Respiratory complex I deficiency results in low nitric oxide levels, induction of hemoglobin and upregulation of fermentation pathways

Plant Physiology and Biochemistry

Volumn 63, Issue , 2013, Pages 185-190

  Shah, Jay K ^a   Cochrane, Devin W ^a   De Paepe, Rosine ^b   Igamberdiev, Abir U ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

Aconitase; CMS tobacco mutant; Complex I; Fermentation; Nitric oxide (NO); Non symbiotic hemoglobin

Indexed keywords

ACONITATE HYDRATASE; HEMOGLOBIN; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); VEGETABLE PROTEIN;

ARTICLE; FERMENTATION; GENE EXPRESSION REGULATION; METABOLISM; TOBACCO;

ACONITATE HYDRATASE; ELECTRON TRANSPORT COMPLEX I; FERMENTATION; GENE EXPRESSION REGULATION, PLANT; HEMOGLOBINS; NITRIC OXIDE; PLANT PROTEINS; TOBACCO;

NICOTIANA; NICOTIANA SYLVESTRIS; NICOTIANA TABACUM;

EID: 84871658933     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2012.11.022     Document Type: Article

References (42)

1. Sabar M., De Paepe R., de Kouchkovsky Y. Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol. 2000, 124:1239-1250.
2. Priault P., Fresneau C., Noctor G., De Paepe R., Cornic G., Streb P. The mitochondrial CMSII mutation of Nicotiana sylvestris impairs adjustment of photosynthetic carbon assimilation to higher growth irradiance. J. Exp. Bot. 2006, 57:2075-2085.
3. Dutilleul C., Driscoll S., Cornic G., De Paepe R., Foyer C.H., Noctor G. Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol. 2003, 131:264-275.
4. Noctor G., Dutilleul C., De Paepe R., Foyer C.H. Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J. Exp. Bot. 2004, 55:49-57.
5. Noctor G., De Paepe R., Foyer C.H. Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 2007, 12:125-134.
6. + ratio in transgenic Nicotiana sylvestris. Plant Cell Physiol. 2008, 49:251-263.
7. Szal B., Dabrowska Z., Malmberg G., Gardeström P., Rychter A.M. Changes in energy status of leaf cells as the consequence of mitochondrial genome rearrangement. Planta 2008, 227:697-706.
8. + upon illumination of tobacco plants studied through the influence of mitochondrial electron transport. Biochim. Biophys. Acta 2010, 1797:177-188.
9. Dutilleul C., Lelarge C., Prioul J.L., De Paepe R., Foyer C.H., Noctor G. Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiol. 2005, 139:64-78.
10. Dutilleul C., Garmier M., Noctor G., Mathieu C., Chétrit P., Foyer C.H., de Paepe R. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 2003, 15:1212-1226.
11. Vidal G., Ribas-Carbo M., Garmier M., Dubertret G., Rasmusson A.G., Mathieu C., Foyer C.H., De Paepe R. Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signaling during elicitor-induced cell death in tobacco. Plant Cell 2007, 19:640-655.
12. Juszczuk I.M., Szal B., Rychter A.M. Oxidation-reduction and reactive oxygen species homeostasis in mutant plants with respiratory chain complex I dysfunction. Plant Cell Environ. 2012, 35:296-307.
13. Hager J., Pellny T.K., Mauve C., Lelarge-Trouverie C., De Paepe R., Foyer C.H., Noctor G. Conditional modulation of NAD levels and metabolite profiles in Nicotiana sylvestris by mitochondrial electron transport and carbon/nitrogen supply. Planta 2010, 231:1145-1157.
14. Juszczuk I.M., Flexas J., Szal B., Dabrowska Z., Ribas-Carbo M., Rychter A.M. Effect of mitochondrial genome rearrangement on respiratory activity, photosynthesis, photorespiration and energy status of MSC16 cucumber (Cucumis sativus) mutant. Physiol. Plant. 2007, 131:527-541.
15. Szal B., Łukawska K., Zdolinska K., Rychter A.M. Chilling stress and mitochondrial genome rearrangement in the MSC16 cucumber mutant affect the alternative oxidase and antioxidant defense system to a similar extent. Physiol. Plant. 2009, 137:435-445.
16. Lee B.H., Lee H., Xiong L., Zhu J.K. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 2002, 14:1235-1251.
17. Meyer E.H., Tomaz T., Carroll A.J., Estavillo G., Delannoy E., Tanz S.K., Small I.D., Pogson B.J., Millar A.H. Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 2009, 151:603-619.
