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Plant Biol (Stuttg) 2005; 7(1): 1-14
DOI: 10.1055/s-2004-830447
DOI: 10.1055/s-2004-830447
Acute View
Georg Thieme Verlag Stuttgart KG · New York
Let's Talk about … Chloroplast Import
Weitere Informationen
Publikationsverlauf
Received: March 18, 2004
Accepted: September 13, 2004
Publikationsdatum:
21. Januar 2005 (online)
An Easy Beginning - The Introduction
The double membrane surrounding chloroplasts and other plastids originated from the engulfment of an ancestral cyanobacterium by a eukaryotic host cell, in a process called endosymbiosis ([Weeden, 1981]). During evolution, the genes of the endosymbiont were transferred to the host nuclear genome ([Martin et al., 1998]; [Blanchard and Lynch, 2000]; [Timmis et al., 2004]). Thus, the semi-autonomous genome of modern plastids contains only information for about 150 genes, implying a drastic reduction in genetic information compared to the genome of a modern cyanobacterium, which encodes several thousands of genes ([Leister, 2003]). This raises questions regarding the ability of chloroplasts to maintain various biochemical functions, such as photosynthesis, amino acid, and lipid synthesis. The evolutionary solution is the post-translational import of nuclear encoded proteins into the chloroplasts to fulfill their catalytic functions. Therefore, a complex system of cytosolic targeting, translocation across the two envelope membranes, and a subsequent intraorganellar sorting had to be established. For that, a multi-component complex in the envelope membranes is facilitated (Fig. [1]). This review will present a detailed description of the cytosolic targeting, as well as the translocation of pre-proteins across both chloroplast membranes and will highlight the latest discoveries. Another focus will be to indicate unsolved questions and to propose mechanistic models for cytosolic targeting and translocation.
Fig. 1 A model of the currently known composition of the translocation machinery. The Toc complex consists of two receptor proteins, Toc34 and Toc159, the protein conducting channel Toc75-III, and the dynamically associated Toc64. Two Hsp70 homologues, either projecting to the cytosol or exposed to the intermembrane space, assists translocation across the outer envelope membrane. Toc75-V might form an additional complex with so far unidentified components. Furthermore, Oep16 in association with Toc34 were suggested to be components for an alternative import pathway. The Tic complex, comprising Tic110, Tic62, Tic55, Tic40, Tic22, and Tic20, catalyses transfer of pre-proteins across the inner envelope. The import is driven with the aid of stromal chaperones like Hsp100, Cpn60, and the stromal Hsp70. Finally, the transit peptide (tp) is removed by a stromal processing peptidase (SPP).
Literature
- 1 Aronsson H., Sohrt K., Soll J.. NADPH:Protochlorophyllide oxidoreductase uses the general import route into chloroplasts. Biological Chemistry. (2000); 381 1263-1267
- 2 Bauer J., Chen K., Hiltbunner A., Wehrli E., Eugster M., Schnell D. J., Kessler F.. The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature. (2000); 403 203-207
- 3 Bauer J., Hiltbrunner A., Weibel P., Vidi P. A., Alvarez-Huerta M., Smith M. D., Schnell D. J., Kessler F.. Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane. Journal of Cell Biology. (2002); 159 845-854
- 4 Becker T., Jelic M., Vojta A., Radunz A., Soll J., Schleiff E.. Preprotein recognition by the Toc complex. EMBO Journal. (2004); 23 520-530
- 5 Ben-Shaul A., Ben-Tal N., Honig B.. Statistical thermodynamic analysis of peptide and protein insertion into lipid membranes. Biophysical Journal. (1996); 71 130-137
