The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria

Mitochondrion

Volumn 8, Issue 1, 2008, Pages 47-60

  Rasmusson, Allan G ^a   Geisler, Daniela A ^a   Møller, Ian M ^b  

^a LUND UNIVERSITY   (Sweden)

^b DANISH INSTITUTE OF AGRICULTURAL SCIENCES   (Denmark)

Author keywords

Carbon metabolism; Electron transport chain; NADH; NADPH; Plant mitochondria; Ubiquinone

Indexed keywords

CALCIUM ION; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; UBIQUINONE;

ARABIDOPSIS; ARTICLE; CALCIUM SIGNALING; CARBON METABOLISM; CELL METABOLISM; CELL PH; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENETIC VARIABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION; PLANT GENETICS; PLANT METABOLISM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

ARABIDOPSIS; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; GLYCEROL-3-PHOSPHATE DEHYDROGENASE (NAD+); MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NAD(P)H DEHYDROGENASE (QUINONE); NADH DEHYDROGENASE; PLANTS; SUBSTRATE SPECIFICITY;

MAMMALIA;

EID: 37249058385     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2007.10.004     Document Type: Article

References (154)

1. Adams E., and Frank L. Metabolism of proline and the hydroxyprolines. Annu. Rev. Biochem. 49 (1980) 1005-1061
2. Affourtit C., Krab K., and Moore A.L. Control of plant mitochondrial respiration. Biochim. Biophys. Acta 1504 (2001) 58-69
3. Agius S.C., Bykova N.V., Igamberdiev A.U., and Møller I.M. The internal rotenone-insensitive NADPH dehydrogenase contributes to malate oxidation by potato tuber and pea leaf mitochondria. Physiol. Plant. 104 (1998) 329-336
4. Amarneh B., and Vik S.B. Direct transfer of NADH from malate dehydrogenase to complex I in Escherichia coli. Cell Biochem. Biophys. 42 (2005) 251-261
5. Arkblad E.L., Betsholtz C., Mandoli D., and Rydström J. Characterization of a nicotinamide nucleotide transhydrogenase gene from the green alga Acetabularia acetabulum and comparison of its structure with those of the corresponding genes in mouse and Caenorhabditis elegans. Biochim. Biophys. Acta 1520 (2001) 115-123
6. Armstrong A.F., Logan D.C., Tobin A.K., O'Toole P., and Atkin O.K. Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves. Plant Cell Environ. 29 (2006) 940-949
7. Arron G.P., and Edwards G.E. Oxidation of reduced nicotinamide adenine dinucleotide phosphate by plant mitochondria. Can. J. Biochem. 57 (1979) 1392-1399
8. Atlante A., de Bari L., Valenti D., Pizzuto R., Paventi G., and Passarella S. Transport and metabolism of d-lactate in Jerusalem artichoke mitochondria. Biochim. Biophys. Acta 1708 (2005) 13-22
9. Bartoli C.G., Gomez F., Gergoff G., Guiamet J.J., and Puntarulo S. Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J. Exp. Bot. 56 (2005) 1269-1276
10. Bartoli C.G., Pastori G.M., and Foyer C.H. Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol. 123 (2000) 335-343
11. Brandt U. Energy converting NADH: quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75 (2006) 69-92
12. Braun H.P., and Zabaleta E. Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (complex I) in plants. Physiol. Plant. 129 (2007) 114-122
13. Brown L.J., MacDonald M.J., Lehn D.A., and Moran S.M. Sequence of rat mitochondrial glycerol-3-phosphate dehydrogenase cDNA. Evidence for EF-hand calcium-binding domains. J. Biol. Chem. 269 (1994) 14363-14366
14. Bykova N.V., Rasmusson A.G., Igamberdiev A.U., Gardeström P., and Møller I.M. Two separate transhydrogenase activities are present in plant mitochondria. Biochem. Biophys. Res. Commun. 265 (1999) 106-111
