Regulation of respiration in plants: A role for alternative metabolic pathways

Journal of Plant Physiology

Volumn 168, Issue 12, 2011, Pages 1434-1443

  van Dongen, Joost T ^a   Gupta, Kapuganti J ^a   Ramírez Aguilar, Santiago J ^a   Araújo, Wagner L ^a   Nunes Nesi, Adriano ^a   Fernie, Alisdair R ^a  

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

Author keywords

Glycolysis; Mitochondria; Oxidative phosphorylation; Respiration; TCA cycle

Indexed keywords

CYTOCHROME; OXYGEN; VEGETABLE PROTEIN;

CELL RESPIRATION; DRUG EFFECT; ENZYMOLOGY; METABOLISM; PLANT; REVIEW;

CELL RESPIRATION; CYTOCHROMES; METABOLIC NETWORKS AND PATHWAYS; OXYGEN; PLANT PROTEINS; PLANTS;

EID: 79958769533     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2010.11.004     Document Type: Review

References (151)

1. Acín-Pérez R., Bayona-Bafaluy M.P., Fernández-Silva P., Moreno-Loshuertos R., Pérez-Martos A., Bruno C., et al. Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol Cell 2004, 13:805-815.
2. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004, 55:373-399.
3. Araújo W.L., Nunes-Nesi A., Trenkamp S., Bunik V.I., Fernie A.R. Inhibition of 2-oxoglutarate dehydrogenase in potato tuber suggests the enzyme is limiting for respiration and confirms its importance in nitrogen assimilation. Plant Physiol 2008, 148:1782-1796.
4. Araújo W.L., Ishizaki K., Nunes-Nesi A., Larson T.R., Tohge T., Krahnert I., et al. Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 2010, 22:1549-1563.
5. Armstrong W., Strange M.E., Cringle S., Beckett P.M. Microelectrode and modelling study of oxygen distribution in roots. Ann Bot 1994, 74:287-299.
6. Atkin O.K., Evans J.R., Ball M.C., Lambers H., Pons T.L. Leaf respiration of snow gum in the light and dark. Interactions between temperature and irradiance. Plant Physiol 2000, 122:915-923.
7. Bailey-Serres J., Voesenek L.A. Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 2008, 59:313-339.
8. Balmer Y., Vensel W.H., Tanaka C.K., Hurkman W.J., Gelhaye E., Rouhier N., et al. Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 2004, 101:2642-2647.
9. Benamar A., Rolletschek H., Borisjuk L., Avelange-Macherel M.H., Curien G., Mostefai H.A., et al. Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 2008, 1777:1268-1275.
10. Bendall D.S., Bonner W.D. Cyanide-insensitive respiration in plant mitochondria. Plant Physiol 1971, 47:236-245.
11. Berthold D.A., Andersson M.E., Nordlund P. New insights into the structure and function of the alternative oxidase. Biochim Biophys Acta 2000, 1460:241-254.
12. Boekema E.J., Braun H.P. Supramolecular structure of the mitochondrial oxidative phosphorylation system. J Biol Chem 2007, 5:1-4.
13. Bologa K.L., Fernie A.R., Leisse A., Loureiro M.E., Geigenberger P. A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers. Plant Physiol 2003, 132:2058-2072.
14. Borecký J., Vercesi A.E. Plant uncoupling mitochondrial protein and alternative oxidase: energy metabolism and stress. Biosci Rep 2005, 25:271-286.
15. Borecký J., Maia I.G., Costa A.D.T., Jezek P., Chaimovich H., de Andrade P.B.M., et al. Functional reconstitution of Arabidopsis thaliana plant uncoupling mitochondrial protein (AtPUMP1) expressed in Escherichia coli. FEBS Lett 2001, 505:240-244.
16. Borisjuk L., Rolletschek H. The oxygen status of the developing seed. New Phytol 2009, 182:17-30.
17. Braun H.P., Zabaleta E. Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (complex I) in plants. Physiol Plant 2007, 129:114-122.
18. Buchanan-Wollaston V., Page T., Harrison E., Breeze E., Lim P.O., Nam H.G., et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 2005, 42:567-585.
19. Bunik V.I., Fernie A.R. Metabolic control exerted by the 2-oxoglutarate dehydrogenase reaction: a cross-kingdom comparison of the crossroad between energy production and nitrogen assimilation. Biochem J 2009, 27:405-421.
