Crucial role of (homo)glutathione in nitrogen fixation in Medicago truncatula nodules

New Phytologist

Volumn 192, Issue 2, 2011, Pages 496-506

  El Msehli, Sarra ^a,b   Lambert, Annie ^a   Baldacci Cresp, Fabien ^a   Hopkins, Julie ^a   Boncompagni, Eric ^a   Smiti, Samira Aschi ^b   Hérouart, Didier ^a   Frendo, Pierre ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b FACULTÉ DES SCIENCES DE TUNIS   (Tunisia)

Author keywords

Biological nitrogen fixation; Glutathione; Homoglutathione; Medicago truncatula Sinorhizobium meliloti symbiosis; Nodule; NRC001 promoter

Indexed keywords

DRUG DERIVATIVE; GLUTATHIONE; GLUTATHIONE SYNTHASE; HOMOGLUTATHIONE; PHYTOHORMONE;

BACTERIUM; CORRELATION; ENZYME ACTIVITY; GENE EXPRESSION; LEGUME; NITROGEN FIXATION;

ARTICLE; BARREL MEDIC; BIOSYNTHESIS; DOWN REGULATION; DRUG ANTAGONISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; NODULATION; PHYSIOLOGY; PLANT ROOT; SINORHIZOBIUM MELILOTI; SYMBIOSIS; TRANSGENIC PLANT;

DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GLUTATHIONE; GLUTATHIONE SYNTHASE; MEDICAGO TRUNCATULA; NITROGEN FIXATION; PLANT GROWTH REGULATORS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; ROOT NODULES, PLANT; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

BACTERIA (MICROORGANISMS); MEDICAGO TRUNCATULA; RHIZOBIACEAE; SINORHIZOBIUM MELILOTI;

EID: 80053259072     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03810.x     Document Type: Article

References (57)

