The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins

Plant Cell

Volumn 16, Issue 12, 2004, Pages 3285-3303

  Carter, Clay ^a   Pan, Songqin ^a   Zouhar, Jan ^a   Avila, Emily L ^a   Girke, Thomas ^a   Raikhel, Natasha V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PROTEINS; TISSUE;

ARABIDOPSIS THALIANA; MEMBRANE PROTEINS; VACUOLAR PROTEINS;

PLANTS (BOTANY);

BIOSYNTHESIS; LIQUID CHROMATOGRAPHY; MASS SPECTROSCOPY; PLANT TISSUES; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; MEMBRANE PROTEIN; PEPTIDE; PROTEIN SUBUNIT; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SNARE PROTEIN; VESICULAR TRANSPORT PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL VACUOLE; CHEMISTRY; CYTOSKELETON; ISOLATION AND PURIFICATION; MEMBRANE FUSION; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PLANT LEAF; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; PROTEOMICS; PROTOPLAST; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOSKELETON; MEMBRANE FUSION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDES; PLANT LEAVES; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; PROTEOME; PROTEOMICS; PROTOPLASTS; SIGNAL TRANSDUCTION; SNARE PROTEINS; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 15744385479     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.027078     Document Type: Article

References (81)

1. Ahmed, S.U., Rojo, E., Kovaleva, V., Venkataraman, S., Dombrowski, J.E., Matsuoka, K., and Raikhel, N.V. (2000). The plant vacuolar sorting receptor AtELP is involved in transport of NH(2)-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J. Cell Biol. 149, 1335-1344.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Balmer, Y., Koller, A., del Val, G., Manieri, W., Schurmann, P., and Buchanan, B.B. (2003). Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc. Natl. Acad. Sci. USA 100, 370-375.
4. Bannai, H., Tamada, Y., Maruyama, O., Nakai, K., and Miyano, S. (2002). Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18, 298-305.
5. Bednarek, S.Y., and Raikhel, N.V. (1991). The barley lectin carboxyl-terminal propeptide is a vacuolar protein sorting determinant in plants. Plant Cell 3, 1195-1206.
6. Bird, D.A., and Facchini, P.J. (2001). Berberine bridge enzyme, a key branch-point enzyme in benzylisoquinoline alkaloid biosynthesis, contains a vacuolar sorting determinant. Planta 213, 888-897.
7. Blancaflor, E.B. (2002). The cytoskeleton and gravitropism in higher plants. J. Plant Growth Regul. 21, 120-136.
8. Bock, J.B., Matern, H.T., Peden, A.A., and Scheller, R.H. (2001). A genomic perspective on membrane compartment organization. Nature 409, 839-841.
9. Boyce, J.M., Coates, D., Fricker, M.D., and Evans, D.E. (1994). Genomic sequence of a calnexin homolog from Arabidopsis thaliana. Plant Physiol. 106, 1691.
10. Bradford, M.M. (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.
11. Buchanan, B.B., Gruissem, W., and Jones, R.L. (2000). Biochemistry and Molecular Biology of Plants. (Rockville, MD: American Society of Plant Physiologists).
12. Cānovas, F.M., Dumas-Gaudot, E., Recorbet, G., Jorrin, J., Mock, H.P., and Rossignol, M. (2004). Plant proteome analysis. Proteomics 4, 285-298.
13. De, D.N. (2000). Plant Cell Vacuoles. (Collingwood, Australia: CSIRO Publishing).
14. 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.
15. Frigerio, L., Jolliffe, N.A., Di Cola, A., Felipe, D.H., Paris, N., Neuhaus, J.M., Lord, J.M., Ceriotti, A., and Roberts, L.M. (2001). The internal propeptide of the ricin precursor carries a sequence-specific determinant for vacuolar sorting. Plant Physiol. 126, 167-175.
16. Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J.B., Rudella, A., Sun, Q., and Wijk, K.J. (2004). In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: New proteins, new functions, and a plastid proteome database. Plant Cell 16, 478-499.
17. Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P.H., Steele-Mortimer, O., Paiement, J., Bergeron, J.J., and Desjardins, M. (2002). Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110, 119-131.
18. Garin, J., Diez, R., Kieffer, S., Dermine, J.F., Duclos, S., Gagnon, E., Sadoul, R., Rondeau, C., and Desjardins, M. (2001). The phagosome proteome: Insight into phagosome functions. J. Cell Biol. 152, 165-180.
19. Girke, T., Ozkan, M., Carter, D., and Raikhel, N.V. (2003). Towards a modeling infrastructure for studying plant cells. Plant Physiol. 132, 410-414.
20. Gomord, V., Denmat, L.A., Fitchette-Laine, A.C., Satiat-Jeunemaitre, B., Hawes, C., and Faye, L. (1997). The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER. Plant J. 11, 313-325.
21. Gruis, D., Schulze, J., and Jung, R. (2004). Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases. Plant Cell 16, 270-290.
22. Gu, S., Chen, J., Dobos, K.M., Bradbury, E.M., Belisle, J.T., and Chen, X. (2003). Comprehensive proteomic profiling of the membrane constituents of a Mycobacterium tuberculosis strain. Mol. Cell Proteomics 2, 1284-1296.
23. Hara-Nishimura, I.I., Shimada, T., Hatano, K., Takeuchi, Y., and Nishimura, M. (1998). Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10, 825-836.
24. Hayashi, Y., Yamada, K., Shimada, T., Matsushima, R., Nishizawa, N.K., Nishimura, M., and Hara-Nishimura, I. (2001). A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Plant Cell Physiol. 42, 894-899.
25. Heazlewood, J.L., Tonti-Filippini, J.S., Gout, A.M., Day, D.A., Whelan, J., and Millar, A.H. (2004). Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16, 241-256.
26. Hicks, G.R., Rojo, E., Hong, S., Carter, D.G., and Raikhel, N.V. (2004). Geminating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol. 134, 1227-1239.
27. Holwerda, B.C., Padgett, H.S., and Rogers, J.C. (1992). Proaleurain vacuolar targeting is mediated by short contiguous peptide interactions. Plant Cell 4, 307-318.
28. Jiang, L., and Rogers, J.C. (1998). Integral membrane protein sorting to vacuoles in plant cells: Evidence for two pathways. J. Cell Biol. 143, 1183-1199.
29. Jin, J.B., Kim, Y.A., Kim, S.J., Lee, S.H., Kim, D.H., Cheong, G.W., and Hwang, I. (2001). A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13, 1511-1526.
30. Kato, T., Morita, M.T., Fukaki, H., Yamauchi, Y., Uehara, M., Niihama, M., and Tasaka, M. (2002a). SGR2, a phospholipase-like protein, and ZIG/SGR4, a SNARE, are involved in the shoot gravitropism of Arabidopsis. Plant Cell 14, 33-46.
31. Kato, T., Morita, M.T., and Tasaka, M. (2002b). Role of endodermal cell vacuoles in shoot gravitropism. J. Plant Growth Regul. 21, 113-119.
32. Kelly, P.J., Bones, A., and Rossiter, J.T. (1998). Sub-cellular immunolocalization of the glucosinolate sinigrin in seedlings of Brassica juncea. Planta 206, 370-377.
33. Koide, Y., Matsuoka, K., Ohto, M., and Nakamura, K. (1999). The N-terminal propeptide and the C terminus of the precursor to 20-kilo-dalton potato tuber protein can function as different types of vacuolar sorting signals. Plant Cell Physiol. 40, 1152-1159.
34. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L.L. (2001). Predicting transmembrane protein topology with a Hidden Markov Model: Application to complete genomes. J. Mol. Biol. 305, 567-580.
35. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
36. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
37. Matsui, T., Nakayama, H., Yoshida, K., and Shinmyo, A. (2003). Vesicular transport route of horseradish C1a peroxidase is regulated by N- and C-terminal propeptides in tobacco cells. Appl. Microbiol. Biotechnol. 262, 517-522.
