Recognition and envelope translocation of chloroplast preproteins

Journal of Experimental Botany

Volumn 56, Issue 419, 2005, Pages 2287-2320

  Bédard, Jocelyn ^a   Jarvis, Paul ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Chloroplast; Chloroplast protein import; Membrane translocation; Organelle biology; Plastid; Protein targeting; Tic; Toc; Translocon

Indexed keywords

BIOLOGICAL MEMBRANES; BIOSYNTHESIS; CYTOLOGY; ENZYMES; PHOTOSYNTHESIS; PLANTS (BOTANY);

CHLOROPLAST PROTEIN IMPORT; CHLOROPLASTS; MEMBRANE TRANSLOCATION; ORGANELLE BIOLOGY; PLASTIDS; PROTEIN TARGETING; TIC; TOC; TRANSLOCON;

PROTEINS;

MEMBRANE PROTEIN; PROTEIN PRECURSOR; VEGETABLE PROTEIN;

CHLOROPLAST; METABOLISM; PHOTOSYNTHESIS; PROTEIN TRANSPORT; REVIEW; RIBOSOME;

CHLOROPLASTS; MEMBRANE PROTEINS; PHOTOSYNTHESIS; PLANT PROTEINS; PROTEIN PRECURSORS; PROTEIN TRANSPORT; RIBOSOMES;

EID: 23944431704     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/eri243     Document Type: Review

References (197)

1. Abbas-Terki T, Donzé O, Briand PA, Picard D. 2001. Hsp104 interacts with Hsp90 cochaperones in respiring yeast. Molecular and Cellular Biology 21, 7569-7575.
2. Abe Y, Shodai T, Muto T, Mihara K, Torii H, Nishikawa S, Endo T, Kohda D. 2000. Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100, 551-560.
3. Akita M, Nielsen E, Keegstra K. 1997. Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. Journal of Cell Biology 136, 983-994.
4. Aldridge C, Maple J, Møller SG. 2005. The molecular biology of plastid division in higher plants. Journal of Experimental Botany 56, 1061-1077.
5. Aronsson H, Combe J, Jarvis P. 2003a. Unusual nucleotide-binding properties of the chloroplast protein import receptor, atToc33. FEBS Letters 544, 79-85.
6. Aronsson H, Sohrt K, Soll J. 2000. NADPH:protochlorophyllide oxidoreductase uses the general import route into chloroplasts. Biological Chemistry 381, 1263-1267.
7. Aronsson H, Sundqvist C, Dahlin C. 2003b. POR hits the road: import and assembly of a plastid protein. Plant Molecular Biology 51, 1-7.
8. Aronsson H, Sundqvist C, Timko MP, Dahlin C. 2001. Characterisation of the assembly pathway of the pea NADPH:protochlorophyllide (Pchlide) oxidoreductase (POR), with emphasis on the role of its substrate, Pchlide. Physiologia Plantarum 111, 239-244.
9. Bähring R, Milligan CJ, Vardanyan V, Engeland B, Young BA, Dannenberg J, Waldschutz R, Edwards JP, Wray D, Pongs O. 2001. Coupling of voltage-dependent potassium channel inactivation and oxidoreductase active site of Kvbeta subunits. Journal of Biological Chemistry 276, 22923-22929.
10. Baldwin A, Wardle A, Patel R, Dudley P, Park SK, Twell D, Inoue K, Jarvis P. 2005. A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiology 138, 715-733.
11. Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, Schnell D, Kessler F. 2000. The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403, 203-207.
12. Bauer J, Hiltbrunner A, Weibel P, Vidi PA, Alvarez-Huerta M, Smith MD, Schnell DJ, Kessler F. 2002. Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane. Journal of Cell Biology 159, 845-854.
13. Becker T, Hritz J, Vogel M, Caliebe A, Bukau B, Soll J, Schleiff E. 2004a. Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Molecular Biology of the Cell 15, 5130-5144.
14. Becker T, Jelic M, Vojta A, Radunz A, Soll J, Schleiff E. 2004b. Preprotein recognition by the Toc complex. EMBO Journal 23, 520-530.
15. Blair GE, Ellis RJ. 1973. Protein synthesis in chloroplasts. I. Light-driven synthesis of the large subunit of fraction I protein by isolated pea chloroplasts. Biochimica et Biophysica Acta 319, 223-234.
16. Blobel G, Sabatini DD. 1971. Ribosome-membrane interactions in eukaryotic cells. In: Manson LA, ed. Biomembranes, Vol. 2. New York: Plenum, 193-195.
