Targeting of nucleus-encoded proteins to chloroplasts in plants

New Phytologist

Volumn 179, Issue 2, 2008, Pages 257-285

  Jarvis, Paul ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Chloroplast envelope; Chloroplast protein import; Plastid biogenesis; Preprotein; Protein targeting; TIC; TOC; Transit peptide

Indexed keywords

VEGETABLE PROTEIN;

CHLOROPLAST; DICOTYLEDON; GENOME; LEGUME; PEPTIDE; PROTEIN; PROTEOMICS;

ACTIVE TRANSPORT; CELL NUCLEUS; CHLOROPLAST; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; REVIEW;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; CHLOROPLASTS; PLANT PROTEINS; PROTEIN TRANSPORT;

ARABIDOPSIS; PISUM SATIVUM;

EID: 47249152709     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2008.02452.x     Document Type: Review

References (270)

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. America T, Hageman J, Guera A, Rook F, Archer K, Keegstra K, Weisbeek P. 1994. Methotrexate does not block import of a DHFR fusion protein into chloroplasts. Plant Molecular Biology 24 : 283 294.
5. Andersson MX, Goksör M, Sandelius AS. 2007. Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. Journal of Biological Chemistry 282 : 1170 1174.
6. Aronsson H, Boij P, Patel R, Wardle A, Töpel M, Jarvis P. 2007. Toc64/OEP64 is not essential for the efficient import of proteins into chloroplasts in Arabidopsis thaliana. Plant Journal 52 : 53 68.
7. Aronsson H, Combe J, Patel R, Jarvis P. 2006. In vivo assessment of the significance of phosphorylation of the Arabidopsis chloroplast protein import receptor, atToc33. FEBS Letters 580 : 649 655.
8. Aronsson H, Sohrt K, Soll J. 2000. NADPH:Protochlorophyllide oxidoreductase uses the general import route into chloroplasts. Biological Chemistry 381 : 1263 1267.
9. Aronsson H, Sundqvist C, Dahlin C. 2003. POR hits the road: import and assembly of a plastid protein. Plant Molecular Biology 51 : 1 7.
10. Aronsson H, Sundqvist C, Timko MP, Dahlin C. 2001. Characterization 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.
11. Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, Mitsui T. 2005. Involvement of alpha-amylase I-1 in starch degradation in rice chloroplasts. Plant & Cell Physiology 46 : 858 869.
12. Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I. 2008. AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nature Cell Biology 10 : 220 227.
13. Baier M, Dietz KJ. 2005. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. Journal of Experimental Botany 56 : 1449 1462.
14. 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 : 1 19.
15. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S. 2002. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18 : 298 305.
16. 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.
17. 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.
18. Becker T, Hritz J, Vogel M, Caliebe A, Bukau B, Soll J, Schleiff E. 2004b. Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Molecular Biology of the Cell 15 : 5130 5144.
19. Becker T, Jelic M, Vojta A, Radunz A, Soll J, Schleiff E. 2004a. Preprotein recognition by the Toc complex. EMBO Journal 23 : 520 530.
20. Bédard J, Jarvis P. 2005. Recognition and envelope translocation of chloroplast preproteins. Journal of Experimental Botany 56 : 2287 2320.
21. Bédard J, Jarvis P. 2008. Green light for chloroplast outer-membrane proteins. Nature Cell Biology 10 : 120 122.
22. Bédard J, Kubis S, Bimanadham S, Jarvis P. 2007. Functional similarity between the chloroplast translocon component, Tic40, and the human co-chaperone, Hsp70-interacting protein (Hip). Journal of Biological Chemistry 282 : 21404 21414.
23. Benning C, Xu C, Awai K. 2006. Nonvesicular and vesicular lipid trafficking involving plastids. Current Opinion in Plant Biology 9 : 241 247.
24. Bhushan S, Kuhn C, Berglund AK, Roth C, Glaser E. 2006. The role of the N-terminal domain of chloroplast targeting peptides in organellar protein import and miss-sorting. FEBS Letters 580 : 3966 3972.
25. 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.
26. Blobel G, Sabatini DD. 1971. Ribosome-membrane interactions in eukaryotic cells. In : Manson LA, ed. Biomembranes. New York, NY, USA : Plenum, 193 195.
27. Bohnert M, Pfanner N, van der Laan M. 2007. A dynamic machinery for import of mitochondrial precursor proteins. FEBS Letters 581 : 2802 2810.