15. Campbell W.H. Nitrate reductase structure, function and regulation: Bridging the gap between biochemistry and physiology. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 (1999) 277-303
16. Cardenas L., McKenna S.T., Kunkel J.G., and Hepler P.K. NAD(P)H oscillates in pollen tubes and is correlated with tip growth. Plant Physiol. 142 (2006) 1460-1468
17. Cardol P., Vanrobaeys F., Devreese B., Van Beeumen J., Matagne R.F., and Remacle C. Higher plant-like subunit composition of mitochondrial complex I from Chlamydomonas reinhardtii: 31 conserved components among eukaryotes. Biochim. Biophys. Acta 1658 (2004) 212-224
18. Carneiro P., Duarte M., and Videira A. The main external alternative NAD(P)H dehydrogenase of Neurospora crassa mitochondria. Biochim. Biophys. Acta 1608 (2004) 45-52
19. Carneiro P., Duarte M., and Videira A. The external alternative NAD(P)H dehydrogenase NDE3 is localized both in the mitochondria and in the cytoplasm of Neurospora crassa. J. Mol. Biol. 368 (2007) 1114-1121
20. Chinopoulos C., and Adam-Vizi V. Calcium, mitochondria and oxidative stress in neuronal pathology. Novel aspects of an enduring theme. FEBS J. 273 (2006) 433-450
21. Clifton R., Lister R., Parker K.L., Sappl P.G., Elhafez D., Millar A.H., Day D.A., and Whelan J. Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58 (2005) 193-212
22. de Vries S., Van Witzenburg R., Grivell L.A., and Marres C.A.M. Primary structure and import pathway of the rotenone-insensitive NADH-ubiquinone oxidoreductase of mitochondria from Saccharomyces cerevisiae. Eur. J. Biochem. 203 (1992) 587-592
23. 1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16 (2004) 3413-3425
24. Donald S.P., Sun X.Y., Hu C.A.A., Yu J., Mei J.M., Valle D., and Phang J.M. Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species. Cancer Res. 61 (2001) 1810-1815
25. Dry I.B., and Wiskich J.T. Characteristics of glycine and malate oxidation by pea leaf mitochondria - evidence of differential access to NAD and respiratory chains. Austr. J. Plant Physiol. 12 (1985) 329-339
26. Duarte M., Peters M., Schulte U., and Videira A. The internal alternative NADH dehydrogenase of Neurospora crassa mitochondria. Biochem. J. 371 (2003) 1005-1011
27. Dudkina N.V., Eubel H., Keegstra W., Boekema E.J., and Braun H.P. Structure of a mitochondrial supercomplex formed by respiratory chain complexes I and III. Proc. Natl. Acad. Sci. USA 102 (2005) 3225-3229
28. Dudkina N.V., Heinemeyer J., Sunderhaus S., Boekema E.J., and Braun H.P. Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends Plant Sci. 11 (2006) 232-240
29. Dutilleul C., Driscoll S., Cornic G., De Paepe R., Foyer C.H., and Noctor G. Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol. 131 (2003) 264-275
30. Dutilleul C., Lelarge C., Prioul J.L., De Paepe R., Foyer C.H., and 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. 139 (2005) 64-78
31. Dym O., Pratt E.A., Ho C., and Eisenberg D. The crystal structure of d-lactate dehydrogenase, a peripheral membrane respiratory enzyme. Proc. Natl. Acad. Sci. USA 97 (2000) 9413-9418
32. Eastmond P.J. Glycerol-insensitive Arabidopsis mutants: Gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress. Plant J. 37 (2004) 617-625
33. Ebbighausen H., Chen J., and Heldt H.W. Oxaloacetate translocator in plant mitochondria. Biochim. Biophys. Acta 810 (1985) 184-199