17. Bölter B, May T, Soll J. 1998a. A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide. FEBS Letters 441, 59-62.
18. Bołlter B, Soll J, Schulz A, Hinnah S, Wagner R. 1998b. Origin of a chloroplast protein importer. Proceedings of the National Academy of Sciences, USA 95, 15831-15836.
19. Bourne HR, Sanders DA, McCormick F. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117-127.
20. Bruce BD. 2000. Chloroplast transit peptides: structure, function and evolution. Trends in Cell Biology 10, 440-447.
21. Bruce BD. 2001. The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochimica et Biophysica Acta 1541, 2-21.
22. Bukau B, Horwich AL. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
23. Caliebe A, Grimm R, Kaiser G, Lubeck J, Soll J, Heins L. 1997. The chloroplastic protein import machinery contains a Rieske-type iron- sulfur cluster and a mononuclear iron-binding protein. EMBO Journal 16, 7342-7350.
24. Chen K, Chen X, Schnell DJ. 2000a. Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiology 122, 813-822.
25. Chen K, Chen X, Schnell DJ. 2000b. Mechanism of protein import across the chloroplast envelope. Biochemical Society Transactions 28, 485-491.
26. Chen X, Smith MD, Fitzpatrick L, Schnell DJ. 2002. In vivo analysis of the role of atTic20 in protein import into chloroplasts. The Plant Cell 14, 641-654.
27. Chew O, Lister R, Qbadou S, Heazlewood JL, Soll J, Schleiff E, Millar AH, Whelan J. 2004. A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor. FEBS Letters 557, 109-114.
28. Chew O, Whelan J. 2004. Just read the message: a model for sorting of proteins between mitochondria and chloroplasts. Trends in Plant Science 9, 318-319.
29. Chou ML, Fitzpatrick LM, Tu SL, Budziszewski G, Potter-Lewis S, Akita M, Levin JZ, Keegstra K, Li HM. 2003. Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO Journal 22, 2970-2980.
30. Chua NH, Schmidt GW. 1978. In vitro synthesis, transport, and assembly of ribulose 1,5-bisphosphate carboxylase subunits. Basic Life Sciences 11, 325-347.
31. Clark SA, Theg SM. 1997. A folded protein can be transported across the chloroplast envelope and thylakoid membranes. Molecular Biology of the Cell 8, 923-934.
32. Cline K, Werner-Washburne M, Andrews J, Keegstra K. 1984. Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiology 75, 675-678.
33. Cline K, Werner-Washburne M, Lubben TH, Keegstra K. 1985. Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts. Journal of Biological Chemistry 260, 3691-3696.
34. Constan D, Froehlich JE, Rangarajan S, Keegstra K. 2004a. A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiology 136, 3605-3615.
35. Constan D, Patel R, Keegstra K, Jarvis P. 2004b. An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. The Plant Journal 38, 93-106.
36. Curran SP, Leuenberger D, Leverich EP, Hwang DK, Beverly KN, Koehler CM. 2004. The role of Hot13p and redox chemistry in the mitochondrial TIM22 import pathway. Journal of Biological Chemistry 279, 43744-43751.
37. Dahlin C, Aronsson H, Almkvist J, Sundqvist C. 2000. Proto- chlorophyllide-independent import of two NADPH:Pchlide oxidoreductase proteins (PORA and PORB) from barley into isolated plastids. Physiologia Plantarum 109, 298-303.
38. Dahlin C, Cline K. 1991. Developmental regulation of the plastid protein import apparatus. The Plant Cell 3, 1131-1140.
39. Dobberstein B, Blobel G, Chua NH. 1977. In vitro synthesis and processing of a putative precursor for the small subunit of ribulose-1,5-bisphosphate carboxylase of Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences, USA 74, 1082-1085.
40. Endo T, Yamamoto H, Esaki M. 2003. Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles. Journal of Cell Science 116, 3259-3267.
41. Friedman AL, Keegstra K. 1989. Chloroplast protein import: quantitative analysis of precursor binding. Plant Physiology 89, 993-999.
42. Frydman J, Höhfeld J. 1997. Chaperones get in touch: the Hip-Hop connection. Trends in Biochemical Science 22, 87-92.
43. Fulgosi H, Soll J. 2002. The chloroplast protein import receptors Toc34 and Toc159 are phosphorylated by distinct protein kinases. Journal of Biological Chemistry 277, 8934-8940.
44. Gatto Jr GJ, Geisbrecht BV, Gould SJ, Berg JM. 2000. Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nature Structural Biology 7, 1091-1095.
