The emerging roles of nitric oxide (NO) in plant mitochondria

Plant Science

Volumn 181, Issue 5, 2011, Pages 520-526

  Gupta, Kapuganti J ^a,b   Igamberdiev, Abir U ^c   Manjunatha, Girigowda ^g   Segu, Shruthi ^e   Moran, Jose F ^f   Neelawarne, Bagyalakshmi ^d   Bauwe, Hermann ^a   Kaiser, Werner M ^b  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^d CENTRAL FOOD TECHNOLOGICAL RESEARCH INSTITUTE   (India)

^e MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^f CSIC   (Spain)

^g UNIVERSITY OF HORTICULTURAL SCIENCES   (India)

Author keywords

Chemiluminescence; Fluorescence; Mitochondria; Nitric oxide; Nitric oxide synthase; Nitrite

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE REDUCTASE; VEGETABLE PROTEIN;

ARTICLE; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL HYPOXIA; ELECTRON TRANSPORT; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANT; SIGNAL TRANSDUCTION;

CELL HYPOXIA; ELECTRON TRANSPORT; MITOCHONDRIA; MODELS, BIOLOGICAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE REDUCTASES; OXIDATION-REDUCTION; PLANT PROTEINS; PLANTS; SIGNAL TRANSDUCTION;

EID: 80052406379     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2011.03.018     Document Type: Article

References (78)