28. Bölter B, May T, Soll J. 1998. A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide. FEBS Letters 441 : 59 62.
29. Bourne HR, Sanders DA, McCormick F. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature 349 : 117 127.
30. Brink S, Fischer K, Klösgen RB, Flügge UI. 1995. Sorting of nuclear-encoded chloroplast membrane proteins to the envelope and the thylakoid membrane. Journal of Biological Chemistry 270 : 20808 20815.
31. Brix J, Dietmeier K, Pfanner N. 1997. Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, and Tom70. Journal of Biological Chemistry 272 : 20730 20735.
32. Bruce BD. 1998. The role of lipids in plastid protein transport. Plant Molecular Biology 38 : 223 246.
33. Bruce BD. 2000. Chloroplast transit peptides: structure, function and evolution. Trends in Cell Biology 10 : 440 447.
34. Bruce BD. 2001. The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochimica et Biophysica Acta 1541 : 2 21.
35. Bukau B, Horwich AL. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92 : 351 366.
36. 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.
37. Chen K, Chen X, Schnell DJ. 2000. Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiology 122 : 813 822.
38. Chen KY, Li HM. 2007. Precursor binding to an 880-kDa Toc complex as an early step during active import of protein into chloroplasts. Plant Journal 49 : 149 158.
39. Chen LJ, Li HM. 1998. A mutant deficient in the plastid lipid DGD is defective in protein import into chloroplasts. Plant Journal 16 : 33 39.
40. Chen MH, Huang LF, Li HM, Chen YR, Yu SM. 2004. Signal peptide-dependent targeting of a rice alpha-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiology 135 : 1367 1377.
41. Chen X, Smith MD, Fitzpatrick L, Schnell DJ. 2002. In vivo analysis of the role of atTic20 in protein import into chloroplasts. Plant Cell 14 : 641 654.
42. 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.
43. Chigri F, Hörmann F, Stamp A, Stammers DK, Bölter B, Soll J, Vothknecht UC. 2006. Calcium regulation of chloroplast protein translocation is mediated by calmodulin binding to Tic32. Proceedings of the National Academy of Sciences, USA 103 : 16051 16056.
44. Chigri F, Soll J, Vothknecht UC. 2005. Calcium regulation of chloroplast protein import. Plant Journal 42 : 821 831.
45. Chou ML, Chu CC, Chen LJ, Akita M, Li HM. 2006. Stimulation of transit-peptide release and ATP hydrolysis by a cochaperone during protein import into chloroplasts. Journal of Cell Biology 175 : 893 900.
46. 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.
47. Chua NH, Schmidt GW. 1978. In vitro synthesis, transport, and assembly of ribulose 1,5-bisphosphate carboxylase subunits. Basic Life Sciences 11 : 325 347.
48. 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.
49. 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.
50. 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.
51. Constan D, Froehlich JE, Rangarajan S, Keegstra K. 2004b. A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiology 136 : 3605 3615.
52. Constan D, Patel R, Keegstra K, Jarvis P. 2004a. An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant Journal 38 : 93 106.
53. Crotty WJ, Ledbetter MC. 1973. Membrane continuities involving chloroplasts and other organelles in plant cells. Science 182 : 839 841.
54. 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.
55. Dabney-Smith C, van Den Wijngaard PW, Treece Y, Vredenberg WJ, Bruce BD. 1999. The C terminus of a chloroplast precursor modulates its interaction with the translocation apparatus and PIRAC. Journal of Biological Chemistry 274 : 32351 32359.
56. Dahlin C, Aronsson H, Almkvist J, Sundqvist C. 2000. Protochlorophyllide- independent import of two NADPH:Pchlide oxidoreductase proteins (PORA and PORB) from barley into isolated plastids. Physiologia Plantarum 109 : 298 303.
57. Dahlin C, Cline K. 1991. Developmental regulation of the plastid protein import apparatus. Plant Cell 3 : 1131 1140.
58. Della-Cioppa G, Bauer SC, Klein BK, Shah DM, Fraley RT, Kishore GM. 1986. Translocation of the precursor of 5-enolpyruvylshikimate-3-phosphate synthase into chloroplasts of higher plants in vitro. Proceedings of the National Academy of Sciences, USA 83 : 6873 6877.
59. 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.
60. Duchêne AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters NM, Zaepfel M, Marechal-Drouard L, Small ID. 2005. Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 102 : 16484 16489.
61. Duy D, Wanner G, Meda AR, von Wiren N, Soll J, Philippar K. 2007. PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19 : 986 1006.
