Anoxic nitric oxide cycling in plants: Participating reactions and possible mechanisms

Physiologia Plantarum

Volumn 138, Issue 4, 2010, Pages 393-404

  Igamberdiev, Abir U ^a   Bykova, Natalia V ^a   Shah, Jay K ^a   Hill, Robert D ^b  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOPROTEIN; NITRATE; NITRIC OXIDE; NITRITE; OXYGEN;

BIOLOGICAL MODEL; CELL MEMBRANE; CELL ORGANELLE; METABOLISM; PLANT; REVIEW;

CELL MEMBRANE; HEMEPROTEINS; MODELS, BIOLOGICAL; NITRATES; NITRIC OXIDE; NITRITES; ORGANELLES; OXYGEN; PLANTS;

EID: 77952067882     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2009.01314.x     Document Type: Review

References (84)

1. Alegria AE, Sanchez S, Quintana I. Quinone-enhanced ascorbate reduction of nitric oxide: role of quinone redox potential. Free Radic Res 2004, 38:1107-1112.
2. Angelo M, Singel DJ, Stamler JS. An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc Natl Acad Sci USA 2006, 103:8366-8371.
3. Basu S, Grubina R, Huang J, Conradie J, Huang Z, Jeffers A, Jiang A, He X, Azarov I, Seibert R, Mehta A, Patel R, King SB, Hogg N, Ghosh A, Gladwin MT, Kim-Shapiro DB. Catalytic generation of N2O3 by the concerted nitrite reductase and anhydrase activity of hemoglobin. Nat Chem Biol 2007, 3:785-794.
4. Basu S, Azarova NA, Font MD, King SB, Hogg N, Gladwin MT, Shiva S, Kim-Shapiro DB. Nitrite reductase activity of cytochrome c. J Biol Chem 2008, 283:32590-32597.
5. Bethke PC, Badger MR, Jones RL. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 2004, 16:332-341.
6. Brunori M, Forte E, Arese M, Mastronicola D, Giuffrè A, Sarti P. Nitric oxide and the respiratory enzyme. Biochim Biophys Acta 2006, 1757:1144-1154.
7. Brooks J. The action of nitrite on haemoglobin in the absence of oxygen. Proc R Soc London B Biol Sci 1937, 123:368-382.
8. Bykova NV, Igamberdiev AU, Ens W, Hill RD. Identification of an intermolecular disulfide bond in barley hemoglobin. Biochem Biophys Res Commun 2006, 347:301-309.
9. Castello PR, David PS, McClure T, Crook Z, Poyton RO. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab 2006, 3:277-287.
10. Castello PR, Woo DK, Ball K, Wojcik J, Liu L, Poyton RO. Oxygen-regulated isoforms of cytochrome c oxidase have differential effects on its nitric oxide production and on hypoxic signaling. Proc Natl Acad Sci USA 2008, 105:8203-8208.
11. Castresana J, Sarasate M. Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biochem Sci 1995, 20:443-448.
12. Cooper CE. Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector? Trends Biochem Sci 2002, 27:33-39.
13. Cooper CE. Competitive, reversible, physiological? Inhibition of mitochondrial cytochrome oxidase by nitric oxide. IUBMB Life 2003, 55:591-597.
14. Coufal DE, Tavares P, Pereira AS, Hyunh BH, Lippard SJ. Reactions of nitric oxide with the reduced non-heme diiron center of the soluble methane monooxygenase hydroxylase. Biochemistry 1999, 38:4504-4513.
15. Crawford NM. Mechanisms for nitric oxide synthesis in plants. J Exp Bot 2006, 57:471-478.
16. Dean JV, Harper JE. Nitric oxide and nitrous oxide production by soybean and winged bean during the in vivo nitrate reductase assay. Plant Physiol 1986, 82:718-723.
17. Dean JV, Harper JE. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol 1988, 88:389-395.
18. De Oliveira HC, Wulff A, Saviani EE, Salgado I. Nitric oxide degradation by potato tuber mitochondria: evidence for the involvement of external NAD(P)H dehydrogenases. Biochim Biophys Acta 2008, 1777:470-476.
19. Dordas C, Hasinoff BB, Igamberdiev AU, Manac'h N, Rivoal J, Hill RD. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J 2003, 35:763-770.