1. Rébeillé F., Macherel D., Mouillon J.-M., Garin J., Douce R. Folate biosynthesis in higher plants: purification and molecular cloning of a bifunctional 6-hydroxymethyl-7 8-dihydropterin pyrophosphokinase/7,8-dihydropteroate synthase localized in mitochondria. EMBO J. 1997, 16:947-957.
2. Zorov D.B., Krasnikov B.F., Kuzminova A.E., Vysokikh M.Yu., Zorova L.D. Mitochondria revisited. Alternative functions of mitochondria. Biosci. Rep. 1997, 17:507-520.
3. Bartoli C.G., Pastori G.M., Foyer C.H. Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol. 2000, 123:335-344.
4. Kowaltowski A.J. Alternative mitochondrial functions in cell physiopathology: beyond ATP production. Braz. J. Med. Biol. Res. 2000, 33:241-250.
5. Balk J., Leaver C.J. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 2001, 13:1803-1818.
6. Bauwe H., Hagemann M., Fernie A.R. Photorespiration: players, partners and origin. Trends Plant Sci. 2010, 15:330-336.
7. Rhoads D.M, Subbaiah C.C. Mitochondrial retrograde regulation in plants. Mitochondrion 2007, 7:177-194.
8. Kaiser W.M., Gupta K.J., Planchet E. Higher plant mitochondria as a source for NO. vol. 6 2007, 1-14. Springer, Berlin. L. Lamattina, J.C. Polacco (Eds.).
9. Besson-Bard A., Pugin A., Wendehenne D. New insights into nitric oxide signalling in plants. Annu. Rev. Plant Biol. 2008, 59:21-39.
10. Wilson I.D., Neill S.J., Hancock J.T. Nitric oxide synthesis and signalling in plants. Plant Cell Environ. 2008, 31:622-631.
11. Baudouin E. The language of nitric oxide signalling. Plant Biol. 2011, 13:233-242.
12. Gupta K.J., Hincha D.K., Mur L.A.J. NO way to treat a cold. New Phytol. 2011, 189:360-363.
13. Delledonne M., Xia Y., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature 1998, 394:585-588.
14. Garcia-Mata C., Lamattina L. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 2001, 126:1196-1204.
15. Graziano M., Beligni M.V., Lamattina L. Nitric oxide improves internal iron availability in plants. Plant Physiol. 2002, 130:1852-1859.
16. Zhao M.G., Tian Q.Y., Zhang W.H. Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol. 2007, 144:206-217.
17. Zhao M.G., Chen L., Zhang L.-L., Zhang W.-H. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. 2009, 151:755-767.
18. Gupta K.J., Fernie A.R., Kaiser W.M., van Dongen J.T. On the origins of nitric oxide. Trends Plant Sci. 2011, 16:160-168.
19. Igamberdiev A.U., Bykova N.V., Shah J.K., Hill R.D. Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol. Plant. 2010, 138:393-404.
20. Moreau M., Lindermayr C., Durner J., Klessig D.F. NO synthesis and signalling in plants: where do we stand?. Physiol. Plant. 2010, 138:372-383.
21. Tischner R., Planchet E., Kaiser W.M. Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett. 2004, 576:151-155.
22. Gupta K.J., Stoimenova M., Kaiser W.M. 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.
23. Gupta K.J., Kaiser W.M. Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol. 2010, 51:576-584.
24. Stoimenova M., Igamberdiev A.U., Gupta K.J., Hill R.D. Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 2007, 226:465-474.
25. Moir J.W. Cytochrome c from Paracoccus denitrificans: spectroscopic studies consistent with a role for the protein in nitric oxide metabolism. Biochim. Biophys. Acta 1999, 1430:65-72.
26. Nohl H., Staniek K., Kozlov A.V. Involvement of mammalian mitochondria in recycling of the NO-metabolite nitrite to nitric monoxide. Free Radic. Biol. Med. 1999, 27:S82.
27. Kozlov A.V., Staniek K., Nohl H. Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett. 1999, 454:127-130.
28. Escobar M.A., Geisler D.A., Rasmusson A.G. Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. Plant J. 2006, 45:775-788.
29. Planchet E., Gupta K.J., Sonoda M., Kaiser W.M. 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.
30. Sugiura M., Georgescu M.N., Takahashi M. A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant Cell Physiol. 2007, 48:1022-1035.
31. Laus M.N., 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.
32. Planchet E., Kaiser W.M. Nitric oxide (NO) detection by DAF fluorescence and chemiluminescence: a comparison using abiotic and biotic NO sources. J. Exp. Bot. 2006, 57:3043-3055.
33. Sakihama Y., Nakamura S., Yamasaki H. Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol. 2002, 43:290-297.
34. Zeidler D., Zähringer U., Dubery I., Hartung I., Bors W., Hutzler P., Durner J. Innate immunity in Arabidopsis thaliana lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc. Natl. Acad. Sci. U.S.A. 2004, 102:15811-15816.
35. Mur L.A., Santosa I.E., Laarhoven L.J., Holton N.J., Harren F.J., Smith A.R. Laser photoacoustic detection allows in planta detection of nitric oxide in tobacco following challenge with avirulent and virulent Pseudomonas syringae pathovars. Plant Physiol. 2005, 138:1247-1258.
36. Conrath U., Amoroso G., Köhle H., Sültemeyer D.F. Non-invasive online detection of nitric oxide from plants and some other organisms by mass spectrometry. Plant J. 2004, 38:1015-1022.
37. Corpas F.J., et al. Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol. 2009, 184:9-14.
38. Lacza Z., Pankotai E., Csordás A., Gero D., Kiss L., Horváth E.M., Kollai M., Busija D.W., Szabó C. Mitochondrial NO and reactive nitrogen species production: does mtNOS exist?. Nitric Oxide 2006, 14:162-168.
39. Smart D.R., Bloom A.J. Wheat leaves emit nitrous oxide during nitrate assimilation. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:7875-7878.
40. Gupta K.J., Igamberdiev A.U., Kaiser W.M. New insights into the mitochondrial nitric oxide production pathways. Plant Signal. Behav. 2010, 5:999-1001.
41. Vanin A.F., Svistunenko D.A., Mikoyan V.D., Serezhenkov V.A., Fryer M.J., Baker N.R., Cooper C.E. 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.
42. Daff S. NO synthase: structures and mechanisms. Nitric Oxide: Biol. Chem. 2010, 23:1-11.
43. Giulivi C., Poderoso J.J., Boveris A. Production of nitric oxide by mitochondria. J. Biol. Chem. 1998, 273:11038-11043.
