Chloroplast protein import: Reverse genetic approaches

Current Genomics

Volumn 7, Issue 4, 2006, Pages 235-244

  Oreb, Mislav ^a   Reger, Katharina ^a   Schleiff, Enrico ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Arabidopsis thaliana; Knock out analysis; Protein import; Tic components; Toc components

Indexed keywords

ARABIDOPSIS PROTEIN; CARRIER PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN 90; MEMBRANE PROTEIN; NUCLEAR PROTEIN; RECEPTOR PROTEIN; REGULATOR PROTEIN; SCAFFOLD PROTEIN; TRANSLOCON; TRANSLOCON AT THE INNER CHLOROPLAST MEMBRANE PROTEIN 32; TRANSLOCON AT THE INNER CHLOROPLAST MEMBRANE PROTEIN 40; TRANSLOCON AT THE OUTER CHLOROPLAST MEMBRANE PROTEIN 159; TRANSLOCON AT THE OUTER CHLOROPLAST MEMBRANE PROTEIN 33; TRANSLOCON AT THE OUTER CHLOROPLAST MEMBRANE PROTEIN 34; TRANSLOCON AT THE OUTER CHLOROPLAST MEMBRANE PROTEIN 64; TRANSLOCON AT THE OUTER CHLOROPLAST MEMBRANE PROTEIN 75; UNCLASSIFIED DRUG;

ARABIDOPSIS; CELL ORGANELLE; CHLOROPLAST GENETICS; COMPLEX FORMATION; CYTOSOL; GENE EXPRESSION PROFILING; GENE TRANSLOCATION; IN VIVO STUDY; MOLECULAR EVOLUTION; NONHUMAN; OUTER MEMBRANE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; TRANSCRIPTION REGULATION;

ARABIDOPSIS THALIANA;

EID: 33748990112     PISSN: 13892029     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920206778427004     Document Type: Review

References (90)