62. Eckart K, Eichacker L, Sohrt K, Schleiff E, Heins L, Soll J. 2002. A Toc75-like protein import channel is abundant in chloroplasts. EMBO Reports 3 : 557 562.
63. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2 : 953 971.
64. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300 : 1005 1016.
65. Emanuelsson O, Nielsen H, von Heijne G. 1999. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Science 8 : 978 984.
66. Ertel F, Mirus O, Bredemeier R, Moslavac S, Becker T, Schleiff E. 2005. The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. Journal of Biological Chemistry 280 : 28281 28289.
67. Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N. 2003. Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Molecular & Cellular Proteomics 2 : 325 345.
68. Foth BJ, McFadden GI. 2003. The apicoplast: a plastid in Plasmodium falciparum and other Apicomplexan parasites. International Review of Cytology 224 : 57 110.
69. Friedman AL, Keegstra K. 1989. Chloroplast protein import: quantitative analysis of precursor binding. Plant Physiology 89 : 993 999.
70. Frydman J, Höhfeld J. 1997. Chaperones get in touch: the Hip-Hop connection. Trends in Biochemical Sciences 22 : 87 92.
71. 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.
72. Gaikwad A, Tewari KK, Kumar D, Chen W, Mukherjee SK. 1999. Isolation and characterisation of the cDNA encoding a glycosylated accessory protein of pea chloroplast DNA polymerase. Nucleic Acids Research 27 : 3120 3129.
73. Gakh O, Cavadini P, Isaya G. 2002. Mitochondrial processing peptidases. Biochimica et Biophysica Acta 1592 : 63 77.
74. Gentle IE, Burri L, Lithgow T. 2005. Molecular architecture and function of the Omp85 family of proteins. Molecular Microbiology 58 : 1216 1225.
75. Guera A, America T, van Waas M, Weisbeek PJ. 1993. A strong protein unfolding activity is associated with the binding of precursor chloroplast proteins to chloroplast envelopes. Plant Molecular Biology 23 : 309 324.
76. Gutensohn M, Fan E, Frielingsdorf S, Hanner P, Hou B, Hust B, Klösgen RB. 2006. Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. Journal of Plant Physiology 163 : 333 347.
77. 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. Plant Journal 23 : 771 783.
78. Haas BJ, Wortman JR, Ronning CM, Hannick LI, Smith RK Jr., Maiti R, Chan AP, Yu C, Farzad M, Wu D et al. 2005. Complete reannotation of the Arabidopsis genome: methods, tools, protocols and the final release. BMC Biology 3 : 7.
79. Hawkins J, Bodén M. 2006. Detecting and sorting targeting peptides with neural networks and support vector machines. Journal of Bioinformatics and Computational Biology 4 : 1 18.
80. von Heijne G, Nishikawa K. 1991. Chloroplast transit peptides. The perfect random coil? FEBS Letters 278 : 1 3.
81. 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.
82. Highfield PE, Ellis RJ. 1978. Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271 : 420 424.
83. Hiltbrunner A, Bauer J, Vidi PA, Infanger S, Weibel P, Hohwy M, Kessler F. 2001. 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.
84. 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.
85. Hinnah SC, Hill K, Wagner R, Schlicher T, Soll J. 1997. Reconstitution of a chloroplast protein import channel. EMBO Journal 16 : 7351 7360.
86. 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.
87. Hirohashi T, Hase T, Nakai M. 2001. Maize nonphotosynthetic ferredoxin precursor is mis-sorted to the intermembrane space of chloroplasts in the presence of light. Plant Physiology 125 : 2154 2163.
88. 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.
89. Hofmann NR, Theg SM. 2003. Physcomitrella patens as a model for the study of chloroplast protein transport: conserved machineries between vascular and nonvascular plants. Plant Molecular Biology 53 : 621 632.
90. Hofmann NR, Theg SM. 2005a. Protein- and energy-mediated targeting of chloroplast outer envelope membrane proteins. Plant Journal 44 : 917 927.
91. Hofmann NR, Theg SM. 2005b. Toc64 is not required for import of proteins into chloroplasts in the moss Physcomitrella patens. Plant Journal 43 : 675 687.
92. Hofmann NR, Theg SM. 2005c. Chloroplast outer membrane protein targeting and insertion. Trends in Plant Science 10 : 450 457.
93. Höglund A, Dönnes P, Blum T, Adolph HW, Kohlbacher O. 2006. MultiLoc: prediction of protein subcellular localization using N-terminal targeting sequences, sequence motifs and amino acid composition. Bioinformatics 22 : 1158 1165.
