Inhibition of 2-oxoglutarate dehydrogenase in potato tuber suggests the enzyme is limiting for respiration and confirms its importance in nitrogen assimilation

Plant Physiology

Volumn 148, Issue 4, 2008, Pages 1782-1796

  Araújo, Wagner L ^a   Nunes Nesi, Adriano ^a   Trenkamp, Sandra ^a   Bunik, Victoria I ^b   Fernie, Alisdair R ^a  

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

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

SOLANUM TUBEROSUM; TUBER (TRUFFLE);

EID: 57749098561     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.126219     Document Type: Article

References (92)

1. Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schuurmann P, Droux M, et al (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101: 2642-2647
2. Biryukov AI, Bunik VI, Zhukov YN, Khurs EN, Khomutov RM (1996) Succinyl phosphonate inhibits α-ketoglutarate oxidative decarboxylation, catalyzed by α-ketoglutarate dehydrogenase complexes from E. coli and pigeon breast muscle. FEBS Lett 382: 167-170
3. Bologa KL, Fernie AR, Leisse A, Loureiro ME, Geigenberger P (2003) A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers. Plant Physiol 132: 2058-2072
4. Bowman EJ, Ikuma H, Stein HJ (1976) Citric acid cycle activity in mitochondria isolated from mung bean hypocotyls. Plant Physiol 58: 426-432
5. Bunik VI (2000) Increased catalytic performance of the 2-oxoacid dehydrogenase complexes in the presence of thioredoxin, a thiol-disulfide oxidoreductase. J Mol Catal B Enzym 8: 165-174
6. Bunik VI (2003) 2-Oxo acid dehydrogenase complexes in redox regulation. Eur J Biochem 270: 1036-1042
7. Bunik VI, Biryukov AI, Zhukov Yu N (1992) Inhibition of pigeon breast muscle α-ketoglutarate dehydrogenase by phosphonate analogues of α-ketoglutarate. FEBS Lett 303: 197-201
8. Bunik VI, Denton TT, Xu H, Thompson CM, Cooper AJL, Gibson GE (2005) Phosphonate analogues of alpha-ketoglutarate inhibit the activity of the alpha-ketoglutarate complex isolated from brain and in cultured cells. Biochemistry 44: 10552-10561
9. Bunik VI, Pavlova OG (1997) Inhibition of pigeon breast muscle alpha-ketoglutarate dehydrogenase by structural analogs of alpha-ketoglutarate. Biochemistry (Mosc) 62: 1012-1020
10. Bunik VI, Raddatz G, Wanders R, Reiser G (2006) Brain pyruvate and 2-oxoglutarate dehydrogenase complexes are mitochondrial targets of the CoA ester of the Refsum disease marker phytanic acid. FEBS Lett 580: 3551-3557
11. Bunik VI, Romash OG, Gomazkova VS (1991) Effect of α-ketoglutarate and its structural analogues on hysteretic properties of α-ketoglutarate dehydrogenase. FEBS Lett 278: 147-150
12. Bunik VI, Schloss JV, Pinto JT, Gibson GE, Cooper AJL (2007) Enzyme-catalyzed side reactions with molecular oxygen may contribute to cell signaling and neurodegenerative diseases. Neurochem Res 32: 871-891
13. Bunik VI, Westphal AH, de Kok A (2000) Kinetic properties of the 2-oxoglutarate dehydrogenase complex from Azotobacter vinelandii. Evidence for the formation of a precatalytic complex with 2-oxoglutarate. Eur J Biochem 267: 3583-3591
14. Burton WG (1989) The Potato, Ed 3. Longman Scientific and Technical, Harlow, UK
15. Canvin DT, Beevers H (1961) Sucrose synthesis from acetate in the germinating castor bean: kinetics and pathway. J Biol Chem 236: 988-995
16. Carrari F, Nunes-Nesi A, Gibon Y, Lytovchenko A, Loureiro ME, Fernie AR (2003) 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 133: 1322-1335
17. Chen F-L, Cullimore JV (1988) Two isoenzymes of NADH-dependent glutamate synthase in root nodules of Phaseolus vulgaris L.: purification, properties and activity changes during nodule development. Plant Physiol 88: 1411-1417
18. Cooney GJ, Taegtmeyer H, Newsholme EA (1981) Tricarboxylic acid cycle flux and enzyme activities in the isolated working rat heart. Biochem J 200: 701-703
19. Cornu S, Pireaux JC, Gerard J, Dizengremel P (1996) NAD(P)(+)-dependent isocitrate dehydrogenases in mitochondria purified from Picea abies seedlings. Physiol Plant 96: 312-318