1. Dyall, S.D., Brown, M.T., Johnson, P.J. Ancient invasions: from endosymbionts to organelles. Science 2004, 304: 253-257.
2. Timmis, J.N., Ayliffe, M.A., Huang, C.Y., Martin, W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 2004, 5: 123-135.
3. Reumann, S., Inoue, K., Keegstra, K. Evolution of the general protein import pathway of plastids. Mol. Membr. Biol. 2005, 22: 73-86.
4. Schleiff, E., Soll, J. Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep. 2005, 6: 1023-1027.
5. Waegemann, K., Soll, J. Phosphorylation of the transit sequence of chloroplast precursor proteins. J. Biol. Chem. 1996, 271: 6545-6554.
6. May, T., Soll, J. 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell. 2000, 12: 53-64.
7. Qbadou, S., Becker, T., Mirus, O., Tews, I., Soll, J., Schleiff, E. The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J. 2006, 25: 1836-1847.
8. Seedorf, M., Waegemann, K., Soll, J. A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J. 1995, 7; 401-411.
9. Kessler, F., Blobel, G., Patel, H.A., Schnell, D.J. Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 1994, 266: 1035-1039.
10. Perry, S.E., Keegstra, K. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 1994, 6: 93-105.
11. Hirsch, S., Muckel, E., Heemeyer, F., von Heijne, G., Soll, J. A receptor component of the chloroplast protein translocation machinery. Science 1994, 266: 1989-1992.
12. Schnell, D.J., Kessler, F., Blobel, G. Isolation of components of the chloroplast protein import machinery. Science 1994, 266: 1007-1012.
13. Schleiff, E., Soll, J., Küchler, M., Kühlbrandt, W., Harrer, R. Characterization of the translocon of the outer envelope of chloroplasts. J. Cell Biol. 2003, 160: 541-551.
14. Sohrt, K., Soll, J. Toc64, a new component of the protein translocon of chloroplasts. J. Cell Biol. 2000, 148: 1213-1221.
15. Becker, T., Hritz, J., Vogel, M., Caliebe, A., Bukau, B., Soll, J., Schleiff, E. Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Mol. Biol. Cell. 2004, 15: 5130-5144.
16. Kourtz, L., Ko, K. The early stage of chloroplast protein import involves Com70. J. Biol. Chem. 1997, 272: 2808-2813.
17. Marshall, J.S., DeRocher, A.E., Keegstra, K., Vierling, E. Identification of heat shock protein hsp70 homologues in chloroplasts. Proc. Natl. Acad. Sci. USA 1990, 87: 374-378.
18. Soll, J., Schleiff, E. Protein import into chloroplasts. Nat. Rev. Mol. Cell. Biol. 2004, 5: 198-208.
19. Jarvis, P., Robinson, C. Mechanisms of protein import and routing in chloroplasts. Curr. Biol. 2004, 14: R1064-1077.
20. Gutensohn, M., Fan, E., Frielingsdorf, S., Hanner, P., Hou, B., Hust, B.; Klösgen, R.B. Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. J. Plant Physiol. 2006, 163: 333-347.
21. Kessler, F., Schnell, D.J. Chloroplast protein import: solve the GTPase riddle for entry. Trends Cell. Biol. 2004, 14: 334-338.
22. Jelic, M., Soll, J., Schleiff, E. Two Toc34 homologues with different properties. Biochem. 2003, 42: 5906-5916.
23. Becker, T., Jelic, M., Vojta, A., Radunz, A., Soll, J., Schleiff, E. Preprotein recognition by the Toc complex. EMBO J. 2004, 23: 520-530.
24. Jelic, M., Sveshnikova, N., Motzkus, M., Horth, P., Soll, J., Schleiff, E. The chloroplast import receptor Toc34 functions as preprotein-regulated GTPase. Biol. Chem. 2002, 383: 1875-1883.
25. Sveshnikova, N., Soll, J., Schleiff, E. Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proc. Natl. Acad. Sci. USA 2000, 97: 4973-4978.
26. Schleiff, E., Jelic, M., Soll, J. A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc. Natl. Acad. Sci. USA 2003, 100: 4604-4609.
27. Kouranov, A., Chen, X., Fuks, B., Schnell, D.J. Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J. Cell Biol. 1998, 143: 991-1002.
28. Heins, L., Mehrle, A., Hemmler, R., Wagner, R., Küchler, M., Hörmann, F., Sveshnikov, D., Soll, J. The preprotein conducting channel at the inner envelope membrane of plastids. EMBO J. 2002, 21: 2616-2625.
29. Kessler, F., Blobel, G. Interaction of the protein import and folding machineries of the chloroplast. Proc. Natl. Acad. Sci. USA 1996, 93: 7684-7689.
30. Jackson, D.T., Froehlich, J.E., Keegstra, K. The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. J. Biol. Chem. 1998, 273: 16583-16588.
31. Inaba, T., Li, M., Alvarez-Huerta, M., Kessler, F., Schnell, D.J. at Tic110 functions as a scaffold for coordinating the stromal events of protein import into chloroplasts. J. Biol. Chem. 2003, 278: 38617-38627.
32. Akita, M., Nielsen, E., Keegstra, K. Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J. Cell Biol. 1997, 136: 983-994.
33. Nielsen, E., Akita, M., Davila-Aponte, J., Keegstra, K. Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 1997, 16: 935-46.
34. De Los Rios, P., Ben-Zvi, A., Slutsky, O., Azem, A., Goloubinoff, P. Hsp70 chaperones accelerate protein translocation and the unfolding of stable protein aggregates by entropic pulling. Proc. Natl. Acad. Sci. USA 2006, 103: 6166-6171.