20. Burke P.V., Poyton R.O. Structure/function of oxygen-regulated isoforms in cytochrome c oxidase. J Exp Biol 1998, 201:1163-1175.
21. Bykova N.V., Egsgaard H., Møller I.M. Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett 2003, 540:141-146.
22. Carrari F., Nunes-Nesi A., Gibon Y., Lytovchenko A., Loureiro M.E., Fernie A.R. Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiol 2003, 133:1322-1335.
23. Carroll A.D., Fox G.G., Laurie S., Phillips R., Ratcliffe R.G., Stewart G.R. Ammonium assimilation and the role of Y-aminobutyric acid in pH homeostasis in carrot cell suspensions. Plant Physiol 1994, 106:513-520.
24. Chivasa S., Ndimba B.K., Simon W.J., Lindsey K., Slabas A.R. Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 2005, 17:3019-3034.
25. Cho Y.H., Yoo S.D., Sheen J. Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 2006, 127:579-589.
26. Cousins A.B., Pracharoenwattana I., Zhou W., Smith S.M., Badger M.R. Peroxisomal malate dehydrogenase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release. Plant Physiol 2008, 148:786-795.
27. Crawford L.A., Bown A.W., Breitkreuz K.E., Guinel F.C. The synthesis of [gamma]-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiol 1994, 104:865-871.
28. Davies H.V., Shepherd L.V.T., Burrell M.M., Carrari F., Urbanczyk-Wochniak E., Leisse A., et al. Modulation of fructokinase activity of potato (Solanum tuberosum) results in substantial shifts in tuber metabolism. Plant Cell Physiol 2005, 46:1103-1115.
29. de Sousa C.A.F., Sodek L. Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and subsequent return to normoxia. Environ Exp Bot 2003, 50:1-8.
30. Diaz F., Fukui H., Garcia S., Moraes C.T. Cytochrome c oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol Cell Biol 2006, 26:4872-4881.
31. Dodd A.N., Kudla J., Sanders D. The language of calcium signaling. Annu Rev Plant Biol 2010, 61:593-620.
32. Drew M.C., He C.J., Morgan P.W. Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 2000, 5:123-127.
33. Dudkina N.V., Eubel H., Keegstra W., Boekema E.J., Braun H.P. Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III. Proc Natl Acad Sci USA 2005, 102:3225-3229.
34. Dutilleul C., Garmier M., Noctor G., Mathieu C., Chetrit P., Foyer C.H., et al. 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.
35. 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.
36. Engqvist M., Drincovich M.F., Flügge U.I., Maurino V.G. Two d-2-hydroxy-acid dehydrogenases in Arabidopsis thaliana with catalytic capacities to participate in the last reactions of the methylglyoxal and beta-oxidation pathways. J Biol Chem 2009, 284:25026-25037.
37. Eubel H., Jansch L., Braun H.P. New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II. Plant Physiol 2003, 133:274-286.
38. Eubel H., Heinemeyer J., Sunderhaus S., Braun H.P. Respiratory chain supercomplexes in plant mitochondria. Plant Physiol Biochem 2004, 42:937-942.
39. Felle H.H. pH: signal and messenger in plant cells. Plant Biol 2001, 3:577-591.
40. Felle H.H. pH regulation in anoxic plants. Ann Bot 2005, 96:519-532.
41. Fernie A.R., Tauberger E., Lytovchenko A., Roessner U., Willmitzer L., Trethewey R.N. Antisense repression of cytosolic phosphoglucomutase in potato (Solanum tuberosum) results in severe growth retardation, reduction in tuber number and altered carbon metabolism. Planta 2002, 214:510-520.
42. Fernie A.R., Tiessen A., Stitt M., Willmitzer L., Geigenberger P. Altered metabolic fluxes result from shifts in metabolite levels in sucrose phosphorylase-expressing potato tubers. Plant Cell Environ 2002, 25:1219-1232.
43. Fernie A.R., Carrari F., Sweetlove L.J. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 2004, 7:254-261.