1. Alkhalfioui F, Renard M, Frendo P, Keichinger C, Meyer Y, Gelhaye E, Hirasawa M, Knaff DB, Ritzenthaler C, Montrichard F. 2008. A novel type of thioredoxin dedicated to symbiosis in legumes. Plant Physiology 148: 424-435.
2. Baier MC, Barsch A, Kuster H, 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 Physiology 145: 1600-1618.
3. Barker DG, Bianchi S, Blondon F, Dattée Y, Duc G, Flament P, Galusci P, Génier G, Guy P, Muel X et al. 1990. Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Molecular Biology Reporter 8: 40-49.
4. Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP. 2010. Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22: 376-391.
5. Baudouin E, Pieuchot L, Engler G, Pauly N, Puppo A. 2006. Nitric oxide is formed in Medicago truncatula-Sinorhizobium meliloti functional nodules. Molecular Plant-Microbe Interactions 19: 970-975.
6. Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC. 2000. Reactive oxygen species and antioxidants in legume nodules. Physiologia Plantarum 109: 372-381.
7. 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. Molecular Plant-Microbe Interactions 14: 695-700.
8. Chang C, Damiani I, Puppo A, Frendo P. 2009. Redox changes during the legume-rhizobium symbiosis. Molecular Plant 2: 370-377.
9. Cook DR, VandenBosch K, de Bruinj FJ, Huguet T. 1997. Model legumes get the nod. Plant Cell 9: 275-280.
10. Dalton DA, Joyner SL, Becana M, Iturbe-Ormaetxe I, Chatfield JM. 1998. Antioxidant defenses in the peripheral cell layers of legume root nodules. Plant Physiology 116: 37-43.
11. Dalton DA, Langeberg L, Treneman NC. 1993. Correlations between the ascorbate-glutathione pathway and effectiveness in legume root nodules. Physiologia Plantarum 84: 365-370.
12. Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evan HJ. 1986. Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proceedings of the National Academy of Sciences, USA 83: 3811-3815.
13. Evans PJ, Gallesi D, Mathieu C, Hernandez MJ, de Felipe M, Halliwell B, Puppo A. 1999. Oxidative stress occurs during soybean nodule senescence. Planta 208: 73-79.
14. Fahey RC, Newton GL. 1987. Determination of low-molecular-weight thiols using monobromobimane fluorescent labeling and high-performence liquid chromatography. In: Jakoby WB, Griffith OW, eds. Methods in Enzymology. San Diego, USA: Academic Press, 85-96.
15. Foyer CH, Noctor G. 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants & Redox Signaling 11: 861-905.
16. Frendo P, Gallesi D, Turnbullet 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 Journal 17: 215-219.
17. Frendo P, Harrison J, Norman C, Hernandez Jimenez MJ, Van de Sype G, Gilabert A, Puppo A. 2005. Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Molecular Plant-Microbe Interactions 18: 254-259.
18. Frendo P, Jimenez MJ, Mathieu C, Duret L, Gallesi D, Van de Sype G, Herouart D, Puppo A. 2001. A Medicago truncatula homoglutathione synthetase is derived from glutathione synthetase by gene duplication. Plant Physiology 126: 1706-1715.
19. 2 fixation, carbon metabolism and oxidative damage in nodules of dark stressed Common Bean plants. Plant Physiology 113: 1193-1201.
20. Gogorcena Y, Iturbe-Ormaetxe I, Escuredo PR, Becana M. 1995. Antioxidant defenses against activated oxygen in pea nodules subjected to water stress. Plant Physiology 108: 753-759.
21. Groten K, Dutilleul C, van Heerden PD, Vanacker H, Bernard S, Finkemeier I, Dietz KJ, Foyer CH. 2006. Redox regulation of peroxiredoxin and proteinases by ascorbate and thiols during pea root nodule senescence. FEBS Letters 580: 1269-1276.
22. Groten K, Vanacker H, Dutilleul C, Bastian F, Bernard S, Carzaniga R, Foyer CH. 2005. The roles of redox processes in pea nodule development and senescence. Plant, Cell & Environment 28: 1293-1304.
23. Gutierrez-Alcala G, Gotor C, Meyer AJ, Fricker M, Vega JM, Romero LC. 2000. Glutathione biosynthesis in Arabidopsis trichome cells. Proceedings of the National Academy of Sciences, USA 97: 11108-11113.
24. Hardy RW, Holsten RD, Jackson EK, Burns RC. 1968. The acetylene-ethylene assay for n(2) fixation: laboratory and field evaluation. Plant Physiology 43: 1185-1207.
25. Harrison J, Jamet A, Muglia CI, Van de Sype G, Aguilar OM, Puppo A, Frendo P. 2005. Glutathione plays a fundamental role in growth and symbiotic capacity of Sinorhizobium meliloti. Journal of Bacteriology 187: 168-174.
26. Harrison J, Puppo A, Frendo P. 2003. The synthesis and the roles of glutathione and homoglutathione in legumes. Advances in Plant Physiology 6: 385-412.
27. Hemerly AS, Ferreira P, de Almeida Engler J, Van Montagu M, Engler G, Inze D. 1993. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 1711-1723.
28. Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P. 2007. Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225: 1597-1602.
29. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC. 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nature Reviews. Microbiology 5: 619-633.
30. Karimi M, Inze D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7: 193-195.
31. Kokotek W, Lotz W. 1989. Construction of a lacZ-kanamycin-resistance cassette, useful for site-directed mutagenesis and as a promoter probe. Gene 84: 467-471.
32. Koprivova A, Mugford ST, Kopriva S. 2010. Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Reports 29: 1157-1167.
33. Kotting O, Kossmann J, Zeeman SC, Lloyd JR. 2010. Regulation of starch metabolism: the age of enlightenment? Current Opinion in Plant Biology 13: 321-329.
34. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
35. Lopez M, Herrera-Cervera JA, Iribarne C, Tejera NA, Lluch C. 2008. Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. Journal of Plant Physiology 165: 641-650.
36. Marino D, Gonzalez EM, 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. Journal of Experimental Botany 57: 665-673.
37. Marino D, Hohnjec N, Kuster H, Moran JF, Gonzalez EM, Arrese-Igor C. 2008. Evidence for transcriptional and post-translational regulation of sucrose synthase in pea nodules by the cellular redox state. Molecular Plant-Microbe Interactions 21: 622-630.
38. Marino D, Pucciariello C, Puppo A, Frendo P. 2009. The redox state, a referee of the legume-rhizobia symbiotic game. Advances in Botanical Research: Oxidative Stress and Redox Regulation in Plants 52: 115-151.
39. Masson-Boivin C, Giraud E, Perret X, Batut J. 2009. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends in Microbiology 17: 458-466.
40. Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M. 2003. Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiology 133: 499-509.
41. Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M. 1999. Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiology 121: 879-888.
42. Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A, Kondorosi E. 2003. A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiology 132: 161-173.
43. Meyer Y, Buchanan BB, Vignols F, Reichheld JP. 2009. Thioredoxins and glutaredoxins: unifying elements in redox biology. Annual Review of Genetics 43: 335-367.
44. Mitra RM, Long SR. 2004. Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula/Sinorhizobium meliloti symbiosis. Plant Physiology 134: 595-604.
45. Oldroyd GE, Downie JA. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology 59: 519-546.
46. Ott T, Sullivan J, James EK, Flemetakis E, Gunther C, Gibon Y, Ronson C, Udvardi M. 2009. Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules. Molecular Plant-Microbe Interactions 22: 800-808.
47. Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK. 2005. Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Current Biology 15: 531-535.
48. Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH. 2005. Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytologist 165: 683-701.
49. Quandt H-J, Pühler A, Broer I. 1993. Transgenic root nodules of Vicia hirsuta: a fast and efficient system for the study of gene expression in indeterminate-type nodules. Molecular Plant-Microbe Interactions 6: 699-706.
50. Redondo FJ, de la Pena TC, Morcillo CN, Lucas MM, Pueyo JJ. 2009. Overexpression of flavodoxin in bacteroids induces changes in antioxidant metabolism leading to delayed senescence and starch accumulation in alfalfa root nodules. Plant Physiology 149: 1166-1178.
51. Rigaud J, Puppo A. 1975. Indole-3-acetic acid catabolism by soybean bacteroids. Journal of General Microbiology 88: 223-228.
52. Rouhier N, Lemaire SD, Jacquot JP. 2008. The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annual Review of Plant Biology 59: 143-166.
53. Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inzé D, May MJ. 1997. Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proceedings of the National Academy of Sciences, USA 94: 2745-2750.
54. Van de Velde W, Guerra JC, De Keyser A, De Rycke R, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S. 2006. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiology 141: 711-720.
55. Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H et al. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327: 1122-1126.
56. Vieweg MF, Hohnjec N, Kuster H. 2005. Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220: 757-766.
57. Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath G, Kelemen Z, Tarayre S, Roudier F, Mergaert P, Kondorosi A et al. 2003. Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15: 2093-2105.