Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism

Plant Journal

Volumn 81, Issue 5, 2015, Pages 723-735

  Sainz, Martha ^a   Calvo Begueria, Laura ^a   Pérez Rontomé, Carmen ^a   Wienkoop, Stefanie ^b   Abián, Joaquín ^c   Staudinger, Christiana ^c   Bartesaghi, Silvina ^d,e   Radi, Rafael ^d   Becana, Manuel ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF VIENNA   (Austria)

^c INST D INVESTIGACIONS B   (Spain)

^d UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^e DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

Author keywords

Glycine max; leghemoglobin; legume nodules; nitrogen dioxide; peroxynitrite; Phaseolus vulgaris; protein tyrosine nitration

Indexed keywords

AMINO ACIDS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; NITRATES; NITRIC OXIDE; NITROGEN FIXATION; NITROGEN OXIDES; PORPHYRINS; PROTEINS;

GLYCINE MAX; LEGHEMOGLOBIN; LEGUME NODULES; NITROGEN DIOXIDES; PEROXYNITRITES; PHASEOLUS VULGARIS; PROTEIN TYROSINE NITRATIONS;

NITRATION;

GLYCINE MAX; PHASEOLUS VULGARIS;

3-NITROTYROSINE; HEME; HYDROGEN PEROXIDE; LEGHEMOGLOBIN; NITRIC ACID DERIVATIVE; NITRIC OXIDE; NITRITE; NITROGEN DIOXIDE; PEROXYNITROUS ACID; TYROSINE;

ANALOGS AND DERIVATIVES; GENETICS; METABOLISM; OXIDATIVE STRESS; PHASEOLUS; PROTEIN PROCESSING; SOYBEAN;

HEME; HYDROGEN PEROXIDE; LEGHEMOGLOBIN; NITRATES; NITRIC OXIDE; NITRITES; NITROGEN DIOXIDE; OXIDATIVE STRESS; PEROXYNITROUS ACID; PHASEOLUS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SOYBEANS; TYROSINE;

EID: 84923508152     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12762     Document Type: Article

References (54)

