Reactive oxygen species, nitric oxide and glutathione: A key role in the establishment of the legume-Rhizobium symbiosis?

Plant Physiology and Biochemistry

Volumn 40, Issue 6-8, 2002, Pages 619-624

  Hérouart, Didier ^a   Baudouin, Emmanuel ^a   Frendo, Pierre ^a   Harrison, Judith ^a   Santos, Renata ^b   Jamet, Alexandre ^a   Van de Sype, Ghislaine ^a   Touati, Danièle ^b   Puppo, Alain ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b INSTITUT JACQUES MONOD   (France)

Author keywords

Glutathione; Nitric oxide; Reactive oxygen species; Rhizobium legume symbiosis

Indexed keywords

BACTERIA (MICROORGANISMS); MEDICAGO SATIVA; RHIZOBIACEAE; RHIZOBIUM;

EID: 0036619735     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0981-9428(02)01415-8     Document Type: Conference Paper

References (52)

1. W.K. Alderton, C.E. Cooper, R.G. Knowles, Nitric oxide synthases: structure, function and inhibition. Biochem J. 357 (2001) 593-615.
2. C.J. Baker, E.W. Orlandi, Active oxygen in plant pathogenesis, Annu. Rev. Phytopathol. 33 (1995) 299-321.
3. C. Baron, P.C. Zambryski, The plant response in pathogenesis, symbiosis, and wounding: Variations on a common theme? Annu. Rev. Genet. 29 (1995) 107-129.
4. C.S. Bestwick, I.R. Brown, M.H.R. Bennett, J.W. Mansfield, Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola, Plant Cell 9 (1997) 209-221.
5. C. Bowler, R. Fluhr, The role of calcium and activated oxygens as signals for controlling cross-tolerance, Trends Plant Sci. 5 (2000) 241-245.
6. D. Cook, D. Dreyer, D. Bonnet, M. Howell, E. Nony, K. Vanden-Bosch, Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti, Plant Cell 7 (1995) 43-55.
7. M. Cueto, O. Hernandez-Perera, R. Martin, M.L. Bentura, J. Rodrigo, S. Lamas, et al., Presence of nitric oxide synthase activity in roots and nodules from Lupinus albus, FEBS Lett. 398 (1996) 159-164.
8. J.F. Dat, S. Vandenabeele, E. Vranova, M. Van Montagu, D. Inze, F. Van Breusegem, Dual action of the active oxygen species during plant stress responses, Cell Mol. Life Sci. 57 (2000) 779-795.
9. M. David, M.L. Daveran, J. Batut, A. Dedieu, O. Domergue, J. Ghai, et al., Cascade regulation of nif gene expression in Rhizobium meliloti, Cell 54 (1988) 671-683.
10. M. Delledonne, I. Murgia, D. Ederle, P.F. Sbicego, A. Biodani, A. Polverari, et al., Reactive oxygen intermediates modulate nitric oxide signaling in the plant hypersensitive disease resistance response, Plant Physiol. Biochem. 40 (2002) (in press).
11. M. Delledonne, Y. Xia, R.A. Dixon, C. Lamb, Nitric oxide functions as a signal in plant disease resistance, Nature 394 (1998) 585-588.
12. M. Delledonne, J. Zeier, A. Marocco, C. Lamb, Signal interactions between nitric oxide and reactive oxygen intermdiates in the plant hypersensitive disease resistance response, Proc. Natl. Acad Sci. USA 98 (2001) 13454-13459.
13. M.A. Djordjevic, D.W. Gabriel, B.G. Rolfe, Rhizobium: The refined parasite of legumes, Annu. Rev. Phytopathol. 25 (1987) 145-168.
14. S. Dorey, F. Baillieul, P. Saindrenan, B. Fritig, S. Kauffmann, Tobacco class I and Il catalases are differentially expressed during elicitor-induced hypersensitive cell death and localized acquired resistance, Mol. Plant-Microbe Interact. ll (1998) 1l02-1109.
15. J. Durner, D.F. Klessig, Nitric oxide as a signal in plants, Curr. Opin. Plant Biol. 2 (1999) 369-374.