94. Hönlinger A, Kübrich M, Moczko M, Gärtner F, Mallet L, Bussereau F, Eckerskorn C, Lottspeich F, Dietmeier K, Jacquet M et al. 1995. The mitochondrial receptor complex: Mom22 is essential for cell viability and directly interacts with preproteins. Molecular and Cellular Biology 15 : 3382 3389.
95. 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.
96. 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.
97. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Research 35 : W585 W587.
98. Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM. 2006. The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugar-signaling mechanism in Arabidopsis. Plant Cell 18 : 1226 1238.
99. Hust B, Gutensohn M. 2006. Deletion of core components of the plastid protein import machinery causes differential arrest of embryo development in Arabidopsis thaliana. Plant Biology 8 : 18 30.
100. Inaba T, Alvarez-Huerta M, Li M, Bauer J, Ewers C, Kessler F, Schnell DJ. 2005. Arabidopsis Tic110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell 17 : 1482 1496.
101. 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.
102. Inoue H, Akita M. 2008. Three sets of translocation intermediates are formed during the early stage of protein import into chloroplasts. Journal of Biological Chemistry 283 : 7491 7502.
103. Inoue K, Baldwin AJ, Shipman RL, Matsui K, Theg SM, Ohme-Takagi M. 2005. Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. Journal of Cell Biology 171 : 425 430.
104. Inoue K, Keegstra K. 2003. A polyglycine stretch is necessary for proper targeting of the protein translocation channel precursor to the outer envelope membrane of chloroplasts. Plant Journal 34 : 661 669.
105. 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. Plant Journal 39 : 354 365.
106. 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.
107. Ivey RA 3rd., Bruce BD. 2000. In vivo and in vitro interaction of DnaK and a chloroplast transit peptide. Cell Stress & Chaperones 5 : 62 71.
108. 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.
109. Jackson-Constan D, Akita M, Keegstra K. 2001. Molecular chaperones involved in chloroplast protein import. Biochimica et Biophysica Acta 1541 : 102 113.
110. Jackson-Constan D, Keegstra K. 2001. Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiology 125 : 1567 1576.
111. Jarvis P. 2004. Organellar proteomics: chloroplasts in the spotlight. Current Biology 14 : R317 R319.
112. Jarvis P. 2007. The proteomes of chloroplasts and other plastids. In : Šamaj J, Thelen JJ, eds. Plant proteomics. Heidelberg, Germany : Springer-Verlag, 207 225.
113. 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.
114. Jarvis P, Robinson C. 2004. Mechanisms of protein import and routing in chloroplasts. Current Biology 14 : R1064 R1077.
115. Jarvis P, Soll J. 2002. Toc, Tic, and chloroplast protein import. Biochimica et Biophysica Acta 1590 : 177 189.
116. Jelic M, Soll J, Schleiff E. 2003. Two Toc34 homologues with different properties. Biochemistry 42 : 5906 5916.
117. 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.
118. 3 chamber for proteolysis. EMBO Journal 25 : 1977 1986.
119. Keegstra K, Cline K. 1999. Protein import and routing systems of chloroplasts. Plant Cell 11 : 557 570.
120. Keenan RJ, Freymann DM, Stroud RM, Walter P. 2001. The signal recognition particle. Annual Review of Biochemistry 70 : 755 775.
121. 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.
122. 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.
123. Kessler F, Schnell DJ. 2002. A GTPase gate for protein import into chloroplasts. Nature Structural Biology 9 : 81 83.
124. Kessler F, Schnell DJ. 2004. Chloroplast protein import: solve the GTPase riddle for entry. Trends in Cell Biology 14 : 334 338.
125. Kessler F, Schnell DJ. 2006. The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic 7 : 248 257.
126. Kikuchi S, Hirohashi T, Nakai M. 2006. Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant & Cell Physiology 47 : 363 371.
127. Kim C, Apel K. 2004. Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell 16 : 88 98.
128. 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. Plant Journal 42 : 329 340.
129. 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.
130. Knight JS, Gray JC. 1995. The N-terminal hydrophobic region of the mature phosphate translocator is sufficient for targeting to the chloroplast inner envelope membrane. Plant Cell 7 : 1421 1432.
131. 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.
132. 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.
133. Kouranov A, Wang H, Schnell DJ. 1999. Tic22 is targeted to the intermembrane space of chloroplasts by a novel pathway. Journal of Biological Chemistry 274 : 25181 25186.