1. Álvarez, M.N., Trujillo, M., and, Radi, R., (2002) Peroxynitrite formation from biochemical and cellular fluxes of nitric oxide and superoxide. Methods Enzymol. 359, 353-366.
2. Álvarez, C., Lozano-Juste, J., Romero, L.C., García, I., Gotor, C., and, Leõn, J., (2011) Inhibition of Arabidopsis O-acetylserine(thiol)lyase A1 by tyrosine nitration. J. Biol. Chem. 286, 578-586.
3. Appleby, C.A., and, Bergersen, F.J., (1980) Preparation and experimental use of leghaemoglobin. In Methods for Evaluating Biological Nitrogen Fixation (, Bergersen, F.J., ed.). Chichester: Wiley, pp. 315-335.
4. Arrese-Igor, C., Gordon, A.J., Minchin, F.R., and, Denison, R.F., (1998) Nitrate entry and nitrite formation in the infected region of soybean nodules. J. Exp. Bot. 49, 41-48.
5. Aviram, I., Wittenberg, B.A., and, Wittenberg, J.B., (1978) The reaction of ferrous leghemoglobin with hydrogen peroxide to form leghemoglobin (IV). J. Biol. Chem. 253, 5685-5689.
6. Balanbali, B., Kamisaki, Y., Martin, E., and, Murad, F., (1999) Requirements for heme and thiols for the nonezymatic modification of nitrotyrosine. Proc. Natl Acad. Sci. USA, 96, 13136-13141.
7. Bartesaghi, S., Trujillo, M., Denicola, A., Folkes, L., Wardman, P., and, Radi, R., (2004) Reactions of desferrioxamine with peroxynitrite-derived carbonate and nitrogen dioxide radicals. Free Radic. Biol. Med. 36, 471-483.
8. Bartesaghi, S., Valez, V., Trujillo, M., Peluffo, G., Romero, N., Zhang, H., Kalyanaraman, B., and, Radi, R., (2006) Mechanistic studies of peroxynitrite-mediated tyrosine nitration in membranes using the hydrophobic probe N-t-BOC-L-tyrosine tert-butyl ester. Biochemistry, 45, 6813-6825.
9. Becana, M., and, Klucas, R.V., (1992) Oxidation and reduction of leghemoglobin in root nodules of leguminous plants. Plant Physiol. 98, 1217-1221.
10. 2 fixation by nitrate. I. Nitrate effects on nitrate-reductase activities of bacteroids and nodule cytosol. Planta, 180, 40-45.
11. Becana, M., Matamoros, M.A., Udvardi, M., and, Dalton, D.A., (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytol. 188, 960-976.
12. Begara-Morales, J.C., Chaki, M., Sánchez-Calvo, B., Mata-Pérez, C., Leterrier, M., Palma, J.M., Barroso, J.B., and, Corpas, F.J., (2013) Protein tyrosine nitration in pea roots during development and senescence. J. Exp. Bot. 64, 1121-1134.
13. Bondoc, L.L., and, Timkovich, R., (1989) Structural characterization of nitrimyoglobin. J. Biol. Chem. 264, 6134-6145.
14. Castro, L., Eiserich, J.P., Sweeney, S., Radi, R., and, Freeman, B.A., (2004) Cytochrome c: a catalyst and target of nitrite-hydrogen peroxide-dependent protein nitration. Arch. Biochem. Biophys. 421, 99-107.
15. Cecconi, D., Orzetti, S., Vandelle, E., Rinalducci, S., Zolla, L., and, Delledonne, M., (2009) Protein nitration during defense response in Arabidopsis thaliana. Electrophoresis, 30, 2460-2468.
16. Chaki, M., Valderrama, R., Fernández-Ocaña, A.M., et al. (2011) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant, Cell Environ. 34, 1803-1818.
17. Corpas, F.J., del Río, L.A., and, Barroso, J.B., (2007) Need of biomarkers of nitrosative stress in plants. Trends Plant Sci. 12, 436-438.
18. Cueto, M., Hernández-Perera, O., Martín, R., Bentura, M.L., Rodrigo, J., Lamas, S., and, Golvano, M.P., (1996) Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Lett. 398, 159-164.
19. Egelhofer, V., Hoehenwarter, W., Lyon, D., Weckwerth, W., and, Wienkoop, S., (2013) Using ProtMAX to create high-mass-accuracy precursor alignments from label-free quantitative mass spectrometry data generated in shotgun proteomics experiments. Nat. Protoc. 8, 595-601.
20. Escuredo, P.R., Minchin, F.R., Gogorcena, Y., Iturbe-Ormaetxe, I., Klucas, R.V., and, Becana, M., (1996) Involvement of activated oxygen in nitrate-induced senescence of pea root nodules. Plant Physiol. 110, 1187-1195.
21. Evans, P.J., Gallesi, D., Mathieu, C., Hernández, M.J., de Felipe, M.R., Halliwell, B., and, Puppo, A., (1999) Oxidative stress occurs during soybean nodule senescence. Planta, 208, 73-79.
22. Fuchsman, W.H., and, Appleby, C.A., (1979) Separation and determination of the relative concentrations of the homogenous components of soybean leghemoglobin by isoelectric focusing. Biochim. Biophys. Acta, 579, 314-324.
23. Galetskiy, D., Lohscheider, J.N., Kononikhin, A.S., Popov, I.A., Nikolaev, E.N., and, Adamska, I., (2011) Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress. Plant Mol. Biol. 77, 461-473.
24. 2 fixation, carbon metabolism, and oxidative damage in nodules of dark-stressed common bean plants. Plant Physiol. 113, 1193-1201.
25. Gow, A., Duran, D., Thom, S.R., and, Ischiropoulos, H., (1996) Carbon dioxide enhancement of peroxynitrite-mediated protein tyrosine nitration. Arch. Biochem. Biophys. 333, 42-48.
26. Herold, S., (2004) Nitrotyrosine, dityrosine, and nitrotryptophan formation from metmyoglobin, hydrogen peroxide, and nitrite. Free Radic. Biol. Med. 36, 565-579.
27. Herold, S., and, Puppo, A., (2005a) Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules? J. Biol. Inorg. Chem. 10, 935-945.
