Arabidopsis peroxisome proteomics

Frontiers in Plant Science

Volumn 4, Issue APR, 2013, Pages

  Bussell, John D ^a   Behrens, Christof ^b   Ecke, Wiebke ^b   Eubel, Holger ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

Free flow electrophoresis; Functional proteomics; Peroxisome; Protein:protein interaction; Subcellular localization; Targeted quantitation of proteins

Indexed keywords

EID: 84896830318     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00101     Document Type: Review

References (81)

1. Arabidopsis Genome Initiative. (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
2. Baker, A., Graham, I. A., Holdsworth, M., Smith, S. M., and Theodoulou, F. L. (2006). Chewing the fat: beta-oxidation in signalling and development. Trends Plant Sci. 11, 124-132.
3. Baker, A., and Sparkes, I. A. (2005). Peroxisome protein import: some answers, more questions. Curr. Opin. Plant Biol. 8, 640-647.
4. Bauwe, H., Hagemann, M., and Fernie, A. R. (2010). Photorespiration: players, partners and origin. Trends Plant Sci. 15, 330-336.
5. Bernhardt, K., Wilkinson, S., Weber, A. P., and Linka, N. (2012). A peroxisomal carrier delivers NAD(+) and contributes to optimal fatty acid degradation during storage oil mobilization. Plant J. 69, 1-13.
6. Blum, T., Briesemeister, S., and Kohlbacher, O. (2009). MultiLoc2: integrating phylogeny and Gene Ontology terms improves subcellular protein localization prediction. BMC Bioinformatics 10:274. doi: 10.1186/1471-2105-10-274
7. Boatright, J., Negre, F., Chen, X., Kish, C. M., Wood, B., Peel, G., et al. (2004). Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 135, 1993-2011.
8. Braun, H. P., and Eubel, H. (2012). "Organellar proteomics: close insights into the spatial breakdown and functional dynamics of plant primary metabolism" in Genomics of Chloroplasts and Mitochondria, Vol. 35, Advances in Photosynthesis and Respiration, eds R. Bock and V. Knoop (Dordrecht: Springer), 357-378.
9. Chowdhary, G., Kataya, A. R., Lingner, T., and Reumann, S. (2012). Non-canonical peroxisome targeting signals: identification of novel PTS1 tripeptides and characterization of enhancer elements by computational permutation analysis. BMC Plant Biol. 12:142. doi: 10.1186/1471-2229-12-142
10. Cooper, T. G., and Beevers, H. (1969). Beta oxidation in glyoxysomes from castor bean endosperm. J. Biol. Chem. 244, 3514-3520.
11. de Duve, C. (1969a). Evolution of the peroxisome. Ann. N. Y. Acad. Sci. 168, 369-381.
12. de Duve, C. (1969b). The peroxisome: a new cytoplasmic organelle. Proc. R. Soc. Lond. B Biol. Sci. 173, 71-83.
13. de Duve, C., and Baudhin, P. (1966). Peroxisomes (microbodies and related particles). Physiol. Rev. 46, 323-357.
14. DeSouza, L. V., Taylor, A. M., Li, W., Minkoff, M. S., Romaschin, A. D., Colgan, T. J., et al. (2008). Multiple reaction monitoring of mTRAQ-labeled peptides enables absolute quantification of endogenous levels of a potential cancer marker in cancerous and normal endometrial tissues. J. Proteome Res. 7, 3525-3534.
15. Eckert, J. H., and Johnsson, N. (2003). Pex10p links the ubiquitin conjugating enzyme Pex4p to the protein import machinery of the peroxisome. J. Cell Sci. 116, 3623-3634.
16. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
17. Emanuelsson, O., Nielsen, H., and von Heijne, G. (1999). ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8, 978-984.
18. Eubel, H., Meyer, E. H., Taylor, N. L., Bussel, J. D., O'Toole N., Heazlewood, J. L., et al. (2008). Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol. 148, 1809-1829.
19. Fukao, Y., Hayashi, M., Nishimura, I. H., and Nishimura, M. (2003). Novel glyoxysomal protein kinase, GPK1, identified by proteomic analysis of glyoxysomes in etiolated cotyledons of Arabidopsis thaliana. Plant Cell Physiol. 44, 1002-1012.
20. Fukao, Y., Hayashi, M., and Nishimura, M. (2002). Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol. 43, 689-696.
21. Gavin, A. C., Bosche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., et al. (2002). Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147.
22. Gerber, S. A., Rush, J., Stemman O., Kirschner, M. W., and Gygi, S. P. (2003). Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. U.S.A. 100, 6940-6945.
23. Germain, V., Rylott, E. L., Larson, T. R., Sherson, S. M., Bechtold, N., Carde, J. P., et al. (2001). Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid beta-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant J. 28, 1-12.
24. Gould, S. J., Krisans, S., Keller, G. A., and Subramani, S. (1990). Antibodies directed against the peroxisomal targeting signal of firefly luciferase recognize multiple mammalian peroxisomal proteins. J. Cell Biol. 110, 27-34.
25. Goyer, A., Johnson, T. L., Olsen, L. J., Collakova, E., Shachar-Hill, Y., Rhodes, D., et al. (2004). Characterization and metabolic function of a peroxisomal sarcosine and pipecolate oxidase from Arabidopsis. J. Biol. Chem. 279, 16947-16953.
26. Graham, I. A. (2008). Seed storage oil mobilization. Annu. Rev. Plant Biol. 59, 115-142.
27. Hayashi, M., Toriyama, K., Kondo, M., and Nishimura, M. (1998). 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid beta-oxidation. Plant Cell 10, 183-195.
28. Heineke, D., Bykova, N., Gardestrom, P., and Bauwe, H. (2001). Metabolic response of potato plants to an antisense reduction of the P-protein of glycine decarboxylase. Planta 212, 880-887.
29. Helm, M., Luck, C., Prestele, J., Hierl, G., Huesgen, P. F., Frohlich, T., et al. (2007). Dual specificities of the glyoxysomal/peroxisomal processing protease Deg15 in higher plants. Proc. Natl. Acad. Sci. U.S.A. 104, 11501-11506.
30. Hoepfner, D., Schildknegt, D., Braakman, I., Philippsen, P., and Tabak, H. F. (2005). Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122, 85-95.
31. Hu, J., Baker, A., Bartel, B., Linka, N., Mullen, R. T., Reumann, S., et al. (2012). Plant peroxisomes: biogenesis and function. Plant Cell 24, 2279-2303.
32. Islinger, M., Eckerskorn, C., and Völkl, A. (2010). Free-flow electrophoresis in the proteomic era: a technique in flux. Electrophoresis 31, 1754-1763.
33. Kato, A., Takeda-Yoshikawa, Y., Hayashi, M., Kondo, M., Hara-Nishimura, I., and Nishimura, M. (1998). Glyoxysomal malate dehydrogenase in pumpkin: cloning of a cDNA and functional analysis of its presequence. Plant Cell Physiol. 39, 186-195.
34. Kaur, N., and Hu, J. (2011). Defining the plant peroxisomal proteome: from Arabidopsis to rice. Front. Plant Sci. 2:103. doi: 10.3389/fpls.2011.00103
35. Kebeish, R., Niessen, M., Thiruveedhi, K., Bari, R., Hirsch, H. J., Rosenkranz, R., et al. (2007). Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol. 25, 593-599.
36. Kerrien, S., Aranda, B., Breuza, L., Bridge, A., Broackes-Carter, F., Chen, C., et al. (2012). The IntAct molecular database in 2012. Nucleic Acids Res. 40, D841-D846.
37. Klempien, A., Kaminaga, Y., Qualley, A., Nagegowda, D. A., Widhalm, J. R., Orlova, I., et al. (2012). Contribution of CoA ligases to benzenoid biosynthesis in petunia flowers. Plant Cell 24, 2015-2030.
38. Kliebenstein, D. J., D'Aauria, J. C., Behere, A. S., Kim, J. H., Gunderson, K. L., Breen, J. N., et al. (2007). Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J. 51, 1062-1076.
39. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., et al. (2006). Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643.