134. Kourtz L, Ko K. 1997. The early stage of chloroplast protein import involves Com70. Journal of Biological Chemistry 272 : 2808 2813.
135. 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. Plant Journal 41 : 412 428.
136. Kovacheva S, Bédard J, Wardle A, Patel R, Jarvis P. 2007. Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant Journal 50 : 364 379.
137. Krimm I, Gans P, Hernandez JF, Arlaud GJ, Lancelin JM. 1999. A coil-helix instead of a helix-coil motif can be induced in a chloroplast transit peptide from Chlamydomonas reinhardtii. European Journal of Biochemistry 265 : 171 180.
138. 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. Plant Cell 15 : 1859 1871.
139. Kubis S, Patel R, Combe J, Bédard J, Kovacheva S, Lilley K, Biehl A, Leister D, Ríos G, Koncz C, Jarvis P. 2004. Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16 : 2059 2077.
140. Küchler M, Decker S, Hörmann F, Soll J, Heins L. 2002. Protein import into chloroplasts involves redox-regulated proteins. EMBO Journal 21 : 6136 6145.
141. Larkum AW, Lockhart PJ, Howe CJ. 2007. Shopping for plastids. Trends in Plant Science 12 : 189 195.
142. Lee DW, Lee S, Lee GJ, Lee KH, Kim S, Cheong GW, Hwang I. 2006. Functional characterization of sequence motifs in the transit peptide of Arabidopsis small subunit of Rubisco. Plant Physiology 140 : 466 483.
143. Lee KH, Kim DH, Lee SW, Kim ZH, Hwang I. 2002. In vivo import experiments in protoplasts reveal the importance of the overall context but not specific amino acid residues of the transit peptide during import into chloroplasts. Molecules and Cells 14 : 388 397.
144. 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.
145. 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. Plant Cell 13 : 2175 2190.
146. Leheny EA, Theg SM. 1994. Apparent inhibition of chloroplast protein import by cold temperatures is due to energetic considerations not membrane fluidity. Plant Cell 6 : 427 437.
147. Leister D. 2003. Chloroplast research in the genomic age. Trends in Genetics 19 : 47 56.
148. Li HM, Kesavulu MM, Su PH, Yeh YH, Hsiao CD. 2007. Toc GTPases. Journal of Biomedical Science 14 : 505 508.
149. Li M, Schnell DJ. 2006. Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. Journal of Cell Biology 175 : 249 259.
150. Lopez-Juez E. 2007. Plastid biogenesis, between light and shadows. Journal of Experimental Botany 58 : 11 26.
151. Lopez-Juez E, Pyke KA. 2005. Plastids unleashed: their development and their integration in plant development. International Journal of Developmental Biology 49 : 557 577.
152. 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.
153. Lübeck J, Heins L, Soll J. 1997. A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. Journal of Cell Biology 137 : 1279 1286.
154. 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.
155. 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.
156. Madueño F, Napier JA, Gray JC. 1993. Newly imported Rieske iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 5 : 1865 1876.
157. Marc P, Margeot A, Devaux F, Blugeon C, Corral-Debrinski M, Jacq C. 2002. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Reports 3 : 159 164.
158. 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.
159. Martin T, Sharma R, Sippel C, Waegemann K, Soll J, Vothknecht UC. 2006. A protein kinase family in Arabidopsis phosphorylates chloroplast precursor proteins. Journal of Biological Chemistry 281 : 40216 40223.
160. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proceeding of the National Academy of Sciences, USA 99 : 12246 12251.
161. 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.
162. May T, Soll J. 2000. 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12 : 53 64.
163. Millar AH, Whelan J, Small I. 2006. Recent surprises in protein targeting to mitochondria and plastids. Current Opinion in Plant Biology 9 : 610 615.
164. Miras S, Salvi D, Ferro M, Grunwald D, Garin J, Joyard J, Rolland N. 2002. Noncanonical transit peptide for import into the chloroplast. Journal of Biological Chemistry 277 : 47770 47778.
165. Miras S, Salvi D, Piette L, Seigneurin-Berny D, Grunwald D, Reinbothe C, Joyard J, Reinbothe S, Rolland N. 2007. Toc159- and Toc75-independent import of a transit sequence-less precursor into the inner envelope of chloroplasts. Journal of Biological Chemistry 282 : 29482 29492.
166. Moberg P, Stahl A, Bhushan S, Wright SJ, Eriksson A, Bruce BD, Glaser E. 2003. Characterization of a novel zinc metalloprotease involved in degrading targeting peptides in mitochondria and chloroplasts. Plant Journal 36 : 616 628.