20. Dordas C, Hasinoff BB, Rivoal J, Hill RD. Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 2004, 219:66-72.
21. Doyle MP, Pickering RA, DeWeert TM, Hoekstra JW, Pater D. Kinetics and mechanism of the oxidation of human deoxyhemoglobin by nitrites. J Biol Chem 1981, 256:12393-12398.
22. Ducluzeau A-L, van Lis R, Duval S, Schoepp-Cothenet B, Russell MJ, Nitschke W. Was nitric oxide the first deep electron sink? Trends Biochem Sci 2009, 34:9-15.
23. Duff SM, Wittenberg JB, Hill RD. Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands. J Biol Chem 1997, 272:16746-16752.
24. Feelisch M, Fernandez BO, Bryan NS, Garcia-Saura MF, Bauer S, Whitlock DR, Ford PC, Janero DR, Rodriguez J, Ashrafian H. Tissue processing of nitrite in hypoxia: an intricate interplay of nitric oxide-generating and scavenging systems. J Biol Chem 2008, 283:33927-33934.
25. Gardner PR, Gardner AM, Brashear WT, Suzuki T, Hvitved AN, Setchell KD, Olson JS. Hemoglobins dioxygenate nitric oxide with high fidelity. J Inorg Biochem 2006, 100:542-550.
26. Gladwin MT, Kim-Shapiro DB. The functional nitrite reductase activity of the heme-globins. Blood 2008, 112:2636-2647.
27. Gladwin MT, Grubina R, Doyle MP. The new chemical biology of nitrite reactions with hemoglobin: R-state catalysis, oxidative denitrosylation, and nitrite reductase/anhydrase. Acc Chem Res 2009, 42:157-167.
28. Goshima N, Mukai T, Suemori M, Takahashi M, Caboche M, Morikawa H. Emission of nitrous oxide (N2O) from transgenic tobacco expressing antisense NiR mRNA. Plant J 1999, 19:75-80.
29. Grubina R, Huang Z, Shiva S, Joshi MS, Azarov I, Basu S, Ringwood LA, Jiang A, Hogg N, Kim-Shapiro DB, Gladwin MT. Concerted nitric oxide formation and release from the simultaneous reactions of nitrite with deoxy- and oxyhemoglobin. J Biol Chem 2007, 282:12916-12927.
30. Gupta KJ, Stoimenova M, Kaiser WM. In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J Exp Bot 2005, 56:2601-2609.
31. Halliwell B, Zhao K, Whiteman M. Nitric oxide and peroxynitrite. The ugly, the uglier and the not so good: a personal view of recent controversies. Free Radic Res 1999, 31:651-669.
32. Hallstrom CK, Gardner AM, Gardner PR. Nitric oxide metabolism in mammalian cells: substrate and inhibitor profiles of a NADPH-cytochrome P450 oxidoreductase-coupled microsomal nitric oxide dioxygenase. Free Radic Biol Med 2004, 37:216-228.
33. Harper JE. Evolution of nitrogen oxide(s) during in vivo nitrate reductase assay of soybean leaves. Plant Physiol 1981, 68:1488-1493.
34. Hashimoto M, Takamiya S, Yokota T, Nakajima Y, Yamakura F, Sugio S, Aoki T. Ascaris suum cytochrome b5, an adult-specific secretory protein reducing oxygen-avid ferric hemoglobin. Arch Biochem Biophys 2008, 471:42-49.
35. Hebelstrup KH, Igamberdiev AU, Hill RD. Metabolic effects of hemoglobin gene expression in plants. Gene 2007, 398:86-93.
36. Hoshi Y, Hazeki O, Tamura M. Oxygen dependence of redox state of copper in cytochrome oxidase in vitro. J Appl Physiol 1993, 74:1622-1627.
37. Huang X, von Rad U, Durner J. Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 2002, 215:914-923.
38. Huang KT, Keszler A, Patel N, Patel RP, Gladwin MT, Kim-Shapiro DB, Hogg N. The reaction between nitrite and deoxyhemoglobin. Reassessment of reaction kinetics and stoichiometry. J Biol Chem 2005, 280:31126-31131.
39. Hunt PW, Klok EJ, Trevaskis B, Watts RA, Ellis MH, Peacock WJ, Dennis ES. Increased level of hemoglobin 1 enhances survival of hypoxic stress and promotes early growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 2002, 99:17197-171202.
