Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1998 Sep;10(9):1539–1550. doi: 10.1105/tpc.10.9.1539

Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis.

C Xiang 1, D J Oliver 1
PMCID: PMC144077  PMID: 9724699

Abstract

Glutathione plays a pivotal role in protecting plants from environmental stresses, oxidative stress, xenobiotics, and some heavy metals. Arabidopsis plants treated with cadmium or copper responded by increasing transcription of the genes for glutathione synthesis, gamma-glutamylcysteine synthetase and glutathione synthetase, as well as glutathione reductase. The response was specific for those metals whose toxicity is thought to be mitigated through phytochelatins, and other toxic and nontoxic metals did not alter mRNA levels. Feeding experiments suggested that neither oxidative stress, as results from exposure to H2O2, nor oxidized or reduced glutathione levels were responsible for activating transcription of these genes. Jasmonic acid also activated the same suite of genes, which suggests that it might be involved in the signal transduction pathway for copper and cadmium. Jasmonic acid treatment increased mRNA levels and the capacity for glutathione synthesis but did not alter the glutathione content in unstressed plants, which supports the idea that the glutathione concentration is controlled at multiple levels.

Full Text

The Full Text of this article is available as a PDF (326.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen R. D. Dissection of Oxidative Stress Tolerance Using Transgenic Plants. Plant Physiol. 1995 Apr;107(4):1049–1054. doi: 10.1104/pp.107.4.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen R. D., Webb R. P., Schake S. A. Use of transgenic plants to study antioxidant defenses. Free Radic Biol Med. 1997;23(3):473–479. doi: 10.1016/s0891-5849(97)00107-x. [DOI] [PubMed] [Google Scholar]
  3. Blechert S., Brodschelm W., Hölder S., Kammerer L., Kutchan T. M., Mueller M. J., Xia Z. Q., Zenk M. H. The octadecanoic pathway: signal molecules for the regulation of secondary pathways. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4099–4105. doi: 10.1073/pnas.92.10.4099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bowler C., Alliotte T., De Loose M., Van Montagu M., Inzé D. The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J. 1989 Jan;8(1):31–38. doi: 10.1002/j.1460-2075.1989.tb03345.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chen W., Chao G., Singh K. B. The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J. 1996 Dec;10(6):955–966. doi: 10.1046/j.1365-313x.1996.10060955.x. [DOI] [PubMed] [Google Scholar]
  6. Conconi A., Smerdon M. J., Howe G. A., Ryan C. A. The octadecanoid signalling pathway in plants mediates a response to ultraviolet radiation. Nature. 1996 Oct 31;383(6603):826–829. doi: 10.1038/383826a0. [DOI] [PubMed] [Google Scholar]
  7. Creelman R. A., Mullet J. E. Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4114–4119. doi: 10.1073/pnas.92.10.4114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Creelman R. A., Mullet J. E. Oligosaccharins, brassinolides, and jasmonates: nontraditional regulators of plant growth, development, and gene expression. Plant Cell. 1997 Jul;9(7):1211–1223. doi: 10.1105/tpc.9.7.1211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Creelman R. A., Tierney M. L., Mullet J. E. Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4938–4941. doi: 10.1073/pnas.89.11.4938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Creelman Robert A., Mullet John E. BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):355–381. doi: 10.1146/annurev.arplant.48.1.355. [DOI] [PubMed] [Google Scholar]
  11. De Vos C. H., Vonk M. J., Vooijs R., Schat H. Glutathione Depletion Due to Copper-Induced Phytochelatin Synthesis Causes Oxidative Stress in Silene cucubalus. Plant Physiol. 1992 Mar;98(3):853–858. doi: 10.1104/pp.98.3.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DeRocher E. J., Bohnert H. J. Development and Environmental Stress Employ Different Mechanisms in the Expression of a Plant Gene Family. Plant Cell. 1993 Nov;5(11):1611–1625. doi: 10.1105/tpc.5.11.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Doares S. H., Syrovets T., Weiler E. W., Ryan C. A. Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4095–4098. doi: 10.1073/pnas.92.10.4095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dron M., Clouse S. D., Dixon R. A., Lawton M. A., Lamb C. J. Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6738–6742. doi: 10.1073/pnas.85.18.6738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fahey R. C., Newton G. L. Determination of low-molecular-weight thiols using monobromobimane fluorescent labeling and high-performance liquid chromatography. Methods Enzymol. 1987;143:85–96. doi: 10.1016/0076-6879(87)43016-4. [DOI] [PubMed] [Google Scholar]
