Redox changes during the legume-rhizobium symbiosis

Molecular Plant

Volumn 2, Issue 3, 2009, Pages 370-377

  Chang, Christine ^a   Damiani, Isabelle ^a   Puppo, Alain ^a   Frendo, Pierre ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Cell differentiation specialization; Gene regulation; Legume; Oxidative and photo oxidative stress; Symbiosis

Indexed keywords

RHIZOBIACEAE; RHIZOBIUM;

ANTIOXIDANT; HYDROGEN PEROXIDE; OXYGEN; REACTIVE OXYGEN METABOLITE; SCAVENGER;

AEROBIC METABOLISM; APOPTOSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; LEGUME; METABOLISM; NITROGEN FIXATION; OSMOTIC PRESSURE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

AEROBIOSIS; ANTIOXIDANTS; APOPTOSIS; FABACEAE; FREE RADICAL SCAVENGERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYDROGEN PEROXIDE; NITROGEN FIXATION; OSMOTIC PRESSURE; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN; PHOTOSYNTHESIS; PLANT DISEASES; REACTIVE OXYGEN SPECIES; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 75749131324     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssn090     Document Type: Review

References (85)

1. Albus, U., Baier, R., Holst, O., Pühler, A., and Niehaus, K. (2001). Suppression of an elicitor-induced oxidative burst reaction in Medicago sativa cell cultures by Sinorhizobium meliloti lipopolysaccharides. New Phytologist. 151, 597-606.
2. Alesandrini, F., Mathis, R., Sype, G. V. d, Hérouart, D., and Puppo, A. (2003). Possible roles for a cysteine protease and hydrogen peroxide in soybean nodule development and senescence. New Phytologist. 158, 131-138.
3. Alkhalfioui, F., Renard, M., Frendo, P., Keichinger, C., Meyer, Y., Gelhaye, E., Hirasawa, M., Knaff, D. B., Ritzenthaler, C., and Montrichard, F. (2008). A novel type of thioredoxin dedicated to symbiosis in legumes. Plant Physiol. 148, 424-435.
4. Ampe, F., Kiss, E., Sabourdy, F., and Batut, J. (2003). Transcriptome analysis of Sinorhizobium meliloti during symbiosis. Genome Biol. 4, R15.
5. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399.
6. Aydi, S., Drevon, J. J., and Abdelly, C. (2004). Effect of salinity on root-nodule conductance to the oxygen diffusion in the Medicago truncatula-Sinorhizobium meliloti symbiosis. Plant Physiol. Biochem. 42, 833-840.
7. Baier, M. C., Barsch, A., Kuster, H., and Hohnjec, N. (2007). Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol. 145, 1600-1618.
8. Becana, M., and Klucas, R. V. (1992). Transition metals in legume root nodules. Iron dependant free radical production increases during nodule senescence. Proc. Natl Acad. Sci. U S A. 87, 7295-7299.
9. Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K. S., Terskikh, A. V., and Lukyanov, S. (2006). Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods. 3, 281-286.
10. Beveridge, C. A., Mathesius, U., Rose, R. J., and Gresshoff, P. M. (2007). Common regulatory themes in meristem development and whole-plant homeostasis. Curr. Opin. Plant Biol. 10, 44-51.
11. Brewin, N. J. (2004). Plant cell wall remodelling in the rhizobium-legume symbiosis. Critical Reviews in Plant Sciences. 23, 293-316.
12. Bueno, P., Soto, M. J., Rodriguez-Rosales, M. P., Sanjuan, J., Olivares, J., and Donaire, J. P. (2001). Time-course of lipoxygenase, antioxidant enzyme activities and H2O2 accumulation during early stages of Rhizobium legume symbiosis. New Phytol. 152, 91-96.
13. Cardenas, L., Martinez, A., Sanchez, F., and Quinto, C. (2008). Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant J. 27, in press.
