen, X.F., Hu, J., Chang, X. Zhu, Y.G. (2003) Transgenic tobacco plants overexpressing cotton glutathione S-transferase (GST) show enhanced resistance to methyl viologen. J. Plant Physiol. 160, 1305 1311.
71. Zettl, R., Schell, J. 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.
72. Zhou, J. Goldsbrough, P.B. (1993) An Arabidopsis gene with homology to glutathione S-transferases is regulated by ethylene. Plant Mol. Biol. 22, 517 523.
73. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D., Felix, G. Boller, T. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428, 764 767.