45. Geissler A, Krimmer T, Bomer U, Guiard B, Rassow J, Pfanner N. 2000. Membrane potential-driven protein import into mitochondria. The sorting sequence of cytochrome b(2) modulates the deltapsi-dependence of translocation of the matrix-targeting sequence. Molecular Biology of the Cell 11, 3977-3991.
46. Gutensohn M, Pahnke S, Kolukisaoglu U, et al. 2004. Characterization of a T-DNA insertion mutant for the protein import receptor atToc33 from chloroplasts. Molecular Genetics and Genomics 272, 379-396.
47. Gutensohn M, Schulz B, Nicolay P, Flügge UI. 2000. Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. The Plant Journal 23, 771-783.
48. Halperin T, Ostersetzer O, Adam Z. 2001. ATP-dependent association between subunits of Clp protease in pea chloroplasts. Planta 213, 614-619.
49. Heins L, Mehrle A, Hemmler R, Wagner R, Küchler M, Hörmann F, Sveshnikov D, Soll J. 2002. The preprotein conducting channel at the inner envelope membrane of plastids. EMBO Journal 21, 2616-2625.
50. Highfield PE, Ellis RJ. 1978. Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271, 420-424.
51. Hill K, Model K, Ryan MT, Dietmeier K, Martin F, Wagner R, Pfanner N. 1998. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 395, 516-521.
52. Hiltbrunner A, Bauer J, Alvarez-Huerta M, Kessler F. 2001a. Protein translocon at the Arabidopsis outer chloroplast membrane. Biochemical and Cell Biology 79, 629-635.
53. Hiltbrunner A, Bauer J, Vidi PA, Infanger S, Weibel P, Hohwy M, Kessler F. 2001b. Targeting of an abundant cytosolic form of the protein import receptor at Toc159 to the outer chloroplast membrane. Journal of Cell Biology 154, 309-316.
54. Hiltbrunner A, Grunig K, Alvarez-Huerta M, Infanger S, Bauer J, Kessler F. 2004. AtToc90, a new GTP-binding component of the Arabidopsis chloroplast protein import machinery. Plant Molecular Biology 54, 427-440.
55. Hinnah SC, Hill K, Wagner R, Schlicher T, Soll J. 1997. Reconstitution of a chloroplast protein import channel. EMBO Journal 16, 7351-7360.
56. Hinnah SC, Wagner R, Sveshnikova N, Harrer R, Soll J. 2002. The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides. Biophysical Journal 83, 899-911.
57. Hirohashi T, Hase T, Nakai M. 2001. Maize non-photosynthetic ferredoxin precursor is mis-sorted to the intermembrane space of chloroplasts in the presence of light. Plant Physiology 125, 2154-2163.
58. Hirsch S, Muckel E, Heemeyer F, von Heijne G, Soll J. 1994. A receptor component of the chloroplast protein translocation machinery. Science 266, 1989-1992.
59. Hörmann F, Küchler M, Sveshnikov D, Oppermann U, Li Y, Soll J. 2004. Tic32, an essential component in chloroplast biogenesis. Journal of Biological Chemistry 279, 34756-34762.
60. Horst M, Hilfiker-Rothenfluh S, Oppliger W, Schatz G. 1995. Dynamic interaction of the protein translocation systems in the inner and outer membranes of yeast mitochondria. EMBO Journal 14, 2293-2297.
61. Huang CY, Ayliffe MA, Timmis JN. 2003. Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422, 72-76.
62. Inaba T, Li M, Alvarez-Huerta M, Kessler F, Schnell DJ. 2003. atTic110 functions as a scaffold for coordinating the stromal events of protein import into chloroplasts. Journal of Biological Chemistry 278, 38617-38627.
63. Inoue K, Potter D. 2004. 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. The Plant Journal 39, 354-365.
64. Ivanova Y, Smith MD, Chen K, Schnell DJ. 2004. Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Molecular Biology of the Cell 15, 3379-3392.
65. Ivey 3rd RA, Bruce BD. 2000. In vivo and in vitro interaction of DnaK and a chloroplast transit peptide. Cell Stress Chaperones 5, 62-71.
66. Ivey 3rd RA, Subramanian C, Bruce BD. 2000. Identification of a Hsp70 recognition domain within the rubisco small subunit transit peptide. Plant Physiology 122, 1289-1299.
67. Jackson DT, Froehlich JE, Keegstra K. 1998. The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. Journal of Biological Chemistry 273, 16583-16588.
68. Jackson-Constan D, Keegstra K. 2001. Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiology 125, 1567-1576.
69. Jarvis P. 2004. Organellar proteomics: chloroplasts in the spotlight. Current Biology 14, R317-R319.
70. Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J. 1998. An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282, 100-103.