14. Carol, R. J., and Dolan, L. (2006). The role of reactive oxygen species in cell growth: lessons from root hairs. J. Exp. Bot. 57, 1829-1834.
15. Castro-Sowinski, S., Matan, O., Bonafede, P., and Okon, Y. (2007). A thioredoxin of Sinorhizobium meliloti CE52G is required for melanin production and symbiotic nitrogen fixation. Mol. Plant Microbe Interact. 20, 986-993.
16. Colebatch, G., Desbrosses, G., Ott, T., Krusell, L., Montanari, O., Kloska, S., Kopka, J., and Udvardi, M. K. (2004). Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39, 487-512.
17. Cook, D., Dreyer, D., Bonnet, D., Howell, M., Nony, E., and Vandenbosh, K. (1995). Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell. 7, 43-55.
18. Covarrubias, L., Hernandez-Garcia, D., Schnabel, D., Salas-Vidal, E., and Castro-Obregon, S. (2008). Function of reactive oxygen species during animal development: passive or active? Dev. Biol. 320, 1-11.
19. Dalton, D. A., Hanus, F. J., Russell, S. A., and Evans, H. J. (1987). Purification, properties, and distribution of ascorbate peroxidase in legume root nodules. Plant Physiol. 83, 789-794.
20. Dalton, D. A., Joyner, S. L., Becana, M., Iturbe-Ormaetxe, I., and Chatfield, J. M. (1998). Antioxidant defenses in the peripheral cell layers of legume root nodules. Plant Physiol. 116, 37-43.
21. Dalton, D. A., Langeberg, L., and Treneman, N. C. (1993). Correlations between the ascorbate-glutathione pathway and effectiveness in legume root nodules. Physiol. Plant. 84, 365-370.
22. Dalton, D. A., Post, C. J., and Langeberg, L. (1991). Effects of ambient oxygen and of fixed nitrogen on concentrations of glutathione, ascorbate, and associated enzymes in soybean root nodules. Plant Physiol. 96, 812-818.
23. Davies, B. W., and Walker, G. C. (2007). Identification of novel Sinorhizobium meliloti mutants compromised for oxidative stress protection and symbiosis. J. Bacteriol. 189, 2110-2113.
24. Del Castillo, L. D., Hunt, S., and Layzell, D. B. (1994). The role of oxygen in the regulation of nitrogenase activity in droughtstressed soybean nodules. Plant Physiol. 106, 949-955.
25. Den Herder, J., Lievens, S., Rombauts, S., Holsters, M., and Goormachtig, S. (2007). A symbiotic plant peroxidase involved in bacterial invasion of the tropical legume Sesbania rostrata. Plant Physiol. 144, 717-727.
26. Dénarié, J., and Cullimore, J. (1993) Lipo-oligosaccharide nodulation factors: a new class of signalling molecules mediating recognition and morphogenesis Cell. 74: 951-954.
27. D'Haeze, W., De Rycke, R., Mathis, R., Goormachtig, S., Pagnotta, S., Verplancke, C., Capoen, W., and Holsters, M. (2003). Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Proc. Natl Acad. Sci. U S A. 100, 11789-11794.
28. Dombrecht, B., Heusdens, C., Beullens, S., Verreth, C., Mulkers, E., Proost, P., Vanderleyden, J., and Michiels, J. (2005). Defence of Rhizobiumetli bacteroids against oxidative stress involves a complexly regulated atypical 2-Cys peroxiredoxin. Mol. Microbiol. 55, 1207-1221.
29. Downie, J. A. (2005). Legume haemoglobins: symbiotic nitrogen fixation needs bloody nodules. Curr. Biol. 15, R196-R198.
30. Escurado, P. R., Minchin, F. R., Gogoncena, Y., Iturbe-Ormaetxe, I., Klucas, R. V., and Becana, M. (1996). Involved of activated oxygen in nitrate induced senescence of pea root nodules. Plant Physiol. 110, 1187-1195.