- 6 Blanchard J. L., Lynch M.. Organellar genes: why do they end up in the nucleus?. Trends in Genetics. (2000); 16 315-320
- 7 Bölter B., Soll J., Hill K., Helmmer R., Wagner R.. A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO Journal. (1999); 18 5505-5516
- 8 Bruce B. D.. The role of lipids in plastid protein transport. Plant Molecular Biology. (1998); 38 223-246
- 9 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 ironbinding protein. EMBO Journal. (1997); 16 7342-7350
- 10 Chen D., Schnell D. J.. Insertion of the 34-kDa chloroplast protein import component, IAP34, into the chloroplast outer membrane is dependent on its intrinsic GTPbinding capacity. Journal of Biological Chemistry. (1997); 272 6614-6620
- 11 Chen K., Chen X., Schnell D. J.. Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiology. (2000); 122 813-822
- 12 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
- 13 Cline K.. Gateway to the chloroplast. Nature. (2000); 403 148-149
- 14 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 Journal. (2003); 22 2970-2980
- 15 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 Journal. (2004); 38 93-106
- 16 Dorne A. J., Jojard J., Block M. A., Dource R.. Localization of phosphatidylcholine in outer envelope membrane of spinach chloroplasts. Journal of Cell Biology. (1985); 100 1690-1697
- 17 Eckart K., Eichacker L., Sohrt K., Schleiff E., Heins L., Soll J.. A Toc75-like protein import channel is abundant in chloroplasts. EMBO Reports. (2002); 3 557-562
- 18 Endo T., Kawamura K., Nakai M.. The chloroplast-targeting domain of plastocyanin transit peptide can form a helical structure but does not have a high affinity for lipid bilayers. European Journal of Biochemistry. (1992); 207 671-675
- 19 Ferro M., Salvi D., Brugiere S., Miras S., Kowalski S., Louwagie M., Garin J., Joyard J., Rolland N.. Proteomics of the Chloroplast Envelope Membranes from Arabidopsis thaliana. Molecular and Cellular Proteomics. (2003); 2 325-345
- 20 Fischer K., Weber A., Arbinger B., Brink A., Eckerskorn C., Flügge U. I.. The 24 kDa outer envelope membrane protein from spinach chloroplast: molecular cloning, in vivo expression and import pathway of a protein with unusual properties. Plant Molecular Biology. (1994); 25 167-177
- 21 Flügge U. I., Hinz G.. Energy dependence of protein translocation into chloroplasts. European Journal of Biochemistry. (1986); 160 563-570
- 22 Froehlich J. E., Itoh A., Howe G. A.. Tomato allene oxidase synthase and fatty acid hydroperoxide lyase, two cytochrome P450 s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiology. (2001); 125 306-317
- 23 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 Journal. (2000); 23 771-783
- 24 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 Journal. (2002); 21 2616-2625
- 25 Hiltbrunner A., Bauer J., Vidi P. A., Infanger S., Weibel P., Hohwy M., Kessler F.. Targeting of an abundant cytosolic form of the protein import receptor at Toc159 to the outer chloroplast membrane. Journal of Cell Biology. (2001); 154 309-316
- 26 Hinnah S. C., Hill K., Wagner R., Schlicher T., Soll J.. Reconstitution of a chloroplast protein import channel. EMBO Journal. (1997); 16 7351-7360
- 27 Hinnah S. C., Wagner R., Sveshnikova N., Harrer R., Soll J.. The chloroplast protein import channel toc75: pore properties and interaction with transit peptides. Biophysical Journal. (2002); 83 899-911
- 28 Hirohashi T., Hase T., Nakai M.. Maize non-photosynthetic ferredoxin precursor is missorted to the intermembrane space of chloroplasts in the presence of light. Plant Physiology. (2001); 125 2154-2163
- 29 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
- 30 Hohfeld J., Minami Y., Hartl F. U.. Hip, a novel cochaperone involved in eukaryotic Hsc70/Hsp40 reaction cycle. Cell. (1995); 83 589-598
