The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5

Molecular Biology of the Cell

Volumn 16, Issue 2, 2005, Pages 573-583

  Woodward, Andrew W ^a   Bartel, Bonnie ^a  

^a RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MEMBRANE PROTEIN; MUTANT PROTEIN; PEROXIN; PROTEIN PEROXIN 5; PROTEIN PEROXIN 7; PROTEIN PTS1; PROTEIN PTS2; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; COTYLEDON; FATTY ACID OXIDATION; GENE ISOLATION; GENE MUTATION; GENE TARGETING; NONHUMAN; PEROXISOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; BLOTTING, WESTERN; GENES, PLANT; GREEN FLUORESCENT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PEROXISOMES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS;

EID: 12844279810     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-05-0422     Document Type: Article

References (82)

1. Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., and Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9, 841-857.
2. Aida, M., Vernoux, T., Furutani, M., Traas, J., and Tasaka, M. (2002). Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129, 3965-3974.
3. Albertini, M., Rehling, P., Erdmann, R., Girzalsky, W., Kiel, J.A.K.W., Veenhuis, M., and Kunau, W. H. (1997). Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell 89, 83-92.
4. Alonso, J. M. et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
5. Asamizu, E., Nakamura, Y., Sato, S., and Tabata, S. (2000). A large scale analysis of cDNA in Arabidopsis thaliana: generation of 12,028 non-redundant expressed sequence tags from normalized and size-selected cDNA libraries. DNA Res. 7, 175-180.
6. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Strahl, K. (1995). Short Protocols in Molecular Biology, New York: John Wiley and Sons, Inc.
7. Bartel, B., LeClere, S., Magidin, M., and Zolman, B. K. (2001). Inputs to the active indole-3-acetic acid pool: de novo synthesis, conjugate hydrolysis, and indole-3-butyric acid β-oxidation. J. Plant Growth Regul. 20, 198-216.
8. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S. R., Griffiths-Jones, S., Howe, K. L., Marshall, M., and Sonnhammer, E. L. (2002). The Pfam protein families database. Nucleic Acid Res. 30, 276-280.
9. Beevers, H. (2002). Early research on peroxisomes in plants. In: Plant Peroxisomes: Biochemistry, Cell Biology, and Biotechnological Applications, ed. A. Baker and I. A. Graham, Dordrecht, The Netherlands: Kluwer, 1-17.
10. Bevan, M. (1984). Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 22, 8711-8721.
11. Braverman, N., Dodt, G., Gould, S. J., and Valle, D. (1998). An isoform of Pex5p, the human PTS1 receptor, is required for the import of PTS2 proteins into peroxisomes. Hum. Mol. Genet. 7, 1195-1205.
12. Braverman, N., Steel, G., Obie, C., Moser, A., Moser, H., Gould, S. J., and Valle, D. (1997). Human PEX7 encodes the peroxisomal PTS2 receptor and is responsible for rhizomelic chondrodysplasia punctata. Nat. Genet. 15, 369-376.
13. Brickner, D. G., Brickner, J. H., and Olsen, L. J. (1998). Sequence analysis of a cDNA encoding Pex5p, a peroxisomal targeting signal type 1 receptor from Arabidopsis. Plant Physiol 118, 330.
14. Chang, C. C., Warren, D. S., Sacksteder, K. A., and Gould, S. J. (1999). PEX12 interacts with PEX5 and PEX10 and acts downstream of receptor docking in peroxisomal matrix protein import. J. Cell Biol. 147, 761-773.
15. Charlton, W. A., and López-Huertas, E. (2002). PEX genes in plants and other organisms. In: Plant Peroxisomes: Biochemistry, Cell Biology, and Biotechnoiogical Applications, ed. A. Baker and I. A. Graham, Dordrecht, The Netherlands: Kluwer, 385-426.
16. Clough, S. J., and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
17. Collins, C. S., Kalish, J. E., Morrell, J. C., McCaffery, J. M., and Gould, S. J. (2000). The peroxisome biogenesis factors Pex4p, Pex22p, Pex1p, and Pex6p act in the terminal steps of peroxisomal matrix protein import. Mol. Cell Biol. 20, 7516-7526.
18. Dammai, V., and Subramani, S. (2001). The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisome matrix and recycled to the cytosol. Cell 105, 187-196.
19. Davis, S. J., and Vierstra, R. D. (1998). Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants. Plant Mol. Biol. 36, 521-528.
20. Dodt, G., Braverman, N., Wong, C., Moser, A., Moser, H. W., Watkins, P., Valle, D., and Gould, S. J. (1995). Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat. Genet. 9, 115-125.
21. Dodt, G., and Gould, S. J. (1996). Multiple PEX genes are required for proper subcellular distribution and stability of Pex5p, the PTS1 receptor: evidence that PTS1 protein import is mediated by a cycling receptor. J. Cell Biol. 135, 1763-1774.
22. Dodt, G., Warren, D., Becker, E., Rehling, P., and Gould, S. J. (2001). Domain mapping of human PEX5 reveals functional and structural similarities to Saccharomyces cerevisiae Pex18p and Pex21p. J. Biol. Chem. 276, 41769-41781.
23. Einwächter, H., Sowinski, S., Kunau, W. H., and Schliebs, W. (2001). Yarrowia lipolytica Pex20p, Saccharomyces cerevisiae Pex18p/Pex21p and mammalian Pex5pL fulfil a common function in the early steps of the peroxisomal PTS2 import pathway. EMBO Rep. 2, 1035-1039.
24. Flynn, C. R., Mullen, R. T., and Trelease, R. N. (1998). Mutational analyses of a type 2 peroxisomal targeting signal that is capable of directing oligomeric protein import into tobacco BY-2 glyoxysomes. Plant J. 16, 709-720.
25. Footitt, S., Slocombe, S. P., Larner, V., Kurup, S., Wu, Y., Larson, T., Graham, I., Baker, A., and Holdsworth, M. (2002). Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J. 21, 2912-2922.
26. Froman, B. E., Edwards, P. C., Bursch, A. G., and Dehesh, K. (2000). ACX3, a novel medium-chain acyl-Coenzyme A oxidase from Arabidopsis. Plant Physiol. 123, 733-741.
27. Fulda, M., Schnurr, J., Abbadi, A., Heinz, E., and Browse, J. (2004). Peroxisomal acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16, 394-405.
28. Fulda, M., Shockey, J., Werber, M., Wolter, F. P., and Heinz, E. (2002). Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid β-oxidation. Plant J. 32, 93-103.
29. Gälweiler, L., Guan, C, Müller, A., Wisman, E., Mendgen, K., Yephremov, A., and Palme, K. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226-2230.
30. Gatto, G. J., Jr., Geisbrecht, B. V., Gould, S. J., and Berg, J. M. (2000). Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat. Struct. Biol. 7, 1091-1095.
31. Gerhardt, B. (1992). Fatty acid degradation in plants. Prog. Lipid Res. 31, 417-446.
32. Germain, V., Rylott, E. L., Larson, T. R., Sherson, S. M., Bechntold, N., Carde, J. P., Bryce, J. H., Graham, I. A., and Smith, S. M. (2001). Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid β-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant J. 28, 1-12.
33. Gould, S. J., Keller, G. A., Hosken, N., Wilkinson, J., and Subramani, S. (1989). A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108, 1657-1664.
34. Graham, I. A., and Eastmond, P. J. (2002). Pathways of straight and branched chain fatty acid catabolism in higher plants. Prog. Lipid Res. 41, 156-181.
35. Gurvitz, A., Langer, S., Piskacek, M., Hamilton, B., Ruis, H., and Hartig, A. (2000). Predicting the function and subcellular location of Caenorhabditis elegans proteins similar to Saccharomyces cerevisiae β-oxidation enzymes. Yeast 17, 188-200.
36. Hardtke, C. S., and Berleth, T. (1998). The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405-1411.
37. Haughn, G.W., and Somerville, C. (1986). Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204, 430-434.
38. Hayashi, M., Nito, K., Toriyama-Kato, K., Kondo, M., Yamaya, T., and Nishimura, M. (2000). AtPex14p maintains peroxisomal functions by determining protein targeting to three kinds of plant peroxisomes. EMBO J. 19, 5701-5710.
39. Hayashi, M., Toriyama, K., Kondo, M., and Nishimura, M. (1998). 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid β-oxidation. Plant Cell 10, 183-195.
40. Hooks, M.A., Kellas, F., and Graham, I.A. (1999). Long-chain acyl-CoA oxidases of Arabidopsis. Plant J. 20, 1-13.
41. Hu, J., Aguirre, M., Peto, C., Alonso, J., Ecker, J., and Chory, J. (2002). A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 297, 405-409.
42. Johnson, T. L., and Olsen, L. J. (2001). Building new models for peroxisome biogenesis. Plant Physiol. 127, 731-739.
43. Johnson, T. L., and Olsen, L. J. (2003). Import of the peroxisomal targeting signal type 2 protein 3-ketoacyl-Coenzyme A thiolase into glyoxysomes. Plant Physiol. 133, 1991-1999.
44. Kamada, T., Nito, K., Hayashi, H., Mano, S., Hayashi, M., and Nishimura, M. (2003). Functional differentiation of peroxisomes revealed by expression profiles of peroxisomal genes in Arabidopsis thaliana. Plant Cell Physiol. 44, 1275-1289.
45. Kato, A., Hayashi, M., Takeuchi, Y., and Nishimura, M. (1996). cDNA cloning and expression of a gene for 3-ketoacyl-CoA thiolase in pumpkin cotyledons. Plant Mol. Biol. 31, 843-852.
46. Kindl, H. (1993). Fatty acid degradation in plant peroxisomes: function and biosynthesis of the enzymes involved. Biochimie 75, 225-230.
47. L-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396.
48. LeClere, S., and Bartel, B. (2001). A library of Arabidopsis 35S-cDNA lines for identifying novel mutants. Plant Mol. Biol. 46, 695-703.
49. Liepman, A. H., and Olsen, L. J. (2001). Peroxisomal alanine: glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant J. 25, 487-498.
50. Lin, Y., Sun, L., Nguyen, L. V., Rachubinski, R. A., and Goodman, H. M. (1999). The Pex16p homolog SSE1 and storage organelle formation in Arabidopsis seeds. Science 284, 328-330.
51. Ludwig-Müller, J., Sass, S., Sutter, E. G., Wodner, M., and Epstein, E. (1993). Indole-3-butyric acid in Arabidopsis thaliana. I. Identification and quantification. Plant Growth Regul. 13, 179-187.
52. Matsumura, T., Otera, H., and Fujiki, Y. (2000). Disruption of the interaction of the longer isoform of Pex5p, Pex5pL, with Pex7p abolishes peroxisome targeting signal type 2 protein import in mammals. Study with a novel PEX5-impaired CHO cell mutant. J. Biol. Chem. 275, 21715-21721.
53. Monroe-Augustus, M. (2004). Genetic approaches to elucidating the mechanisms of indole-3-acetic acid and indole-3-butyric acid function in Arabidopsis thaliana. PhD thesis, Rice University, Houston.
54. Motley, A. M. et al. (1997). Rhizomelic chondrodysplasia punctata is a peroxisomal protein targeting disease caused by a non-functional PTS2 receptor. Nat. Genet. 15, 377-380.
55. Motley, A. M., Hettema, E. H., Ketting, R., Plasterk, R., and Tabak, H. F. (2000). Caenorhabditis elegans has a single pathway to target matrix proteins to peroxisomes. EMBO Rep. 1, 40-46.
56. Mukai, S., Ghaedi, K., and Fujiki, Y. (2002). Intracellular localization, function, and dysfunction of the peroxisome-targeting signal type 2 receptor, Pex7p, in mammalian cells. J. Biol. Chem. 277, 9548-9561.
57. Mullen, R. T. (2002). Targeting and import of matrix proteins into peroxisomes. In: Plant Peroxisomes: Biochemistry, Cell Biology, and Biotechnological Applications, ed. A. Baker and I. A. Graham, Dordrecht, The Netherlands: Kluwer, 339-383.
58. Mullen, R. T., Flynn, C. R., and Trelease, R. N. (2001). How are peroxisomes formed? The role of the endoplasmic reticulum and peroxins. Trends Plant Sci. 6, 256-261.
59. Neuberger, G., Maurer-Stroh, S., Eisenhaber, B., Hartig, A., and Eisenhaber, F. (2003). Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J. Mol. Biol. 328, 567-579.
60. Nito, K., Hayashi, M., and Nishimura, M. (2002). Direct interaction and determination of binding domains among peroxisomal import factors in Arabidopsis thaliana. Plant Cell Physiol. 43, 355-366.
61. Osumi, T., Tsukamoto, T., Hata, S., Yokota, S., Miura, S., Fujiki, Y., Hajikata, M., Miyazawa, S., and Hashimoto, T. (1991). Amino-terminal presequence of the precursor of peroxisomal 3-ketoacyl-CoA thiolase is a cleavable signal peptide for peroxisomal targeting. Biochem. Biophys. Res. Commun. 181, 947-954.
62. Purdue, P. E., Yang, X., and Lazarow, P. B. (1998). Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J. Cell Biol. 143, 1859-1869.
63. Purdue, P. E., Zhang, J. W., Skoneczny, M., and Lazarow, P. B. (1997). Rhizomelic chondrodysplasia punctata is caused by deficiency of human PEX7, a homologue of the yeast PTS2 receptor. Nat. Genet. 15, 381-384.
64. Rehling, P., Marzioch, M., Niesen, F., Wittke, E., Veenhuis, M., and Kunau, W. H. (1996). The import receptor for the peroxisomal targeting signal 2 (PTS2) in Saccharomyces cerevisiae is encoded by the PAS7 gene. EMBO J. 15, 2901-2913.
65. Reumann, S. (2002). The photorespiratory pathway of leaf peroxisomes. In: Plant Peroxisomes: Biochemistry, Cell biology, and Biotechnological Applications, ed. A. Baker and I. A. Graham, Dordrecht, The Netherlands: Kluwer Academic Publishers, 141-189.
66. 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.
67. Rylott, E. L., Rogers, C. A., Gilday, A. D., Edgell, T., Larson, T. R., and Graham, I. A. (2003). Arabidopsis mutants in short- and medium-chain acyl-CoA oxidase activities accumulate acyl-CoAs and reveal that fatty acid β-oxidation is essential for embryo development. J. Biol. Chem. 278, 21370-21377.
68. Schmid, K. J., Sörensen, T. R., Stracke, R., Törjek, O., Altmann, T., Mitchell-Olds, T., and Weisshaar, B. (2003). Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res. 13, 1250-1257.
69. Schumann, U., Gietl, C., and Schmid, M. (1999). Sequence analysis of a cDNA encoding Pex7p, a peroxisomal targeting signal 2 receptor from Arabidopsis thaliana. Plant Physiol. 120, 339
70. Schumann, U., Wanner, G., Veenhuis, M., Schmid, M., and Gietl, C. (2003). AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc. Natl. Acad. Sci. USA 100, 9626-9631.
71. Sichting, M., Schell-Steven, A., Prokisch, H., Erdmann, R., and Rottensteiner, H. (2003). Pex7p and Pex20p of Neurospora crassa function together in PTS2-dependent protein import into peroxisomes. Mol. Biol. Cell 14, 810-821.
72. Sparkes, I. A., Brandizzi, F., Slocombe, S. P., El-Shami, M., Hawes, C., and Baker, A. (2003). An Arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiol. 133, 1809-1919.
73. Sparkes, I. A., and Baker, A. (2002). Peroxisome biogenesis and protein import in plants, animals and yeasts: enigma and variations? (Review). Mol. Membr. Biol. 19, 171-185.
74. Stasinopoulos, T. C., and Hangarter, R. P. (1990). Preventing photochemistry in culture media by long-pass light filters alters growth of cultured tissues. Plant Physiol. 93, 1365-1369.
75. Takada, S., Hibara, K., Ishida, T., and Tasaka, M. (2001). The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128, 1127-1135.
76. van den Brink, D. M., Brites, P., Haasjes, J., Wierzbicki, A. S., Mitchell, J., Lambert-Hamill, M., de Belleroche, J., Jansen, G. A., Waterham, H. R., and Wanders, R.J.A. (2003). Identification of PEX7 as the second gene involved in Refsum disease. Am. J. Hum. Genet. 72, 471-477.
77. Wasternack, C., and Hause, B. (2002). Jamonates and octadecanoids: signals in plant stress responses and development. Prog. Nucleic Acid Res. Mol. Biol. 72, 165-221.
78. Yamada, K. et al. (2003). Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302, 842-846.
79. Zolman, B. K., and Bartel, B. (2004). An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proc. Natl. Acad, Sci. USA 101, 1786-1791.
80. Zolman, B. K., Monroe-Augustus, M., Thompson, B., Hawes, J. W., Krukenberg, K. A., Matsuda, S.P.T., and Bartel, B. (2001a). chy1, an Arabidopsis mutant with impaired β-oxidation, is defective in a peroxisomal β-hydroxyisobutyryl-CoA hydrolase. J. Biol. Chem. 276, 31037-31046.
81. Zolman, B. K., Silva, I. D., and Bartel, B. (2001b). The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal-fatty acid β-oxidation. Plant Physiol. 127, 1266-1278.
82. 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.