34. Elhafez D., Murcha M.W., Clifton R., Soole K.L., Day D.A., and Whelan J. Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant Cell Physiol. 47 (2006) 43-54
35. Elthon T.E., and Stewart C.R. Sub-mitochondrial location and electron-transport characteristics of enzymes involved in proline oxidation. Plant Physiol. 67 (1981) 780-784
36. Escobar M.A., Franklin K.A., Svensson A.S., Salter M.G., Whitelam G.C., and Rasmusson A.G. Light regulation of the Arabidopsis respiratory chain. Multiple discrete photoreceptor responses contribute to induction of type II NAD(P)H dehydrogenase genes. Plant Physiol. 136 (2004) 2710-2721
37. Escobar M.A., Geisler D.A., and Rasmusson A.G. Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. Plant J. 45 (2006) 775-788
38. Escobar, M.A., Rasmusson, A.G., 2005. Photocontrol of respiratory type II NAD(P)H dehydrogenase genes: Cryptochrome, but not hy5, is a critical component of light signaling. In: van der Est, A., Bruce, D. (Eds.), Photosynthesis: Fundamental Aspects to Global Perspectives, Springer, Berlin, pp. 909-911.
39. Eubel H., Jänsch L., and Braun H.-P. New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II. Plant Physiol. 133 (2003) 274-286
40. Feilner T., Hultschig C., Lee J., Meyer S., Immink R.G., Koenig A., Possling A., Seitz H., Beveridge A., Scheel D., Cahill D.J., Lehrach H., Kreutzberger J., and Kersten B. High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Mol. Cell. Proteomics 4 (2005) 1558-1568
41. Felle H.H. pH: signal and messenger in plant cells. Plant Biol. 3 (2001) 577-591
42. Felle H.H., Kondorosi E., Kondorosi A., and Schultze M. How alfalfa root hairs discriminate between nod factors and oligochitin elicitors. Plant Physiol. 124 (2000) 1373-1380
43. Fernie A.R., Carrari F., and Sweetlove L.J. Respiratory metabolism: Glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 7 (2004) 254-261
44. Figueroa P., Leon G., Elorza A., Holuigue L., and Jordana X. Three different genes encode the iron-sulfur subunit of succinate dehydrogenase in Arabidopsis thaliana. Plant Mol. Biol. 46 (2001) 241-250
45. Finnegan P.M., Soole K.L., and Umbach A.L. Alternative mitochondrial electron transport proteins in higher plants. In: Day D.A., Millar A.H., and Whelan J. (Eds). Plant Mitochondria: From Genome to Function (2004), Kluwer Academic Publishers., Dordrecht 163-230
46. Flexas J., Bota J., Galmes J., Medrano H., and Ribas-Carbo M. Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol. Plant. 127 (2006) 343-352
47. Flügge U.I., and Heldt H.W. Metabolite translocators of the chloroplast envelope. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42 (1991) 129-144
48. Fredlund K.M., Rasmusson A.G., and Møller I.M. Oxidation of external NAD(P)H by purified mitochondria from fresh and aged red beetroots (Beta vulgaris L). Plant Physiol. 97 (1991) 99-103
49. Friedrich T., Steinmüller K., and Weiss H. The proton-pumping respiratory complex I of bacteria and mitochondria and its homolog in chloroplasts. FEBS Lett. 367 (1995) 107-111
50. Geisler D.A., Broselid C., Hederstedt L., and Rasmusson A.G. Ca2+binding and Ca2+independent respiratory NADH and NADPH dehydrogenases of Arabidopsis thaliana. J. Biol. Chem 282 (2007) 28455-28464
51. Giegé P., Heazlewood J.L., Roessner-Tunali U., Millar A.H., Fernie A.R., Leaver C.J., and Sweetlove L.J. Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15 (2003) 2140-2151