38. Matsuoka, K., Higuchi, T., Maeshima, M., and Nakamura, K. (1997). A vacuolar-type H+-ATPase in a nonvacuolar organelle is required for sorting of soluble vacuolar protein precursors in tobacco cells. Plant Cell 9, 533-546.
39. Matsuoka, K., and Nakamura, K. (1991). Propeptide of a precursor to a plant vacuolar protein required for vacuolar targeting. Proc. Natl. Acad. Sci. USA 88, 834-838.
40. Matsuoka, K., and Neuhaus, J.-M. (1999). Cis-elements of protein transport to the plant vacuoles. J. Exp. Bot. 50, 165-174.
41. Matsushima, R., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2003). A novel ER-derived compartment, the ER body, selectively accumulates a beta-glucosidase with an ER-retention signal in Arabidopsis. Plant J. 33, 493-502.
42. McKnight, T.D., Roessner, C.A., Devagupta, R., Scott, A.I., and Nessler, C.L. (1990). Nucleotide sequence of a cDNA encoding the vacuolar protein strictosidine synthase from Catharanthus roseus. Nucleic Acids Res. 18, 4939.
43. Melchers, L.S., Sela-Buurlage, M.B., Vloemans, S.A., Woloshuk, C.P., Van Roekel, J.S., Pen, J., van den Elzen, P.J., and Cornelissen, B.J. (1993). Extracellular targeting of the vacuolar tobacco proteins AP24, chitinase and beta 1,3-glucanase in transgenic plants. Plant Mol. Biol. 21, 583-593.
44. Mootha, V.K., et al. (2003). Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115, 629-640.
45. Morita, M.T., Kato, T., Nagafusa, K., Saito, C., Ueda, T., Nakano, A., and Tasaka, M. (2002). Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. Plant Cell 14, 47-56.
46. Neuhaus, J.M., Sticher, L., Meins, F., Jr., and Boller, T. (1991). A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc. Natl. Acad. Sci. USA 88, 10362-10366.
47. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6.
48. Peltier, J.B., Friso, G., Kalume, D.E., Roepstorff, P., Nilsson, F., Adamska, I., and van Wijk, K.J. (2000). Proteomics of the chloroplast: Systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12, 319-341.
49. Peters, C., Bayer, M.J., Bühler, S., Andersen, J.S., Mann, M., and Mayer, A. (2001). Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 409, 581-588.
50. Potocky, M., Elias, M., Profotova, B., Novotna, Z., Valentova, O., and Zarsky, V. (2003). Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217, 122-130.
51. Roitsch, T., Balibrea, M.E., Hofmann, M., Proels, R., and Sinha, A.K. (2003). Extracellular invertase: Key metabolic enzyme and PR protein. J. Exp. Bot. 54, 513-524.
52. Rojo, E., Gillmor, C.S., Kovaleva, V., Somerville, C.R., and Raikhel, N.V. (2001). VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell 1, 303-310.
53. Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V., and Fletcher, J.C. (2002). CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14, 969-977.
54. Rojo, E., Zouhar, J., Carter, C., Kovaleva, V., and Raikhel, N.V. (2003a). A unique mechanism for protein processing and degradation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100, 7389-7394.
55. Rojo, E., Zouhar, J., Kovaleva, V., Hong, S., and Raikhel, N.V. (2003b). The AtC-VPS protein complex is localized to the tonoplast and the prevacuolar compartment in Arabidopsis. Mol. Biol. Cell. 14, 361-369.
56. Ryan, C.A. (1980). Wound-regulated synthesis and vacuolar compartmentation of proteinase inhibitors in plant leaves. Curr. Top. Cell. Regul. 17, 1-23.
57. Sanderfoot, A.A., Assaad, F.F., and Raikhel, N.V. (2000). The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiol. 124, 1558-1569.
58. Sanderfoot, A.A., Kovaleva, V., Bassham, D.C., and Raikhel, N.V. (2001). Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol. Biol. Cell 12, 3733-3743.
59. Sanderfoot, A.A., Kovaleva, V., Zheng, H., and Raikhel, N.V. (1999). The t-SNARE AtVAM3p resides on the prevacuolar compartment in Arabidopsis root cells. Plant Physiol. 121, 929-938.