44. Finnegan P.F., Soole K.L., Umbach A.L. Alternative mitochondrial electron transport proteins in higher plants. Plant mitochondria: from genome to function 2004, Kluwer Academic Publishers, Dordrecht. D.A. Day, A.H. Millar, J. Whelan (Eds.).
45. Fiorani F., Umbach A.L., Siedow J.N. The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol 2005, 139:1795-1805.
46. Frerman F.E. Reaction of electron-transfer flavoprotein ubiquinone oxidoreductase with the mitochondrial respiratory chain. Biochim Biophys Acta 1987, 893:161-169.
47. Frerman F.E. Acyl-CoA dehydrogenases, electron transfer flavoprotein and electron transfer flavoprotein dehydrogenase. Biochem Soc Trans 1988, 16:416-418.
48. Garmier M., Carroll A.J., Delannoy E., Vallet C., Day D.A., Small I.D., et al. Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol 2008, 148:1324-1341.
49. Geigenberger P. Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 2003, 6:247-256.
50. Geigenberger P., Fernie A.R., Gibon Y., Christ M., Stitt M. Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol Chem 2000, 381:723-740.
51. Geigenberger P., Regierer B., Nunes-Nesi A., Leisse A., Urbanczyk-Wochniak E., Springer F., et al. Inhibition of de novo pyrimidine synthesis in growing potato tubers leads to a compensatory stimulation of the pyrimidine salvage pathway and a subsequent increase in biosynthetic performance. Plant Cell 2005, 17:2077-2088.
52. Geigenberger P., Riewe D., Fernie A.R. The central regulation of plant physiology by adenylates. Trends Plant Sci 2010, 15:98-105.
53. Geisler D.A., Broselid C., Hederstedt L., Rasmusson A.G. Ca2+-binding and Ca2+-independent respiratory NADH and NADPH dehydrogenases of Arabidopsis thaliana. J Biol Chem 2007, 282:28455-28464.
54. Gelhaye E., Rouhier N., Gérard J., Jolivet Y., Gualberto J., Navrot N., et al. A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci USA 2004, 101:14545-14550.
55. Giege P., Heazlewood J.L., Roessner-Tunali U., Millar A.H., Fernie A.R., Leaver C.J., et al. Enzymes of glycolysis are functionally associated with the mitochondrion of Arabidopsis cells. Plant Cell 2003, 15:2140-2151.
56. Graham J.W., Williams T.C., Morgan M., Fernie A.R., Ratcliffe R.G., Sweetlove L.J. Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 2007, 19:3723-3738.
57. Gu L., Jones A.D., Last R.L. Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. Plant J 2010, 61:579-590.
58. Gupta K.J., Zabalza A., van Dongen J.T. Regulation of respiration when the oxygen availability changes. Physiol Plant 2009, 137:383-391.
59. Hajirezaei M.R., Sonnewald U., Viola R., Carlise S., Dennis S., Stitt M. Transgenic potato plants with strongly decreased expression of pyrophosphate-fructose-6-phosphate phosphotransferase show no visible phenotype and only minor changes in metabolic fluxes in their tubers. Planta 1994, 192:16-30.
60. Hajirezaei M.R., Biemelt S., Peisker M., Lytovchenko A., Fernie A.R., Sonnewald U. The influence of cytosolic phosphorylating glyceraldehyde 3-phosphate dehydrogenase (GAPC) on potato tuber metabolism. J Exp Bot 2006, 57:2363-2377.
61. Heazlewood J.L., Millar A.H. AMPDB: the Arabidopsis mitochondrial protein database. Nucleic Acids Res 2005, 33:605-610.
62. Heinemeyer J., Lewejohann D., Braun H.P. Blue-native gel electrophoresis for the characterization of protein complexes in plants. Methods Mol Biol 2007, 355:343-352.
63. Hoefnagel M., Rich P.R., Zhang Q., Wiskich J.T. Substrate kinetics of the plant mitochondrial alternative oxidase and the effects of pyruvate. Plant Physiol 1997, 115:1145-1153.
64. Huang S., Colmer T.D., Millar A.H. Does anoxia tolerance involve altering the energy currency towards PPi?. Trends Plant Sci 2008, 13:221-227.
65. Huang S., Taylor N.L., Narsai R., Eubel H., Whelan J., Millar A.H. Experimental analysis of the rice mitochondrial proteome, its biogenesis, and heterogeneity. Plant Physiol 2009, 149:719-734.