- 31 Hörmann F., Küchler M., Sveshnikov D., Oppermann U., Li Y., Soll J.. Tic32, an essential component in chloroplast biogenesis. Journal of Biological Chemistry. (2004); 279 34756-34762
- 32 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. Molecular Biology of the Cell. (2004); 15 3379-3392
- 33 Ivey III. R. A., Bruce B. D.. In vivo and in vitro interaction of DnaK and a chloroplast transit peptide. Cell Stress and Chaperones. (2000); 5 62-71
- 34 Ivey III. R. A., Subramanian C., Bruce B. D.. Identification of a Hsp70 recognition domain within the rubisco small subunit transit peptide. Plant Physiology. (2000); 122 1289-1299
- 35 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. Journal of Biological Chemistry. (1998); 273 16583-16588
- 36 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
- 37 Jelic M., Sveshnikova N., Motzkus M., Hörth P., Soll J., Schleiff E.. The chloroplast import receptor Toc34 functions as preprotein regulated GTPase. Biological Chemistry. (2002); 383 1875-1883
- 38 Jelic M., Soll J., Schleiff E.. Two Toc34 homologues with different properties. Biochemistry. (2003); 42 5906-5916
- 39 Kamp D., Sieberg T., Haest C. W.. Inhibition and stimulation of phospholipid scrambling activity. Consequences for lipid asymmetrie, echinocytosis, and microvesiculation of erythrocytes. Biochemistry. (2001); 40 9438-9446
- 40 Keegstra K., Cline K.. Protein import and routing systems of chloroplasts. Plant Cell. (1999); 11 557-570
- 41 Kessler F., Blobel G., Patel H. A., Schnell D. J.. Identification of two GTPbinding proteins in the chloroplast protein import machinery. Science. (1994); 266 1035-1039
- 42 Kessler F., Blobel G.. Interaction of the protein import and folding machineries in the chloroplast. Proceedings of the National Academy of Sciences of the USA. (1996); 93 7684-7689
- 43 Kim C., Apel K.. Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell. (2004); 16 88-98
- 44 Kleffmann T., Russenberger D., von Zychlinski A., Christopher W., Sjolander K., Gruissem W., Baginsky S.. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biology. (2004); 14 354-362
- 45 Ko K., Budd D., Wu C., Seibert F., Kourtz L., Ko Z. W.. 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. (1995); 270 28601-28608
- 46 Kourtz L., Ko K.. The early stage of chloroplast protein import involves Com70. Journal of Biological Chemistry. (1997); 272 2808-2813
- 47 Kouranov A., Schnell D. J.. Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts. Journal of Cell Biology. (1997); 139 1677-1685
- 48 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. Journal of Biological Chemistry. (1998); 143 991-1002
- 49 Kubis S., Baldwin A., Patel R., Razzaq A., Dupree P., Lilley K., Kurth J., Leister D., Jarvis P.. The Arabidopsis ppi1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell. (2003); 15 1859-1871
- 50 Küchler M., Decker S., Soll J., Heins L.. Protein import into chloroplasts involves redox-regulated proteins. EMBO Journal. (2002); 21 6136-6145
- 51 Lee Y. J., Kim D. H., Kim Y. W., Hwang I.. Identification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane system in vivo. Plant Cell. (2001); 13 2175-2190
- 52 Lee K. H., Kim S. J., Lee Y. J., Jin J. B., Hwang I.. The M domain of atToc159 plays an essential role in the import of proteins into chloroplasts and chloroplast biogenesis. Journal of Biological Chemistry. (2003); 278 36794-36805
- 53 Lee Y. J., Sohn E. J., Lee K. H., Lee D. W., Hwang I.. The transmembrane domain of AtTco64 and its C-terminal lysine-rich flanking region are targeting signals to the chloroplast outer envelope membrane. Molecular Cell. (2004); 17 281-291