71. Jarvis P, Robinson C. 2004. Mechanisms of protein import and routing in chloroplasts. Current Biology 14, R1064-R1077.
72. Jarvis P, Soll J. 2002. Toc, Tic, and chloroplast protein import. Biochimica et Biophysica Acta 1590, 177-189.
73. Jelic M, Soll J, Schleiff E. 2003. Two Toc34 homologues with different properties. Biochemistry 42, 5906-5916.
74. Jelic M, Sveshnikova N, Motzkus M, Horth P, Soll J, Schleiff E. 2002. The chloroplast import receptor Toc34 functions as preprotein-regulated GTPase. Biological Chemistry 383, 1875-1883.
75. Keegstra K, Cline K. 1999. Protein import and routing systems of chloroplasts. The Plant Cell 11, 557-570.
76. Keenan RJ, Freymann DM, Stroud RM, Walter P. 2001. The signal recognition particle. Annual Review of Biochemistry 70, 755-775.
77. Kessler F, Blobel G. 1996. Interaction of the protein import and folding machineries of the chloroplast. Proceedings of the National Academy of Sciences, USA 93, 7684-7689.
78. Kessler F, Blobel G, Patel HA, Schnell DJ. 1994. Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266, 1035-1039.
79. Kessler F, Schnell DJ. 2002. A GTPase gate for protein import into chloroplasts. Nature Structural Biology 9, 81-83.
80. Kessler F, Schnell DJ. 2004. Chloroplast protein import: solve the GTPase riddle for entry. Trends in Cell Biology 14, 334-338.
81. Kim C, Apel K. 2004. Substrate-dependent and organ-specific chloroplast protein import in planta. The Plant Cell 16, 88-98.
82. Kim C, Ham H, Apel K. 2005. Multiplicity of different cell- and organ-specific import routes for the NADPH-protochlorophyllide oxidoreductases A and B in plastids of Arabidopsis seedlings. The Plant Journal 42, 329-340.
83. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S. 2004. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biology 14, 354-362.
84. Ko K, Banerjee S, Innes J, Taylor D, Ko Z. 2004. The Tic40 translocon components exhibit preferential interactions with different forms of the Oee1 plastid protein precursor. Functional Plant Biology 31, 285-294.
85. Ko K, Budd D, Wu C, Seibert F, Kourtz L, Ko ZW. 1995. Isolation and characterization of a cDNA clone encoding a member of the Com44/Cim44 envelope components of the chloroplast protein import apparatus. Journal of Biological Chemistry 270, 28601-28608.
86. Komiya T, Rospert S, Koehler C, Looser R, Schatz G, Mihara K. 1998. Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: evidence for the 'acid chain' hypothesis. EMBO Journal 17, 3886-3898.
87. Kouranov A, Chen X, Fuks B, Schnell DJ. 1998. Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. Journal of Cell Biology 143, 991-1002.
88. Kouranov A, Schnell DJ. 1997. Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts. Journal of Cell Biology 139, 1677-1685.
89. Kourtz L, Ko K. 1997. The early stage of chloroplast protein import involves Com70. Journal of Biological Chemistry 272, 2808-2813.
90. Kovacheva S, Bédard J, Patel R, Dudley P, Twell D, Ríos G, Koncz C, Jarvis P. 2005. In vivo studies on the roles of Tic110, Tic40, and Hsp93 during chloroplast protein import. The Plant Journal 41, 412-428.
91. Kovermann P, Truscott KN, Guiard B, Rehling P, Sepuri NB, Muller H, Jensen RE, Wagner R, Pfanner N. 2002. Tim22, the essential core of the mitochondrial protein insertion complex, forms a voltage-activated and signal-gated channel. Molecular Cell 9, 363-373.
92. Kubis S, Baldwin A, Patel R, Razzaq A, Dupree P, Lilley K, Kurth J, Leister D, Jarvis P. 2003. The Arabidopsis ppi1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. The Plant Cell 15, 1859-1871.
93. Kubis S, Patel R, Combe J, et al. 2004. Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. The Plant Cell 16, 2059-2077.
94. Küchler M, Decker S, Hörmann F, Soll J, Heins L. 2002. Protein import into chloroplasts involves redox-regulated proteins. EMBO Journal 21, 6136-6145.
95. Lamb JR, Tugendreich S, Hieter P. 1995. Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends in Biochemical Science 20, 257-259.
96. Lee KH, Kim SJ, Lee YJ, Jin JB, Hwang I. 2003. The M domain of atToc159 plays an essential role in the import of proteins into chloroplasts and chloroplast biogenesis. Journal of Biological Chemistry 278, 36794-36805.