66. Ishizaki K., Larson T.R., Schauer N., Fernie A.R., Graham I.A., Leaver C.J. The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 2005, 17:2587-2600.
67. Ishizaki K., Schauer N., Larson T.R., Graham I.A., Fernie A.R., Leaver C.J. The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J 2006, 47:751-760.
68. Ito J., Taylor N.L., Castleden I., Weckwerth W., Millar A.H., Heazlewood J.L. Survey of the Arabidopsis thaliana mitochondrial phosphoproteome. Proteomics 2009, 17:4229-4240.
69. Jezek P., Houstek J., Drahota Z. Alkaline pH, membrane-potential, and magnesium cations are negative modulators of purine nucleotide inhibition of H+ and Cl- transport through the uncoupling protein of brown adipose-tissue mitochondria. J Bioenerg Biomembr 1988, 20:603-622.
70. Jezek P., Costa A.D.T., Vercesi A.E. Evidence for anion-translocating plant uncoupling mitochondrial protein in potato mitochondria. J Biol Chem 1996, 271:32743-32748.
71. Kadenbach B., Ramzan R., Wen L., Vogt S. New extension of the Mitchell Theory for oxidative phosphorylation in mitochondria of living organisms. Biochim Biophys Acta 2010, 1800:205-212.
72. Kolbe A., Oliver S.N., Fernie A.R., Stitt M., van Dongen J.T., Geigenberger P. Combined transcript and metabolite profiling of Arabidopsis leaves reveals fundamental effects of the thiol-disulfide status on plant metabolism. Plant Physiol 2006, 141:412-422.
73. Krause F., Scheckhuber C.Q., Werner A., Rexroth S., Reifschneider N.H., Dencher N.A., et al. Supramolecular organization of cytochrome c oxidase- and alternative oxidase-dependent respiratory chains in the filamentous fungus Podospora anserina. J Biol Chem 2004, 18:26453-26461.
74. Lambers H. Cyanide resistant respiration: a nonphosphorylating electron transport pathway acting as an energy overflow. Plant Physiol 1982, 55:478-485.
75. Lancien M., Ferrario-Mery S., Roux V., Bismuth E., Masclaux C., Hirel B., et al. Simultaneous expression of NAD-dependent isocitrate dehydrogenase and other Krebs cycle genes after nitrate resupply to short-term nitrogen-starved tobacco. Plant Physiol 1999, 120:717-725.
76. Lee C.P., Eubel H., O'Toole N., Millar A.H. Heterogeneity of the mitochondrial proteome for photosynthetic and non-photosynthetic Arabidopsis metabolism. Mol Cell Proteomics 2008, 7:1297-1316.
77. Lehmann M., Schwarzlander M., Obata T., Sirikantaramas A., Burow M., Olsen C., et al. The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Mol Plant 2009, 2:390-406.
78. Lemire J., Mailloux R., Auger C., Whalen D., Appanna V.D. Pseudomonas fluorescens orchestrates a fine metabolic-balancing act to counter aluminium toxicity. Environ Microbiol 2010, 12:1384-1390.
79. Mackenzie S., McIntosh L. Higher plant mitochondria. Plant Cell 1999, 11:571-585.
80. Maxwell D.P., Wang Y., McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 1999, 96:8271-8276.
81. McCammon M.T., Epstein C.B., Przybyla-Zawislak B., McAlister-Henn L., Butow R.A. Global transcription analysis of Krebs tricarboxylic acid cycle mutants reveals an alternating pattern of gene expression and effects on hypoxic and oxidative genes. Mol Biol Cell 2003, 14:958-967.
82. McDonald A.E., Vanlerberghe G.C. Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp Biochem Physiol 2006, 1:357-364.
83. Melo A.M., Duarte M., Møller I.M., Prokisch H., Dolan P.L., Pinto L., et al. The external calcium-dependent NADPH dehydrogenase from Neurospora crassa mitochondria. J Biol Chem 2001, 276:3947-3951.
84. Michalecka A.M., Svensson A.S., Johansson F.I., Agius S.C., Johanson U., Brennicke A., et al. Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol 2003, 133:642-652.
85. Michalecka A.M., Agius S.C., Møller I.M., Rasmusson A.G. Identification of a mitochondrial external NADPH dehydrogenase by overexpression in transgenic Nicotiana sylvestris. Plant J 2004, 3:415-425.