52. Grandier-Vazeille X., Bathany K., Chaignepain S., Camougrand N., Manon S., and Schmitter J.M. Yeast mitochondrial dehydrogenases are associated in a supramolecular complex. Biochemistry 40 (2001) 9758-9769
53. Hagedorn P.H., Flyvbjerg H., and Møller I.M. Modeling NADH turnover in plant mitochondria. Physiol. Plant. 120 (2004) 370-385
54. Hanning I., and Heldt H.W. On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L.) leaves partitioning between respiration and export of redox equivalents and precursors for nitrate assimilation products. Plant Physiol. 103 (1993) 1147-1154
55. Hansford R.G. Role of calcium in respiratory control. Med. Sci. Sports Exerc. 26 (1994) 44-51
56. Heazlewood J.L., Howell K.A., and Millar A.H. Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochim. Biophys. Acta 1604 (2003) 159-169
57. Heineke D., Riens B., Grosse H., Hoferichter P., Peter U., Flügge U.I., and Heldt H.W. Redox transfer across the inner chloroplast envelope membrane. Plant Physiol. 95 (1991) 1131-1137
58. Hodges M. Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53 (2002) 905-916
59. Igamberdiev A.U., Bykova N.V., and Gardeström P. Involvement of cyanide-resistant and rotenone-insensitive pathways of mitochondrial electron transport during oxidation of glycine in higher plants. FEBS Lett. 412 (1997) 265-269
60. Igamberdiev A.U., and 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 1606 (2003) 117-125
61. Ishizaki K., Larson T.R., Schauer N., Fernie A.R., Graham I.A., and Leaver C.J. The critical role of Arabidopsis electron-transfer flavoprotein: Ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17 (2005) 2587-2600
62. Ishizaki K., Schauer N., Larson T.R., Graham I.A., Fernie A.R., and Leaver C.J. The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J. 47 (2006) 751-760
63. Johansson F.I., Michalecka A.M., Møller I.M., and Rasmusson A.G. Oxidation and reduction of pyridine nucleotides in alamethicin-permeabilised plant mitochondria. Biochem. J. 380 (2004) 193-202
64. Joseph-Horne T., Hollomon D.W., and Wood P.M. Fungal respiration: a fusion of standard and alternative components. Biochim. Biophys. Acta 1504 (2001) 179-195
65. Juszczuk I.M., Bykova N.V., and Møller I.M. Protein phosphorylation in plant mitochondria. Physiol. Plant. 129 (2007) 90-103
66. Kalapos M.P. Methylglyoxal in living organisms - chemistry, biochemistry, toxicology and biological implications. Toxicol. Lett. 110 (1999) 145-175
67. Kasimova M.R., Grigiene J., Krab K., Hagedorn P.H., Flyvbjerg H., Andersen P.E., and Møller I.M. The free NADH concentration is kept constant in plant mitochondria under different metabolic conditions. Plant Cell 18 (2006) 688-698
68. Kerscher S.J. Diversity and origin of alternative NADH: ubiquinone oxidoreductases. Biochim. Biophys. Acta 1459 (2000) 274-283
69. Kiyosue T., Yoshiba Y., Yamaguchi-Shinozaki K., and Shinozaki K. A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8 (1996) 1323-1335
70. Knight H., Trewavas A.J., and Knight M.R. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8 (1996) 489-503
71. Kramer R., and Palmieri F. Molecular aspects of isolated and reconstituted carrier proteins from animal mitochondria. Biochim. Biophys. Acta 974 (1989) 1-23
72. Kristensen B.K., Askerlund P., Bykova N.V., Egsgaard H., and Møller I.M. Identification of oxidised proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry. Phytochemistry 65 (2004) 1839-1851
73. Krömer S. Respiration during photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46 (1995) 45-70