28. Herold, S., and, Puppo, A., (2005b) Kinetics and mechanistic studies of the reactions of metleghemoglobin, ferrylleghemoglobin, and nitrosylleghemoglobin with reactive nitrogen species. J. Biol. Inorg. Chem. 10, 946-957.
29. Herold, S., and, Shivashankar, K., (2003) Metmyoglobin and methemoglobin catalyze the isomerization of peroxynitrite to nitrate. Biochemistry, 42, 14036-14046.
30. Jun, H.K., Sarath, G., Moran, J.F., Becana, M., Klucas, R.V., and, Wagner, F.W., (1994) Characteristics of modified leghemoglobins isolated from soybean (Glycine max Merr.) root nodules. Plant Physiol. 104, 1231-1236.
31. Kundu, S., Blouin, G.C., Premer, S.A., Sarath, G., Olson, J.S., and, Hargrove, M.S., (2004) Tyrosine B10 inhibits stabilization of bound carbon monoxide and oxygen in soybean leghemoglobin. Biochemistry, 43, 6241-6252.
32. Lee, K.K., Shearman, L., Erickson, B.K., and, Klucas, R.V., (1995) Ferric leghemoglobin in plant-attached leguminous nodules. Plant Physiol. 109, 261-267.
33. Lozano-Juste, J., Colom-Moreno, R., and, Leõn, J., (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J. Exp. Bot. 62, 3501-3517.
34. Martinez, A., Peluffo, G., Petruk, A. A., et al. (2014) Structural and molecular basis of the peroxynitrite-mediated nitration and inactivation of Trypanosoma cruzi iron-superoxide dismutases (Fe-SODs) A and B. J. Biol. Chem. 289, 12760-12778.
35. 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 Radic. Biol. Med. 24, 1242-1249.
36. Meakin, G.E., Bueno, E., Jepson, B., Bedmar, E.J., Richardson, D.J., and, Delgado, M.J., (2007) The contribution of bacteroidal nitrate and nitrite reduction to the formation of nitrosylleghaemoglobin complexes in soybean root nodules. Microbiology, 153, 411-419.
37. Melo, P.M., Silva, L.S., Ribeiro, I., Seabra, A.R., and, Carvalho, H.G., (2011) Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration. Plant Physiol. 157, 1505-1517.
38. 2: formation of heme-protein cross-links and dimeric species. Biochim. Biophys. Acta, 1251, 17-22.
39. Moreau, S., Davies, M.J., Mathieu, D., Hérouart, D., and, Puppo, A., (1996) Leghemoglobin-derived radicals. Evidence for multiple protein-derived radicals and the initiation of peribacteroid membrane damage. J. Biol. Chem. 271, 32557-32562.
40. Navascués, J., Pérez-Rontomé, C., Gay, M., Marcos, M., Yang, F., Walker, F.A., Desbois, A., Abián, J., and, Becana, M., (2012) Leghemoglobin green derivatives with nitrated hemes evidence production of highly reactive nitrogen species during aging of legume nodules. Proc. Natl Acad. Sci. USA, 109, 2660-2665.
41. Nicolis, S., Monzani, E., Roncone, R., Gianelli, L., and, Casella, L., (2004) Metmyoglobin-catalyzed exogenous and endogenous tyrosine nitration by nitrite and hydrogen peroxide. Chem. Eur. J. 10, 2281-2290.
42. Otsuka, M., Marks, S.A., Winnica, D.E., Amoscato, A.A., Pearce, L.L., and, Peterson, J., (2010) Covalent modifications of hemoglobin by nitrite anion: formation kinetics and properties of nitrihemoglobin. Chem. Res. Toxicol. 23, 1786-1795.
43. Petruk, A.A., Bartesaghi, S., Trujillo, M., Estrin, D.A., Murgida, D., Kalyanaraman, B., Marti, M.A., and, Radi, R., (2012) Molecular basis of intramolecular electron transfer in proteins during radical-mediated oxidations: computer simulation studies in model tyrosine-cysteine peptides in solution. Arch. Biochem. Biophys. 525, 82-91.
44. Pfeiffer, N.E., Torres, C.M., and, Wagner, F.W., (1983) Proteolytic activity in soybean root nodules. Activity in host cell cytosol and bacteroids throughout physiological development and senescence. Plant Physiol. 71, 797-802.
45. Pladys, D., Barthe, P., and, Rigaud, J., (1988) Changes in intracellular pH in French-bean nodules induced by senescence and nitrate treatment. Plant Sci. 56, 99-106.
46. Prasad, J.C., Goldstone, J.V., Camacho, C.J., Vajda, S., and, Stegeman, J.J., (2007) Ensemble modeling of substrate binding to cytochromes P450: analysis of catalytic differences between CYP1A orthologs. Biochemistry, 46, 2640-2654.
47. 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.
48. Radi, R., (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc. Natl Acad. Sci. USA, 101, 4003-4008.
49. Sakamoto, A., Sakurao, S.H., Fukunaga, K., Matsubara, T., Ueda-Hashimoto, M., Tsukamoto, S., Takahashi, M., and, Morikawa, H., (2004) Three distinct Arabidopsis hemoglobins exhibit peroxidase-like activity and differentially mediate nitrite-dependent protein nitration. FEBS Lett. 572, 27-32.
50. Schopfer, F.J., Baker, P.R.S., and, Freeman, B.A., (2003) NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response? Trends Biochem. Sci. 28, 646-654.
51. Söderling, A., Hultman, L., Delbro, D., Højrup, P., and, Caidahl, K., (2007) Reduction of the nitro group during sample preparation may cause underestimation of the nitration level in 3-nitrotyrosine immunoblotting. J. Chromatogr. B, 851, 277-286.
52. Tanou, G., Filippou, P., Belghazi, M., Job, D., Diamantidis, G., Fotopoulos, V., and, Molassiotis, A., (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 72, 585-599.
53. - reaction. Proc. Natl Acad. Sci. USA, 99, 12691-12696.
54. Van der Vliet, A., Eiserich, J.P., Halliwell, B., and, Cross, C.E., (1997) Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. J. Biol. Chem. 272, 7617-7625.