31. Evans, P. J., Gallesi, D., Mathieu, C., Hernandez, M. J., de Felipe, M., Halliwell, B., and Puppo, A. (1999). Oxidative stress occurs during soybean nodule senescence. Planta. 208, 73-79.
32. Fischer, H. M. (1994). Genetic regulation of nitrogen fixation in rhizobia. Microbiol. Rev. 58, 352-386.
33. Frendo, P., Harrison, J., Norman, C., Hernandez Jimenez, M. J., Van de Sype, G., Gilabert, A., and Puppo, A. (2005). Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Mol. Plant Microbe Interact. 18, 254-259.
34. Galvez, L., Gonzalez, E. M., and Arrese-Igor, C. (2005). Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J. Exp. Bot. 56, 2551-2561.
35. Gechev, T. S., Van Breusegem, F., Stone, J. M., Denev, I., and Laloi, C. (2006). Reactive oxygen species as signals thatmodulate plant stress responses and programmed cell death. Bioessays. 28, 1091-1101.
36. Gogorcena, Y., Gordon, A. J., Escuredo, P. R., Minchin, F. R., Witty, J. F., Moran, J. F., and Becana, M. (1997). N2 fixation, carbon metabolism and oxidative damage in nodules of dark stressed Common Bean plants. Plant Physiol. 113, 1193-1201.
37. Goormachtig, S., Capoen, W., and Holsters, M. (2004). Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends Plant Sci. 9, 518-522.
38. Groten, K., Dutilleul, C., van Heerden, P. D., Vanacker, H., Bernard, S., Finkemeier, I., Dietz, K. J., and Foyer, C. H. (2006). Redox regulation of peroxiredoxin and proteinases by ascorbate and thiols during pea root nodule senescence. FEBS Lett. 580, 1269-1276.
39. Gunther, C., Schlereth, A., Udvardi, M., and Ott, T. (2007). Metabolism of reactive oxygen species is attenuated in leghemoglobindeficient nodules of Lotus japonicus. Mol. Plant Microbe Interact. 20, 1596-1603.
40. Harrison, J., Jamet, A., Muglia, C. I., Van de Sype, G., Aguilar, O. M., Puppo, A., and Frendo, P. (2005). Glutathione plays a fundamental role in growth and symbiotic capacity of Sinorhizobium meliloti. J. Bacteriol. 187, 168-174.
41. Ivashuta, S., Liu, J., Liu, J., Lohar, D. P., Haridas, S., Bucciarelli, B., VandenBosch, K. A., Vance, C. P., Harrison, M. J., and Gantt, J. S. (2005). RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell. 17, 2911-2921.
42. Jamet, A., Mandon, K., Puppo, A., and Herouart, D. (2007). H2O2 is required for optimal establishment of the Medicago sativa/Sinorhizobium meliloti symbiosis. J. Bacteriol. 189, 8741-8745.
43. Jamet, A., Sigaud, S., Van de Sype, G., Puppo, A., and Herouart, D. (2003). Expression of the bacterial catalase genes during Sinorhizobium meliloti-Medicago sativa symbiosis and their crucial role during the infection process. Mol. Plant Microbe Interact. 16, 217-225.
44. Jebara, S., Jebara, M., Limam, F., and Aouani, M. E. (2005). Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J. Plant Physiol. 162, 929-936.
45. Jones, K. M., Kobayashi, H., Davies, B. W., Taga, M. E., and Walker, G. C. (2007). How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5, 619-633.
46. Jones, K. M., Sharopova, N., Lohar, D. P., Zhang, J. Q., VandenBosch, K. A., and Walker, G. C. (2008). Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide- deficient mutant. Proc. Natl Acad. Sci. U S A. 105, 704-709.
47. Lee, M. Y., et al. (2005). Induction of thioredoxin is required for nodule development to reduce reactive oxygen species levels in soybean roots. Plant Physiol. 139, 1881-1889.
48. Loferer, H., Bott, M., and Hennecke, H. (1993). Bradyrhizobium japonicum TlpA, a novel membrane-anchored thioredoxin-like protein involved in the biogenesis of cytochrome aa3 and development of symbiosis. EMBO J. 12, 3373-3383.