40. Kunz, H. H., Scharnewski, M., Feussner, K., Feussner, I., Flugge, U. I., Fulda, M., et al. (2009). The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell 21, 2733-2749.
41. Lamberto, I., Percudani, R., Gatti, R., Folli, C., and Petrucco, S. (2010). Conserved alternative splicing of Arabidopsis transthyretin-like determines protein localization and S-allantoin synthesis in peroxisomes. Plant Cell 22, 1564-1574.
42. Lee, K. Y., Thorneycroft, D., Achuthan, P., Hermjakob, H., and Ideker, T. (2010). Mapping plant interactomes using literature curated and predicted protein-protein interaction data sets. Plant Cell 22, 997-1005.
43. Lee, S., Kaminaga, Y., Cooper, B., Pichersky, E., Dudareva, N., and Chapple, C. (2012). Benzoylation and sinapoylation of glucosinolate R-groups in Arabidopsis. Plant J. 72, 411-422.
44. Lingard, M. J., and Bartel, B. (2009). Arabidopsis LON2 is necessary for peroxisomal function and sustained matrix protein import. Plant Physiol. 151, 1354-1365.
45. Lingard, M. J., Gidda, S. K., Bingham, S., Rothstein, S. J., Mullen, R. T., and Trelease, R. N. (2008). Arabidopsis PEROXIN11c-e, FISSION1b, and DYNAMIN-RELATED PROTEIN3A cooperate in cell cycle-associated replication of peroxisomes. Plant Cell 20, 1567-1585.
46. Lingard, M. J., Monroe-Augustus, M., and Bartel, B. (2009). Peroxisome-associated matrix protein degradation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106, 4561-4566.
47. Lingard, M. J., and Trelease, R. N. (2006). Five Arabidopsis peroxin 11 homologs individually promote peroxisome elongation, duplication or aggregation. J. Cell Sci. 119, 1961-1972.
48. Lingner, T., Kataya, A. R., Antonicelli, G. E., Benichou, A., Nilssen, K., Chen, X.-Y., et al. (2011). Identification of novel plant peroxisomal targeting signals by a combination of machine learning methods and in vivo subcellular targeting analysis. Plant Cell 23, 1556-1572.
49. Lisenbee, C. S., Lingard, M. J., and Trelease, R. N. (2005). Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J. 43, 900-914.
50. Ma, C., and Reumann, S. (2008). Improved prediction of peroxisomal PTS1 proteins from genome sequences based on experimental subcellular targeting analyses as exemplified for protein kinases from Arabidopsis. J. Exp. Bot. 59, 3767-3779.
51. Makkar, R. S., Contreras, M. A., Paintlia, A. S., Smith, B. T., Haq, E., and Singh, I. (2006). Molecular organization of peroxisomal enzymes: protein-protein interactions in the membrane and in the matrix. Arch. Biochem. Biophys. 451, 128-140.
52. Mullen, R. T., and Trelease, R. N. (2006). The ER-peroxisome connection in plants: development of the "ER semi-autonomous peroxisome maturation and replication" model for plant peroxisome biogenesis. Biochim. Biophys. Acta 1763, 1655-1668.
53. Oshima, Y., Kamigaki, A., Nakamori, C., Mano, S., Hayashi, M., Nishimura, M., et al. (2008). Plant catalase is imported into peroxisomes by Pex5p but is distinct from typical PTS1 import. Plant Cell Physiol. 49, 671-677.
54. Palma, J. S., Corpas, F. J., and del Rio, L. A. (2009). Proteome of plant peroxisomes: new perspectives on the role of these cell organelles in cell biology. Proteomics 9, 2301-2312.
55. Peterhansel, C., and Maurino, V. G. (2011). Photorespiration redesigned. Plant Physiol. 155, 49-55.
56. Pracharoenwattana, I., and Smith, S. M. (2008). When is a peroxisome not a peroxisome? Trends Plant Sci. 13, 522-525.
57. Qualley, A. V., Widhalm, J. R., Adebesin, F., Kish, C. M., and Dudareva, N. (2012). Completion of the core beta-oxidative pathway of benzoic acid biosynthesis in plants. Proc. Natl. Acad. Sci. U.S.A. 109, 16383-16388.
58. Reumann, S. (2004). Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol. 135, 783-800.