86. Millar A.H., Wiskich J.T., Whelan J., Day D.A. Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett 1993, 329:259-262.
87. Millar A.H., Hoefnagel M.H.N., Day D.A., Wiskich J.T. Specificity of the organic acid activation of alternative oxidase in plant mitochondria. Plant Physiol 1996, 111:613-618.
88. Miyashita Y., Dolferus R., Ismond K.P., Good A.G. Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana. Plant J 2007, 49:1108-1112.
89. 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 1997, 100:85-90.
90. Møller I.M. Plant mitochondria and oxidative stress: electron transport. NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Phys 2001, 52:561-591.
91. Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT. Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytologist, doi:10.1111/j.1469-8137.2010.03589.x.
92. Navet R., Douette P., Puttine-Marique F., Sluse-Goffart C.M., Jarmuszkiewicz W., Sluse F.E. Regulation of uncoupling protein activity in phosphorylating potato tuber mitochondria. FEBS Lett 2005, 579:4437-4442.
93. Nicholls D.G., Locke R.M. Thermogenic mechanisms in brown fat. Physiol Rev 1984, 64:1-64.
94. Nunes-Nesi A., Carrari F., Lytovchenko A., Smith A.M.O., Loureiro M.E., Ratcliffe R.G., et al. Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 2005, 137:611-622.
95. Nunes-Nesi A., Carrari F., Gibon Y., Sulpice R., Lytovchenko A., Fisahn J., et al. Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 2007, 50:1093-1106.
96. Oliver S.N., Lunn J.E., Urbanczyk-Wochniak E., Lytovchenko A., van Dongen J.T., Faix B., et al. Decreased expression of cytosolic pyruvate kinase in potato tubers leads to a decline in pyruvate resulting in an in vivo repression of the alternative oxidase. Plant Physiol 2008, 148:1640-1654.
97. Pilkis S.J., Granner D.K. Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Physiol 1992, 54:885-889.
98. Plaxton W.C. The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 1996, 47:185-214.
99. Plaxton W.C., Podesta F.E. The functional organization and control of plant respiration. Crit Rev Plant Sci 2006, 25:159-198.
100. Podesta F.E., Plaxton W.C. Kinetic and regulatory properties of cytosolic pyruvate kinase from germinating castor oil seeds. Biochem J 1991, 279:495-501.
101. Podesta F.E., Plaxton W.C. Association of phosphoenolpyruvate phosphatase activity with the cytosolic pyruvate kinase of germinating mung beans. Plant Physiol 1991, 97:1329-1333.
102. Puntarulo S., Cederbaum A.I. Effect of oxygen concentration on microsomal oxidation of ethanol and generation of oxygen radicals. Biochem J 1988, 251:787-794.
103. Rasmusson A.G., Svensson A.S., Knoop V., Grohmann L., Brennicke A. Homologues of yeast and bacterial rotenone-insensitive NADH dehydrogenases in higher eukaryotes: two enzymes are present in potato mitochondria. Plant J 1999, 20:79-87.
104. Rasmusson A.G., Soole K.L., Elthon T.E. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu Rev Plant Biol 2004, 55:23-39.
105. Rasmusson A.G., Geisler D.A., Møller I.M. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 2008, 8:47-60.
106. Rasmusson A.G., Fernie A.R., van Dongen J.T. Alternative oxidase: a defence against metabolic fluctuations?. Physiol Plant 2009, 137:371-382.
107. Reggiani R., Hochkoeppler A., Bertani A. Polyamines in rice seedlings under oxygen-deficit stress. Plant Physiol 1989, 91:1197-1201.
108. Reggiani R., Nebuloni M., Mattana M., Brambilla I. Anaerobic accumulation of amino acids in rice roots: role of the glutamine synthetase/glutamate synthase cycle. Amino Acids 2000, 18:207-217.
109. Regierer B., Fernie A.R., Springer F., Perez-Melis A., Leisse A., Koehl K., et al. Starch content and yield increase as a result of altering adenylate pools in transgenic plants. Nat Biotechnol 2002, 20:1256-1260.