49. Lohar, D. P., Haridas, S., Gantt, J. S., and Vandenbosch, K. A. (2007). A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New Phytol. 173, 39-49.
50. Lopez, M., Herrera-Cervera, J. A., Iribarne, C., Tejera, N. A., and Lluch, C. (2008). Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. J. Plant Physiol. 165, 641-650.
51. Loscos, J., Matamoros, M. A., and Becana, M. (2008). Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant. Physiol. 146, 1282-1292.
52. Marino, D., Gonzalez, E. M., and Arrese-Igor, C. (2006). Drought effects on carbon and nitrogen metabolism of pea nodules can be mimicked by paraquat: evidence for the occurrence of two regulation pathways under oxidative stresses. J. Exp. Bot. 57, 665-673.
53. Marino, D., Hohnjec, N., Kuster, H., Moran, J. F., Gonzalez, E. M., and Arrese-Igor, C. (2008). Evidence for transcriptional and posttranslational regulation of sucrose synthase in pea nodules by the cellular redox state. Mol. Plant Microbe Interact. 21, 622-630.
54. Matamoros, M. A., Baird, L. M., Escuredo, P. R., Dalton, D. A., Minchin, F. R., Iturbe-Ormaetxe, I., Rubio, M. C., Moran, J. F., Gordon, A. J., and Becana, M. (1999a). Stress induced legume root nodule senescence. Physiological, biochemical and structural alterations. Plant Physiol. 121, 97-112.
55. Matamoros, M. A., Moran, J. F., Iturbe-Ormaetxe, I., Rubio, M. C., and Becana, M. (1999b). Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol. 121, 879-888.
56. Mathieu, C., Moreau, S., Frendo, P., Puppo, A., and Davies, M. J. (1998). Direct detection of radicals in intact soybean nodules: presence of nitric oxide leghemoglobin complexes. Free Rad. Bio. Med. 24, 1242-1249.
57. Meyer, A. J., Brach, T., Marty, L., Kreye, S., Rouhier, N., Jacquot, J. P., and Hell, R. (2007). Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J. 52, 973-986.
58. Moller, I. M., Jensen, P. E., and Hansson, A. (2007). Oxidative modifications to cellular components in plants. Annu. Rev. Plant. Biol. 58, 459-481.
59. Moran, J. F., Becana, M., Iturbe-Ormaetxe, I., Frechilla, S., Klucas, R. V., and Aparicio-Tejo, P. (1994). Drought induces oxidative stress in pea plants. Planta. 194, 346-352.
60. Muglia, C., Comai, G., Spegazzini, E., Riccillo, P. M., and Aguilar, O. M. (2008). Glutathione produced by Rhizobium tropici is important to prevent early senescence in common bean nodules. FEMS Microbiol. Lett. 23, in press.
61. Noctor, G., De Paepe, R., and Foyer, C. H. (2007). Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 12, 125-134.
62. Nott, A., Jung, H. S., Koussevitzky, S., and Chory, J. (2006). Plastidto-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57, 739-759.
63. Oldroyd, G. E., and Downie, J. A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546.
64. Ott, T., van Dongen, J. T., Gunther, C., Krusell, L., Desbrosses, G., Vigeolas, H., Bock, V., Czechowski, T., Geigenberger, P., and Udvardi, M. K. (2005). Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr. Biol. 15, 531-535.
65. Overmyer, K., Brosche, M., and Kangasjarvi, J. (2003). Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 8, 335-342.
66. Pasternak, M., Lim, B., Wirtz, M., Hell, R., Cobbett, C. S., and Meyer, A. J. (2008). Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J. 53, 999-1012.
67. Peck, M. C., Fisher, R. F., and Long, S. R. (2006). Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J. Bacteriol. 188, 5417-5427.