74. Krömer S., and Heldt H.W. Respiration of pea leaf mitochondria and redox transfer between the mitochondrial and extramitochondrial compartment. Biochim. Biophys. Acta 1057 (1991) 42-50
75. Laloi M. Plant mitochondrial carriers: an overview. Cell. Mol. Life Sci. 56 (1999) 918-944
76. Larsson C., Påhlman I.L., Ansell R., Rigoulet M., Adler L., and Gustafsson L. The importance of the glycerol 3-phosphate shuttle during aerobic growth of Saccharomyces cerevisiae. Yeast 14 (1998) 347-357
77. Lenaz G., Fato R., Genova M.L., Bergamini C., Bianchi C., and Biondi A. Mitochondrial complex I: structural and functional aspects. Biochim. Biophys. Acta 1757 (2006) 1406-1420
78. Leon G., Holuigue L., and Jordana X. Mitochondrial complex II is essential for gametophyte development in Arabidopsis. Plant Physiol. 143 (2007) 1534-1546
79. 1-pyrroline-5-carboxylate dehydrogenase domains of the multifunctional Escherichia coli putA protein. J. Mol. Biol. 243 (1994) 950-956
80. Luttik M.A.H., Overkamp K.M., Kotter P., de Vries S., van Dijken J.P., and Pronk J.T. The Saccharomyces cerevisiae NDE1 and NDE2 genes encode separate mitochondrial NADH dehydrogenases catalyzing the oxidation of cytosolic NADH. J. Biol. Chem. 273 (1998) 24529-24534
81. Mani S., Van De Cotte B., Van Montagu M., and Verbruggen N. Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiol. 128 (2002) 73-83
82. Martin W., and Herrmann R.G. Gene transfer from organelles to the nucleus: how much, what happens, and why?. Plant Physiol. 118 (1998) 9-17
83. Maxwell D.P., Wang Y., and McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA 96 (1999) 8271-8276
84. Maxwell S.A., and Rivera A. Proline oxidase induces apoptosis in tumor cells, and its expression is frequently absent or reduced in renal carcinomas. J. Biol. Chem. 278 (2003) 9784-9789
85. 2+ precedes stomatal closure. Nature 343 (1990) 186-188
86. Melo A.M., Bandeiras T.M., and Teixeira M. New insights into type II NAD(P)H: Quinone oxidoreductases. Microbiol. Mol. Biol. Rev. 68 (2004) 603-616
87. Melo A.M.P., Duarte M., Møller I.M., Prokisch H., Dolan P.L., Pinto L., Nelson M.A., and Videira A. The external calcium-dependent NADPH dehydrogenase from Neurospora crassa mitochondria. J. Biol. Chem. 276 (2001) 3947-3951
88. Melo A.M.P., Roberts T.H., and Møller I.M. Evidence for the presence of two rotenone-insensitive NAD(P)H dehydrogenases on the inner surface of the inner membrane of potato tuber mitochondria. Biochim. Biophys. Acta 1276 (1996) 133-139
89. Meyer E.H., Heazlewood J.L., and Millar A.H. Mitochondrial acyl carrier proteins in Arabidopsis thaliana are predominantly soluble matrix proteins and none can be confirmed as subunits of respiratory complex I. Plant Mol. Biol. 64 (2007) 319-327
90. Michalecka A.M., Agius S.C., Møller I.M., and Rasmusson A.G. Identification of a mitochondrial external NADPH dehydrogenase by overexpression in transgenic Nicotiana sylvestris. Plant J. 37 (2004) 415-425
91. Michalecka A.M., Svensson A.S., Johansson F.I., Agius S.C., Johanson U., Brennicke A., Binder S., and Rasmusson A.G. Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol. 133 (2003) 642-652
92. Millar A.H., Eubel H., Jänsch L., Kruft V., Heazlewood J.L., and Braun H.P. Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol. Biol. 56 (2004) 77-90
93. Millar A.H., Mittova V., Kiddle G., Heazlewood J.L., Bartoli C.G., Theodoulou F.L., and Foyer C.H. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 133 (2003) 443-447