20. Coruzzi G, Last R (2000) Amino acids. In BB Buchanan, W Gruissem, RL Jones, eds, Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD, pp 358-410
21. Craig DW, Wedding RT (1980a) Regulation of the 2-oxoglutarate dehydrogenase lipoate succinyltransferase complex from cauliflower by nucleotide: steady state kinetic studies. J Biol Chem 255: 5763-5768
22. Craig DW, Wedding RT (1980b) Regulation of the 2-oxoglutarate dehydrogenase lipoate succinyltransferase complex from cauliflower by nucleotide: pre-steady state kinetics and physical studies. J Biol Chem 255: 5769-5775
23. Dry IB, Wiskich JT (1985) Inhibition of 2-oxoglutarate oxidation in plant mitochondria by pyruvate. Biochem Biophys Res Commun 133: 397-403
24. Dry IB, Wiskich JT (1987) 2-Oxoglutarate dehydrogenase and pyruvate dehydrogenase activities in plant mitochondria: interaction via a common coenzyme A pool. Arch Biochem Biophys 257: 92-99
25. Dutilleul C, Lelarge C, Prioul JL, De Paepe R, Foyer CH, Noctor G (2005) 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: 64-78
26. Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13: 14-19
27. Fernie AR, Carrari F, Sweetlove LJ (2004a) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport chain. Curr Opin Plant Biol 7: 254-261
28. Fernie AR, Roessner U, Geigenberger P (2001a) The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers (Solanum tuberosum). Plant Physiol 125: 1967-1977
29. Fernie AR, Roessner U, Trethewey RN, Willmitzer L (2001b) The contribution of plastidial phosphoglucomutase to the control of starch synthesis within the potato tuber. Planta 213: 418-426
30. Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001c) Fructose 2,6-bisphosphate activates pyrophosphate:fructose-6-phosphate:1- phosphotransferase and increases triose-phosphate to hexose-phosphate cycling in heterotrophic cells. Planta 212: 250-263
31. Fernie AR, Trethewey RN, Krotzky A, Willmitzer L (2004b) Metabolite profiling: from diagnostics to systems biology. Nat Rev Mol Cell Biol 5: 763-769
32. Foyer CH, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 382: 585-593
33. Fritz C, Mueler C, Matt P, Feil R, Stitt M (2006) Impact of the C-N status on the amino acid profile in tobacco source leaves. Plant Cell Environ 29: 2055-2076
34. Gálvez S, Lancien M, Hodges M (1999) Are isocitrate dehydrogenases and 2-oxoglutarate involved in the regulation of glutamate synthesis? Trends Plant Sci 4: 484-490
35. Geigenberger P, Fernie AR, Gibon Y, Christ M, Stitt M (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol Chem 381: 723-740
36. Geigenberger P, Reimholz R, Geiger M, Merlo L, Canale V, Stitt M (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201: 502-518
37. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Hohne M, Hendriks JHM, Palacios N, Cross J, Selbig J, Stitt M (2004) A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes in enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16: 3304-3325
38. Gibson GE, Blass JP, Flint Beal M, Bunik V (2005) The α-ketoglutarate complex: a mediator between mitochondria and oxidative stress in neurodegeneration. Mol Neurobiol 31: 43-63
39. GiegéP, Heazlewood JL, Roessner-Tunali U, Millar AH, Fernie AR, Leaver CJ, Sweetlove LJ (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15: 2140-2151
40. Hedden P, Kamiya Y (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annu Rev Plant Physiol Plant Mol Biol 48: 431-460
41. Hodges M (2002) Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J Exp Bot 53: 905-916
42. Hodges M, Fleish V, Galves S, Bismuth E (2003) Higher plant NADP dependent isocitrate dehydrogenases, ammonium assimilation and NADPH production. Plant Physiol Biochem 41: 577-585
43. Hooks MA, Turner JE, Murphy EC, Johnston KA, Burr S, Jaroslawski S (2007) The Arabidopsis ALDP protein homologue COMATOSE is instrumental in peroxisomal acetate metabolism. Biochem J 406: 399-406