40. Igamberdiev AU, Hill RD. Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 2004, 55:2473-2482.
41. Igamberdiev AU, Hill RD. Plant mitochondrial function during anaerobiosis. Ann Bot 2009, 103:259-268.
42. Igamberdiev AU, Seregélyes C, Manac'h N, Hill RD. NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 2004a, 219:95-102.
43. Igamberdiev AU, Bykova NV, Ens W, Hill RD. Dihydrolipoamide dehydrogenase from porcine heart catalyzes NADH-dependent scavenging of nitric oxide. FEBS Lett 2004b, 568:146-150.
44. Igamberdiev AU, Baron K, Manac'h-Little N, Stoimenova M, Hill RD. The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Ann Bot 2005, 96:557-564.
45. Igamberdiev AU, Bykova NV, Hill RD. Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. Planta 2006, 223:1033-1040.
46. Jancura D, Antalik M, Berka V, Palmer G, Fabian M. Filling the catalytic site of cytochrome c oxidase with electrons. Reduced CuB facilitates internal electron transfer to heme a3. J Biol Chem 2006, 281:20003-20010.
47. Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES. Expression profile analysis of the low oxygen response in Arabidopsis root cultures. Plant Cell 2002, 14:2481-2494.
48. Kozlov AV, Staniek K, Nohl H. Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett 1999, 454:127-130.
49. Kurtz DM. Flavo-diiron enzymes: nitric oxide or dioxygen reductases? Dalton Trans 2007, 37:4115-4121.
50. Laus MN, Soccio M, Trono D, Cattivelli L, Pastore D. Plant inner membrane anion channel (PIMAC) function in plant mitochondria. Plant Cell Physiol 2008, 49:1039-1055.
51. Li H, Samouilov A, Liu X, Zweier JL. Characterization of the effects of oxygen on xanthine oxidase-mediated nitric oxide formation. J Biol Chem 2004, 279:16939-16946.
52. Li H, Cui H, Kundu TK, Alzawahra W, Zweier JL. Nitric oxide production from nitrite occurs primarily in tissues not in the blood: critical role of xanthine oxidase and aldehyde oxidase. J Biol Chem 2008, 283:17855-17863.
53. Mason MG, Nicholls P, Wilson MT, Cooper CE. Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proc Natl Acad Sci USA 2006, 103:708-713.
54. Meyer C, Lea US, Provan F, Kaiser WM, Lillo C. Is nitrate reductase a major player in the plant NO (nitric oxide) game? Photosynth Res 2005, 83:181-189.
55. Millar AH, Day DA. Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 1996, 398:155-158.
56. Millar AH, Eubel H, Jänsch L, Kruft V, Heazlewood JL, Braun HP. Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol Biol 2004, 56:77-90.
57. Moore AL, Carré JE, Affourtit C, Albury MS, Crichton PG, Kita K, Heathcote P. Compelling EPR evidence that the alternative oxidase is a diiron carboxylate protein. Biochim Biophys Acta 2008, 1777:327-30.
58. Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF. AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J Biol Chem 2008, 283:32957-32967.
59. Morikawa H, Takahashi M, Sakamoto A, Matsubara T, Arimura GI, Kawamura Y, Fukunaga K, Fujita K, Sakurai N, Hirata T, Ide H, Nonoyama N, Suzuki H. Formation of unidentified nitrogen in plants: an implication for a novel nitrogen metabolism. Planta 2004, 219:14-22.
60. Nagababu E, Ramasamy S, Abernethy DR, Rifkind JM. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J Biol Chem 2003, 278:46349-46356.
61. Nohl H, Staniek K, Kozlov AV. The existence and significance of a mitochondrial nitrite reductase. Redox Rep 2005, 10:281-286.
62. Paitian NA, Markossian KA, Nalbandyan RM. The effect of nitrite on cytochrome oxidase. Biochem Biophys Res Communs 1985, 133:1104-1111.