68. Peleg-Grossman, S., Volpin, H., and Levine, A. (2007). Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. J. Exp. Bot. 58, 1637-1649.
69. Pitzschke, A., Forzani, C., and Hirt, H. (2006). Reactive oxygen species signaling in plants. Antioxid. Redox Signal. 8, 1757-1764.
70. Puppo, A., Groten, K., Bastian, F., Carzaniga, R., Soussi, M., Lucas, M. M., de Felipe, M. R., Harrison, J., Vanacker, H., and Foyer, C. H. (2005). Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol. 165, 683-701.
71. Puppo, A., Herrada, G., and Rigaud, J. (1991). Lipid peroxidation in peribacteroid membranes from French-bean nodules. Plant Physiol. 96, 826-830.
72. Puppo, A., Rigaud, J., and Job, D. (1981). Role of superoxide anion in leghemoglobin autoxidation. Plant Science Let. 22, 353-360.
73. Ramu, S. K., Peng, H. M., and Cook, D. R. (2002). Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Mol. Plant Microbe Interact. 15, 522-528.
74. Rivero, R. M., Kojima, M., Gepstein, A., Sakakibara, H., Mittler, R., Gepstein, S., and Blumwald, E. (2007). Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl Acad. Sci. U S A. 104, 19631-19636.
75. Rubio, M. C., James, E. K., Clemente, M. R., Bucciarelli, B., Fedorova, M., Vance, C. P., and Becana, M. (2004). Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Mol. Plant Microbe Interact. 17, 1294-1305.
76. Santos, R., Herouart, D., Sigaud, S., Touati, D., and Puppo, A. (2001). Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol. Plant Microbe Interact. 14, 86-89.
77. Serraj, R., Roy, G., and Drevon, J. J. (1994). Salt stress induces a decrease in the oxygen uptake of soybean nodules and in their permeability to oxygen diffusion. Physiologia Plantarum. 91, 161-168.
78. Shao, H. B., Chu, L. Y., Shao, M. A., Jaleel, C. A., and Mi, H. M. (2008). Higher plant antioxidants and redox signaling under environmental stresses. C. R. Biol. 331, 433-441.
79. Shaw, S. L., and Long, S. R. (2003). Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol. 132, 2196-2204.
80. Sieberer, B. J., Timmers, A. C., and Emons, A. M. (2005). Nod factors alter the microtubule cytoskeleton in Medicago truncatula root hairs to allow root hair reorientation. Mol. Plant Microbe Interact. 18, 1195-1204.
81. Sigaud, S., Becquet, V., Frendo, P., Puppo, A., and 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.
82. Van de Velde, W., Guerra, J. C., De Keyser, A., De Rycke, R., Rombauts, S., Maunoury, N., Mergaert, P., Kondorosi, E., Holsters, M., and Goormachtig, S. (2006). Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol. 141, 711-720.
83. vanHeerden, P. D., Kiddle, G., Pellny, T. K., Mokwala, P. W., Jordaan, A., Strauss, A. J., de Beer, M., Schluter, U., Kunert, K. J., and Foyer, C. H. (2008). Roles for the regulation of respiration and the oxygen diffusion barrier in soybean in the protection of symbiotic nitrogen fixation from chilling-induced inhibition and shoots from premature senescence. Plant Physiol. 148, 316-327.
84. Vargas, C., Wu, G., Davies, A. E., and Downie, J. A. (1994). Identification of a gene encoding a thioredoxin-like product necessary for cytochrome c biosynthesis and symbiotic nitrogen fixation in Rhizobium leguminosarum. J. Bacteriol. 176, 4117-4123.
85. Wei, H., and Layzell, D. B. (2006). Adenylate-coupled ion movement: a mechanism for the control of nodule permeability to O2 diffusion. Plant Physiol. 141, 280-287.