94. Millenaar F.F., and Lambers H. The alternative oxidase: in vivo regulation and function. Plant Biol. 5 (2003) 2-15
95. Moore C.S., Cook-Johnson R.J., Rudhe C., Whelan J., Day D.A., Wiskich J.T., and Soole K.L. Identification of AtNDI1, an internal non-phosphorylating NAD(P)H dehydrogenase in Arabidopsis mitochondria. Plant Physiol. 133 (2003) 1968-1978
96. Møller I.M. The oxidation of cytosolic NAD(P)H by external NAD(P)H dehydrogenases in the respiratory chain of plant mitochondria. Physiol. Plant. 100 (1997) 85-90
97. 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. 52 (2001) 561-591
98. Møller I.M., Jensen P.E., and Hansson A. Oxidative modifications to cellular components in plants. Annu. Rev. Plant Biol. 58 (2007) 459-481
99. 2+ in the oxidation of exogenous NADH by Jerusalem artichoke (Helianthus tuberosus) mitochondria. Biochem. J. 194 (1981) 487-495
100. Møller I.M., and Kristensen B.K. Protein oxidation in plant mitochondria detected as oxidized tryptophan. Free Radical Biol. Med. 40 (2006) 430-435
101. Møller I.M., and Palmer J.M. Charge screening by cations affects the conformation of the mitochondrial inner membrane - a study of exogenous NAD(P)H oxidation in plant mitochondria. Biochem. J. 195 (1981) 583-588
102. Møller I.M., and Palmer J.M. The inhibition of exogenous NAD(P)H oxidation in plant mitochondria by chelators and mersalyl as a function of pH. Physiol. Plant. 53 (1981) 413-420
103. Møller I.M., and Palmer J.M. Direct evidence for the presence of a rotenone-resistant NADH dehydrogenase on the inner surface of the inner membrane of plant mitochondria. Physiol. Plant. 54 (1982) 267-274
104. Møller I.M., Rasmusson A.G., and Fredlund K.M. NAD(P)H-ubiquinone oxidoreductases in plant mitochondria. J. Bioenerg. Biomembr. 25 (1993) 377-384
105. Nanjo T., Kobayashi M., Yoshiba Y., Kakubari Y., Yamaguchi-Shinozaki K., and Shinozaki K. Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett. 461 (1999) 205-210
106. Nash D., and Wiskich J.T. Properties of substantially chlorophyll free pea leaf mitochondria prepared by sucrose density gradient separation. Plant Physiol. 71 (1983) 627-634
107. Nicholls D.G., and Ferguson S.J. Bioenergetics 3 (2002), Academic Press, London
108. Noctor G., Dutilleul C., De Paepe R., and 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. 55 (2004) 49-57
109. Noctor G., and Foyer C.H. A re-evaluation of the ATP: NADPH budget during C-3 photosynthesis: a contribution from nitrate assimilation and its associated respiratory activity? J. Exp. Bot. 49 (1998) 1895-1908
110. Plaxton W.C., and Podesta F.E. The functional organization and control of plant respiration. Crit. Rev. Plant Sci. 25 (2006) 159-198
111. Purvis A.C., and Shewfelt R.L. Does the alternative pathway ameliorate chilling injury in sensitive plant tissues. Physiol. Plant. 88 (1993) 712-718
112. Påhlman I.L., Larsson C., Averet N., Bunoust O., Boubekeur S., Gustafsson L., and Rigoulet M. Kinetic regulation of the mitochondrial glycerol-3-phosphate dehydrogenase by the external NADH dehydrogenase in Saccharomyces cerevisiae. J. Biol. Chem. 277 (2002) 27991-27995
113. Raghavendra A.S., and Padmasree K. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8 (2003) 546-553
114. Raha S., Myint A.T., Johnstone L., and Robinson B.H. Control of oxygen free radical formation from mitochondrial complex I: roles for protein kinase A and pyruvate dehydrogenase kinase. Free Radical Biol. Med. 32 (2002) 421-430