44. Igamberdiev AU, Gardeström P (2003) 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: 117-125
45. Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ (2005) The critical role of Arabidopsis electron-transfer flavoprotein: ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17: 2587-2600
46. Ishizaki K, Schauer N, Larson TR, Graham IA, Fernie AR, Leaver CJ (2006) The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J 47: 751-760
47. Jenner HL, Winning BM, Millar AH, Tomlinson KM, Leaver CJ, Hill SA (2001) NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiol 126: 1139-1149
48. Journet EP, Bonner WD, Douce R (1982) Glutamate metabolism triggered by oxaloacetate in intact plant mitochondria. Arch Biochem Biophys 214: 366-375
49. Kahl G (1974) Metabolism in plant storage tissue slices. Bot Rev 40: 263-314
50. Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T (2001) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13: 681-693
51. Kolbe A, Oliver SN, Fernie AR, Stitt M, van Dongen JT, Geigenberger P (2006) Combined transcript and metabolite profiling of Arabidopsis leaves reveals fundamental effects of the thiol-disulfide status on plant metabolism. Plant Physiol 141: 412-422
52. Kopka J, Schauer N, Krueger S, Birkmeyer C, Usadel B, Bergmuller E, Dormann P, Weckwerth W, Gibon Y, Stitt M, et al (2005) GMD@CSB. DB: the Golm Metabolome Database. Bioinformatics 21: 1635-1638
53. Kumar MJ, Nicholls DG, Andersen JK (2003) Oxidative alpha-ketoglutarate dehydrogenase inhibitionvia subtle elevations inmonoamine oxidase B levels results in loss of spare respiratory capacity: implications for Parkinson's disease. J Biol Chem 278: 46432-46439
54. Laurent S, Chen H, Bédu S, Ziarelli F, Peng L, Zhang CC (2005) Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. Proc Natl Acad Sci USA 102: 9907-9912
55. Lemaire SD, Guillon B, Le Maréchal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 101: 7475-7480
56. Lemaitre T, Urbanczyk-Wochniak E, Flesch V, Bismuth E, Fernie AR, Hodges M (2007) NAD-dependent isocitrate dehydrogenase mutants of Arabidopsis suggest the enzyme is not limiting for nitrogen assimilation. Plant Physiol 144: 1546-1558
57. Less H, Galili G (2008) Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol 147: 316-30
58. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protocols 1: 387-396
59. McCormack JG, Denton RM (1979) The effects of calcium ions and adenine nucleotides on the activity of pig heart 2-oxoglutarate dehydrogenase complex. Biochem J 180: 533-544
60. Merlo L, Geigenberger P, Hajirezaei M, Stitt M (1993) Changes of carbohydrates, metabolites and enzyme activities in potato tubers during development and within a single tuber along a stolon-apex gradient. J Plant Physiol 142: 392-402
61. Millar AH, Hill SA, Leaver CJ (1999) Plant mitochondrial 2-oxoglutarate dehydrogenase complex: purification and characterization in potato. Biochem J 343: 327-334
62. Millar AH, Knorpp C, Leaver CJ, Hill SA (1998) Plant mitochondrial pyruvate dehydrogenase complex: purification and identification of catalytic components in potato. Biochem J 334: 571-576
63. Millar AH, Leaver CJ (2000) The cytotoxic lipid peroxidation product, 4-hydroxy-2-nonenal, specifically inhibits decarboxylating dehydrogenases in the matrix of plant mitochondria. FEBS Lett 481: 117-121
64. Mü ller C, Scheible WR, Stitt M, Krapp A (2001) Influence of malate and 2-oxoglutarate expression on the NIA transcript level and nitrate reductase activity in tobacco leaves. Plant Cell Environ 24: 191-203
65. +)-isocitrate dehydrogenase and oxoglutarate dehydrogenase from the yeast Saccharomyces cerevisiae and rat heart. Biochem J 303: 461-465
66. Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8: 87-99
67. Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 50: 1093-1106
68. Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AMO, Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 137: 611-622