  16. Fogel S., Welch J. W. Tandem gene amplification mediates copper resistance in yeast. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5342–5346. doi: 10.1073/pnas.79.17.5342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Foyer C. H., Souriau N., Perret S., Lelandais M., Kunert K. J., Pruvost C., Jouanin L. Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol. 1995 Nov;109(3):1047–1057. doi: 10.1104/pp.109.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fürst P., Hu S., Hackett R., Hamer D. Copper activates metallothionein gene transcription by altering the conformation of a specific DNA binding protein. Cell. 1988 Nov 18;55(4):705–717. doi: 10.1016/0092-8674(88)90229-2. [DOI] [PubMed] [Google Scholar]
  19. Griffith O. W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem. 1980 Jul 15;106(1):207–212. doi: 10.1016/0003-2697(80)90139-6. [DOI] [PubMed] [Google Scholar]
  20. Grill E., Winnacker E. L., Zenk M. H. Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci U S A. 1987 Jan;84(2):439–443. doi: 10.1073/pnas.84.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Grill E., Winnacker E. L., Zenk M. H. Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science. 1985 Nov 8;230(4726):674–676. doi: 10.1126/science.230.4726.674. [DOI] [PubMed] [Google Scholar]
  22. Gundlach H., Müller M. J., Kutchan T. M., Zenk M. H. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2389–2393. doi: 10.1073/pnas.89.6.2389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Howden R., Goldsbrough P. B., Andersen C. R., Cobbett C. S. Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol. 1995 Apr;107(4):1059–1066. doi: 10.1104/pp.107.4.1059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jamai A., Tommasini R., Martinoia E., Delrot S. Characterization of Glutathione Uptake in Broad Bean Leaf Protoplasts. Plant Physiol. 1996 Aug;111(4):1145–1152. doi: 10.1104/pp.111.4.1145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kim S. R., Choi J. L., Costa M. A., An G. Identification of G-Box Sequence as an Essential Element for Methyl Jasmonate Response of Potato Proteinase Inhibitor II Promoter. Plant Physiol. 1992 Jun;99(2):627–631. doi: 10.1104/pp.99.2.627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mason H. S., DeWald D. B., Mullet J. E. Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell. 1993 Mar;5(3):241–251. doi: 10.1105/tpc.5.3.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. May M. J., Leaver C. J. Arabidopsis thaliana gamma-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast, and Escherichia coli homologs. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10059–10063. doi: 10.1073/pnas.91.21.10059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. May M. J., Leaver C. J. Oxidative Stimulation of Glutathione Synthesis in Arabidopsis thaliana Suspension Cultures. Plant Physiol. 1993 Oct;103(2):621–627. doi: 10.1104/pp.103.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Meister A., Anderson M. E. Glutathione. Annu Rev Biochem. 1983;52:711–760. doi: 10.1146/annurev.bi.52.070183.003431. [DOI] [PubMed] [Google Scholar]
  30. Mulcahy R. T., Gipp J. J. Identification of a putative antioxidant response element in the 5'-flanking region of the human gamma-glutamylcysteine synthetase heavy subunit gene. Biochem Biophys Res Commun. 1995 Apr 6;209(1):227–233. doi: 10.1006/bbrc.1995.1493. [DOI] [PubMed] [Google Scholar]
  31. Noctor G., Strohm M., Jouanin L., Kunert K. J., Foyer C. H., Rennenberg H. Synthesis of Glutathione in Leaves of Transgenic Poplar Overexpressing [gamma]-Glutamylcysteine Synthetase. Plant Physiol. 1996 Nov;112(3):1071–1078. doi: 10.1104/pp.112.3.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Orvar B. L., McPherson J., Ellis B. E. Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J. 1997 Feb;11(2):203–212. doi: 10.1046/j.1365-313x.1997.11020203.x. [DOI] [PubMed] [Google Scholar]