97. Lee YJ, Kim DH, Kim YW, Hwang I. 2001. Identification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane system in vivo. The Plant Cell 13, 2175-2190.
98. Lee YJ, Sohn EJ, Lee KH, Lee DW, Hwang I. 2004. The transmembrane domain of AtToc64 and its C-terminal lysine-rich flanking region are targeting signals to the chloroplast outer envelope membrane. Molecular Cells 17, 281-291.
99. Leheny EA, Theg SM. 1994. Apparent inhibition of chloroplast protein import by cold temperatures is due to energetic considerations not membrane fluidity. The Plant Cell 6, 427-437.
100. Leister D. 2003. Chloroplast research in the genomic age. Trends in Genetics 19, 47-56.
101. Lu H, Allen S, Wardleworth L, Savory P, Tokatlidis K. 2004. Functional TIM10 chaperone assembly is redox-regulated in vivo. Journal of Biological Chemistry 279, 18952-18958.
102. Lübeck J, Soll J, Akita M, Nielsen E, Keegstra K. 1996. Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO Journal 15, 4230-4238.
103. Ma Y, Kouranov A, LaSala SE, Schnell DJ. 1996. Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope. Journal of Cell Biology 134, 315-327.
104. Macasev D, Newbigin E, Whelan J, Lithgow T. 2000. How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiology 123, 811-816.
105. Margulis L. 1970. The origin of eukaryotic cells. New Haven: Yale University Press.
106. Marshall JS, DeRocher AE, Keegstra K, Vierling E. 1990. Identification of heat shock protein hsp70 homologues in chloroplasts. Proceedings of the National Academy of Sciences, USA 87, 374-378.
107. Martin J, Mahlke K, Pfanner N. 1991. Role of an energized inner membrane in mitochondrial protein import. Delta psi drives the movement of presequences. Journal of Biological Chemistry 266, 18051-18057.
108. Matlack KE, Misselwitz B, Plath K, Rapoport TA. 1999. BiP acts as a molecular ratchet during posttranslational transport of prepro-alpha factor across the ER membrane. Cell 97, 553-564.
109. May T, Soll J. 2000. 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. The Plant Cell 12, 53-64.
110. McFadden GI. 2001. Chloroplast origin and integration. Plant Physiology 125, 50-53.
111. Meisinger C, Ryan MT, Hill K, Model K, Lim JH, Sickmann A, Muller H, Meyer HE, Wagner R, Pfanner N. 2001. Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with preproteins, small tom proteins, and import receptors. Molecular and Cellular Biology 21, 2337-2348.
112. Miras S, Salvi D, Ferro M, Grunwald D, Garin J, Joyard J, Rolland N. 2002. Non-canonical transit peptide for import into the chloroplast. Journal of Biological Chemistry 277, 47770-47778.
113. Mullet JE. 1988. Chloroplast development and gene expression. Annual Review of Plant Physiology and Plant Molecular Biology 39, 475-502.
114. Muto T, Obita T, Abe Y, Shodai T, Endo T, Kohda D. 2001. NMR identification of the Tom20 binding segment in mitochondrial presequences. Journal of Molecular Biology 306, 137-143.
115. Nada A, Soll J. 2004. Inner envelope protein 32 is imported into chloroplasts by a novel pathway. Journal of Cell Science 117, 3975-3982.
116. Nakrieko KA, Mould RM, Smith AG. 2004. Fidelity of targeting to chloroplasts is not affected by removal of the phosphorylation site from the transit peptide. European Journal of Biochemistry 271, 509-516.
117. Nelson N, Ben-Shem A. 2004. The complex architecture of oxygenic photosynthesis. Nature Reviews of Molecular and Cell Biology 5, 971-982.
118. Neupert W, Brunner M. 2002. The protein import motor of mitochondria. Nature Reviews of Molecular and Cell Biology 3, 555-565.
119. Nielsen E, Akita M, Davila-Aponte J, Keegstra K. 1997. Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO Journal 16, 935-946.
120. Oblong JE, Lamppa GK. 1992. Identification of two structurally related proteins involved in proteolytic processing of precursors targeted to the chloroplast. EMBO Journal 11, 4401-4409.
121. Olsen LJ, Keegstra K. 1992. The binding of precursor proteins to chloroplasts requires nucleoside triphosphates in the intermembrane space. Journal of Biological Chemistry 267, 433-439.
122. Olsen LJ, Theg SM, Selman BR, Keegstra K. 1989. ATP is required for the binding of precursor proteins to chloroplasts. Journal of Biological Chemistry 264, 6724-6729.
