The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes

Journal of Experimental Botany

Volumn 61, Issue 5, 2010, Pages 1441-1453

  Babujee, Lavanya ^a,d   Wurtz, Virginie ^b   Ma, Changle ^a,e   Lueder, Franziska ^a,f   Soni, Pradeep ^c   Van Dorsselaer, Alain ^b   Reumann, Sigrun ^a,c  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^c UNIVERSITY OF STAVANGER   (Norway)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e SECTION OF MOLECULAR BIOLOGY   (United States)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Acyl activating enzyme; Enoyl CoA hydratase isomerase; Mass spectrometry; Phylloquinone; Proteome analysis; Short chain dehydrogenase; Subcellular targeting

Indexed keywords

PHYTOMENADIONE; PROTEOME; VEGETABLE PROTEIN;

ARTICLE; BIOLOGICAL MODEL; ENZYMOLOGY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; PEROXISOME; PLANT LEAF; POLYACRYLAMIDE GEL ELECTROPHORESIS; SPINACH; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MODELS, BIOLOGICAL; PEROXISOMES; PLANT LEAVES; PLANT PROTEINS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPINACIA OLERACEA; TANDEM MASS SPECTROMETRY; VITAMIN K 1;

ARABIDOPSIS; CYANOBACTERIA; EMBRYOPHYTA; SPINACIA OLERACEA;

EID: 77949359431     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq014     Document Type: Article

References (58)

