Reactive oxygen species and antioxidants in legume nodules

Physiologia Plantarum

Volumn 109, Issue 4, 2000, Pages 372-381

  Becana, Manuel ^a   Dalton, David A ^b   Moran, Jose F ^a   Iturbe Ormaetxe, Iñaki ^a   Matamoros, Manuel A ^a   Rubio, Maria C ^a  

^a CSIC   (Spain)

^b REED COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; ASCORBATE PEROXIDASE; ASCORBIC ACID; HEMOGLOBIN; IRON; LEGUME; METABOLITE; NODULATION; OXIDATION; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

EID: 0033889209     PISSN: 00319317     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1399-3054.2000.100402.x     Document Type: Review

References (78)

1. Ames BN, Cathcart R, Schwiers E, Hochstein P (1981) Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc Natl Acad Sci USA 78: 6858-6862
2. Appleby CA (1984) Leghemoglobin and Rhizobium respiration. Annu Rev Plant Physiol 35: 443-478
3. Arp DJ, Burris RH (1979) Purification and properties of the paniculate hydrogenase from the bacteroids of soybean root nodules. Biochim Biophys Acta 570: 221-230
4. Asada K (1999) The water-water cycle in chloroplasts: Scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601-639
5. Baron C, Zambryski PC (1995) The plant response in pathogenesis, symbiosis, and wounding: Variations on a common theme? Annu Rev Gen 29: 107-129
6. Bashor CJ, Dalton DA (1999) Effects of exogenous application and stem infusion of ascorbate on soybean (Glycine max) root nodules. New Phytol 142: 19-26
7. Becana M, Klucas RV (1990) Enzymatic and nonenzymatic mechanisms for ferric leghemoglobin reduction in legume root nodules. Proc Natl Acad Sci USA 87: 7295-7299
8. Becana M, Klucas RV (1992) Transition metals in legume root nodules: Iron-dependent free radical production increases during nodule senescence. Proc Natl Acad Sci USA 89: 8958-8962
9. Becana M, Salin ML (1989) Superoxide dismutases in nodules of leguminous plants. Can J Bot 67: 415-421
10. Becana M, Paris FJ, Sandalio LM, del Río LA (1989) Isoenzymes of superoxide dismutase in nodules of Phaseolus bulgaris L., Pisum sativum L., and Vigna unguiculata (L.) Walp. Plant Physiol 90: 1286-1292
11. Becana M, Moran JF, Iturbe-Ormaetxe I (1998) Iron-dependent oxygen free radical generation in plants subjected to environmental stress: Toxicity and antioxidant protection. Plant Soil 201: 137-147
12. Bowler C, Van Camp W, Van Montagu M, Inzé D (1994) Superoxide dismutases in plants. Crit Rev Plant Sci 13: 199-218
13. Chinoy JJ (1984) The Role of Ascorbic Acid in Growth, Differentiation, and Metabolism of Plants. Martinus Nijhoff/Dr. Junk, The Hague
14. Coba de la Peña T, Frugier F, McKhann HI, Bauer P, Brown S, Kondorosi A, Crespi M (1997) A carbonic anhydrase gene is induced in the nodule primordium and its cell-specific expression is controlled by the presence of Rhizobium during development. Plant J 11: 407-420
15. Comba ME, Benavides MP, Tomaro ML (1998) Effect of salt stress on antioxidant defence system in soybean root nodules. Aust J Plant Physiol 25: 665-671
16. Cook D, Dreyer D, Bonnet D, Howell M, Nony E, VandenBosch K (1995) Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7: 43-55
17. Dalton DA (1995) Antioxidant defenses of plants and fungi. In: Ahmad S (ed.) Oxidative Stress and Antioxidant Defenses in Biology. Chapman and Hall, New York, NY, pp 298-355. ISBN 0-412-03971-0
18. Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci USA 83: 3811-3815
19. Dalton DA, Langeberg L, Robbins M (1992) Purification and characterization of monodehydroascorbate reductase from soybean root nodules. Arch Biochem Biophys 292: 281-286
20. Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WR, Vance CP, Sarath G (1993a) Subcellular localization of oxygen defense enzymes in soybean (Glycine max [L.] Merr.) root nodules. Plant Physiol 102: 481-489
21. Dalton DA, Langeberg L, Treneman N (1993b) Correlations between the ascorbate-glutathione pathway and effectiveness in legume root nodules. Physiol Plant 87: 365-370
22. Dalton DA, Joyner SL, Becana M, Iturbe-Ormaetxe I, Chatfield JM (1998) Enhanced antioxidant defenses in the peripheral cell layers of legume root nodules. Plant Physiol 116: 37-43
23. del Río LA, Sandalio LM, Corpas FJ, López-Huertas E, Palma JM, Pastori GM (1998) Activated oxygen-mediated metabolic functions of leaf peroxisomes. Physiol Plant 104: 673-680
