Nitric oxide inhibits succinate dehydrogenase-driven oxygen consumption in potato tuber mitochondria in an oxygen tension-independent manner

Biochemical Journal

Volumn 449, Issue 1, 2013, Pages 263-273

  Simonin, Vagner ^a   Galina, Antonio ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Heterotrophic plant tissue; Mitochondrion; Nitric oxide; Succinate dehydrogenase

Indexed keywords

ADENOSINE DIPHOSPHATE; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; THENOYLTRIFLUOROACETONE; UBIQUINONE;

ARTICLE; ELECTRON; KINETICS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN TENSION; POTATO; PRIORITY JOURNAL;

ANIMALS; BRAIN CHEMISTRY; MICE; MITOCHONDRIA; MITOCHONDRIA, LIVER; NITRIC OXIDE; NITRIC OXIDE DONORS; OXYGEN; OXYGEN CONSUMPTION; SOLANUM TUBEROSUM; SUBMITOCHONDRIAL PARTICLES; SUCCINATE DEHYDROGENASE;

MAMMALIA; SOLANUM TUBEROSUM;

EID: 84870946958     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120396     Document Type: Article

References (50)

1. Neill, S. J., Desikan, R., Clarke, A. and Hancock, J. T. (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128, 13-16 (Pubitemid 34115307)
2. Correa-Aragunde, N., Graziano, M., Chevalier, C. and Lamattina, L. (2005) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J. Exp. Bot. 57, 581-588
3. Tewari, R. K., Kim, S., Hahn, E. J. and Paek, K. Y. (2008) Involvement of nitric oxide-induced NADPH oxidase in adventitious root growth and antioxidant defense in Panax ginseng. Plant Biotechnol. Rep. 2, 113-122 (Pubitemid 351814526)
4. Lombardo, M. C., Graziano, M., Polacco, J. C. and Lamattina, L. (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signaling Behav. 1, 28-33
5. Arasimowicz, M. and Floryszak-Wieczorek, J. (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci. 172, 876-887 (Pubitemid 46517737)
6. Davis, K. L., Martin, E., Turko, I. V. and Murad, F. (2001) Novel effects of nitric oxide. Annu. Rev. Pharmacol. Toxicol. 41, 203-236 (Pubitemid 32385888)
7. Schmidt, H. H. W. and Walter, U. (1994) NO at work. Cell 78, 919-925
8. Lindermayr, C., Saalbach, G. and Durner, J. (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 137, 921-930 (Pubitemid 43138164)
9. Besson-Bard, A., Pugin, A. and Wendehenne, D. (2008) New insights into nitric oxide signaling in plants. Annu. Rev. Plant Biol. 59, 21-39 (Pubitemid 351813022)
10. Stamler, J. S., Lamas, S. and Fang, F. C. (2001) Nitrosylation. The prototypic redox-based signaling mechanism. Cell 106, 675-683 (Pubitemid 32900659)
11. Wang, D., Qian, L., Xiong, H., Liu, J., Neckameyer, W. S., Oldham, S., Xia, K., Wang, J., Bodmer, R. and Zhang, Z. (2006) Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila . Proc. Natl. Acad. Sci. U.S.A. 103, 13520-13525 (Pubitemid 44380140)
12. Summers, J. E., Ratcliffe, R. G. and Jackson, M. B. (2000) Anoxia tolerance in the aquatic monocot Potamogetonpectinatus absence of oxygen stimulates elongation in association with an unusually large pasteur effect. J. Exp. Bot. 51, 1413-1422 (Pubitemid 30627057)
13. Cleeter, M. W., Cooper, J. M., Darley-Usmar, V. M., Moncada, S. and Schapira, A. H. (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide: implications for neurodegenerative diseases. FEBS Lett. 345, 50-54 (Pubitemid 24154664)
14. Blokhina, O. and Fagerstedt, K. V. (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol. Plant. 138, 447-462
15. Dordas, C., Hasinoff, B. B., Igamberdiev, A. U., Manac'h, N., Rivoal, J. and Hill, R. D. (2003) Expression of a stress-induced haemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J. 35, 763-770 (Pubitemid 37143723)