60. Sato, M.H., Nakamura, N., Ohsumi, Y., Kouchi, H., Kondo, M., Hara-Nishimura, I., Nishimura, M., and Wada, Y. (1997). The AtVAM3 encodes a syntaxin-related molecule implicated in the vacuolar assembly in Arabidopsis thaliana. J. Biol. Chem. 272, 24530-24535.
61. Schafer, D.A. (2004). Regulating actin dynamics at membranes: A focus on dynamin. Traffic 5, 463-469.
62. Schubert, M., Petersson, U.A., Haas, B.J., Funk, C., Schroder, W.P., and Kieselbach, T. (2002). Proteome map of the chloroplast lumen of Arabidopsis thaliana. J. Biol. Chem. 277, 8354-8365.
63. Shimada, T., et al. (2003). Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J. Biol. Chem. 278, 32292-32299.
64. Shimaoka, T., Ohnishi, M., Sazuka, T., Mitsuhashi, N., Hara-Nishimura, I., Shimazaki, K.I., Maeshima, M., Yokota, A., Tomizawa, K.I., and Mimura, T. (2004). Isolation of intact vacuoles and proteomic analysis of tonoplast from suspension-cultured cells of Arabidopsis thaliana. Plant Cell Physiol. 45, 672-683.
65. Singh-Zocchi, M., Andreasen, A., and Zocchi, G. (1999). Osmotic pressure contribution of albumin to colloidal interactions. Proc. Natl. Acad. Sci. USA 96, 6711-6715.
66. Surpin, M., and Raikhel, N. (2004). Traffic jams affect plant development and signal transduction. Nat. Rev. Mol. Cell Biol. 5, 100-109.
67. Surpin, M., Zheng, H., Morita, M.T., Saito, C., Avila, E., Blakeslee, J.J., Bandyopadhyay, A., Kovaleva, V., Carter, D., Murphy, A., Tasaka, M., and Raikhel, N. (2003). The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15, 2885-2899.
68. Sze, H., Schumacher, K., Muller, M.L., Padmanaban, S., and Taiz, L. (2002). A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H(+)-ATPase. Trends Plant Sci. 7, 157-161.
69. Szponarski, W., Sommerer, N., Boyer, J.C., Rossignol, M., and Gibrat, R. (2004). Large-scale characterization of integral proteins from Arabidopsis vacuolar membrane by two-dimensional liquid chromatography. Proteomics 4, 397-406.
70. Tian, G.W., et al. (2004). High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 35, 25-38.
71. Tusnády, G.E., and Simon, I. (1998). Principles governing amino acid composition of integral membrane proteins: Applications to topology prediction. J. Mol. Biol. 283, 489-506.
72. van Den Hazel, H.B., Kielland-Brandt, M.C., and Winther, J.R. (1996). Review: Biosynthesis and function of yeast vacuolar proteases. Yeast 12, 1-16.
73. Vitale, A., and Raikhel, N.V. (1999). What do proteins need to reach different vacuoles? Trends Plant Sci. 4, 149-155.
74. Wang, X. (2004). Lipid signaling. Curr. Opin. Plant Biol. 7, 329-336.
75. Wang, Y., Sun, J., and Chitnis, P. (2000). Proteomic study of the peripheral proteinsfrom thylakoid membranes of the cyanobacterium Synechocystis sp. PCC6803. Electrophoresis 21, 1746-1754.
76. Whitelegge, J.P. (2002). Plant proteomics: BLASTing out of a MudPIT. Proc. Natl. Acad. Sci. USA 99, 11564-11566.
77. Wickner, W. (2002). Yeast vacuoles and membrane fusion pathways. EMBO J 21, 1241-1247.
78. Wickner, W., and Haas, A. (2000). Yeast homotypic vacuole fusion: A window on organelle trafficking mechanisms. Annu. Rev. Biochem. 69, 247-275.
79. Yamada, K., Matsushima, R., Nishimura, M., and Hara-Nishimura, I. (2001). A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing Arabidopsis leaves. Plant Physiol. 127, 1626-1634.
80. Yamaguchi, K., von Knoblauch, K., and Subramanian, A.R. (2000). The plastid ribosomal proteins. Identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275, 28455-28465.
81. Zhou, H., and Zhou, Y. (2003). Predicting the topology of transmembrane helical proteins using mean burial propensity and a hidden-Markov-model based method. Protein Sci. 12, 1547-1555.