35. Stahl, T., Glockmann, C., Soll, J., Heins, L. Tic40, a new "old" subunit of the chloroplast protein import translocon. J. Biol. Chem. 1999, 274: 37467-37472.
36. Chou, M.L., Fitzpatrick, L.M., Tu, S.L., Budziszewski, G., Potter-Lewis, S., Akita, M., Levin, J.Z., Keegstra, K., Li, H.M. Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J. 2003, 22: 2970-2980.
37. Goloubinoff, P., Christeller, J.T., Gatenby, A.A., Lorimer, G.H. Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfoleded state depends on two chaperonin proteins and Mg-ATP. Nature 1989, 342: 884-889.
38. Al-Babili, S., von Lintig, J., Haubruck, H., Beyer, P. A novel, soluble form of phytoene desaturase from Narcissus pseudonarcissus chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association and enzymatic activation. Plant J. 1996, 9: 601-612.
39. Drzymalla, C., Schroda, M., Beck, C.F. (1996) Light-inducible gene HSP70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii. Plant Mol. Biol. 1996, 31: 1185-1194.
40. Oblong, J.E., Lamppa, G.K. Identification of two structurally related proteins involved in proteolytic processing of precursors targeted to the chloroplast. EMBO J. 1992, 11: 4401-4409.
41. VanderVere, P.S., Bennett, T.M., Oblong, J.E., Lamppa, G.K. A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases. Proc. Natl. Acad. Sci. USA 1995, 92: 7177-7181.
42. Richter, S., Lamppa, G.K. Stromal processing peptidase binds transit peptides and initiates their ATP-dependent turnover in chloroplasts. J. Cell Biol. 1999, 147: 33-44.
43. Fulgosi, H., Soll, J. The chloroplast protein import receptors Toc34 and Toc159 are phosphorylated by distinct protein kinases. J. Biol. Chem. 2002, 277: 8934-8940.
44. Caliebe, A., Grimm, R., Kaiser, G., Lübeck, J., Soll, J., Heins, L. The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J. 1997, 16: 7342-7350.
45. Küchler, M., Decker, S., Hörmann, F., Soll, J., Heins, L. Protein import into chloroplasts involves redox-regulated proteins. EMBO J. 2002, 21: 6136-6145.
46. Hörmann, F., Küchler, M., Sveshnikov, D., Oppermann, U., Li, Y., Soll, J. Tic32, an essential component in chloroplast biogenesis. J. Biol. Chem. 2004, 279: 34756-63472.
47. Chigri, F., Soll, J., Vothknecht, U.C. Calcium regulation of chloroplast protein import. Plant J. 2005, 42: 821-831.
48. Li, H., Chen, L.J. A novel chloroplastic outer membrane-targeting signal that functions at both termini of passenger polypeptides. J. Biol. Chem. 1997, 272: 10968-10974.
49. Jarvis, P., Chen, L.J., Li, H., Peto, C.A., Fankhauser, C., Chory, J. An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 1998, 282: 100-103.
50. Gutensohn, M., Schulz, B., Nicolay, P., Flügge, U.I. Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J. 2000, 23: 771-783.
51. Kubis, S., Baldwin, A., Patel, R., Razzaq, A., Dupree, P., Lilley, K., Kurth, J., Leister, D., Jarvis, P. The Arabidopsis ppil mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell. 2003, 15: 1859-1871.
52. Vojta, A., Alavi, M., Becker, T., Hörmann, F., Küchler, M., Soll, J., Thomson, R., Schleiff, E. The protein translocon of the plastid envelopes. J. Biol. Chem. 2004, 279: 21401-21405.
53. Yu, T.S., Li, H. Chloroplast protein translocon components atToc159 and atToc33 are not essential for chloroplast biogenesis in guard cells and root cells. Plant Physiol. 2001, 127: 90-96.
54. Constan, D., Patel, R., Keegstra, K., Jarvis, P. An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J. 2004, 38: 93-106.
55. Gutensohn, M., Pahnke, S., Kolukisaoglu, U., Schulz, B., Schierhorn, A., Voigt, A., Hust, B., Rollwitz, I., Stockel, J., Geimer, S., Albrecht, V., Flügge, U.I., Klösgen, R.B. Characterization of a TDNA insertion mutant for the protein import receptor atToc33 from chloroplasts. Mol. Genet. Genomics 2004, 272: 379-396.
56. Aronsson, H., Combe, J., Patel, R., Jarvis, P. In vivo assessment of the significance of phosphorylation of the Arabidopsis chloroplast protein import receptor, atToc33. FEBS Lett. 2006, 580: 649-655.
57. Jackson-Constan, D., Keegstra, K. Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol. 2001, 125: 1567-1576.
58. Hiltbrunner, A., Grunig, K., Alvarez-Huerta, M., Infanger, S., Bauer, J., Kessler, F. AtToc90, a new GTP-binding component of the Arabidopsis chloroplast protein import machinery. Plant Mol. Biol. 2004, 54: 427-440.
59. Bauer, J., Chen, K., Hiltbunner, A., Wehrli, E., Eugster, M., Schnell, D., Kessler, F. The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 2000, 403: 203-207.
60. Asano, T., Yoshioka, Y., Machida, Y. A defect in atToc159 of Arabidopsis thaliana causes severe defects in leaf development. Genes Genet. Syst. 2004, 79: 207-212.
61. Kubis, S., Patel, R., Combe, J., Bedard, J., Kovacheva, S., Lilley, K., Biehl, A., Leister, D., Rios, G., Koncz, C., Jarvis, P. Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 2004, 16: 2059-2077.
62. Ivanova, Y., Smith, M.D., Chen, K., Schnell, D.J. Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell 2004, 15: 3379-3392