110. Rhoads D.M., Umbach A.L., Sweet C.R., Lennon A.M., Rauch G.S., Siedow J.N. Regulation of the cyanide-resistant alternative oxidase of plant mitochondria. Identification of the cysteine residue involved in alpha-keto acid stimulation and intersubunit disulfide bond formation. J Biol Chem 1998, 13:30750-30756.
111. Rial E., Poustie A., Nicholls D.G. Brown-adipose-tissue mitochondria - the regulation of the 32000-Mr uncoupling protein by fatty-acids and purine nucleotides. Eur J Biochem 1983, 137:197-203.
112. Ribas-Carbo M., Berry J.A., Yakir D., Giles L., Robinson S.A., Lennon A.M., et al. Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. Plant Physiol 1995, 109:829-837.
113. Rocha M., Licausi F., Araújo W.L., Nunes-Nesi A., Sodek L., Fernie A.R., et al. Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 2010, 152:1501-1513.
114. Rocha M., Sodek L., Licausi F., Hameed M.W., Dornelas M.C., van Dongen J.T. Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress. Amino Acids 2010, 39:1043-1053.
115. Saviani E.E., Da Silva A.J., Martins I.S. Photoaffinity labelling of the uncoupling protein from potato tuber mitochondria. Plant Physiol Biochem 1997, 35:701-706.
116. Schäfer E., Dencher N.A., Vonck J., Parcej D.N. Three-dimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria. Biochemistry 2007, 6:12579-12585.
117. Schägger H., Pfeiffer K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 2000, 19:1777-1783.
118. Schägger H., Pfeiffer K. The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexes. J Biol Chem 2001, 276:37861-37867.
119. Semenza G.L. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J 2007, 405:1-9.
120. Shen W., Wei Y., Dauk M., Zheng Z., 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 2003, 11:92-96.
121. Shen W., Wei Y., Dauk M., Tan Y., Taylor D.C., Selvaraj G., et al. Involvement of a glycerol-3-phosphate dehydrogenase in modulating the NADH/NAD+ ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 2006, 18:422-441.
122. Sienkiewicz-Porzucek A., Nunes-Nesi A., Sulpice R., Lisec J., Centeno D.C., Carillo P., et al. Mild reductions in mitochondrial citrate synthase activity result in a compromised nitrate assimilation and reduced leaf pigmentation but have no effect on photosynthetic performance or growth. Plant Physiol 2008, 147:115-127.
123. Sienkiewicz-Porzucek A., Sulpice R., Osorio S., Krahnert I., Leisse A., Urbanczyk-Wochniak E., et al. Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Mol Plant 2010, 3:156-173.
124. Singh R., Lemire J., Mailloux R.J., Chenier D., Hamel R., Appanna V.D. An ATP and oxalate generating variant tricarboxylic acid cycle counters aluminum toxicity in Pseudomonas fluorescens. PLoS ONE 2009, 4:e7344.
125. Skutnik M., Rychter A.M. Differential response of antioxidant systems in leaves and roots of barley subjected to anoxia and post-anoxia. J Plant Physiol 2009, 166:926-937.
126. Smith A.M.O., Ratcliffe R.G., Sweetlove L.J. Activation and function of mitochondrial uncoupling protein in plants. J Biol Chem 2004, 279:51944-51952.
127. Studart-Guimarães C., Fait A., Nunes-Nesi A., Carrari F., Usadel B., Fernie A.R. Reduced expression of succinyl-coenzyme a ligase can be compensated for by up-regulation of the - aminobutyrate shunt in illuminated tomato leaves. Plant Physiol 2007, 145:626-639.
128. Sweetlove L.J., Lytovchenko A., Morgan M., Nunes-Nesi A., Taylor N.L., Baxter C.J., et al. Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc Natl Acad Sci USA 2006, 103:19587-19592.
129. Sweetlove L.J., Beard K.F., Nunes-Nesi A., Fernie A.R., Ratcliffe R.G. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 2010, 15:462-470.
130. Tadege M., Dupuis I.I., Kuhlemeier C. Ethanolic fermentation: new functions for an old pathway. Trends Plant Sci 1999, 4:320-325.
131. Teusink B., Passarge J., Reijenga C.A., Esgalhado E., van der Weijden C.C., Schepper M., et al. Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur J Biochem 2000, 267:5313-5329.