63. Pearce LL, Kanai AJ, Birder LA, Pitt BR, Peterson J. The catabolic fate of nitric oxide: the nitric oxide oxidase and peroxynitrite reductase activities of cytochrome oxidase. J Biol Chem 2002, 277:13556-13562.
64. Perazzolli M, Romero-Puertas MC, Delledonne M. Modulation of nitric oxide bioactivity by plant haemoglobins. J Exp Bot 2006, 57:479-488.
65. Pihlatie M, Ambus P, Rinne J, Pilegaard K, Vesala T. Plant-mediated nitrous oxide emissions from beech (Fagus sylvatica) leaves. New Phytol 2005, 168:93-98.
66. Planchet E, Gupta KJ, Sonoda M, Kaiser WM. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 2005, 41:732-743.
67. Poderoso JJ, Carreras MC, Lisdero C, Riobó N, Schöpfer F, Boveris A. Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch Biochem Biophys 1996, 328:85-92.
68. Ruitenberg M, Kannt A, Bamberg E, Fendler K, Michel H. Reduction of cytochrome c oxidase by a second electron leads to proton translocation. Nature 2002, 417:99-102.
69. Sarti P, Giuffré A, Forte E, Mastronicola D, Barone MC, Brunori M. Nitric oxide and cytochrome c oxidase: mechanisms of inhibition and NO degradation. Biochem Biophys Res Communs 2000, 274:183-187.
70. Smagghe BJ, Trent JT, Hargrove MS. NO dioxygenase activity in hemoglobins is ubiquitous in vitro, but limited by reduction in vivo. PLoS ONE 2008, 3:e2039.
71. Smagghe BJ, Hoy JA, Percifield R, Kundu S, Hargrove MS, Sarath G, Hilbert JL, Watts RA, Dennis ES, Peacock WJ, Dewilde S, Moens L, Blouin GC, Olson JS, Appleby CA. Correlations between oxygen affinity and sequence classifications of plant hemoglobins. Biopolymers 2009, 91:1083-1096.
72. Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD. Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 2007, 226:465-474.
73. Stubauer G, Giuffrè A, Brunori M, Sarti P. Cytochrome c oxidase does not catalyze the anaerobic reduction of NO. Biochem Biophys Res Communs 1998, 245:459-465.
74. Sugiura M, Georgescu MN, Takahashi M. A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant Cell Physiol 2007, 48:1022-1035.
75. Tischner R, Planchet E, Kaiser WM. Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett 2004, 576:151-155.
76. Vanin AF, Svistunenko DA, Mikoyan VD, Serezhenkov VA, Fryer MJ, Baker NR, Cooper CE. Endogenous superoxide production and the nitrite/nitrate ratio control the concentration of bioavailable free nitric oxide in leaves. J Biol Chem 2004, 279:24100-24107.
77. Vanin AF, Bevers LM, Slama-Schwok A, van Faassen EE. Nitric oxide synthase reduces nitrite to NO under anoxia. Cell Mol Life Sci 2007, 64:96-103.
78. Walters CL, Taylor AM. The reduction of nitrite by skeletal muscle mitochondria. Biochim Biophys Acta 1965, 96:522-524.
79. Wilson MT, Torres J. Reactions of nitric oxide with copper containing oxidases; cytochrome c oxidase and laccase. IUBMB Life 2004, 56:7-11.
80. Wilson I, Neill SJ, Hancock JT. Nitric oxide synthesis and signalling in plants. Plant Cell Environ 2008, 31:622-631.
81. Wulff A, Oliveira HC, Saviani EE, Salgado I. 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 2009, 21:132-139.
82. Yamasaki H, Sakihama Y. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 2000, 468:89-92.
83. Zemojtel T, Fröhlich A, Palmieri MC, Kolanczyk M, Mikula I, Wyrwicz LS, Wanker EE, Mundlos S, Vingron M, Martasek P, Durner J. Plant nitric oxide synthase: a never-ending story? Trends Plant Sci 2006, 11:524-525.
84. Zhao X-J, Sampath V, Caughey VS. Cytochrome c oxidase catalysis of the reduction of nitric oxide to nitrous oxide. Biochem Biophys Res Commun 1995, 212:1054-1060.