123. Pain D, Blobel G. 1987. Protein import into chloroplasts requires a chloroplast ATPase. Proceedings of the National Academy of Sciences, USA 84, 3288-3292.
124. Peeters N, Small I. 2001. Dual targeting to mitochondria and chloroplasts. Biochimica et Biophysica Acta 1541, 54-63.
125. Perry SE, Keegstra K. 1994. Envelope membrane proteins that interact with chloroplastic precursor proteins. The Plant Cell 6, 93-105.
126. Rassow J, Dekker PJ, van Wilpe S, Meijer M, Soll J. 1999. The preprotein translocase of the mitochondrial inner membrane: function and evolution. Journal of Molecular Biology 286, 105-120.
127. Rehling P, Brandner K, Pfanner N. 2004. Mitochondrial import and the twin-pore translocase. Nature Reviews of Molecular and Cell Biology 5, 519-530.
128. Reinbothe S, Mache R, Reinbothe C. 2000. A second, substrate-dependent site of protein import into chloroplasts. Proceedings of the National Academy of Sciences, USA 97, 9795-9800.
129. Reinbothe S, Pollmann S, Springer A, James RJ, Tichtinsky G, Reinbothe C. 2005. A role of Toc33 in the protochlorophyllide-dependent plastid import pathway of NADPH:protochlorophyllide oxidoreductase (POR) A. The Plant Journal 42, 1-12.
130. Reinbothe S, Quigley F, Gray J, Schemenewitz A, Reinbothe C. 2004a. Identification of plastid envelope proteins required for import of protochlorophyllide oxidoreductase A into the chloroplast of barley. Proceedings of the National Academy of Sciences, USA 101, 2197-2202.
131. Reinbothe S, Quigley F, Springer A, Schemenewitz A, Reinbothe C. 2004b. The outer plastid envelope protein Oep16: role as precursor translocase in import of protochlorophyllide oxidoreductase A. Proceedings of the National Academy of Sciences, USA 101, 2203-2208.
132. Reumann S, Davila-Aponte J, Keegstra K. 1999. The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proceedings of the National Academy of Sciences, USA 96, 784-789.
133. Reumann S, Keegstra K. 1999. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends in Plant Science 4, 302-307.
134. Rial DV, Arakaki AK, Ceccarelli EA. 2000. Interaction of the targeting sequence of chloroplast precursors with Hsp70 molecular chaperones. European Journal of Biochemistry 267, 6239-6248.
135. Richter S, Lamppa GK. 1999. Stromal processing peptidase binds transit peptides and initiates their ATP-dependent turnover in chloroplasts. Journal of Cell Biology 147, 33-44.
136. Richter S, Lamppa GK. 2002. Determinants for removal and degradation of transit peptides of chloroplast precursor proteins. Journal of Biological Chemistry 277, 43888-43894.
137. Richter S, Lamppa GK. 2003. Structural properties of the chloroplast stromal processing peptidase required for its function in transit peptide removal. Journal of Biological Chemistry 278, 39497-39502.
138. Rudhe C, Clifton R, Chew O, Zemam K, Richter S, Lamppa G, Whelan J, Glaser E. 2004. Processing of the dual targeted precursor protein of glutathione reductase in mitochondria and chloroplasts. Journal of Molecular Biology 343, 639-647.
139. Sánchez-Pulido L, Devos D, Genevrois S, Vicente M, Valencia A. 2003. POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. Trends in Biochemical Science 28, 523-526.
140. Scheffzek K, Ahmadian MR, Wittinghofer A. 1998. GTPase-activating proteins: helping hands to complement an active site. Trends in Biochemical Science 23, 257-262.
141. Schirmer EC, Glover JR, Singer MA, Lindquist S. 1996. HSP100/Clp proteins: a common mechanism explains diverse functions. Trends in Biochemical Science 21, 289-296.
142. Schleiff E, Eichacker LA, Eckart K, Becker T, Mirus O, Stahl T, Soll J. 2003a. Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope. Protein Science 12, 748-759.
143. Schleiff E, Jelic M, Soll J. 2003b. A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proceedings of the National Academy of Sciences, USA 100, 4604-4609.
144. Schleiff E, Klösgen RB. 2001. Without a little help from 'my' friends: direct insertion of proteins into chloroplast membranes? Biochimica et Biophysica Acta 1541, 22-33.
145. Schleiff E, Soll J, Kuchler M, Kuhlbrandt W, Harrer R. 2003c. Characterization of the translocon of the outer envelope of chloroplasts. Journal of Cell Biology 160, 541-551.