24. Dimitrijevic L, Puppo A, Rigaud J (1984) Superoxide dismutase activities in Rhizobium phaseoli bacteria and bacteroids. Arch Microbiol 139: 174-178
25. Drolet G, Dumbroff EB, Legge RL, Thompson JE (1986) Radical scavenging properties of polyamines. Phytochemistry 25: 367-371
26. Escuredo PR, Minchin FR, Gogorcena Y, Iturbe-Ormaetxe I, Klucas RV, Becana M (1996) Involvement of activated oxygen in nitrate-induced senescence of pea root nodules. Plant Physiol 110: 1187-1195
27. Evans PJ, Gallesi D, Mathieu C, Hernández MJ, De Felipe MR, Halliwell B, Puppo A (1999) Oxidative stress occurs during soybean nodule senescence. Planta 208: 73-79
28. Francis AJ, Alexander M (1972) Catalase activity and nitrogen fixation in legume root nodules. Can J Microbiol 18: 861-864
29. 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
30. Fujihara S, Abe H, Minakawa Y, Akao S, Yoneyama T (1994) Polyamines in nodules from various plant-microbe symbiotic associations. Plant Cell Physiol 35: 1127-1134
31. Gogorcena Y, Iturbe-Ormaetxe I, Escuredo PR, Becana M (1995) Antioxidant defenses against activated oxygen in pea nodules subjected to water stress. Plant Physiol 108: 753-759
32. 2 fixation, carbon metabolism, and oxidative damage in nodules of dark-stressed common bean plants. Plant Physiol 113: 1193-1201
33. Halliwell B, Gutteridge JMC (1990) Role of free radicals and catalytic metal ions in human disease: An overview. Methods Enzymol 186: 1-85
34. Hirsch AM (1992) Developmental biology of legume nodulation. New Phytol 122: 211-237
35. Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44: 483-511
36. Ji L, Wood S, Becana M, Klucas RV (1991) Purification and characterization of soybean root nodule ferric leghemoglobin reductase. Plant Physiol 96: 32-37
37. Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114: 275-284
38. Jones DK, Dalton DA, Rosell FI, Raven EL (1998) Class I heme peroxidases: Characterization of soybean ascorbate peroxidase. Arch Biochem Biophys 360: 173-178
39. Jun HK, Sarath G, Moran JF, Becana M, Klucas RV, Wagner FW (1994) Characteristics of modified leghemoglobins isolated from soybean (Glycine max Merr.) root nodules. Plant Physiol 104: 1231-1236
40. Kaneko Y, Newcomb EH (1987) Cytochemical localization of uricase and catalase in developing root nodules of soybean. Protoplasma 140: 1-12
41. Klapheck S (1988) Homoglutathione: Isolation, quantification, and occurrence in legumes. Physiol Plant 74: 727-732
42. Klapheck S, Zopes H, Levels HG, Bergmann L (1988) Properties and localization of the homoglutathione synthetase from Phaseolus coccineus leaves. Physiol Plant 74: 733-739
43. Ko MP, Huang PY, Huang JS, Barker KR (1987) The occurrence of phytoferritin and its relationship to effectiveness of soybean nodules. Plant Physiol 83: 299-305
44. Lee KK, Shearman LL, Erickson BK, Klucas RV (1995) Ferric leghemoglobin in plant-attached leguminous nodules. Plant Physiol 109: 261-267
45. Lorenzo C, Lucas MM, Vivo A, de Felipe MR (1990) Effect of nitrate on peroxisome ultrastructure and catalase activity in nodules of Lupinus albus L. cv. Multolupa. J Exp Bot 41: 1573-1578
46. Lorenzo C, Fernández-Pascual MM, de Felipe MR (1994) Protective enzymes against active oxygen species during nitrate-induced senescence of Lupinus albus nodules. J Plant Physiol 144: 633-640
47. Lucas MM, Van de Sype G, Hérouart D, Hernández MJ, Puppo A, de Felipe MR (1998) Immunolocalization of ferritin in determinate and indeterminate legume root nodules. Protoplasma 204: 61-70
48. Lynch DV, Thompson JE (1984) Lipoxygenase-mediated production of superoxide anion in senescing plant tissue. FEBS Lett 173: 251-254
49. Macnicol PK (1987) Homoglutathione and glutathione synthetases of legume seedlings: Partial purification and substrate specificity. Plant Sci 53: 229-235
50. Martinez-Abarca F, Herrera-Cervera JA, Bueno P, Sanjuan J, Bisseling T, Olivares J (1998) Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol Plant Microbe Interact 11: 153-155
51. Matamoros MA, Baird LM, Escuredo PR, Dalton DA, Minchin FR, Iturbe-Ormaetxe I, Rubio MC, Moran JF, Gordon AJ, Becana M (1999a) Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol 121: 97-111
52. Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999b) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121: 879-888
53. Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biol Biochem 29: 881-888
54. Misra HP, Fridovich I (1971) The generation of superoxide radical during the autoxidation of ferredoxins. J Biol Chem 246: 6886-6890
55. Moran JF, Klucas RV, Grayer RJ, Abian J, Becana M (1997) Complexes of iron with phenolic compounds from soybean nodules and other legume tissues: Prooxidant and antioxidant properties. Free Radic Biol Med 22: 861-870
56. 2: Formation of heme-protein cross-links and dimeric species. Biochim Biophys Acta 1251: 17-22
57. Moreau S, Puppo A, Davies MJ (1995b) The reactivity of ascorbate with different redox states of leghaemoglobin. Phytochemistry 39: 1281-1286
58. Mullineaux PM, Karpinski S, Jiménez A, Cleary SP, Robinson C, Creissen GP (1998) Identification of cDNAs encoding plastid-targeted glutathione peroxidase. Plant J 13: 375-379
59. Noctor G, Foyer CH (1998) Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279
60. Pathirana MS, Samac DA, Roeven R, Yoshioka H, Vance CP, Gantt JS (1997) Analyses of phosphoenolpyruvate carboxylase gene structure and expression in alfalfa nodules. Plant J 12: 293-304
61. Puppo A, Halliwell B (1988) Generation of hydroxyl radicals by soybean nodule leghaemoglobin. Planta 173: 405-410
62. Puppo A, Dimitrijevic L, Rigaud J (1982) Possible involvement of nodule superoxide dismutase and catalase in leghemoglobin protection. Planta 156: 374-379
63. Puppo A, Dimitrijevic L, Trinchant JC, Rigaud J (1986) Acetylene reduction and superoxide dismutase activities in Sesbania rostrata root and stem nodules. Physiol Vég 24: 689-696
64. 2 consumption and superoxide dismutase content in purified mitochondria from soybean root nodules. Plant Sci 50: 3-11
65. Ragland M, Theil EC (1993) Ferritin (mRNA, protein) and iron concentrations during soybean nodule development. Plant Mol Biol 21: 555-560
66. Robinson DL, Pathirana SM, Gantt JS, Vance CP (1996) Immunogold localization of nodule-enhanced phosphoenolpyruvate carboxylase in alfalfa. Plant Cell Environ 19: 602-608
67. Robson RL, Postgate JR (1980) Oxygen and hydrogen in biological nitrogen fixation. Annu Rev Microbiol 34: 183-207
68. Ross EJH, Kramer SB, Dalton DA (1999) Effectiveness of ascorbate and ascorbate peroxidase in promoting nitrogen fixation in model systems. Phytochemistry 52: 1203-1210
69. Santos R, Bocquet S, Puppo A, Touati D (1999) Characterization of an atypical superoxide dismutase from Sinorhizobium meliloti. J Bacteriol 181: 4509-4516
70. Scandalios JG, Guan L, Polidoros AN (1997) Catalases in plants: Gene structure, properties, regulation, and expression. In: Scandalios JG (ed) Oxidative Stress and the Molecular Biology of Antioxidant Defenses. Cold Spring Harbor, New York, NY, pp 343-406. ISBN 0-87969-502-1
71. Schneider K, Schlegel HG (1981) Production of superoxide radicals by soluble hydrogenase from Alcaligenes eutrophus H16. Biochem J 193: 99-107
72. Sigaud S, Becquet V, Frendo P, Puppo A, Hérouart D (1999) Differential regulation of two divergent Sinorhizobium meliloti genes for HPII-like catalases during free-living growth and protective role of both catalases during symbiosis. J Bacteriol 181: 2634-2639
73. Sprent JI (1980) Root nodule anatomy, type of export product and evolutionary origin in some Leguminosae. Plant Cell Environ 3: 35-43
74. Stowers MD, Elkan GH (1981) An inducible iron-containing superoxide dismutase in Rhizobium japonicum. Can J Microbiol 27: 1202-1208
75. Swaraj K, Dhandi S, Sheokand S (1995) Relationship between defense mechanism against activated oxygen species and nodule functioning with progress in plant and nodule development in Cajanus cajan L. Millsp. Plant Sci 112: 65-74
76. Tsang EWT, Bowler C, Hérouart D, Van Camp W, Villarroel R, Genetello C, Van Montagu M, Inzé D (1991) Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell 3: 783-792
77. VandenBosch KA, Newcomb EH (1986) Immunogold localization of nodule-specific uricase in developing soybean root nodules. Planta 167: 425-436
78. Wisniewski JP, Gardner CD, Brewin NJ (1999) Isolation of lipoxygenase cDNA clones from pea nodule mRNA. Plant Mol Biol 39: 775-783