  33. Pearce G., Strydom D., Johnson S., Ryan C. A. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science. 1991 Aug 23;253(5022):895–897. doi: 10.1126/science.253.5022.895. [DOI] [PubMed] [Google Scholar]
  34. Prasad T. K., Anderson M. D., Martin B. A., Stewart C. R. Evidence for Chilling-Induced Oxidative Stress in Maize Seedlings and a Regulatory Role for Hydrogen Peroxide. Plant Cell. 1994 Jan;6(1):65–74. doi: 10.1105/tpc.6.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Prasad T. K., Anderson M. D., Stewart C. R. Localization and Characterization of Peroxidases in the Mitochondria of Chilling-Acclimated Maize Seedlings. Plant Physiol. 1995 Aug;108(4):1597–1605. doi: 10.1104/pp.108.4.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rauser W. E. Phytochelatins. Annu Rev Biochem. 1990;59:61–86. doi: 10.1146/annurev.bi.59.070190.000425. [DOI] [PubMed] [Google Scholar]
  37. Rüegsegger A., Schmutz D., Brunold C. Regulation of Glutathione Synthesis by Cadmium in Pisum sativum L. Plant Physiol. 1990 Aug;93(4):1579–1584. doi: 10.1104/pp.93.4.1579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Scheller H. V., Huang B., Hatch E., Goldsbrough P. B. Phytochelatin synthesis and glutathione levels in response to heavy metals in tomato cells. Plant Physiol. 1987 Dec;85(4):1031–1035. doi: 10.1104/pp.85.4.1031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sekhar K. R., Meredith M. J., Kerr L. D., Soltaninassab S. R., Spitz D. R., Xu Z. Q., Freeman M. L. Expression of glutathione and gamma-glutamylcysteine synthetase mRNA is Jun dependent. Biochem Biophys Res Commun. 1997 May 29;234(3):588–593. doi: 10.1006/bbrc.1997.6697. [DOI] [PubMed] [Google Scholar]
  40. Sharma Y. K., Davis K. R. Ozone-Induced Expression of Stress-Related Genes in Arabidopsis thaliana. Plant Physiol. 1994 Aug;105(4):1089–1096. doi: 10.1104/pp.105.4.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sharma Y. K., Léon J., Raskin I., Davis K. R. 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 U S A. 1996 May 14;93(10):5099–5104. doi: 10.1073/pnas.93.10.5099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Smith I. K. Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiol. 1985 Dec;79(4):1044–1047. doi: 10.1104/pp.79.4.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Steffens J. C., Hunt D. F., Williams B. G. Accumulation of non-protein metal-binding polypeptides (gamma-glutamyl-cysteinyl)n-glycine in selected cadmium-resistant tomato cells. J Biol Chem. 1986 Oct 25;261(30):13879–13882. [PubMed] [Google Scholar]
  44. Thiele D. J. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol Cell Biol. 1988 Jul;8(7):2745–2752. doi: 10.1128/mcb.8.7.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wang C. L., Oliver D. J. Cloning of the cDNA and genomic clones for glutathione synthetase from Arabidopsis thaliana and complementation of a gsh2 mutant in fission yeast. Plant Mol Biol. 1996 Sep;31(6):1093–1104. doi: 10.1007/BF00040827. [DOI] [PubMed] [Google Scholar]
  46. Willekens H., Chamnongpol S., Davey M., Schraudner M., Langebartels C., Van Montagu M., Inzé D., Van Camp W. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 1997 Aug 15;16(16):4806–4816. doi: 10.1093/emboj/16.16.4806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Williams M. E., Foster R., Chua N. H. Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell. 1992 Apr;4(4):485–496. doi: 10.1105/tpc.4.4.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wingate V. P., Lawton M. A., Lamb C. J. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 1988 May;87(1):206–210. doi: 10.1104/pp.87.1.206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wu A. L., Moye-Rowley W. S. GSH1, which encodes gamma-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol Cell Biol. 1994 Sep;14(9):5832–5839. doi: 10.1128/mcb.14.9.5832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Xiang C., Miao Z. H., Lam E. Coordinated activation of as-1-type elements and a tobacco glutathione S-transferase gene by auxins, salicylic acid, methyl-jasmonate and hydrogen peroxide. Plant Mol Biol. 1996 Nov;32(3):415–426. doi: 10.1007/BF00019093. [DOI] [PubMed] [Google Scholar]
  51. van der Kop D. A., Schuyer M., Scheres B., van der Zaal B. J., Hooykaas P. J. Isolation and characterization of an auxin-inducible glutathione S-transferase gene of Arabidopsis thaliana. Plant Mol Biol. 1996 Feb;30(4):839–844. doi: 10.1007/BF00019016. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES