Arabidopsis ABERRANT PEROXISOME MORPHOLOGY9 is a peroxin that recruits the PEX1-PEX6 complex to peroxisomes

Plant Cell

Volumn 23, Issue 4, 2011, Pages 1573-1587

  Goto, Shino ^a,b   Mano, Shoji ^a,b   Nakamori, Chihiro ^a   Nishimura, Mikio ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 79957696639     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.080770     Document Type: Article

References (73)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Arai, Y., Hayashi, M., and Nishimura, M. (2008). Proteomic identification and characterization of a novel peroxisomal adenine nucleotide transporter supplying ATP for fatty acid b-oxidation in soybean and Arabidopsis. Plant Cell 20: 3227-3240.
3. Babujee, L., Wurtz, V., Ma, C., Lueder, F., Soni, P., van Dorsselaer, A., and Reumann, S. (2010). The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes. J. Exp. Bot. 61: 1441-1453.
4. Bell, C.J., and Ecker, J.R. (1994). Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19: 137-144.
5. Birschmann, I., Stroobants, A.K., van den Berg, M., Schäfer, A., Rosenkranz, K., Kunau, W.-H., and Tabak, H.F. (2003). Pex15p of Saccharomyces cerevisiae provides a molecular basis for recruitment of the AAA peroxin Pex6p to peroxisomal membranes. Mol. Biol. Cell 14: 2226-2236.
6. Boisson-Dernier, A., Frietsch, S., Kim, T.-H., Dizon, M.B., and Schroeder, J.I. (2008). The peroxin loss-of-function mutation abstinence by mutual consent disrupts male-female gametophyte recognition. Curr. Biol. 18: 63-68.
7. Bracha-Drori, K., Shichrur, K., Katz, A., Oliva, M., Angelovici, R., Yalovsky, S., and Ohad, N. (2004). Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40: 419-427.
8. Brown, L.A., and Baker, A. (2008). Shuttles and cycles: Transport of proteins into the peroxisome matrix (review). Mol. Membr. Biol. 25: 363-375.
9. 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.
10. 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.
11. Distel, B., et al. (1996). A unified nomenclature for peroxisome biogenesis factors. J. Cell Biol. 135: 1-3.
12. Elgersma, Y., Kwast, L., van den Berg, M., Snyder, W.B., Distel, B., Subramani, S., and Tabak, H.F. (1997). Overexpression of Pex15p, a phosphorylated peroxisomal integral membrane protein required for peroxisome assembly in S. cerevisiae, causes proliferation of the endoplasmic reticulum membrane. EMBO J. 16: 7326-7341.
13. Erdmann, R., Veenhuis, M., Mertens, D., and Kunau, W.-H. (1989). Isolation of peroxisome-deficient mutants of Saccharomyces cerevi-siae. Proc. Natl. Acad. Sci. USA 86: 5419-5423.
14. Eubel, H., Meyer, E.H., Taylor, N.L., Bussell, J.D., O'Toole, N., Heazlewood, J.L., Castleden, I., Small, I.D., Smith, S.M., and Millar, A.H. (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.
15. Faber, K.N., Heyman, J.A., and Subramani, S. (1998). Two AAA family peroxins, PpPex1p and PpPex6p, interact with each other in an ATP-dependent manner and are associated with different subcellular membranous structures distinct from peroxisomes. Mol. Cell. Biol. 18: 936-943.
16. Fan, J., Quan, S., Orth, T., Awai, C., Chory, J., and Hu, J. (2005). The Arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol. 139: 231-239.
17. Footitt, S., Marquez, J., Schmuths, H., Baker, A., Theodoulou, F.L., and Holdsworth, M. (2006). Analysis of the role of COMATOSE and peroxisomal b-oxidation in the determination of germination potential in Arabidopsis. J. Exp. Bot. 57: 2805-2814.
18. Fujiki, Y. (2000). Peroxisome biogenesis and peroxisome biogenesis disorders. FEBS Lett. 476: 42-46.
19. Fukao, Y., Hayashi, Y., Mano, S., Hayashi, M., and Nishimura, M. (2001). Developmental analysis of a putative ATP/ADP carrier protein localized on glyoxysomal membranes during the peroxisome transition in pumpkin cotyledons. Plant Cell Physiol. 42: 835-841.
20. Geisbrecht, B.V., Collins, C.S., Reuber, B.E., and Gould, S.J. (1998). Disruption of a PEX1-PEX6 interaction is the most common cause of the neurologic disorders Zellweger syndrome, neonatal adrenoleuko-dystrophy, and infantile Refsum disease. Proc. Natl. Acad. Sci. USA 95: 8630-8635.
21. Grefen, C., Lalonde, S., and Obrdlik, P. (2007). Split-ubiquitin system for identifying protein-protein interactions in membrane and full-length proteins. Curr. Protoc. Neurosci. 41: 5.27.1-5.27.41.
22. Halbach, A., Landgraf, C., Lorenzen, S., Rosenkranz, K., Volkmer-Engert, R., Erdmann, R., and Rottensteiner, H. (2006). Targeting of the tail-anchored peroxisomal membrane proteins PEX26 and PEX15 occurs through C-terminal PEX19-binding sites. J. Cell Sci. 119: 2508-2517.
23. Hayashi, M., and Nishimura, M. (2006). Arabidopsis thaliana-A model organism to study plant peroxisomes. Biochim. Biophys. Acta 1763: 1382-1391.
24. Hayashi, M., Nito, K., Takei-Hoshi, R., Yagi, M., Kondo, M., Suenaga, A., Yamaya, T., and Nishimura, M. (2002). Ped3p is a peroxisomal ATP-binding cassette transporter that might supply substrates for fatty acid b-oxidation. Plant Cell Physiol. 43: 1-11.
25. Hayashi, M., Toriyama, K., Kondo, M., and Nishimura, M. (1998). 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid b-oxidation. Plant Cell 10: 183-195.
26. Hu, J.P., 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.
27. Huhse, B., Rehling, P., Albertini, M., Blank, L., Meller, K., and Kunau, W.H. (1998). Pex17p of Saccharomyces cerevisiae is a novel peroxin and component of the peroxisomal protein translocation machinery. J. Cell Biol. 140: 49-60.
28. 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.
29. Kamada-Nobusada, T., Hayashi, M., Fukazawa, M., Sakakibara, H., and Nishimura, M. (2008). A putative peroxisomal polyamine oxi-dase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol. 49: 1272-1282.
30. Kamigaki, A., Kondo, M., Mano, S., Hayashi, M., and Nishimura, M. (2009). Suppression of peroxisome biogenesis factor 10 reduces cuticular wax accumulation by disrupting the ER network in Arabi-dopsis thaliana. Plant Cell Physiol. 50: 2034-2046.
31. Kanai, M., Nishimura, M., and Hayashi, M. (2010). A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Plant J. 62: 936-947.
32. 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.
33. Khan, B.R., and Zolman, B.K. (2010). pex5 Mutants that differentially disrupt PTS1 and PTS2 peroxisomal matrix protein import in Arabi-dopsis. Plant Physiol. 154: 1602-1615.
34. Kiel, J.A.K.W., Emmrich, K., Meyer, H.E., and Kunau, W.-H. (2005). Ubiquitination of the peroxisomal targeting signal type 1 receptor, Pex5p, suggests the presence of a quality control mechanism during peroxisomal matrix protein import. J. Biol. Chem. 280: 1921-1930.
35. Konieczny, A., and Ausubel, F.M. (1993). A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4: 403-410.
36. Koroleva, O.A., Tomlinson, M.L., Leader, D., Shaw, P., and Doonan, J.H. (2005). High-throughput protein localization in Arabidopsis using Agrobacterium-mediated transient expression of GFP-ORF fusions. Plant J. 41: 162-174.
37. Kragler, F., Lametschwandtner, G., Christmann, J., Hartig, A., and Harada, J.J. (1998). Identification and analysis of the plant peroxisomal targeting signal 1 receptor NtPEX5. Proc. Natl. Acad. Sci. USA 95: 13336-13341.
38. 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.
39. -DDCt method. Methods 25: 402-408.
40. + uniporters. J. Biol. Chem. 278: 45603-45610.
41. Mano, S., Nakamori, C., Hayashi, M., Kato, A., Kondo, M., and Nishimura, M. (2002). Distribution and characterization of peroxi-somes in Arabidopsis by visualization with GFP: Dynamic morphology and actin-dependent movement. Plant Cell Physiol. 43: 331-341.
42. Mano, S., Nakamori, C., Kondo, M., Hayashi, M., and Nishimura, M. (2004). An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J. 38: 487-498.
43. Mano, S., Nakamori, C., Nito, K., Kondo, M., and Nishimura, M. (2006). The Arabidopsis pex12 and pex13 mutants are defective in both PTS1- and PTS2-dependent protein transport to peroxisomes. Plant J. 47: 604-618.
44. Matsumoto, N., Tamura, S., and Fujiki, Y. (2003). The pathogenic peroxin Pex26p recruits the Pex1p-Pex6p AAA ATPase complexes to peroxisomes. Nat. Cell Biol. 5: 454-460.
45. Meinecke, M., Cizmowski, C., Schliebs, W., Krüger, V., Beck, S., Wagner, R., and Erdmann, R. (2010). The peroxisomal importomer constitutes a large and highly dynamic pore. Nat. Cell Biol. 12: 273-277.