16. J. Durner, D. Wendehenne, D.F. Klessig, Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose, Proc. Natl. Acad. Sci. USA 95 (1998) 10328-10333.
17. P.J. Evans, D. Gallesi, C. Mathieu, M.J. Hernandez, M. de Felipe, B. Halliwell, et al., Oxidative stress occurs during soybean nodule senescence, Planta 208 (1999) 73-79.
18. C.H. Foyer, H. Lopez-Delgado, J.F. Dat, I.M. Scott, Hydrogen peroxide and glutathione-associated mechanisms of acclimatory stress tolerance and signalling, Physiol. Plant. 100 (1997) 241-254.
19. C.H. Foyer, H. Rennenberg, Regulation of glutathione synthesis and its role in abiotic and biotic stress defence, in: C. Brunold (Ed.), Sulfur Nutrition and Sulfur Assimilation in Higher Plants, Paul Haupt, Bern, 2000, pp. 127-153.
20. P. Frendo, D. Gallesi, R. Turnbull, G. Van de Sype, D. Hérouart, A. Puppo, Localisation of glutathione and homoglutathione in Medicago truncatula is correlated to a differential expression of genes involved in their synthesis, Plant J. 17 (1999) 215-219.
21. P. Frendo, M.J. Hernandez Jimenéz, C. Mathieu, L. Duret, D. Gallesi, G. Van de Sype, et al., A Medicago truncatula homoglutathione synthetase is derived from glutathione synthetase by gene duplication, Plant Physiol. 126 (2001) 1706-1715.
22. P. Gamas, F. de Billy, G. Truchet, Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtNl and MtNl3, encoding products homologous to plant defense proteins, Mol. Plant-Microbe Int. 11 (1998) 393-403.
23. W. Gong, B. Hao, M.K. Chan, New mechanistic insights from structural studies of oxygen-sensing domain of Bradyrhizobium japonicum FixL, Biochemistry 39 (2000) 3955-3962.
24. 2 is the likely intermediary signaling molecule for the response, Plant J. 22 (2000) 87-95.
25. J.T. Hancock, R. Desikan, A. Clarke, R.D. Hurst, S.J. Neill, Cell signalling following plant/pathogen interactions involves the generation of reactive oxygen and reactive nitrogen species, Plant Physiol. Biochem. 40 (2002) (in press).
26. D. Hérouart, S. Sigaud, S. Moreau, P. Frendo, D. Touati, A. Puppo, Cloning and characterization of the katA gene of Rhizobium meliloti encoding a hydrogen peroxide-inducible catalase, J. Bacteriol. 178 (1996) 6802-6809.
27. X. Huang, E. Kiefer, U. von Rad, D. Ernst, I. Foissner, J. Durner, Nitric oxide burst and nitric oxide-dependent gene induction in plants, Plant Physiol. Biochem. 40 (2002) 000.
28. C. Lamb, R.A. Dixon, The oxidative burst in plant disease resistance, Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 (1997) 251-275.
29. C. Langebartels, M. Schraudner, W. Heller, D. Ernst, H. Sandermann, Oxidative stress and defense reactions in plants exposed to air pollutants and UV-B radiation, in: D. Inze, M. Van Montagu (Eds.), Oxidative stress in plants, Harwood Academic Publishers, Amsterdam, 2000, pp. 105-135.
30. G.S. Lukat-Rodgers, K.R. Rodgers, Characterization of ferrous FixL-nitric oxide adducts by resonance Raman spectroscopy, Biochemistry 36 (1997) 4178-4187.
31. S.A.H. Mackerness, C.F. John, B. Jordan, B. Thomas, Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide, FEBS Lett. 489 (2001) 237-242.
32. M.A. Matamoros, J.F. Moran, I. Iturbe-Ormaetxe, M.C. Rubio, M. Becana, Glutathione and homoglutathione synthesis in legume root nodules, Plant Physiol. 121 (1999) 879-888.