167. Nada A, Soll J. 2004. Inner envelope protein 32 is imported into chloroplasts by a novel pathway. Journal of Cell Science 117 : 3975 3982.
168. Nakai K, Horton P. 2007. Computational prediction of subcellular localization. Methods in Molecular Biology 390 : 429 466.
169. 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.
170. Nanjo Y, Oka H, Ikarashi N, Kaneko K, Kitajima A, Mitsui T, Muñoz FJ, Rodríguez-López M, Baroja-Fernández E, Pozueta-Romero J. 2006. Rice plastidial N-glycosylated nucleotide pyrophosphatase/ phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 18 : 2582 2592.
171. Nassoury N, Morse D. 2005. Protein targeting to the chloroplasts of photosynthetic eukaryotes: getting there is half the fun. Biochimica et Biophysica Acta 1743 : 5 19.
172. Natesan SK, Sullivan JA, Gray JC. 2005. Stromules: a characteristic cell-specific feature of plastid morphology. Journal of Experimental Botany 56 : 787 797.
173. Nelson N, Ben-Shem A. 2004. The complex architecture of oxygenic photosynthesis. Nature Reviews. Molecular Cell Biology 5 : 971 982.
174. Neuhaus HE, Emes MJ. 2000. Nonphotosynthetic metabolism in plastids. Annual Review of Plant Physiology and Plant Molecular Biology 51 : 111 140.
175. Neupert W, Brunner M. 2002. The protein import motor of mitochondria. Nature Reviews. Molecular Cell Biology 3 : 555 565.
176. Neupert W, Herrmann JM. 2007. Translocation of proteins into mitochondria. Annual Review of Biochemistry 76 : 723 749.
177. 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.
178. 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.
179. 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.
180. Pain D, Blobel G. 1987. Protein import into chloroplasts requires a chloroplast ATPase. Proceeding of the National Academy of Sciences, USA 84 : 3288 3292.
181. Papanikou E, Karamanou S, Economou A. 2007. Bacterial protein secretion through the translocase nanomachine. Nature Reviews. Microbiology 5 : 839 851.
182. Perry SE, Keegstra K. 1994. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 6 : 93 105.
183. Philippar K, Geis T, Ilkavets I, Oster U, Schwenkert S, Meurer J, Soll J. 2007. Chloroplast biogenesis: the use of mutants to study the etioplast-chloroplast transition. Proceedings of the National Academy of Sciences, USA 104 : 678 683.
184. Pilon M, Wienk H, Sips W, de Swaaf M, Talboom I, van 't Hof R, de Korte-Kool G, Demel R, Weisbeek P, de Kruijff B. 1995. Functional domains of the ferredoxin transit sequence involved in chloroplast import. Journal of Biological Chemistry 270 : 3882 3893.
185. Platta HW, Erdmann R. 2007. The peroxisomal protein import machinery. FEBS Letters 581 : 2811 2819.
186. Pollmann S, Springer A, Buhr F, Lahroussi A, Samol I, Bonneville JM, Tichtinsky G, von Wettstein D, Reinbothe C, Reinbothe S. 2007. A plant porphyria related to defects in plastid import of protochlorophyllide oxidoreductase A. Proceedings of the National Academy of Sciences, USA 104 : 2019 2023.
187. Qbadou S, Becker T, Bionda T, Reger K, Ruprecht M, Soll J, Schleiff E. 2007. Toc64 - a preprotein-receptor at the outer membrane with bipartide function. Journal of Molecular Biology 367 : 1330 1346.
188. Qbadou S, Becker T, Mirus O, Tews I, Soll J, Schleiff E. 2006. The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO Journal 25 : 1836 1847.
189. Radhamony RN, Theg SM. 2006. Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends in Cell Biology 16 : 385 387.
190. Ramage L, Junne T, Hahne K, Lithgow T, Schatz G. 1993. Functional cooperation of mitochondrial protein import receptors in yeast. EMBO Journal 12 : 4115 4123.
191. Rapaport D. 2005. How does the TOM complex mediate insertion of precursor proteins into the mitochondrial outer membrane? Journal of Cell Biology 171 : 419 423.
192. Reddick LE, Vaughn MD, Wright SJ, Campbell IM, Bruce BD. 2007. In vitro comparative kinetic analysis of the chloroplast Toc GTPases. Journal of Biological Chemistry 282 : 11410 11426.