63. Alavi-Khorassani Moghadam, M., Schleiff, E. Analysis of expression patterns of translocon subunits of chloroplasts and mitochondria. Plant Sci. 2005, 168: 1533-1539.
64. Hust, B., Gutensohn, M. Deletion of core components of the plastid protein import machinery causes differential arrest of embryo development in Arabidopsis thaliana. Plant Biol. 2006, 8: 18-30.
65. Pollmann, S., Neu, D, Weiler, E.W. Molecular cloning and characterization of an amidase from Arabidopsis thaliana capable of converting indole-3-acetamide into the plant growth hormone, indole-3-acetic acid. Phytochem. 2003, 62: 293-300.
66. Chew, O., Lister, R., Qbadou, S., Heazlewood, J.L., Soll, J., Schleiff, E., Millar, A.H., Whelan, J. A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor. FEBS Lett. 2004, 557: 109-114.
67. Young, J.C., Hoogenraad, N.J., Hartl, F.U. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 2003, 112: 41-50.
68. Schaefer, D.G. A new moss genetics: targeted mutagenesis in Physcomitrella patens. Annu. Rev. Plant Biol. 2002, 53: 477-501.
69. Rosenbaum-Hofmann, N., Theg, S.M. Toc64 is not required for import of proteins into chloroplasts in the moss Physcomitrella patens. Plant J. 2005, 43: 675-687.
70. Hinnah, S.C., Hill, K., Wagner, R., Schlicher, T., Soll, J. Reconstitution of a chloroplast protein import channel. EMBO J. 1997, 16: 7351-7360.
71. Ertel, F., Mirus, O., Bredemeier, R., Moslavac, S., Becker, T., Schleiff, E. The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J. Biol. Chem. 2005, 280: 28281-28289.
72. Davila-Aponte, J.A., Inoue, K. and Keegstra, K. Two chloroplastic protein translocation components, Tic110 and Toc75, are conserved in different plastid types from multiple plant species. Plant Mol. Biol. 2003, 51: 175-181.
73. Moslavac, S., Mirus, O., Bredemeier, R., Soll, J., von Haeseler, A., Schleiff, E. Conserved pore-forming regions in polypeptide-transporting proteins. FEBS J. 2005, 272: 1367-1378.
74. Baldwin, A., Wardle, A., Patel, R., Dudley, P., Park, S.K., Twell, D., Inoue, K., Jarvis, P. A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol. 2005, 138: 715-733.
75. Tranel, P.J., Froehlich, J., Goyal, A., Keegstra, K. A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO J. 1995, 14: 2436-2446.
76. Tranel, P.J., Keegstra, K. A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 1996, 8: 2093-2104.
77. Inoue, K., Baldwin, A.J., Shipman, R.L., Matsui, K., Theg, S.M., Ohme-Takagi, M. Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. J. Cell Biol. 2005, 171: 425-430.
78. Eckart, K., Eichacker, L., Sohrt, K., Schleiff, E., Heins, L., Soll, J. A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep. 2002, 3: 557-562
79. Inoue, K., Potter, D. The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms. Plant J. 2004, 39: 354-365.
80. Lithgow, T., Junne, T., Wachter, C., Schatz, G. Yeast mitochondria lacking the two import receptors Mas20p and Mas70p can efficiently and specifically import precursor proteins. J. Biol. Chem. 1994, 269: 15325-15330.
81. van Wilpe, S., Ryan, M.T., Hill, K., Maarse, A.C., Meisinger, C., Brix, J., Dekker, P.J., Moczko, M., Wagner, R., Meijer, M., Guiard, B., Honlinger, A., Pfanner N. Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature 1999, 401: 485-489
82. Komiya, T., Rospert, S., Koehler, C., Looser, R., Schatz, G., Mihara, K. Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: evidence for the 'acid chain' hypothesis. EMBO J 1998, 17: 3886-3898.
83. Baker, K.P., Schaniel, A., Vestweber, D., Schatz, G. A yeast mitochondrial outer membrane protein essential for protein import and cell viability. Nature 1990, 348: 605-609.
84. Chen, X., Smith, M.D., Fitzpatrick, L., Schnell, D.J. In vivo analysis of the role of atTic20 in protein import into chloroplasts. Plant Cell 2002, 14: 641-654.
85. Kovacheva, S., Bedard, J., Patel, R., Dudley, P., Twell, D., Rios, G., Koncz, C., Jarvis, P. In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J., 2005, 41: 412-428.
86. Inaba, T., Alvarez-Huerta, M., Li, M., Bauer, J., Ewers, C., Kessler, F., Schnell, D.J. Arabidopsis tic110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell 2005, 17: 1482-1496
87. Constan, D., Froehlich, J.E., Rangarajan, S., Keegstra, K. A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol. 2004, 136: 3605-3615
88. Sjogren, L.L., MacDonald, T.M., Sutinen, S., Clarke, A.K. Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiol. 2004, 136: 4114-4126.
89. Ferro, M., Salvi, D., Riviere-Rolland, H., Vermut, T., Seigneurin-Berny, D., Grunwald, D., Garin, J., Joyard, J., Rolland, N. Integral membrane proteins of the chloroplast envelope: identification and subcellular localization of new transporters. Proc. Natl. Acad. Sci. USA 2002, 99: 11487-11492.
90. Sun, C.W., Chen, L.J., Lin, L.C., Li, H.M. Leaf-specific upregulation of chloroplast translocon genes by a CCT motif-containing protein, CIA 2. Plant Cell 2001, 13: 2053-2061.