33. C. Mathieu, S. Moreau, P. Frendo, A. Puppo, M.J. Davies, Direct detection of radicals in intact soybean nodules: presence of nitric oxide-leghemoglobin complexes, Free Rad. Biol. Med. 24 (1998) 1242-1249.
34. M.J. May, K.E. Hammond-Kosack, J.D.G. Jones, Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum, Plant Physiol. 110 (1996) 1367-1379.
35. R. Mittler, X. Feng, M. Cohen, Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco, Plant Cell 10 (1998) 461-473.
36. 2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production by abi and abi2-1 protein phosphatase 2C mutants, Plant Cell 13 (2001) 2513-2523.
37. M. Parniske, C. Zimmermann, P.B. Cregan, D. Werner, Hypersensitive reaction of nodule cells in the Glycine max sp./Bradyrhizobium japonicum symbiosis occurs at the genotype specific level, Bot. Acta 103 (1990) 318-320.
38. S.K. Ramu, H.M. Peng, D. Cook, Rhizobial nod factor triggers a spacially localized oxidative burst that is implicated in early nodulin regulation (Abstr.), International Society for Molecular Plant-Microbe Interactions, St Paul, 1999, pp. 71.
39. R. Sanchez-Fernandez, M. Fricker, L.B. Corben, N.S. White, N. Sheard, C.J. Leaver, et al., Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control, Proc. Natl. Acad. Sci. USA 94 (1997) 2745-2750.
40. R. Santos, D. Hérouart, A. Puppo, D. Touati, Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis, Mol. Microbiol. 38 (2000) 750-759.
41. R. Santos, D. Hérouart, S. Sigaud, D. Touati, A. Puppo, Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction, Mol. Plant-Microbe Interact. 14 (2001) 86-89.
42. S. Sigaud, V. Becquet, P. Frendo, A. Puppo, D. Hérouart, Differential regulation of two divergent HPII-like catalase genes of Sinorhizobium meliloti during free living growth and protective role of both catalases during symbiosis, J. Bacteriol. 181 (1999) 2634-2639.
43. J.G. Streeter, Carbohydrate, organic acid and amino acid composition of bacteroids and cytosol from soybean nodules, Plant Physiol. 85 (1987) 768-773.
44. J.C. Trinchant, J. Rigaud, Nitrite and nitric oxide as inhibitors of nitrogenase from soybean bacteroids, Appl. Environ. Microbiol. 44 (1982) 1385-1388.
45. G. Truchet, P. Roche, P. Lerouge, J. Vasse, S. Camut, F. de Billy, et al., Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa, Nature 351 (1991) 670-673.
46. H. Vanacker, T.L.W. Carver, C.H. Foyer, Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves, Plant Physiol. 117 (1998) 1103-1114.
47. 2 and NO: redox signals in disease resistance, Trends Plant Sci. 3 (1998) 330-334.
48. J. Vasse, F. de Billy, J. Truchet, Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction, Plant J. 4 (1993) 555-566.
49. T. Vernoux, R.C. Wilson, K.A. Seeley, J.P. Reichheld, S. Muroy, S. Brown, et al., The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development, Plant Cell 12 (2000) 97-109.
50. R.J. Wais, C. Galera, G. Oldroyd, R. Catoira, R.V. Penmetsa, D. Cook, et al., Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula, Proc. Natl. Acad Sci. USA 97 (2000) 13407-13412.
51. V.P.M. Wingate, M.A. Lawton, C.J. Lamb, Glutathione causes a massive and selective induction of plant defense genes, Plant Physiol. 87 (1988) 206-210.
52. J.P. Wisniewski, E.A. Rathbun, J.P. Knox, N.J. Brewin, Involvement of diamine oxidase and peroxidase in insolubilization of extracellular matrix: Implications for pea nodule initiation by Rhizobium leguminosarum, Mol. Plant-Microbe Int. 13 (2000) 413-420.