- 54 Leister D.. Chloroplast research in the genomic age. Trends in Genetics. (2003); 19 47-56
- 55 Li H. M., Moore T., Keegstra K.. Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts. Plant Cell. (1991); 3 709-717
- 56 Li H. M., Chen L. J.. Protein targeting and integration signal for the chloroplastic outer envelope membrane. Plant Cell. (1996); 8 2117-2126
- 57 Lübeck J., Soll J.. Nucleoside diphosphate kinase from pea chloroplasts: purification, cDNA cloning and import into chloroplasts. Planta. (1995); 196 668-673
- 58 Lübeck J., Soll J., Akita M., Nielsen E., Keegstra K.. Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO Journal. (1996); 15 4230-4238
- 59 Lübeck J., Heins L., Soll J.. A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. Journal of Cell Biology. (1997); 137 1279-1286
- 60 Marshall J. S., DeRocher A. E., Keegstra K., Vierling E.. Identification of heat shock protein hsp70 homologues in chloroplast. Proceedings of the National Academy of Sciences of the USA. (1990); 87 374-378
- 61 Martin W., Stoebe B., Goremykin S., Hansmann S., Hasewaga M., Kowallik K.. Gene transfer to the nucleus and the evolution of chloroplasts. Nature. (1998); 393 162-165
- 62 May T., Soll J.. 14 - 3 - 3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell. (2000); 12 53-64
- 63 Miras S., Salvi D., Ferro M., Grunwald D., Garin J., Joyard J., Rolland N.. Non-canonical transit peptide for import into the chloroplast. Journal of Biological Chemistry. (2002); 277 47770-47778
- 65 Nada A., Soll J.. Evidence for a novel protein import pathway into chloroplasts. Journal of Cell Sciences. (2004); 117 3975-3982
- 66 Nakrieko K. A., Mould R. M., Smith A. G.. Fidelity of targeting to chloroplasts is not affected by removal of the phosphorylation site from the transit peptide. European Journal of Biochemistry. (2004); 271 509-516
- 67 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 Journal. (1997); 16 935-946
- 68 Oblong J. E., Lamppa G. K.. Identification of two structurally related proteins involved in proteolytic processing of precursor targeted to the chloroplast. EMBO Journal. (1992); 11 4401-4409
- 69 Olsen L. J., Theg S. M., Selman B. R., Keegstra K.. ATP is required for the binding of precursor proteins to chloroplasts. Journal of Biological Chemistry. (1989); 264 6724-6729
- 70 Olsen L. J., Keegstra K.. The binding of precursor proteins to chloroplasts requires nucleoside triphosphates in the intermembrane space. Journal of Biological Chemistry. (1992); 267 433-439
- 71 Perry S. E., Keegstra K.. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell. (1994); 6 93-105
- 72 Pesaresi P., Gardner N. A., Masiero S., Dietzmann A., Eichacker L., Wickner R., Salamini F., Leister D.. Cytoplasmic N-terminal protein acetylation is required for efficient photosynthesis in Arabidopsis. Plant Cell. (2003); 15 1817-1832
- 73 Pilon M., de Boer D. A., Knols S. L., Koppelmann M. H. G. M., van der Graaf R. M., de Kruijff B., Weisbeek P. J.. Expression in Escherichia coli and purification of a translocation-competent precursor of the chloroplast protein ferredoxin. Journal of Biological Chemistry. (1990); 265 3358-3361
- 75 Pilon M., de Kruijff B., Weisbeek P. J.. New insights into the import mechanism of the ferredoxin precursor into chloroplasts. Journal of Biological Chemistry. (1992); 267 2548-2556
- 76 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.. Functional domains of the ferredoxin transit sequence involved in chloroplast import. Journal of Biological Chemistry. (1995); 270 3882-3893
- 77 Pohlmeyer K., Soll J., Steinkamp T., Hinnah H., Wagner R.. Isolation and characterization of an amino acid-selective channel protein present in the chloroplastic outer envelope membrane. Proceedings of the National Academy of Sciences of the USA. (1997); 94 9504-9509