115. Rasmusson, A.G., 1994. Turnover of matrix NADPH and NADH in plant mitochondria. Doctoral Thesis. Lund University. ISBN: 91-628-1143-6.
116. Rasmusson A.G., and Agius S.C. Rotenone-insensitive NAD(P)H dehydrogenases in plants: immunodetection and distribution of native proteins in mitochondria. Plant Physiol. Biochem. 39 (2001) 1057-1066
117. Rasmusson A.G., and Escobar M.A. Light and diurnal regulation of plant respiratory gene expression. Physiol. Plant. 129 (2007) 57-67
118. Rasmusson A.G., Heiser V., Zabaleta E., Brennicke A., and Grohmann L. Physiological, biochemical and molecular aspects of mitochondrial complex I in plants. Biochim. Biophys. Acta 1364 (1998) 101-111
119. Rasmusson A.G., and Møller I.M. Effect of calcium ions and inhibitors on internal NAD(P)H dehydrogenases in plant mitochondria. Eur. J. Biochem. 202 (1991) 617-623
120. Rasmusson A.G., and Møller I.M. NAD(P)H dehydrogenases on the inner surface of the inner mitochondrial membrane studied using inside-out submitochondrial particles. Physiol. Plant. 83 (1991) 357-365
121. Rasmusson A.G., Soole K.L., and Elthon T.E. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu. Rev. Plant Biol. 55 (2004) 23-39
122. Rasmusson A.G., Svensson A.S., Knoop V., Grohmann L., and Brennicke A. Homologues of yeast and bacterial rotenone-insensitive NADH dehydrogenases in higher eukaryotes: two enzymes are present in potato mitochondria. Plant J. 20 (1999) 79-87
123. Rayapati P.J., and Stewart C.R. Solubilization of a proline dehydrogenase from maize (Zea mays L) mitochondria. Plant Physiol. 95 (1991) 787-791
124. Rhoads D.M., and Subbaiah C.C. Mitochondrial retrograde regulation in plants. Mitochondrion 7 (2007) 177-194
125. Rigoulet M., Aguilaniu H., Averet N., Bunoust O., Camougrand N., Grandier-Vazeille X., Larsson C., Pahlman I.L., Manon S., and Gustafsson L. Organization and regulation of the cytosolic NADH metabolism in the yeast Saccharomyces cerevisiae. Mol. Cell. Biochem. (2004) 73-81
126. Roberts T.H., Fredlund K.M., and Møller I.M. Direct evidence for the presence of two external NAD(P)H dehydrogenases coupled to the electron transport chain in plant mitochondria. FEBS Lett. 373 (1995) 307-309
127. Rugolo M., Antognoni F., Flamigni A., and Zannoni D. Effects of polyamines on the oxidation of exogenous NADH by Jerusalem artichoke (Helianthus tuberosus) mitochondria. Plant Physiol. 95 (1991) 157-163
128. Runswick M.J., Fearnley I.M., Skehel J.M., and Walker J.E. Presence of an acyl carrier protein in NADH-ubiquinone oxidoreductase from bovine heart-mitochondria. FEBS Lett. 286 (1991) 121-124
129. + and the potential role of external malate dehydrogenase. Plant Physiol. Biochem. 27 (1989) 855-862
130. Sabar M., De Paepe R., and de Kouchkovsky Y. Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol. 124 (2000) 1239-1249
131. Sackmann U., Zensen R., Röhlen D., Jahnke U., and Weiss H. The acyl-carrier protein in Neurospora crassa mitochondria is a subunit of NADH-ubiquinone reductase (complex I). Eur. J. Biochem. 200 (1991) 463-469
132. Sakano K. Metabolic regulation of pH in plant cells: Role of cytoplasmic pH in defense reaction and secondary metabolism. Internat. Rev. Cytol. 206 (2001) 1-44
133. Seo B.B., Kitajima-Ihara T., Chan E.K.L., Scheffler I.E., Matsuno-Yagi A., and Yagi T. Molecular remedy of complex I defects: Rotenone-insensitive internal NADH-quinone oxidoreductase of Saccharomyces cerevisiae mitochondria restores the NADH oxidase activity of complex I-deficient mammalian cells. Proc. Natl. Acad. Sci. USA 95 (1998) 9167-9171