146. Schleiff E, Soll J, Sveshnikova N, Tien R, Wright S, Dabney-Smith C, Subramanian C, Bruce BD. 2002. Structural and guanosine triphosphate/diphosphate requirements for transit peptide recognition by the cytosolic domain of the chloroplast outer envelope receptor, Toc34. Biochemistry 41, 1934-1946.
147. 2-terminal amino acid sequences of precursor and mature forms of the ribulose-1,5-bisphosphate carboxylase small subunit from Chlamydomonas reinhardtii. Journal of Cell Biology 83, 615-622.
148. Schnell DJ, Blobel G. 1993. Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. Journal of Cell Biology 120, 103-115.
149. Schnell DJ, Blobel G, Keegstra K, Kessler F, Ko K, Soll J. 1997. A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends in Cell Biology 7, 303-304.
150. Schnell DJ, Hebert DN. 2003. Protein translocons: multifunctional mediators of protein translocation across membranes. Cell 112, 491-505.
151. Schnell DJ, Kessler F, Blobel G. 1994. Isolation of components of the chloroplast protein import machinery. Science 266, 1007-1012.
152. Scott SV, Theg SM. 1996. A new chloroplast protein import intermediate reveals distinct translocation machineries in the two envelope membranes: energetics and mechanistic implications. Journal of Cell Biology 132, 63-75.
153. Seedorf M, Waegemann K, Soll J. 1995. A constituent of the chloroplast import complex represents a new type of GTP-binding protein. The Plant Journal 7, 401-411.
154. Shanklin J, DeWitt ND, Flanagan JM. 1995. The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: an archetypal two-component ATP-dependent protease. The Plant Cell 7, 1713-1722.
155. Simon A, Romert A, Gustafson AL, McCaffery JM, Eriksson U. 1999. Intracellular localization and membrane topology of 11-cis retinol dehydrogenase in the retinal pigment epithelium suggest a compartmentalized synthesis of 11-cis retinaldehyde. Journal of Cell Science 112, 549-558.
156. Sjögren LL, MacDonald TM, Sutinen S, Clarke AK. 2004. 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 Physiology 136, 4114-4126.
157. Smith MD, Hiltbrunner A, Kessler F, Schnell DJ. 2002. The targeting of the at Toc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. Journal of Cell Biology 159, 833-843.
158. Smith MD, Rounds CM, Wang F, Chen K, Afitlhile M, Schnell DJ. 2004. atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. Journal of Cell Biology 165, 323-334.
159. Sohrt K, Soll J. 2000. Toc64, a new component of the protein translocon of chloroplasts. Journal of Cell Biology 148, 1213-1221.
160. Sokolenko A, Lerbs-Mache S, Altschmied L, Herrmann RG. 1998. Clp protease complexes and their diversity in chloroplasts. Planta 207, 286-295.
161. Stahl T, Glockmann C, Soll J, Heins L. 1999. Tic40, a new 'old' subunit of the chloroplast protein import translocon. Journal of Biological Chemistry 274, 37467-37472.
162. Sun YJ, Forouhar F, Li Hm HM, Tu SL, Yeh YH, Kao S, Shr HL, Chou CC, Chen C, Hsiao CD. 2002. Crystal structure of pea Toc34, a novel GTPase of the chloroplast protein translocon. Nature Structural Biology 9, 95-100.
163. Sveshnikova N, Grimm R, Soll J, Schleiff E. 2000a. Topology studies of the chloroplast protein import channel Toc75. Biological Chemistry 381, 687-693.
164. Sveshnikova N, Soll J, Schleiff E. 2000b. Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proceedings of the National Academy of Sciences, USA 97, 4973-4978.
165. Taylor AB, Smith BS, Kitada S, Kojima K, Miyaura H, Otwinowski Z, Ito A, Deisenhofer J. 2001. Crystal structures of mitochondrial processing peptidase reveal the mode for specific cleavage of import signal sequences. Structure 9, 615-625.
166. Terlecky SR, Nuttley WM, McCollum D, Sock E, Subramani S. 1995. The Pichia pastoris peroxisomal protein PAS8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO Journal 14, 3627-3634.
167. The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
168. Theg SM, Bauerle C, Olsen LJ, Selman BR, Keegstra K. 1989. Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. Journal of Biological Chemistry 264, 6730-6736.
169. Timmis JN, Ayliffe MA, Huang CY, Martin W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Review of Genetics 5, 123-135.
170. Tranel PJ, Froehlich J, Goyal A, Keegstra K. 1995. A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO Journal 14, 2436-2446.
171. Truscott KN, Brandner K, Pfanner N. 2003. Mechanisms of protein import into mitochondria. Current Biology 13, R326-R337.