- 78 Pohlmeyer K., Soll J., Grimm R., Wagner R.. A high-conductance solute channel in the chloropalstic outer envelope from pea. Plant Cell. (1998); 10 1207-1216
- 79 Resink W. A., Schnell D. J., Weisbeek P. J.. The transit sequence of ferredoxin contains different domains for translocation across the outer and inner membrane of the chloroplast envelope. Journal of Biological Chemistry. (2000); 275 10265-10271
- 80 Qbadou S., Tien R., Soll J., Schleiff E.. Membrane insertion of the chloroplastic outer envelope protein, Toc34. Journal of Cell Sciences. (2003); 116 837-846
- 81 Reinbothe S., Reinbothe C., Holtorf H., Apel K.. Two NADPH:Protochlorophyllide Oxidoreductases in Barley: Evidence for the Selective Disappearance of PORA during the Light-Induced Greening of Etiolated Seedlings. Plant Cell. (1995); 7 1933-1940
- 82 Reinbothe C., Lebedev N., Apel K., Reinbothe S.. Regulation of chloroplast protein import through a protochlorophyllide-responsive transit peptide. Proceedings of the National Academy of Sciences of the USA. (1997); 94 8890-8894
- 83 Reinbothe S., Quigley F., Gray J., Schemenewitz A., Reinbothe C.. Identification of plastid envelope proteins required for import of protochlorophyllide oxidoreductase A into the chloroplast of barley. Proceedings of the National Academy of Sciences of the USA. (2004); 101 2197-2202
- 84 Rial D. V., Arakaki A. K., Ceccarelli E. A.. Interaction of the targeting sequence of chloroplast precursor with Hsp70 molecular chaperones. European Journal of Biochemistry. (2000); 276 6239-6248
- 85 Rial D. V., Ottado J., Ceccarelli E. A.. Precursors with altered affinity for Hsp70 in their transit peptides are efficiently imported into chloroplasts. Journal of Biological Chemistry. (2003); 278 46473-46481
- 86 Richter S., Lamppa G. K.. A chloroplast processing enzyme functions as the general stromal processing peptidase. Proceedings of the National Academy of Sciences of the USA. (1998); 95 7463-7468
- 87 Richter S., Lamppa G. K.. Stromal processing peptidase binds transit peptides and initiates their ATP-dependent turnover in chloroplasts. Journal of Cell Biology. (1999); 147 33-44
- 88 Salomon M., Fischer K., Flügge U. I., Soll J.. Sequence analysis and protein import studies of an outer chloroplast envelope polypeptide. Proceedings of the National Academy of Sciences of the USA. (1990); 87 5778-5782
- 89 Schleiff E., Tien R., Salomon M., Soll J.. Lipid composition of outer leaflet of chloroplast outer envelope determines topology of OEP7. Molecular Biology of the Cell. (2001); 12 4090-4102
- 90 Schleiff E., Motzkus M., Soll J.. Chloroplast protein import inhibition by a soluble factor from wheat germ lysate. Plant Molecular Biology. (2002 a); 50 177-185
- 91 Schleiff E., Soll J., Sveshnikova N., Tien R., Wright S., Dabney-Smith C., Subramanian C., Bruce B. D.. Structural and guanosine triphosphate/diphosphate requirements for transit peptide recognition by the cytosolic domain of the chloroplast outer envelope receptor, Toc34. Biochemistry. (2002 b); 41 1934-1946
- 92 Schleiff E., Eichacker L. A., Eckart K., Becker T., Mirus O., Stahl T., Soll J.. Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope. Protein Science. (2003 a); 12 748-759
- 93 Schleiff E., Jelic M., Soll J.. A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proceedings of the National Academy of Sciences of the USA. (2003 b); 100 4604-4609
- 94 Schleiff E., Soll J., Küchler M., Kühlbrandt W., Harrer R.. Characterization of the translocon of the outer envelope of chloroplasts. Journal of Cell Biology. (2003 c); 160 541-551
- 95 Schnell D. J., Blobel G.. Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. Journal of Cell Biology. (1993); 120 103-115