44. Lacza Z., Snipes J.A., Zhang J., Horváth E.M., Figueroa J.P., Szabó C., Busija D.W. Mitochondrial nitric oxide synthase is not eNOS, nNOS or iNOS. Free Radic. Biol. Med. 2003, 35:1217-1228.
45. Derelle E., Ferraz C., Rombauts S., Rouzé P., Worden A.Z., Robbens S., Partensky F., Degroeve S., Echeynié S., Cooke R., Saeys Y., Wuyts J., Jabbari K., Bowler C., Panaud O., Piégu B., Ball S.G., Ral J.P., Bouget F.Y., Piganeau G., De Baets B., Picard A., Delseny M., Demaille J., Van de Peer Y., Moreau H. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11647-11652.
46. Foresi N., Correa-Aragunde N., Parisi G., Caló G., Salerno G., Lamattina L. Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 2010, 22:3816-3830.
47. Trapido-Rosenthal H.G., Sharp K.H., Galloway T.S., Morall C.E. Nitric oxide and cnidarian-dinoflagellate symbioses: pieces of a puzzle. Am. Zoologist 2001, 41:247-257.
48. Trapido-Rosenthal H.G., Zielke S., Owen R., Buxton L., Boeing B., Bhagooli R., Archer J. Increased zooxanthellae nitric oxide synthase activity is associated with coral bleaching. Biol. Bull. 2005, 208:3-6.
49. Kim D., Yamaguchi K., Oda T. Nitric oxide synthase-like enzyme mediated nitric oxide generation by harmful red tide phytoplankton, Chatoniella marina. J. Plankton Res. 2006, 28:613-620.
50. Vardi A., Bidie K.D., Kwityn C., Hirsh D.J., Thompson S.M., Callow J.A., Falkowski P., Bowler C. A diatom gene regulating nitric oxide signalling and susceptibility to diatom-derived aldehydes. Curr. Biol. 2008, 18:895-899.
51. Kharitonov V.G., Sundquist A.R., Sharma V.S. Kinetics of nitric oxide autoxidation in aqueous solutions. J. Biol. Chem. 1994, 269:5881-5883.
52. Coffey M.J., Natarajan R., Chumley P.H., Coles B., Thimmalapura P.R., Nowell M., Kuhn H., Lewis M.J., Freeman B.A., O'Donnell V.B. Catalytic consumption of nitric oxide by 12/15-lipoxygenase: inhibition of monocyte soluble guanylate cyclase activation. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:8006-8011.
53. Gardner P.R. Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 2005, 99:247-266.
54. Corpas F.J., del Río L.A., Barroso J.B. Need of biomarkers of nitrosative stress in plants. Trends Plant Sci. 2007, 12:436-438.
55. Brown G.C., Borutaite V. Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic. Biol. Med. 2002, 33:1440-1450.
56. Millar A.H., Day D.A. Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett. 1996, 398:155-158.
57. Radi R., Cassina A., Hodara R., Quijano C., Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic. Biol. Med. 2002, 33:1451-1464.
58. Møller I.M. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52:561-591.
59. de Oliveira H.C., Wulff A., Saviani E.E., 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.
60. Poderoso J.J., Carreras M.C., 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.
61. Mur L.A., Carver T.L., Prats E. NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J. Exp. Bot. 2006, 57:489-505.
62. Modolo L.V., Augusto O., Almeida I.M., Magalhaes J.R., Salgado I. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett. 2005, 579:3814-3820.
63. Morot-Gaudry-Talarmain Y., Rockel P., Moureaux T., Quilleré I., Leydecker M.T., Kaiser W.M., Morot-Gaudry J.F. Nitrite accumulation and nitric oxide emission in relation to cellular signaling in nitrite reductase antisense tobacco. Planta 2002, 215:708-715.
64. Spoel S.H., Tada Y., Loake G.J. Post-translational protein modification as a tool for transcription reprogramming. New Phytol. 2010, 186:333-339.
65. Gupta K.J. Protein S-nitrosylation in plants: photorespiratory metabolism and NO signalling. Sci. Signal. 2011, 4:jc1.
66. Palmieri M.C., Lindermayr C., Bauwe H., Steinhauser C., Durner J. Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol. 2010, 152:1514-1528.
67. Herold S., Puppo A. Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules?. J. Biol. Inorg. Chem. 2005, 10:935-945.
68. Kanayama Y., Yamamoto Y. Inhibition of nitrogen fixation in soybean plantssupplied with nitrate II. Accumulation and properties of nitrosylleghemoglobin in nodules. Plant Cell Physiol. 1990, 31:207-214.
69. Kanayama Y., Yamamoto Y. Formation of nitrosylleghemoglobin in nodules of nitrate-treated cowpea and pea plants. Plant Cell Physiol. 1991, 32:19-24.
70. Sánchez C., Gates A.J., Meakin G.E., Uchiumi T., Girard L., Richardson D.J., Bedmar E.J., Delgado M.J. Production of nitric oxide and nitrosylleghemoglobin complexes in soybean nodules in response to flooding. Mol. Plant Microbe Interact. 2010, 23:702-711.
71. Horchani F., Prevot M., Boscari A., Evangelisti E., Meilhoc E., Bruand C., Raymond P., Boncompagni E., Aschi-Smiti S., Puppo A., Brouquisse R. Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol. 2011, 155:1023-1036.
72. Kato K., Kanahama K., Kanayama Y. Involvement of nitric oxide in the inhibition of nitrogenase activity by nitrate in Lotus root nodules. J. Plant Physiol. 2010, 167:238-241.
73. Shimoda Y., Shimoda-Sasakura F., Kucho K., Kanamori N., Nagata M., Suzuki A., Abe M., Higashi S., Uchiumi T. Overexpression of class 1 plant hemoglobin genes enhances symbiotic nitrogen fixation activity between Mesorhizobium loti and Lotus japonicus. Plant J. 2008, 57:254-263.
74. Shimoda Y., Nagata M., Suzuki A., Abe M., Sato S., Kato T., Tabata S., Higashi S., Uchiumi T. Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol. 2005, 46:99-107.
75. Bustos-Sanmamed P., Tovar-Méndez A., Crespi M., Sato S., Tabata S., Becana M. Regulation of nonsymbiotic and truncated hemoglobin genes of Lotus japonicus in plant organs and in response to nitric oxide and hormones. New Phytol. 2011, 189:765-776.
76. Borisjuk L., Macherel D., Benamar A., Wobus U., Rolletschek H. Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol. 2007, 176:813-823.
77. Benamar A., Rolletschek H., Borisjuk L., Avelange-Macherel M.H., Curien G., Mostefai H.A., Andriantsitohaina R., Macherel D. Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim. Biophys. Acta 2008, 1777:1268-1275.
78. Igamberdiev A.U., Hill R.D. Plant mitochondrial function during anaerobiosis. Ann. Bot. 2009, 103:259-268.