46. Merzlyak, E.M., Goedhart, J., Shcherbo, D., Bulina, M.E., Shcheglov, A.S., Fradkov, A.F., Gaintzeva, A., Lukyanov, K.A., Lukyanov, S., Gadella, T.W., and Chudakov, D.M. (2007). Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat. Methods 4: 555-557.
47. Miyata, N., and Fujiki, Y. (2005). Shuttling mechanism of peroxisome targeting signal type 1 receptor Pex5: ATP-independent import and ATP-dependent export. Mol. Cell. Biol. 25: 10822-10832.
48. Mullen, R.T., Flynn, C.R., and Trelease, R.N. (2001). How are perox-isomes formed? The role of the endoplasmic reticulum and peroxins. Trends Plant Sci. 6: 256-261.
49. Nair, D.M., Purdue, P.E., and Lazarow, P.B. (2004). Pex7p translocates in and out of peroxisomes in Saccharomyces cerevisiae. J. Cell Biol. 167: 599-604.
50. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., and Kimura, T. (2007). Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104: 34-41.
51. Nishimura, M., Takeuchi, Y., De Bellis, L., and Hara-Nishimura, I. (1993). Leaf peroxisomes are directly transformed to glyoxysomes during senescence of pumpkin cotyledons. Protoplasma 175: 131-137.
52. 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.
53. Nito, K., Kamigaki, A., Kondo, M., Hayashi, M., and Nishimura, M. (2007). Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants. Plant Cell Physiol. 48: 763-774.
54. + channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proc. Natl. Acad. Sci. USA 101: 12242-12247.
55. Platta, H.W., El Magraoui, F., Schlee, D., Grunau, S., Girzalsky, W., and Erdmann, R. (2007). Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J. Cell Biol. 177: 197-204.
56. Platta, H.W., and Erdmann, R. (2007). The peroxisomal protein import machinery. FEBS Lett. 581: 2811-2819.
57. Platta, H.W., Grunau, S., Rosenkranz, K., Girzalsky, W., and Erdmann, R. (2005). Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol. Nat. Cell Biol. 7: 817-822.
58. Preisig-Müller, R., and Kindl, H. (1993). Thiolase mRNA translated in vitro yields a peptide with a putative N-terminal presequence. Plant Mol. Biol. 22: 59-66.
59. Rehling, P., Skaletz-Rorowski, A., Girzalsky, W., Voorn-Brouwer, T., Franse, M.M., Distel, B., Veenhuis, M., Kunau, W.H., and Erdmann, R. (2000). Pex8p, an intraperoxisomal peroxin of Saccharomyces cerevisiae required for protein transport into peroxisomes binds the PTS1 receptor pex5p. J. Biol. Chem. 275: 3593-3602.
60. Reumann, S., Babujee, L., Ma, C., Wienkoop, S., Siemsen, T., Antonicelli, G.E., Rasche, N., Lüder, F., Weckwerth, W., and Jahn, O. (2007). Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19: 3170-3193.
61. Reumann, S., Ma, C.L., Lemke, S., and Babujee, L. (2004). AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol. 136: 2587-2608.
62. Rottensteiner, H., Kramer, A., Lorenzen, S., Stein, K., Landgraf, C., Volkmer-Engert, R., and Erdmann, R. (2004). Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals. Mol. Biol. Cell 15: 3406-3417.
63. Schueller, N., Holton, S.J., Fodor, K., Milewski, M., Konarev, P., Stanley, W.A., Wolf, J., Erdmann, R., Schliebs, W., Song, Y.H., and Wilmanns, M. (2010). The peroxisomal receptor Pex19p forms a helical mPTS recognition domain. EMBO J. 29: 2491-2500.
64. 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.
65. Shibata, H., Kashiwayama, Y., Imanaka, T., and Kato, H. (2004). Domain architecture and activity of human Pex19p, a chaperone-like protein for intracellular trafficking of peroxisomal membrane proteins. J. Biol. Chem. 279: 38486-38494.
66. Singh, T., Hayashi, M., Mano, S., Arai, Y., Goto, S., and Nishimura, M. (2009). Molecular components required for the targeting of PEX7 to peroxisomes in Arabidopsis thaliana. Plant J. 60: 488-498.
67. 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: 1809-1819.
68. Tamura, S., Yasutake, S., Matsumoto, N., and Fujiki, Y. (2006). Dynamic and functional assembly of the AAA peroxins, Pex1p and Pex6p, and their membrane receptor Pex26p. J. Biol. Chem. 281: 27693-27704.
69. Wain, R.L., and Wightman, F. (1954). The growth regulating activity of certain v-substituted alkyl carboxylic acids in relation to their b-oxidation within the plant. Proc. R. Soc. Lond. B Biol. Sci. 142: 525-536.
70. Wesley, S.V., et al. (2001). Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27: 581-590.
71. 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.
72. Zolman, B.K., Monroe-Augustus, M., Silva, I.D., and Bartel, B. (2005). Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 17: 3422-3435.
73. 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.