L-Galactono-γ-lactone dehydrogenase from Arabidopsis thaliana, a flavoprotein involved in vitamin C biosynthesis

FEBS Journal

Volumn 275, Issue 4, 2008, Pages 713-726

  Leferink, Nicole G H ^a   Van Den Berg, Willy A M ^a   Van Berkel, Willem J H ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Arabidopsis thaliana; Flavoprotein; L galactono 1,4 lactone dehydrogenase; Site directed mutagenesis; Vitamin C biosynthesis

Indexed keywords

ASCORBIC ACID; CYTOCHROME C OXIDASE; FLAVOPROTEIN; HYDROQUINONE; LACTONE DERIVATIVE; LEVO GALACTONO 1,4 LACTONE; LEVO GALACTONO GAMMA LACTONE DEHYDROGENASE; LEVO GULONO 1,4 LACTONE; OXIDOREDUCTASE; OXYGEN; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CATALYSIS; COVALENT BOND; ENZYME BINDING; MICHAELIS CONSTANT; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCORBIC ACID; CATALYSIS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLAVOPROTEINS; LACTONES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS THALIANA;

EID: 38549180253     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.06233.x     Document Type: Article

References (44)

1. Smirnoff N Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35, 291 314.
2. Fraaije MW, Van Berkel WJH, Benen JAE, Visser J Mattevi A (1998) A novel oxidoreductase family sharing a conserved FAD-binding domain. Trends Biochem Sci 23, 206 207.
3. Linster CL Van Schaftingen E (2007) Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J 274, 1 22.
4. Nishikimi M, Fukuyama R, Minoshima S, Shimizu N Yagi K (1994) Cloning and chromosomal mapping of the human nonfunctional gene for l-gulono-gamma-lactone oxidase, the enzyme for l-ascorbic acid biosynthesis missing in man. J Biol Chem 269, 13685 13688.
5. Huh WK, Lee BH, Kim ST, Kim YR, Rhie GE, Baek YW, Hwang CS, Lee JS Kang SO (1998) d-Erythroascorbic acid is an important antioxidant molecule in Saccharomyces cerevisiae. Mol Microbiol 30, 895 903.
6. Salusjärvi T, Kalkkinen N Miasnikov AN (2004) Cloning and characterization of gluconolactone oxidase of Penicillium cyaneo-fulvum ATCC 10431 and evaluation of its use for production of d-erythorbic acid in recombinant Pichia pastoris. Appl Environ Microbiol 70, 5503 5510.
7. Wolucka BA Communi D (2006) Mycobacterium tuberculosis possesses a functional enzyme for the synthesis of vitamin C, l-gulono-1,4-lactone dehydrogenase. FEBS J 273, 4435 4445.
8. Wilkinson SR, Prathalingam SR, Taylor MC, Horn D Kelly JM (2005) Vitamin C biosynthesis in trypanosomes: a role for the glycosome. Proc Natl Acad Sci USA 102, 11645 11650.
9. Logan FJ, Taylor MC, Wilkinson SR, Kaur H Kelly JM (2007) The terminal step in vitamin C biosynthesis in Trypanosoma cruzi is mediated by a FMN-dependent galactonolactone oxidase. Biochem J 407, 419 426.
10. Huh WK, Kim ST, Yang KS, Seok YJ, Hah YC Kang SO (1994) Characterisation of d-arabinono-1,4-lactone oxidase from Candida albicans ATCC 10231. Eur J Biochem 225, 1073 1079.
11. Kiuchi K, Nishikimi M Yagi K (1982) Purification and characterization of l-gulonolactone oxidase from chicken kidney microsomes. Biochemistry 21, 5076 5082.
12. Ôba K, Ishikawa S, Nishikawa M, Mizuno H Yamamoto T (1995) Purification and properties of l-galactono-γ-lactone dehydrogenase, a key enzyme for ascorbic acid biosynthesis, from sweet potato roots. J Biochem (Tokyo) 117, 120 124.
13. Østergaard J, Persiau G, Davey MW, Bauw G Van Montagu M (1997) Isolation of a cDNA coding for l-galactono-γ-lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants. Purification, characterization, cDNA cloning, and expression in yeast. J Biol Chem 272, 30009 30016.
14. Yabuta Y, Yoshimura K, Takeda T Shigeoka S (2000) Molecular characterization of tobacco mitochondrial l-galactono-γ-lactone dehydrogenase and its expression in Escherichia coli. Plant Cell Physiol 41, 666 675.
15. Linster CL, Gomez TA, Christensen KC, Adler LN, Young BD, Brenner C Clarke SG (2007) Arabidopsis VTC2 encodes a GDP-l-galactose phosphorylase, the last unknown enzyme in the Smirnoff-Wheeler pathway to ascorbic acid in plants. J Biol Chem 282, 18879 18885.
16. Agius F, González-Lamothe R, Caballero JL, Muñoz-Blanco J, Botella MA Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a d-galacturonic acid reductase. Nat Biotechnol 21, 177 181.
17. Wolucka BA Van Montagu M (2003) 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, 47483 47490.