132. Tielens A.G.M., Van Hellemond J.J. The electron transport chain in anaerobically functioning eukaryotes. BBA Bioenerg 1998, 1365:71-78.
133. Timm S., Nunes-Nesi A., Pärnik T., Morgenthal K., Wienkoop S., Keerberg O., et al. A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 2008, 20:2848-2859.
134. Umbach A.L., Ng V.S., Siedow J.N. Regulation of plant alternative oxidase activity: a tale of two cysteines. Biochim Biophys Acta 2006, 1757:135-142.
135. Urbanczyk-Wochniak E., Usadel B., Thimm O., Nunes-Nesi A., Carrari F., Davy M., et al. Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Mol Biol 2006, 60:773-792.
136. van der Merwe M.J., Osorio S., Moritz T., Nunes-Nesi A., Fernie A.R. Decreased mitochondrial activities of malate dehydrogenase and fumarase in tomato lead to altered root growth and architecture via diverse mechanisms. Plant Physiol 2009, 149:653-669.
137. van der Merwe M.J., Osorio S., Araújo W.L., Balbo I., Nunes-Nesi A., Maximova E., et al. Tricarboxylic acid cycle activity regulates tomato root growth via effects on secondary cell wall production. Plant Physiol 2010, 153:611-621.
138. van Dongen J.T., Schurr U., Pfister M., Geigenberger P. Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 2003, 131:1529-1543.
139. van Dongen J.T., Roeb G.W., Dautzenberg M., Froehlich A., Vigeolas H., Minchin P.E., et al. Phloem import and storage metabolism are highly coordinated by the low oxygen concentrations within developing wheat seeds. Plant Physiol 2004, 135:1809-1821.
140. van Dongen J.T., Fröhlich A., Ramírez-Aguilar S.J., Schauer N., Fernie A.R., Erban A., et al. Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot 2009, 103:269-280.
141. Vanlerberghe G.C., McIntosh L. Alternative oxidase: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:703-734.
142. Vanlerberghe G.C., Horsey A.K., Weger H.G., Turpin D.H. Anaerobic carbon metabolism by the tricarboxylic acid cycle: Evidence for partial oxidative and reductive pathways during dark ammonium assimilation. Plant Physiol 1989, 91:1551-1557.
143. Vanlerberghe G.C., Feil R., Turpin D.H. Anaerobic metabolism in the N-limited green alga Selenastrum minutum: I. Regulation of carbon metabolism and succinate as a fermentation product. Plant Physiol 1990, 94:1116-1123.
144. Veramendi J., Fernie A.R., Leisse A., Willmitzer L., Trethewey R.N. Potato hexokinase 2 complements transgenic Arabidopsis plants deficient in hexokinase 1 but does not play a key role in tuber carbohydrate metabolism. Plant Mol Biol 2002, 49:491-501.
145. Vercesi A.E., Borecký J., Maia Ide G., Arruda P., Cuccovia I.M., Chaimovich H. Plant uncoupling mitochondrial proteins. Annu Rev Plant Biol 2006, 57:383-404.
146. Vercesi A.E., Martins I.S., Silva M.A.P., Leite H.M.F., Cuccovia I.M., Chaimovich H. Pumping plants. Nature 1995, 375:24-124.
147. Westram A., Lloyd J.R., Rossner U., Riesmeier J.W., Kossmann J. Increases of 3-phosphoglyceric acid in potato plants through antisense reduction of cytoplasmic phosphoglycerate mutase impairs photosynthesis and growth, but does not increase starch contents. Plant Cell Environ 2002, 25:1133-1143.
148. Winkler C., Delvos B., Martin W., Henze K. Purification, microsequencing and cloning of spinach ATP-dependent phosphofructokinase link sequence and function for the plant enzyme. FEBS J 2007, 274:429-438.
149. Yoshida K., Terashima I., Noguchi K. Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis. Plant Cell Physiol 2006, 47:22-31.
150. Zabalza A., van Dongen J.T., Froehlich A., Oliver S.N., Faix B., Gupta K.J., et al. Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 2009, 149:1087-1098.
151. Zimmermann P., Hirsch-Hoffmann M., Henning L., Gruissem W. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 2004, 136:2621-2632.