1. Arai Y, Hayashi M, Nishimura M. 2008. Proteomic analysis of highly purified peroxisomes from etiolated soybean cotyledons. Plant and Cell Physiology 49, 526-539.
2. Boden M, Hawkins J. 2005. Prediction of subcellular localization using sequence-biased recurrent networks. Bioinformatics 21, 2279-2286.
3. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
4. del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB. 2002. Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany 53, 1255-1272.
5. Emanuelsson O, Elofsson A, von Heijne G, Cristobal S. 2003. In silico prediction of the peroxisomal proteome in fungi, plants and animals. Journal of Molecular Biology 330, 443-456.
6. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300, 1005-1016.
7. Eubel H, Meyer EH, Taylor NL, Bussell JD, O'Toole N, Heazlewood JL, Castleden I, Small ID, Smith SM, Millar AH. 2008. Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiology 148, 1809-1829.
8. Fransen M, Van Veldhoven PP, Subramani S. 1999. Identification of peroxisomal proteins by using M13 phage protein VI phage display: molecular evidence that mammalian peroxisomes contain a 2,4-dienoyl-CoA reductase. Biochemica Journal 340, 561-568.
9. Fukao Y, Hayashi M, Hara-Nishimura I, Nishimura M. 2003. Novel glyoxysomal protein kinase, GPK1, identified by proteomic analysis of glyoxysomes in etiolated cotyledons of Arabidopsis thaliana. Plant and Cell Physiology 44, 1002-1012.
10. Fukao Y, Hayashi M, Nishimura M. 2002. Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant and Cell Physiology 43, 689-696.
11. Fulda M, Schnurr J, Abbadi A, Heinz E, Browse J. 2004. Peroxisomal Acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. The Plant Cell 16, 394-405.
12. Fulda M, Shockey J, Werber M, Wolter FP, Heinz E. 2002. Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid beta-oxidation. The Plant Journal 32, 93-103.
13. Goepfert S, Vidoudez C, Rezzonico E, Hiltunen JK, Poirier Y. 2005. Molecular identification and characterization of the Arabidopsis delta(3,5), delta(2,4)-dienoyl-coenzyme A isomerase, a peroxisomal enzyme participating in the beta-oxidation cycle of unsaturated fatty acids. Plant Physiology 138, 1947-1956.
14. Goepfert S, Vidoudez C, Tellgren-Roth C, Delessert S, Hiltunen JK, Poirier Y. 2008. Peroxisomal Delta(3), Delta(2)-enoyl CoA isomerases and evolution of cytosolic paralogues in embryophytes. The Plant Journal 56, 728-742.
15. Gould SG, Keller GA, Subramani S. 1987. Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase. Journal of Cell Biology 105, 2923-2931.
16. Graham IA, Eastmond PJ. 2002. Pathways of straight and branched chain fatty acid catabolism in higher plants. Progress in Lipid Research 41, 156-181.
17. Gross J, Cho WK, Lezhneva L, Falk J, Krupinska K, Shinozaki K, Seki M, Herrmann RG, Meurer J. 2006. A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. Journal of Biological Chemistry 281, 17189-17196.
18. Gross J, Meurer J, Bhattacharya D. 2008. Evidence of a chimeric genome in the cyanobacterial ancestor of plastids. BMC Evolutionary Biology 8, 117.
19. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I, Millar AH. 2007. SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Research 35, D213-D218.
20. Herbert B, Galvani M, Hamdan M, Olivieri E, MacCarthy J, Pedersen S, Righetti PG. 2001. Reduction and alkylation of proteins in preparation of two-dimensional map analysis: why, when, and how? Electrophoresis 22, 2046-2057.
21. Jeno P, Mini T, Moes S, Hintermann E, Horst M. 1995. Internal sequences from proteins digested in polyacrylamide gels. Analytical Biochemistry 224, 75-82.
22. Johnson TW, Zybailov B, Jones AD, Bittl R, Zech S, Stehlik D, Golbeck JH, Chitnis PR. 2001. Recruitment of a foreign quinone into the A1 site of photosystem I. In vivo replacement of plastoquinone-9 by media-supplemented naphthoquinones in phylloquinone biosynthetic pathway mutants of Synechocystis sp. PCC 6803. Journal of Biological Chemistry 276, 39512-39521.
23. Kamada T, Nito K, Hayashi H, Mano S, Hayashi M, Nishimura M. 2003. Functional differentiation of peroxisomes revealed by expression profiles of peroxisomal genes in Arabidopsis thaliana. Plant and Cell Physiology 44, 1275-1289.
24. Kaur N, Reumann S, Hu J. 2009. Peroxisome biogenesis and function. The Arabidopsis book, The American Society of Plant Biologists 1-41.
25. Kikuchi M, Hatano N, Yokota S, Shimozawa N, Imanaka T, Taniguchi H. 2004. Proteomic analysis of rat liver peroxisome: presence of peroxisome-specific isozyme of Lon protease. Journal of Biological Chemistry 279, 421-428.
26. Kim HU, van Oostende C, Basset GJ, Browse J. 2008. The AAE14 gene encodes the Arabidopsis o-succinylbenzoyl-CoA ligase that is essential for phylloquinone synthesis and photosystem-I function. The Plant Journal 54, 272-283.
27. Koo AJ, Chung HS, Kobayashi Y, Howe GA. 2006. Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis. Journal of Biological Chemistry 281, 33511-33520.
28. Kruft V, Eubel H, Jansch L, Werhahn W, Braun HP. 2001. Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiology 127, 1694-1710.