193. Reinbothe C, Lebedev N, Apel K, Reinbothe S. 1997. Regulation of chloroplast protein import through a protochlorophyllide-responsive transit peptide. Proceedings of the National Academy of Sciences, USA 94 : 8890 8894.
194. Reinbothe S, Runge S, Reinbothe C, van Cleve B, Apel K. 1995. Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids. Plant Cell 7 : 161 172.
195. Reiss B, Wasmann CC, Schell J, Bohnert HJ. 1989. Effect of mutations on the binding and translocation functions of a chloroplast transit peptide. Proceedings of the National Academy of Sciences, USA 86 : 886 890.
196. Rensink WA, Schnell DJ, Weisbeek PJ. 2000. The transit sequence of ferredoxin contains different domains for translocation across the outer and inner membrane of the chloroplast envelope. Journal of Biological Chemistry 275 : 10265 10271.
197. 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.
198. Reumann S, Inoue K, Keegstra K. 2005. Evolution of the general protein import pathway of plastids. Molecular Membrane Biology 22 : 73 86.
199. Reumann S, Keegstra K. 1999. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends in Plant Science 4 : 302 307.
200. Reyes-Prieto A, Weber AP, Bhattacharya D. 2007. The origin and establishment of the plastid in algae and plants. Annual Review of Genetics 41 : 147 168.
201. + reductase precursor. Physiologia Plantarum 128 : 618 632.
202. 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.
203. + reductase precursor into chloroplasts is modulated by the region between the transit peptide and the mature core of the protein. European Journal of Biochemistry 269 : 5431 5439.
204. Rial DV, Ottado J, Ceccarelli EA. 2003. Precursors with altered affinity for Hsp70 in their transit peptides are efficiently imported into chloroplasts. Journal of Biological Chemistry 278 : 46473 46481.
205. Richly E, Leister D. 2004. An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329 : 11 16.
206. Richter S, Lamppa GK. 1998. A chloroplast processing enzyme functions as the general stromal processing peptidase. Proceedings of the National Academy of Sciences, USA 95 : 7463 7468.
207. 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.
208. Richter S, Lamppa GK. 2002. Determinants for removal and degradation of transit peptides of chloroplast precursor proteins. Journal of Biological Chemistry 277 : 43888 43894.
209. 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.
210. 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.
211. 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 Sciences 28 : 523 526.
212. Schatz G, Dobberstein B. 1996. Common principles of protein translocation across membranes. Science 271 : 1519 1526.
213. Schein AI, Kissinger JC, Ungar LH. 2001. Chloroplast transit peptide prediction: a peek inside the black box. Nucleic Acids Research 29 : E82.
214. Schemenewitz A, Pollmann S, Reinbothe C, Reinbothe S. 2007. A substrate-independent, 14:3:3 protein-mediated plastid import pathway of NADPH:protochlorophyllide oxidoreductase A. Proceedings of the National Academy of Sciences, USA 104 : 8538 8543.
215. Schleiff E, Eichacker LA, Eckart K, Becker T, Mirus O, Stahl T, Soll J. 2003c. Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope. Protein Science 12 : 748 759.
216. Schleiff E, Jelic M, Soll J. 2003a. A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proceeding of the National Academy of Sciences, USA 100 : 4604 4609.
217. 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.
218. Schleiff E, Soll J, Küchler M, Kuhlbrandt W, Harrer R. 2003b. Characterization of the translocon of the outer envelope of chloroplasts. Journal of Cell Biology 160 : 541 551.
219. 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.
220. 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.
221. 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.
222. 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.
223. Schnell DJ, Hebert DN. 2003. Protein translocons: multifunctional mediators of protein translocation across membranes. Cell 112 : 491 505.
224. Schnell DJ, Kessler F, Blobel G. 1994. Isolation of components of the chloroplast protein import machinery. Science 266 : 1007 1012.
225. 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.
226. Seedorf M, Waegemann K, Soll J. 1995. A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant Journal 7 : 401 411.
227. Silva-Filho MC. 2003. One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations. Current Opinion in Plant Biology 6 : 589 595.
228. Small I, Peeters N, Legeai F, Lurin C. 2004. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4 : 1581 1590.
229. 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.
230. Smith MD. 2006. Protein import into chloroplasts: an ever-evolving story. Canadian Journal of Botany 84 : 531 542.
231. Sohrt K, Soll J. 2000. Toc64, a new component of the protein translocon of chloroplasts. Journal of Cell Biology 148 : 1213 1221.