18. Davey MW, Gilot C, Persiau G, Østergaard J, Han Y, Bauw GC Van Montagu MC (1999) Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiol 121, 535 543.
19. Bartoli CG, Pastori GM Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123, 335 344.
20. Mapson LW Breslow E (1958) Biological synthesis of ascorbic acid: l-galactono-γ-lactone dehydrogenase. Biochem J 68, 395 406.
21. Imai T, Karita S, Shiratori G, Hattori M, Nunome T, Ôba K Hirai M (1998) l-galactono-γ-lactone dehydrogenase from sweet potato: purification and cDNA sequence analysis. Plant Cell Physiol 39, 1350 1358.
22. Mutsuda M, Ishikkawa T, Takeda T Shigeoka S (1995) Subcellular localization and properties of l-galactono-γ-lactone dehydrogenase in spinach leaves. Biosci Biotechnol Biochem 59, 1983 1984.
23. Tamaoki M, Mukai F, Asai N, Nakajima N, Kubo A, Aono M Saji H (2003) Light-controlled expression of a gene encoding l-galactono-γ-lactone dehydrogenase which affects ascorbate pool size in Arabidopsis thaliana. Plant Sci 164, 1111 1117.
24. Siendones E, González-Reyes JA, Santos-Ocaña C, Navas P Córdoba F (1999) Biosynthesis of ascorbic acid in kidney bean. l-galactono-γ-lactone dehydrogenase is an intrinsic protein located at the mitochondrial inner membrane. Plant Physiol 120, 907 912.
25. Fraaije MW Mattevi A (2000) Flavoenzymes: diverse catalysts with recurrent features. Trends Biochem Sci 25, 126 132.
26. 2 from baker's yeast. Eur J Biochem 88, 425 431.
27. Massey V, Müller F, Feldberg R, Schuman M, Sullivan PA, Howell LG, Mayhew SG, Matthews RG Foust GP (1969) The reactivity of flavoproteins with sulfite. Possible relevance to the problem of oxygen reactivity. J Biol Chem 244, 3999 4006.
28. Hefti MH, Milder FJ, Boeren S, Vervoort J van Berkel WJH (2003) A His-tag based immobilization method for the preparation and reconstitution of apoflavoproteins. Biochim Biophys Acta 1619, 139 143.
29. Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D, Petit J, Beauvoit B, Fernie AR, Rothan C et al. (2007) Silencing of the mitochondrial ascorbate synthesizing enzyme l-galactono-1,4-lactone dehydrogenase (l-GalLDH) affects plant and fruit development in tomato. Plant Physiol 145, 1408 1422.
30. Mewies M, McIntire WS Scrutton NS (1998) Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci 7, 7 20.
31. Eliceiri GL, Lai EK McCay PB (1969) Gulonolactone oxidase. Solubilization, properties, and partial purification. J Biol Chem 244, 2641 2645.
32. Sugisawa T, Ojima S, Matzinger PK Hoshino T (1995) Isolation and characterization of a new vitamin C producing enzyme (l-gulono-γ-lactone dehydrogenase) of bacterial origin. Biosci Biotechnol Biochem 59, 190 195.
33. Ould Boubacar AK, Pethe S, Mahy JP Lederer F (2007) Flavocytochrome b2: reactivity of its flavin with molecular oxygen. Biochemistry 46, 13080 13088.
34. Mowat CG, Beaudoin I, Durley RC, Barton JD, Pike AD, Chen ZW, Reid GA, Chapman SK, Mathews FS Lederer F (2000) Kinetic and crystallographic studies on the active site Arg289Lys mutant of flavocytochrome b2 (yeast l-lactate dehydrogenase). Biochemistry 39, 3266 3275.
35. Schiffer A, Fritz G, Kroneck PM Ermler U (2006) Reaction mechanism of the iron-sulfur flavoenzyme adenosine-5'-phosphosulfate reductase based on the structural characterization of different enzymatic states. Biochemistry 45, 2960 2967.
36. Fraaije MW, van den Heuvel RHH, van Berkel WJH Mattevi A (1999) Covalent flavinylation is essential for efficient redox catalysis in vanillyl-alcohol oxidase. J Biol Chem 274, 35514 35520.
37. Fraaije MW, van den Heuvel RHH, van Berkel WJH Mattevi A (2000) Structural analysis of flavinylation in vanillyl-alcohol oxidase. J Biol Chem 275, 38654 38658.
38. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389 3402.
39. Thompson JD, Higgins DG Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673 4680.
40. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
41. 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.
42. Macheroux P (1999) UV-visible spectroscopy as a tool to study flavoproteins. In Flavoprotein Protocols (Chapman SK Reid GA, eds pp 1 7. Humana Press, Totowa.
43. Valpuesta V Botella MA (2004) Biosynthesis of l-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9, 573 577.
44. Ishikawa T, Dowdle J Smirnoff N (2006) Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant 126, 343 355.