29. Lohmann A, Schottler MA, Brehelin C, Kessler F, Bock R, Cahoon EB, Dormann P. 2006. Deficiency in phylloquinone (vitamin K1) methylation affects prenyl quinone distribution, photosystem I abundance, and anthocyanin accumulation in the Arabidopsis AtmenG mutant. Journal of Biological Chemistry 281, 40461-40472.
30. Lopez-Huertas E, Sandalio LM, Del Rio LA. 1995. Integral membrane polypeptides of pea leaf peroxisomes: characterization and response to plant stress. Plant Physiology and Biochemistry 33, 295-302.
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265-275.
32. Ma C, Haslbeck M, Babujee L, Jahn O, Reumann S. 2006. Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiology 141, 47-60.
33. Marelli M, Smith JJ, Jung S, et al. 2004. Quantitative mass spectrometry reveals a role for the GTPase Rho1p in actin organization on the peroxisome membrane. Journal of Cell Biology 167, 1099-1112.
34. Matre P, Meyer C, Lillo C. 2009. Diversity in subcellular targeting of the PP2A B#eta subfamily members. Planta 230, 935-945.
35. Millar AH, Sweetlove LJ, Giege P, Leaver CJ. 2001. Analysis of the Arabidopsis mitochondrial proteome. Plant Physiology 127, 1711-1727.
36. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F. 2003. Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. Journal of Molecular Biology 328, 581-592.
37. Palma JM, Corpas FJ, Del Rio LA. 2009. Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics 9, 2301-2312.
38. Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ. 2000. Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. The Plant Cell 12, 319-341.
39. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567.
40. Reumann S. 2004. Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiology 135, 783-800.
41. Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Luder F, Weckwerth W, Jahn O. 2007. Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. The Plant Cell 19, 3170-3193.
42. Reumann S, Heupel R, Heldt HW. 1994. Compartmentation studies on spinach leaf peroxisomes. II. Evidence for the transfer of reductant from the cytosol to the peroxisomal compartment via a malate shuttle. Planta 193, 167-173.
43. Reumann S, Ma C, Lemke S, Babujee L. 2004. AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiology 136, 2587-2608.
44. Reumann S, Maier E, Benz R, Heldt HW. 1995. The membrane of leaf peroxisomes contains a porin-like channel. Journal of Biological Chemistry 270, 17559-17565.
45. Reumann S, Quan S, Aung K, et al. 2009. In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiology 150, 125-143.
46. Reumann S, Weber AP. 2006. Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled\others remain. Biochimica et Biophysica Acta 1763, 1496-1510.
47. Saleem RA, Smith JJ, Aitchison JD. 2006. Proteomics of the peroxisome. Biochimica et Biophysica Acta 1763, 1541-1551.
48. Schafer H, Nau K, Sickmann A, Erdmann R, Meyer HE. 2001. Identification of peroxisomal membrane proteins of Saccharomyces cerevisiae by mass spectrometry. Electrophoresis 22, 2955-2968.
49. Shimada H, Ohno R, Shibata M, Ikegami I, Onai K, Ohto MA, Takamiya K. 2005. Inactivation and deficiency of core proteins of photosystems I and II caused by genetical phylloquinone and plastoquinone deficiency but retained lamellar structure in a T-DNA mutant of Arabidopsis. The Plant Journal 41, 627-637.
50. Swinkels BW, Gould SJ, Bodnar AG, Rachubinski RA, Subramani S. 1991. A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO Journal 10, 3255-3262.
51. Wessel D, Flugge UI. 1984. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Analytical Biochemistry 138, 141-143.
52. Widhalm JR, van Oostende C, Furt F, Basset GJ. 2009. A dedicated thioesterase of the Hotdog-fold family is required for the biosynthesis of the naphthoquinone ring of vitamin K1. Proceedings of the Natoional Academy of Sciences, USA 106, 5599-5603.
53. Wiese S, Gronemeyer T, Ofman R, et al. 2007. Proteomics characterization of mouse kidney peroxisomes by tandem mass spectrometry and protein correlation profiling. Molecular and Cellular Proteomics 6, 2045-2057.
54. Wiszniewski AA, Zhou W, Smith SM, Bussell JD. 2009. Identification of two Arabidopsis genes encoding a peroxisomal oxidoreductase-like protein and an acyl-CoA synthetase-like protein that are required for responses to pro-auxins. Plant Molecular Biology 69, 503-515.
55. Yu C, Huang AH. 1986. Conversion of serine to glycerate in intact spinach leaf peroxisomes: role of malate dehydrogenase. Archives of Biochemistry and Biophysics 245, 125-133.
56. Zolman BK, Martinez N, Millius A, Adham AR, Bartel B. 2008. Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics 180, 237-251.
57. Zolman BK, Monroe-Augustus M, Thompson B, Hawes JW, Krukenberg KA, Matsuda SP, Bartel B. 2001. chy1, an Arabidopsis mutant with impaired beta-oxidation, is defective in a peroxisomal beta-hydroxyisobutyryl-CoA hydrolase. Journal of Biological Chemistry 276, 31037-31046.
58. Zolman BK, Nyberg M, Bartel B. 2007. IBR3, a novel peroxisomal acyl-CoA dehydrogenase-like protein required for indole-3-butyric acid response. Plant Molecular Biology 64, 59-72.