59. Reumann, S. (2011). Toward a definition of the complete proteome of plant peroxisomes: where experimental proteomics must be completed by bioinformatics. Proteomics 11, 1764-1779.
60. Reumann, S., Babujee, L., Ma, C., Wienkoop, S., Siemens, T., Antonicelli, G. E., et al. (2007). Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19, 3170-3193.
61. Reumann, S., Buchwald, D., and Lingner, T. (2012). PredPlantPTS1: a web server for the prediction of plant peroxisomal proteins. Front. Plant Sci. 3:194. doi: 10.3389/fpls.2012.00194
62. Reumann, S., Ma, C., Lemke, S., and Babujee, L. (2004). AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol. 136, 2587-2608.
63. Reumann, S., Quan, S., Aung, K., Yang, P., Manandhar-Shrestha, K., Holbrook, D., 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 Physiol. 150, 125-143.
64. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Seraphin, B. (1999). A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032.
65. Sapir-Mir, M., Mett, A., Belausov, E., Tal-Meshulam, S., Frydman, A., Gidoni, D., et al. (2008). Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol. 148, 1219-1228.
66. Scherer, G. F., and Morre, D. J. (1978). Action and inhibition of endogenous phospholipases during isolation of plant membranes. Plant Physiol. 62, 933-937.
67. Schuhmann, H., Huesgen, P., Gietl, C., and Adamska, I. (2008). The DEG15 serine protease cleaves peroxisomal targeting signal 2-containing proteins in Arabidopsis. Plant Physiol. 148, 1847-1856.
68. Simkin, A. J., Guirimand, G., Papon, N., Courdavault, V., Thabet, I., Ginis, O., et al. (2011). Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta. Planta 234, 903-914.
69. Strader, L. C., Wheeler, D. L., Christensen, S. E., Berens, J. C., Cohen, J. D., Rampey, R. A., et al. (2011). Multiple facets of Arabidopsis seedling development require indole-3-butyric acid-derived auxin. Plant Cell 23, 984-999.
70. Tanz, S. K., Castleden, I., Hooper, C. M., Vacher, M., Small, I., and Millar, A. H. (2013). SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res. 41, D1185-D1191.
71. Timm, S., Florian, A., Arrivault, S., Stitt, M., Fernie, A., and Bauwe, H. (2012). Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett. 586, 3692-3696.
72. Tolbert, N. E., Oeser, A., Kisaki, T., Hageman, R. H., and Yamazaki, R. K. (1968). Peroxisomes from spinach leaves containing enzymes related to glycolate metabolism. J. Biol. Chem. 243, 5179-5184.
73. Tolbert, N. E., Oeser, A., Yamazaki, R. K., Hageman, R. H., and Kisaki, T. (1969). A survey of plants for leaf peroxisomes. Plant Physiol. 44, 135-147.
74. van der Zand, A., Gent, J., Braakman, I., and Tabak, H. F. (2012). Biochemically distinct vesicles from the endoplasmic reticulum fuse to form peroxisomes. Cell 149, 397-409.
75. Van Leene, J., Boruc, J., De Jaeger, G., Russinova, E., and De Veylder, L. (2011). A kaleidoscopic view of the Arabidopsis core cell cycle interactome. Trends Plant Sci. 16, 141-150.
76. Van Leene, J., Witters, E., Inze, D., and De Jaeger, G. (2008). Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci. 13, 517-520.
77. Wiszniewski, A. A., Zhou, W., Smith, S. M., and Bussell, J. D. (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 Mol. Biol. 69, 503-515.
78. Yates, J. R. III. (2000). Mass spectrometry. From genomics to proteomics. Trends Genet. 16, 5-8.
79. Zhi, W., Wang, M., and She, J.-X. (2011). Selected reaction monitoring (SRM) mass spectrometry without isotope labeling can be used for rapid protein quantification. Rapid Commun. Mass Spectrom. 25, 1583-1588.
80. Zhu, J. K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273.
81. Zolman, B. K., Yoder, A., and Bartel, B. (2000). Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics 156, 1323-1337.