16. Perazzolli, M., Romero-Puertas, M. C. and Delledonne, M. (2006) Modulation of nitric oxide bioactivity by plant haemoglobins. J. Exp. Bot. 57, 479-488 (Pubitemid 43164379)
17. Zhang, Y., Liu, J., Mu, Y., Pei, S., Lun, X. and Chai, F. (2012) Emissions of nitrous oxide, nitrogen oxides and ammonia from a maize field in the North China Plain. J. Environ. Sci. 45, 2956-2961
18. Borisjuk, L. and Rolletschek, H. (2008) Nitric oxide is a versatile sensor of low oxygen stress in plants. Plant Signaling Behav. 3, 391-393 (Pubitemid 351774820)
19. Stoimenova, M., Igamberdiev, A. U., Gupta, K. J. and Hill, R. D. (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226, 465-474 (Pubitemid 46889524)
20. Welter, R., Yu, L. and Yu, C. A. (1996) The effects of nitric oxide on electron transport complexes. Arch. Biochem. Biophys. 331, 9-14 (Pubitemid 26230613)
21. Palmieri, M. C., Lindermayr, C., Bauwe, H., Steinhauser, C. and Durner, J. (2010) Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol. 152, 1514-1528
22. Piantadosi, C. A. (2011) Regulation of mitochondrial processes by protein S-nitrosylation. Biochim. Biophys. Acta 1820, 712-721
23. Papèe, H. M. and Petriconi, G. L. (1964) Formation and decomposition of alkaline 'pernitrite'. Nature 204, 142-144
24. Brown, G. C. and Cooper, C. E. (1994) Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 356, 295-298 (Pubitemid 24376992)
25. Neuburger, M., Journet, E. P., Bligny, R., Carde, J. P. and Douce, R. (1982) Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch. Biochem. Biophys. 217, 312-323
26. Robinson, K. M. and Lemire, B. D. (1995) Flavinylation of succinate: ubiquinone oxidoreductase from Saccharomyces cerevisiae. Methods Enzymol. 260, 34-51
27. Somlo, M. (1965) Induction of lactate-cytochrome c reductases (D- and L-) of aerobic yeast by lactates (D- and L-). Biochim. Biophys. Acta 15, 183-201
28. Kunz, W. S. and Gellerich, F. N. (1993) Quantification of the content of fluorescent flavoproteins in mitochondria from liver, kidney cortex, skeletal muscle, and brain. Biochem. Med. Metab. Biol. 50, 103-110 (Pubitemid 23228530)
29. Tiessen, A., Hendriks, J. H., Stitt, M., Branscheid, A., Gibon, Y., Farré, E. M. and Geigenberger, P. (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14, 2191-2213
30. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
31. Poderoso, J. J. (2009) The formation of peroxynitrite in the applied physiology of mitochondrial nitric oxide. Arch. Biochem. Biophys. 484, 214-20
32. Wulff, A., Oliveira, H. C., Saviani, E. E. and Salgado, I. (2009) Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric Oxide 21, 132-139
33. Aguirre, E., Rodríguez-Juárez, F., Bellelli, A., Gnaiger, E. and Cadenas, S. (2010) Kinetic model of the inhibition of respiration by endogenous nitric oxide in intact cells. Biochim. Biophys. Acta. 1797, 557-565
34. Oestreiche, G., Hogue, P. and Singer, T. P. (1973) Regulation of succinate dehydrogenase in higher plants II. Activation by substrates, reduced coenzyme Q, nucleotides, and anions. Plant Physiol. 52, 622-626
35. Singer, T. P., Oestreicher, G. and Hogue, P. (1973) Regulation of succinate dehydrogenase in higher plants I. Some general characteristics of the membrane-bound enzyme. Plant Physiol. 52, 616-621
36. Affourtit, C., Krab, K., Leach, G. R., Whitehouse, D. G. and Moore, A. L. (2001) New insights into the regulation of plant succinate dehydrogenase. On the role of the protonmotive force. J. Biol. Chem. 276, 32567-32574