232. Soll J, Schleiff E. 2004. Protein import into chloroplasts. Nature Reviews. Molecular Cell Biology 5 : 198 208.
233. 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.
234. Stengel A, Benz P, Balsera M, Soll J, Bölter B. 2008. Tic62 - redox-regulated translocon composition and dynamics. Journal of Biological Chemistry 283 : 6656 6667.
235. Sun YJ, Forouhar F, Li 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.
236. Sveshnikova N, Soll J, Schleiff E. 2000. Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proceedings of the National Academy of Sciences, USA 97 : 4973 4978.
237. 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.
238. Teng YS, Su YS, Chen LJ, Lee YJ, Hwang I, Li HM. 2006. Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane. Plant Cell 18 : 2247 2257.
239. 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.
240. Timmis JN, Ayliffe MA, Huang CY, Martin W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Reviews. Genetics 5 : 123 135.
241. 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.
242. Tranel PJ, Keegstra K. 1996. A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 8 : 2093 2104.
243. Tripp J, Inoue K, Keegstra K, Froehlich JE. 2007. A novel serine/proline-rich domain in combination with a transmembrane domain is required for the insertion of AtTic40 into the inner envelope membrane of chloroplasts. Plant Journal 52 : 824 838.
244. Tsai LY, Tu SL, Li HM. 1999. Insertion of atToc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. Journal of Biological Chemistry 274 : 18735 18740.
245. + reductase upon its import into chloroplasts. FEBS Letters 320 : 198 202.
246. 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. Plant Cell 16 : 2078 2088.
247. Tu SL, Li HM. 2000. Insertion of OEP14 into the outer envelope membrane is mediated by proteinaceous components of chloroplasts. Plant Cell 12 : 1951 1960.
248. 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.
249. Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N et al. 2005. Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nature Cell Biology 7 : 1124 1131.
250. Voigt A, Jakob M, Klösgen RB, Gutensohn M. 2005. At least two Toc34 protein import receptors with different specificities are also present in spinach chloroplasts. FEBS Letters 579 : 1343 1349.
251. Vojta A, Alavi M, Becker T, Hörmann F, Küchler M, Soll J, Thomson R, Schleiff E. 2004. The protein translocon of the plastid envelopes. Journal of Biological Chemistry 279 : 21401 21405.
252. Vojta L, Soll J, Bölter B. 2007a. Protein transport in chloroplasts - targeting to the intermembrane space. FEBS Journal 274 : 5043 5054.
253. Vojta L, Soll J, Bölter B. 2007b. Requirements for a conservative protein translocation pathway in chloroplasts. FEBS Letters 581 : 2621 2624.
254. Waegemann K, Soll J. 1991. Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant Journal 1 : 149 158.
255. 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.
256. 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.
257. 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. Plant Journal 15 : 459 468.
258. 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.
259. Whatley JM. 1978. A suggested cycle of plastid developmental interrelationships. New Phytologist 80 : 489 502.
260. Whatley JM, McLean B, Juniper BE. 1991. Continuity of chloroplast and endoplasmic reticulum membranes in Phaseolus vulgaris. New Phytologist 117 : 209 217.
261. Wienk HL, Wechselberger RW, Czisch M, de Kruijff B. 2000. Structure, dynamics, and insertion of a chloroplast targeting peptide in mixed micelles. Biochemistry 39 : 8219 8227.
262. 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.
263. 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.
264. Yalovsky S, Paulsen H, Michaeli D, Chitnis PR, Nechushtai R. 1992. Involvement of a chloroplast HSP70 heat shock protein in the integration of a protein (light-harvesting complex protein precursor) into the thylakoid membrane. Proceedings of the National Academy of Sciences, USA 89 : 5616 5619.
265. Yan X, Khan S, Hase T, Emes MJ, Bowsher CG. 2006. Differential uptake of photosynthetic and nonphotosynthetic proteins by pea root plastids. FEBS Letters 580 : 6509 6512.
266. Yeh YH, Kesavulu MM, Li HM, Wu SZ, Sun YJ, Konozy EH, Hsiao CD. 2007. Dimerization is important for the GTPase activity of chloroplast translocon components atToc33 and psToc159. Journal of Biological Chemistry 282 : 13845 13853.
267. 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.
268. Yu TS, Li H. 2001. Chloroplast protein translocon components at Toc159 and atToc33 are not essential for chloroplast biogenesis in guard cells and root cells. Plant Physiology 127 : 90 96.
269. 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.
270. 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. Plant Journal 34 : 802 812.