18. Gupta K.J., Igamberdiev A.U. The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 2011, 11:537-543.
19. Leshem Y.Y., Haramaty E. The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. Foliage. J. Plant Physiol. 1996, 148:258-263.
20. Dordas C., Hasinoff B.B., Igamberdiev A.U., Manac'h N., Rivoal J., Hill R.D. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J. 2003, 35:763-770.
21. 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.
22. Garmier M., Carroll A.J., Delannoy E., Vallet C., Day D.A., Small I.D., Millar A.H. Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol. 2008, 148:1324-1341.
23. Gupta K.J., Hebelstrup K.H., Mur L.A., Igamberdiev A.U. Plant hemoglobins: important players at the crossroads between oxygen and nitric oxide. FEBS Lett. 2011, 585:3843-3849.
24. Nie X., Durnin D.C., Igamberdiev A.U., Hill R.D. Cytosolic calcium is involved in the regulation of barley hemoglobin gene expression. Planta 2006, 223:542-549.
25. 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 Bioenerg. 2008, 1777:470-476.
26. Wulff A., Oliveira H.C., Saviani E.E., 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 Biol. Chem. 2009, 21:132-139.
27. Pellny T.K., van Aken O., Dutilleul C., Wolff T., Groten K., Bor M., De Paepe R., Reyss A., van Breusegem F., Noctor G., Foyer C.H. Mitochondrial respiratory pathways modulate nitrate sensing and nitrogen-dependent regulation of plant architecture in Nicotiana sylvestris. Plant J. 2008, 54:976-992.
28. Correa-Aragunde N., Graziano M., Lamattina L. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 2004, 218:900-905.
29. Fernández-Marcos M., Sanz L., Lewis D.R., Muday G.K., Lorenzo O. Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18506-18511.
30. Lanteri M.L., Laxalt A.M., Lamattina L. Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol. 2008, 147:188-198.
31. Djebbar R., Rzigui T., Pétriacq P., Mauve C., Priault P., Fresneau C., De Paepe M., Florez-Sarasa I., Benhassaine-Kesri G., Streb P., Gakière B., Cornic G., De Paepe R. Respiratory complex I deficiency induces drought tolerance by impacting leaf stomatal and hydraulic conductances. Planta 2012, 235:603-614.
32. García-Mata C., Lamattina L. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 2002, 128:790-792.
33. Navarre D.A., Wendehenne D., Durner J., Noad R., Klessig D.F. Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol. 2000, 122:573-582.
34. Gupta K.J., Shah J.K., Brotman Y., Jahnke K., Willmitzer L., Kaiser W.M., Bauwe H., Igamberdiev A.U. Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J. Exp. Bot. 2012, 63:1773-1784.
35. Flint D.H., Tuminello J.F., Emptage M.H. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem. 1993, 268:22369-22376.
36. Vanlerberghe G.C., Day D.A., Wiskich J.T., Vanlerberghe A.E., McIntosh L. Alternative oxidase activity in tobacco leaf mitochondria (dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation). Plant Physiol. 1995, 109:353-361.
37. Cvetkovska M., Vanlerberghe G.C. Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol. 2012, 195:32-39.
38. Igamberdiev A.U., Gardeström P. Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim. Biophys. Acta 2003, 1606:117-125.
39. Florez-Sarasa I., Araújo W.L., Wallström S.V., Rasmusson A.G., Fernie A.R., Ribas-Carbo M. Light-responsive metabolite and transcript levels are maintained following a dark-adaptation period in leaves of Arabidopsis thaliana. New Phytol. 2012, 195:136-148.
40. Trevaskis B., Watts R.A., Andersson C.R., Llewellyn D.J., Hargrove M.S., Olson J.S., Dennis E.S., Peacock W.J. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:12230-12234.
41. Racker E. Spectrophotometric measurements of the enzymatic formation of fumaric and cis-aconitic acids. Biochim. Biophys. Acta 1950, 4:211-214.
42. 2 deficit in barley aleurone layers. Plant Physiol. 1984, 75:566-572.