37. Gabrielson, K. L., Hogue, B. A., Bohr, V. A., Cardounel, A. J., Nakajima, W., Kofler, J., Zweier, J. L., Rodriguez, E. R., Martin, L. J., de Souza-Pinto, N. C. and Bressler, J. (2001) Mitochondrial toxin 3-nitropropionic acid induces cardiac and neurotoxicity differentially in mice. Am. J. Pathol. 159, 1507-1520 (Pubitemid 32947979)
38. Nelson, B. D., Norling, B., Persson, B. and Ernster, L. (1971) Effect of thenoyltrifluoroacetone on the interaction of succinate dehydrogenase and cytochrome b in ubiquinone-depleted submitochondrial particles. Biochem. Biophys. Res. Commun. 44, 1312-1320
39. Morales, J., Mogi, T., Mineki, S., Takashima, E., Mineki, R., Hirawake, H., Sakamoto, K., Omura, S. and Kita, K. (2009) Novel mitochondrial complex II isolated from Trypanosoma cruzi is composed of 12 peptides including a heterodimeric Ip subunit. J. Biol. Chem. 284, 7255-7263
40. Millar, A. H., Eubel, H., Jänsch, L., Kruft, V., Heazlewood, J. L. and Braun, H. P. (2004) Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol. Biol. 56, 77-90 (Pubitemid 40134262)
41. Borutaité, V. and Brown, G. C. (1996) Rapid reduction of nitric oxide by mitochondria, and reversible inhibition of mitochondrial respiration by nitric oxide. Biochem. J. 315, 295-259
42. Kurz, C. R., Kissner, R., Nauser, T., Perrin, D. and Koppenol, W. H. (2003) Rapid scavenging of peroxynitrous acid by monohydroascorbate. Free Radical Biol. Med. 35, 1529-1537 (Pubitemid 37532904)
43. Borisjuk, L., Macherel, D., Benamar, A., Wobus, U. and Rolletschek, H. (2007) Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol. 176, 813-823 (Pubitemid 350098813)
44. Camacho-Pereira, J., Meyer, L. E., Machado, L. B., Oliveira, M. F. and Galina, A. (2009) Reactive oxygen species production by potato tuber mitochondria is modulated by mitochondrial bound hexokinase activity. Plant Physiol. 149, 1099-1110
45. de Oliveira, H. C., Wulff, A., Saviani, E. E. and Salgado, I. (2008) Nitric oxide degradation by potato tuber mitochondria: evidence for the involvement of external NAD(P)H dehydrogenases. Biochim. Biophys. Acta 1777, 470-476
46. Martínez-Espinosa, R. M., Cole, J. A., Richardson, D. J. and Watmough, N. J. (2011) Enzymology and ecology of the nitrogen cycle. Biochem. Soc. Trans. 39, 175-178
47. Allègre, A., Silvestre, J., Morard, P., Kallerhoff, J. and Pinelli, E. (2004) Nitrate reductase regulation in tomato roots by exogenous nitrate: a possible role in tolerance to long-term root anoxia. J. Exp. Bot. 55, 2625-2634 (Pubitemid 40025077)
48. Fuentes, D., Meneses, M., Nunes-Nesi, A., Araújo, W. L., Tapia, R., Gómez, I., Holuigue, L., Gutiérrez, R. A., Fernie, A. R. and Jordana, X. (2011) A deficiency in the flavoprotein of Arabidopsis mitochondrial complex II results in elevated photosynthesis and better growth in nitrogen-limiting conditions. Plant Physiol. 157, 1114-1127
49. Inoue, M., Sato, E. F., Nishikawa, M., Park, A. M., Kira, Y., Imada, I. and Utsumi, K. (2003) Cross talk of nitric oxide, oxygen radicals, and superoxide dismutase regulates the energy metabolism and cell death and determines the fates of aerobic life. Antioxid. Redox. Signaling 5, 475-484 (Pubitemid 37087408)
50. Pflüger, K. and de Lorenzo, V. (2008) Evidence of in vivo cross talk between the nitrogen-related and fructose-related branches of the carbohydrate phosphotransferase system of Pseudomonas putida . J. Bacteriol. 190, 3374-3380 (Pubitemid 351581433)