Skip to main content
Log in

Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Glutathione (GSH) is one of the main antioxidants in plants. Legumes have the specificity to produce a GSH homolog, homoglutathione (hGSH). We have investigated the regulation of GSH and hGSH synthesis by nitric oxide (NO) in Medicago truncatula roots. Analysis of the expression level of gamma-glutamylcysteine synthetase (γ-ECS), glutathione synthetase (GSHS) and homoglutathione synthetase (hGSHS) after treatment with sodium nitroprusside (SNP) and nitrosoglutathione (GSNO), two NO-donors, showed that γ-ecs and gshs genes are up regulated by NO treatment whereas hgshs expression is not. Differential accumulation of GSH was correlated to gene expression in SNP-treated roots. Our results provide the first evidence that GSH synthesis pathway is regulated by NO in plants and that there is a differential regulation between gshs and hgshs in M. truncatula.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Abbreviations

γ-EC:

Gamma-glutamylcysteine

γ-ECS:

Gamma-glutamylcysteine synthetase

FeCN:

Ferricyanide

GSH:

Glutathione

GSHS:

Glutathione synthetase

GSNO:

Nitrosoglutathione

hGSH:

Homoglutathione

hGSHS:

Homoglutathione synthetase

JA:

Jasmonic acid

NO:

Nitric oxide

SNP:

Sodium nitroprusside

References

  • Beligni MV, Lamattina L (1999) Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Nitric Oxide 3:199–208

    Article  PubMed  CAS  Google Scholar 

  • Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  PubMed  CAS  Google Scholar 

  • Boisson-dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogene-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14:695–700

    PubMed  CAS  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459

    Article  PubMed  CAS  Google Scholar 

  • de Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol 130:698–708

    Article  PubMed  Google Scholar 

  • Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314–16318

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:3004.1–3004.10

    Article  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333

    Article  PubMed  CAS  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059

    Article  PubMed  CAS  Google Scholar 

  • Frendo P, Gallesi D, Turnbull R, Van de Sype G, Hérouart D, Puppo A (1999) Localisation of glutathione and homoglutathione in Medicago truncatula is correlated to a differential expression of genes involved in their synthesis. Plant J 17:215–219

    Article  CAS  Google Scholar 

  • Graziano M, Beligni MV, Lamattina L (2002) Nitric oxide improves internal iron availability in plants. Plant Physiol 130:1852–1859

    Article  PubMed  CAS  Google Scholar 

  • Grun S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516

    Article  PubMed  CAS  Google Scholar 

  • Harrison J, Puppo A, Frendo P (2003) The synthesis and the roles of glutathione and homoglutathione in legumes. Adv Plant Physiol 6:385–412

    Google Scholar 

  • Hogg N (2000) Biological chemistry and clinical potential of S-nitrosothiols. Free Radic Biol Med 28:1478–1486

    Article  PubMed  CAS  Google Scholar 

  • Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218:938–946

    Article  PubMed  CAS  Google Scholar 

  • Kim JM, Kim H, Kwon SB, Lee SY, Chung SC, Jeong DW, Min BM (2004) Intracellular glutathione status regulates mouse bone marrow monocyte-derived macrophage differentiation and phagocytic activity. Biochem Biophys Res Commun 325:101–108

    Article  PubMed  CAS  Google Scholar 

  • Klapheck S (1988) Homoglutathione: isolation, quantification and occurrence in legumes. Physiol Plant 74:727–732

    Article  CAS  Google Scholar 

  • Klapheck S, Chrost B, Starke J, Zimmermann H (1992) γ-glutamyl-cysteinylserine—a new homologue of glutathione in plants of the family Poaceae. Bot Acta 105:174–179

    CAS  Google Scholar 

  • Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842

    Article  PubMed  CAS  Google Scholar 

  • Kuo PC, Abe KY (1996) Nitric oxide-associated regulation of hepatocyte glutathione synthesis is a guanylyl cyclase-independent event. Surgery 120:309–314

    Article  PubMed  CAS  Google Scholar 

  • Matamoros MA, Baird LM, Escuredo PR, Dalton DA, Minchin FR, Iturbe-Ormaetxe I, Rubio MC, Moran JF, Gordon AJ, Becana M (1999) Stress induced legume root nodule senescence. Physiological, biochemical and structural alterations. Plant Physiol 121:97–112

    Article  PubMed  CAS  Google Scholar 

  • Mayer B, Hemmens B (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 22:477–481

    Article  PubMed  CAS  Google Scholar 

  • Meuwly P, Thibault P, Rauser WE (1993) γ-glutamylcysteinylglutamic acid—a new homologue of glutathione in maize seedlings exposed to cadmium. FEBS Lett 336:472–476

    Article  PubMed  CAS  Google Scholar 

  • Moellering D, McAndrew J, Patel RP, Cornwell T, Lincoln T, Cao X, Messina JL, Forman HJ, Jo H, Darley-Usmar VM (1998) Nitric oxide-dependent induction of glutathione synthesis through increased expression of gamma-glutamylcysteine synthetase. Arch Biochem Biophys 358:74–82

    Article  PubMed  CAS  Google Scholar 

  • Murgia I, Delledonne M, Soave C (2002) Nitric oxide mediates iron-induced ferritin accumulation in Arabidopsis. Plant J 30:521–528

    Article  PubMed  CAS  Google Scholar 

  • Murgia I, de Pinto MC, Delledonne M, Soave C, De Gara L (2004) Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death, and cell redox state in plant cells. J Plant Physiol 161:777–783

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Foyer C (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cardenas ML, Ryan CA (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol 130:487–493

    Article  PubMed  CAS  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide response transcripts in Arabidopsis. Plant Biotech J 2:359–366

    Article  CAS  Google Scholar 

  • Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe Interact 16:1094–1105

    PubMed  CAS  Google Scholar 

  • Price C (1957) A new thiol in legumes. Nature 180:148–149

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis TA (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  PubMed  CAS  Google Scholar 

  • Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–1902

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol 46:923–930

    Article  PubMed  CAS  Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Hogg N (2004) The mechanism of transmembrane S-nitrosothiol transport. Proc Natl Acad Sci USA 101:7891–7896

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Chiara Pucciariello is the recipient of a Marie Curie fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alain Puppo.

Additional information

G. Innocenti and C. Pucciariello have contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Innocenti, G., Pucciariello, C., Le Gleuher, M. et al. Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225, 1597–1602 (2007). https://doi.org/10.1007/s00425-006-0461-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0461-3

Keywords

Navigation