172. Truscott KN, Kovermann P, Geissler A, Merlin A, Meijer M, Driessen AJ, Rassow J, Pfanner N, Wagner R. 2001. A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nature Structural Biology 8, 1074-1082.
173. + reductase upon its import into chloroplasts. FEBS Letters 320, 198-202.
174. Tu SL, Chen LJ, Smith MD, Su YS, Schnell DJ, Li HM. 2004. Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. The Plant Cell 16, 2078-2088.
175. Tu SL, Li HM. 2000. Insertion of OEP14 into the outer envelope membrane is mediated by proteinaceous components of chloroplasts. The Plant Cell 12, 1951-1960.
176. van den Wijngaard PW, Demmers JA, Thompson SJ, Wienk HL, de Kruijff B, Vredenberg WJ. 2000. Further analysis of the involvement of the envelope anion channel PIRAC in chloroplast protein import. European Journal of Biochemistry 267, 3812-3817.
177. van den Wijngaard PW, Vredenberg WJ. 1997. A 50-picosiemens anion channel of the chloroplast envelope is involved in chloroplast protein import. Journal of Biological Chemistry 272, 29430-29433.
178. van den Wijngaard PW, Vredenberg WJ. 1999. The envelope anion channel involved in chloroplast protein import is associated with Tic110. Journal of Biological Chemistry 274, 25201-25204.
179. VanderVere PS, Bennett TM, Oblong JE, Lamppa GK. 1995. A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases. Proceedings of the National Academy of Sciences, USA 92, 7177-7181.
180. von Heijne G, Nishikawa K. 1991. Chloroplast transit peptides. The perfect random coil? FEBS Letters 278, 1-3.
181. Vrontou E, Economou A. 2004. Structure and function of SecA, the preprotein translocase nanomotor. Biochimica et Biophysica Acta 1694, 67-80.
182. Waegemann K, Soll J. 1991. Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. The Plant Journal 1, 149-158.
183. Waegemann K, Soll J. 1996. Phosphorylation of the transit sequence of chloroplast precursor proteins. Journal of Biological Chemistry 271, 6545-6554.
184. Wallas TR, Smith MD, Sanchez-Nieto S, Schnell DJ. 2003. The roles of toc34 and toc75 in targeting the toc159 preprotein receptor to chloroplasts. Journal of Biological Chemistry 278, 44289-44297.
185. Walsh P, Bursac D, Law YC, Cyr D, Lithgow T. 2004. The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Reports 5, 567-571.
186. Wan J, Blakeley SD, Dennis DT, Ko K. 1996. Transit peptides play a major role in the preferential import of proteins into leucoplasts and chloroplasts. Journal of Biological Chemistry 271, 31227-31233.
187. Wan J, Bringloe D, Lamppa GK. 1998. Disruption of chloroplast biogenesis and plant development upon down-regulation of a chloroplast processing enzyme involved in the import pathway. The Plant Journal 15, 459-468.
188. Weibel P, Hiltbrunner A, Brand L, Kessler F. 2003. Dimerization of Toc-GTPases at the chloroplast protein import machinery. Journal of Biological Chemistry 278, 37321-37329.
189. Whatley JM. 1978. A suggested cycle of plastid developmental interrelationships. New Phytologist 80, 489-502.
190. Wiedemann N, Frazier AE, Pfanner N. 2004. The protein import machinery of mitochondria. Journal of Biological Chemistry 279, 14473-14476.
191. Wirth A, Jung M, Bies C, Frien M, Tyedmers J, Zimmermann R, Wagner R. 2003. The Sec61p complex is a dynamic precursor activated channel. Molecular Cell 12, 261-268.
192. Wu C, Seibert FS, Ko K. 1994. Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein. Journal of Biological Chemistry 269, 32264-32271.
193. Young JC, Hoogenraad NJ, Hartl FU. 2003. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112, 41-50.
194. Young ME, Keegstra K, Froehlich JE. 1999. GTP promotes the formation of early-import intermediates but is not required during the translocation step of protein import into chloroplasts. Plant Physiology 121, 237-244.
195. Yu TS, Li H. 2001. Chloroplast protein translocon components atToc159 and atToc33 are not essential for chloroplast biogenesis in guard cells and root cells. Plant Physiology 127, 90-96.
196. Zhang XP, Glaser E. 2002. Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends in Plant Science 7, 14-21.
197. Zhong R, Wan J, Jin R, Lamppa G. 2003. A pea antisense gene for the chloroplast stromal processing peptidase yields seedling lethals in Arabidopsis: survivors show defective GFP import in vivo. The Plant Journal 34, 802-812.