69. +-linked dehydrogenases from plant mitochondria. Plant Physiol 94: 189-193
70. Picault N, Palmieri L, Pisano I, Hodges M, Palmieri F (2002) Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria: bacterial expression, reconstitution, functional characterization, and tissue distribution. J Biol Chem 277: 24204-24211
71. Plaxton WC, Podesta FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25: 159-198
72. Purnell MP, Skopelitis DS, Roubelakis-Angelakis KA, Botella JR (2005) Modulation of higher-plant NAD(H)-dependent glutamate dehydrogenase activity in transgenic tobacco via alteration of beta subunit levels. Planta 222: 167-180
73. Randall DD, Miernyk JA (1990) The mitochondrial pyruvate dehydrogenase complex. In PJ Lea, ed, Methods in Plant Biochemistry: Enzymes of Primary Metabolism, Vol 3. Academic Press, London, pp 175-199
74. Rasmusson AG, Geisler DA, Møller IM (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8: 47-60
75. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolite profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29
76. 13C labelled isotopes. Plant J 39: 668-679
77. Runquist M, Kruger NJ (1999) Control of gluconeogenesis by isocitrate lyase in endosperm of germinating castor bean seedlings. Plant J 19: 423-431
78. Saito K, Kobayashi M, Tanaka Y, Gong Z, Yamazaki M (1999) Direct evidence for anthocyanidin synthase as a 2 oxoglutarate dependent oxygenase: molecular cloning and functional expression of cDNA from a red form of Perilla frutescens. Plant J 17: 181-189
79. 13C]glutamate metabolism in cerebellar granule neurons. J Neurosci Res 83: 450-458
80. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, et al (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24: 447-454
81. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L, et al (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579: 1332-1337
82. Schneidereit J, Häusler RE, Fiene G, Kaiser WM, Weber APM (2006) Antisense repression reveals a crucial role of the plastidic 2-oxoglutarate/malate translocator DiT1 at the interface between carbon and nitrogen metabolism. Plant J 45: 206-224
83. Schönbrunn-Hanebeck E, Laber B, Amrhein N (1990) Slow-binding inhibition of the Escherichia coli pyruvate dehydrogenase multienzyme complex by acetylphosphinate. Biochemistry 29: 4880-4885
84. Sienkiewicz-Porzucek A, Nunes-Nesi A, Sulpice R, Lisec J, Centeno DC, Carillo P, Leisse A, Urbanczyk-Wochniak E, Fernie AR (2008) 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 147: 115-27
85. Studart-Guimarães C, Fait A, Nunes-Nesi A, Carrari F, Usadel B, Fernie AR (2007) Reduced expression of succinyl CoA ligase can be compensated for by an upregulation of the g-amino-butyrate (GABA) shunt in illuminated tomato leaves. Plant Physiol 145: 626-639
86. Sweetlove LJ, Fait A, Nunes-Nesi A, Williams T, Fernie AR (2007) The mitochondrion: an integration point in cellular metabolism and signalling. Crit Rev Plant Sci 26: 17-43
87. Sweetlove LJ, Fernie AR (2005) Regulation of metabolic networks: understanding metabolic complexity in the systems biology era. New Phytol 168: 9-24
88. Sweetlove LJ, Heazelwood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32: 891-904
89. Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ (2006) Tomato aromatic amino acid decarboxylases participate in synthesis of the flavour volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc Natl Acad Sci USA 103: 8287-8292
90. Tovar-Méndez A, Miernyk JA, Randall DD (2003) Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur J Biochem 270: 1043-1049
91. Tretter L, Adam-Vizi V (2000) Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of alpha-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J Neurosci 20: 8972-8979
92. Wedding RT, Black MK (1971) Evidence for tighter binding of magnesium-thiamine pyrophosphate to α-ketoglutarate dehydrogenase when activated by adenosine monophosphate. J Biol Chem 246: 4097-4099