134. Shen W., Wei Y., Dauk M., Zheng Z., and Zou J. Identification of a mitochondrial glycerol-3-phosphate dehydrogenase from Arabidopsis thaliana: evidence for a mitochondrial glycerol-3-phosphate shuttle in plants. FEBS Lett. 536 (2003) 92-96
135. + ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 18 (2006) 422-441
136. Siedow J.N., and Umbach A.L. Plant mitochondrial electron transfer and molecular biology. Plant Cell 7 (1995) 821-831
137. Singla-Pareek S.L., Reddy M.K., and Sopory S.K. Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proc. Natl. Acad. Sci. USA 100 (2003) 14672-14677
138. Singla-Pareek S.L., Yadav S.K., Pareek A., Reddy M.K., and Sopory S.K. Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol. 140 (2006) 613-623
139. Svensson A.S., Johansson F.I., Møller I.M., and Rasmusson A.G. Cold stress decreases the capacity for respiratory NADH oxidation in potato leaves. FEBS Lett. 517 (2002) 79-82
140. Svensson A.S., and Rasmusson A.G. Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J. 28 (2001) 73-82
141. Sweetlove L.J., Fait A., Nunes-Nesi A., Williams T., and Fernie A.R. The mitochondrion: an integration point of cellular metabolism and signalling. Crit. Rev. Plant Sci. 26 (2007) 17-43
142. Sweetlove L.J., Lytovchenko A., Morgan M., Nunes-Nesi A., Taylor N.L., Baxter C.J., Eickmeier I., and Fernie A.R. Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc. Natl. Acad. Sci. USA 103 (2006) 19587-19592
143. Valpuesta V., and Botella M.A. Biosynthesis of l-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci. 9 (2004) 573-577
144. Vanlerberghe G.C., and McIntosh L. Alternative oxidase: from gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 (1997) 703-734
145. Verbruggen N., Hua X.J., May M., and VanMontagu M. Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proc. Natl. Acad. Sci. USA 93 (1996) 8787-8791
146. Vercesi A.E., Borecky J., de Godoy Maia I., Arruda P., Cuccovia I.M., and Chaimovich H. Plant uncoupling mitochondrial proteins. Annu. Rev. Plant Biol. 57 (2006) 383-404
147. Vidal G., Ribas-Carbo M., Garmier M., Dubertret G., Rasmusson A.G., Mathieu C., Foyer C.H., and 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 19 (2007) 640-655
148. Vidi P.A., Kanwischer M., Baginsky S., Austin J.R., Csucs G., Dörmann P., Kessler F., and Brehelin C. Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J. Biol. Chem. 281 (2006) 11225-11234
149. Vision T.J., Brown D.G., and Tanksley S.D. The origins of genomic duplications in Arabidopsis. Science 290 (2000) 2114-2117
150. Wiskich J.T., Bryce J.H., Day D.A., and Dry I.B. Evidence for metabolic domains within the matrix compartment of pea leaf mitochondria - implications for photorespiratory metabolism. Plant Physiol. 93 (1990) 611-616
151. Wolucka B.A., and Van Montagu M. GDP-mannose 3',5'-epimerase forms GDP-l-gulose, a putative intermediate for the de novo biosynthesis of vitamin c in plants. J. Biol. Chem. 278 (2003) 47483-47490
152. Ytterberg A.J., Peltier J.B., and van Wijk K.J. Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol. 140 (2006) 984-997
153. Zhang Q., Piston D.W., and Goodman R.H. Regulation of corepressor function by nuclear NADH. Science 295 (2002) 1895-1897
154. Zottini M., Mandolino G., and Zannoni D. Oxidation of external NAD(P)H by mitochondria from taproots and tissue cultures of sugar beet (Beta vulgaris). Plant Physiol. 102 (1993) 579-585