Analysis of a range of catabolic mutants provides evidence that phytanoyl-coenzyme a does not act as a substrate of the electron-transfer flavoprotein/ electron-transfer flavoprotein: Ubiquinone oxidoreductase complex in arabidopsis during dark-induced senescence

Plant Physiology

Volumn 157, Issue 1, 2011, Pages 55-69

  Araújo, Wagner L ^a,b   Ishizaki, Kimitsune ^c   Nunes Nesi, Adriano ^a,b   Tohge, Takayuki ^a   Larson, Tony R ^d   Krahnert, Ina ^a   Balbo, Ilse ^a   Witt, Sandra ^a   Dörmann, Peter ^e   Graham, Ian A ^d   Leaver, Christopher J ^f   Fernie, Alisdair R ^a  

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

^b FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF YORK   (United Kingdom)

^e UNIVERSITY OF BONN   (Germany)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 80052415236     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.182188     Document Type: Article

References (57)

1. Araújo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, et al (2010) 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 22: 1549-1563
2. Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation-an alternative respiratory substrate for stressed plants. Trends Plant Sci (in press)
3. Beckmann JD, Frerman FE (1985) Electron-transfer flavoprotein-ubiquinone oxidoreductase from pig liver: purification and molecular, redox, and catalytic properties. Biochemistry 24: 3913-3921
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
5. Bräutigam A, Weber AP (2011) Do metabolite transport processes limit photosynthesis? Plant Physiol 155: 43-48
6. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin J-F, Wu S-H, Swidzinski J, Ishizaki K, et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvationinduced senescence in Arabidopsis. Plant J 42: 567-585
7. Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15: 266-274
8. Chen M, Galvão RM, Li M, Burger B, Bugea J, Bolado J, Chory J (2010) Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141: 1230-1240
9. Engqvist M, Drincovich MF, Flügge UI, Maurino VG (2009) 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 284: 25026-25037
10. Engqvist MK, Kuhn A, Wienstroer J, Weber K, Jansen EEW, Jakobs C, Weber APM, Maurino VG (2011) Plant D-2-hydroxyglutarate dehydrogenase participates in the catabolism of lysine especially during senescence. J Biol Chem 286: 11382-11390
11. Frerman FE (1988) Acyl-CoA dehydrogenases, electron transfer flavoprotein and electron transfer flavoprotein dehydrogenase. Biochem Soc Trans 16: 416-418
12. Frerman FE, Goodman SI (2001) Defects of electron transfer flavoprotein and electron transfer flavoprotein-ubiquinone oxidoreductase: glutaric acidemia type II. In CR Scriver, WS Sly, B Childs, AL Beaudet, D Valle, eds, The Metabolic and Molecular Bases of Inherited Disease. McGraw- Hill, New York, pp 2357-2365
13. Ghisla S, Thorpe C (2004) Acyl-CoA dehydrogenases: a mechanistic overview. Eur J Biochem 271: 494-508
14. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Höhne 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 of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16: 3304-3325
15. He M, Rutledge SL, Kelly DR, Palmer CA, Murdoch G, Majumder N, Nicholls RD, Pei Z, Watkins PA, Vockley J (2007) A new genetic disorder in mitochondrial fatty acid beta-oxidation: ACAD9 deficiency. Am J Hum Genet 81: 87-103
16. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plantspecific mitochondrial proteins. Plant Cell 16: 241-256
17. Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta 1807: 977-988
18. Hoskins DD, MacKenzie CG (1961) Solubilization and electron transfer flavoprtein requirement of mitochondrial sarcosine dehydrogenase and dimethylglycine dehydrogenase. J Biol Chem 236: 177-183
19. 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
20. 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
21. Jansen GA, Ofman R, Denis S, Ferdinandusse S, Hogenhout EM, Jakobs C, Wanders RJA (1999) Phytanoyl-CoA hydroxylase from rat liver: protein purification and cDNA cloning with implications for the subcellular localization of phytanic acid a-oxidation. J Lipid Res 40: 2244-2254
22. Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet 25: 185-192
23. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmüller E, Dörmann P, Weckwerth W, Gibon Y, Stitt M, et al (2005) GMD@CSBDB: the Golm Metabolome Database. Bioinformatics 21: 1635-1638
24. Kunz HH, Scharnewski M, Feussner K, Feussner I, Flügge UI, Fulda M, Gierth M (2009) The ABC transporter PXA1 and peroxisomal b-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell 21: 2733-2749
25. Larson TR, Graham IA (2001) Technical advance: a novel technique for the sensitive quantification of acyl CoA esters from plant tissues. Plant J 25: 115-125
26. Lehmann M, Schwarzländer M, Obata T, Sirikantaramas S, Burow M, Olsen CE, Tohge T, Fricker MD, Møller BL, Fernie AR, et al (2009) 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 2: 390-406
27. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1: 387-396
28. Luedemann A, Strassburg K, Erban A, Kopka J (2008) TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GCMS)-based metabolite profiling experiments. Bioinformatics 24: 732-737
29. McDonough MA, Kavanagh KL, Butler D, Searls T, Oppermann U, Schofield CJ (2005) Structure of human phytanoyl-CoA 2-hydroxylase identifies molecular mechanisms of Refsum disease. J Biol Chem 280: 41101-41110
30. Mihalik SJ, Morrell JC, Kim DO, Sacksteder KA, Watkins PA, Gould SJ (1997) Identification of PAHX, a Refsum disease gene. Nat Genet 17: 185-189
31. Mihalik SJ, Rainville AM, Watkins PA (1995) Phytanic acid a-oxidation in rat liver peroxisomes: production of a-hydroxyphytanoyl-CoA and formate is enhanced by dioxygenase cofactors. Eur J Biochem 232: 545-551
32. Mukherji M, Chien W, Kershaw NJ, Clifton IJ, Schofield CJ, Wierzbicki AS, Lloyd MD (2001) Structure-function analysis of phytanoyl-CoA 2-hydroxylase mutations causing Refsum's disease. Hum Mol Genet 10: 1971-1982
33. Mukherji M, Schofield CJ, Wierzbicki AS, Jansen GA, Wanders RJ, Lloyd MD (2003) The chemical biology of branched-chain lipid metabolism. Prog Lipid Res 42: 359-376
34. Mur LA, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E, James C, Papp I, Hörtensteiner S, Thomas H, et al (2010) Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol 188: 161-174
35. Oh SA, Lee SY, Chung IK, Lee CH, Nam HG (1996) A senescenceassociated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol 30: 739-754
36. Palmieri F, Pierri CL, De Grassi A, Nunes-Nesi A, Fernie AR (2011) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J 66: 161-181
37. Pogson BJ, Woo NS, Förster B, Small ID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13: 602-609
38. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384-394
39. Pruzinská A, Tanner G, Aubry S, Anders I, Moser S, Müller T, Ongania K-H, Kräutler B, Youn J-Y, Liljegren SJ, et al (2005) Chlorophyll breakdown in senescent Arabidopsis leaves: characterization of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol 139: 52-63
40. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29
41. Roessner-Tunali U, Hegemann B, Lytovchenko A, Carrari F, Bruedigam C, Granot D, Fernie AR (2003) Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol 133: 84-99
42. 13C labelled isotopes. Plant J 39: 669-679
43. Ruzicka FJ, Beinert H (1977) A new iron-sulfur flavoprotein of the respiratory chain: a component of the fatty acid beta oxidation pathway. J Biol Chem 252: 8440-8445
44. 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
45. Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hörtensteiner S (2009) Pheophytin pheophorbide hydrolase (pheophy- tinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21: 767-785
46. Searls T, Butler D, Chien W, Mukherji M, Lloyd MD, Schofield CJ (2005) Studies on the specificity of unprocessed and mature forms of phytanoyl-CoA 2-hydroxylase and mutation of the iron binding ligands. J Lipid Res 46: 1660-1667
47. Sienkiewicz-Porzucek A, Sulpice R, Osorio S, Krahnert I, Leisse A, Urbanczyk-Wochniak E, Hodges M, Fernie AR, Nunes-Nesi A (2010) Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Mol Plant 3: 156-173
48. Studart-Guimarães C, Fait A, Nunes-Nesi A, Carrari F, Usadel B, Fernie AR (2007) Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiol 145: 626-639
49. Taylor DC, Weber N, Hogge LR, Underhill EW (1990) A simple enzymatic method for the preparation of radiolabeled erucoyl-CoA and other longchain fatty acyl-CoAs and their characterization by mass spectrometry. Anal Biochem 184: 311-316
50. Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ (2006) Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc Natl Acad Sci USA 103: 8287-8292
51. Timm S, Nunes-Nesi A, Pärnik T, Morgenthal K, Wienkoop S, Keerberg O, Weckwerth W, Kleczkowski LA, Fernie AR, Bauwe H (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 20: 2848-2859
52. Wanders RJ, Jansen GA, Lloyd MD (2003) Phytanic acid alpha-oxidation, new insights into an old problem: a review. Biochim Biophys Acta 1631: 119-135
53. Wanders RJ, Komen JC (2007) Peroxisomes, Refsum's disease and the a- and v-oxidation of phytanic acid. Biochem Soc Trans 35: 865-869
54. Watmough NJ, Frerman FE (2010) The electron transfer flavoprotein: ubiquinone oxidoreductases. Biochim Biophys Acta 1797: 1910-1916
55. Wierzbicki AS, Lloyd MD, Schofield CJ, Feher MD, Gibberd FB (2002) Refsum's disease: a peroxisomal disorder affecting phytanic acid alphaoxidation. J Neurochem 80: 727-735
56. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9: 383-395
57. Yang Z, Ohlrogge JB (2009) Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and switchgrass and in Arabidopsis b-oxidation mutants. Plant Physiol 150: 1981-1989