- 96 Schnell D. J., Kessler F., Blobel G.. Isolation of components of the chloroplast protein import machinery. Science. (1994); 266 1007-1012
- 97 Seedorf M., Waegemann K., Soll J.. A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant Journal. (1995); 7 401-411
- 98 Smith M. D., Hiltbrunner A., Kessler F., Schnell D. J.. The targeting of the atToc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. Journal of Cell Biology. (2002); 159 833-843
- 99 Smith M. D., Rounds C. M., Wang F., Chen K., Afitlhile M., Schnell D. J.. atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. Journal of Cell Biology. (2004); 165 323-334
- 100 Sohrt K., Soll J.. Toc64, a new component of the protein translocon of chloroplasts. Journal of Cell Biology. (2000); 148 1213-1221
- 101 Soll J., Schleiff E.. Protein import into chloroplasts. Nature Reviews: Molecular Cell Biology. (2004); 5 198-208
- 102 Stahl T., Glockmann C., Soll J., Heins L.. Tic40, a new “old” subunit of the chloroplast protein import translocon. Journal of Biological Chemistry. (1999); 274 37467-37472
- 103 Steponkus P. L., Uemura M., Joseph R. A., Gilmour S. H., Thomashow M. F.. Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA. (1998); 95 14570-14575
- 104 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
- 105 Sun Y. J., Forouhar F., Li H. M., Tu S. L., Yeh Y. H., Kao S., Shr H. L., Chou C. C., Chen C., Hsiao C. D.. Crystal structure of pea Toc34, a novel GTPase of the chloroplastprotein translocon. Nature Structural Biology. (2002); 9 95-100
- 106 Sveshnikova N., Soll J., Schleiff E.. Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proceedings of the National Academy of Sciences of the USA. (2000); 97 4973-4978
- 107 Teyssier E., Block M. A., Garin J., Jojard J., Douce R.. The outer membrane protein E24 of spinach chloroplast envelope: cloning of a cDNA and topological insertion of the protein in the membrane. Comptes Rendus de l'Academie des Science, Series III. (1995); 318 17-25
- 108 Theg S. M., Geske F. J.. Biophysical characterisation of a transit peptide directing chloroplast protein import. Biochemistry. (1992); 31 5053-5060
- 109 Timmis J. N., Ayliffe M. A., Huang C. Y., Martin W.. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Reviews: Genetics. (2004); 5 123-135
- 110 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
- 111 Truscott K. N., Brandner K., Pfanner N.. Mechanisms of protein import into mitochondria. Current Biology. (2003); 13 R326-R337
- 112 Tsai L. Y., Tu S. L., Li H. M.. Insertion of atToc34 into chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. Journal of Biological Chemistry. (1999); 274 18735-18740
- 113 Tu S. L., Li H. M.. Insertion of Oep14 into the outer envelope membrane is mediated by proteinaceous components of chloroplasts. Plant Cell. (2000); 12 1951-1959
- 114 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 recognised family of metalloendopeptidases. Proceedings of the National Academy of Sciences of the USA. (1995); 92 7177-7181
- 115 Vojta A., Alavi M., Becker T., Hörmann F., Küchler M., Soll J., Thomson R., Schleiff E.. The protein translocon of the plastid envelopes. Journal of Biological Chemistry. (2004); 279 21401-21405
- 116 von Heijne G.. Membrane proteins: from sequence to structure. Annual Reviews of Biophysics and Biomolecular Structure. (1994); 23 167-192
- 117 Waegemann K., Paulsen H., Soll J.. Translocation of proteins into isolated chloroplasts require soluble factors to obtain import competence. FEBS Letters. (1990); 161 89-92
- 118 Waegemann K., Soll J.. Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant Journal. (1991); 1 149-158
- 119 Waegemann K., Soll J.. Phosphorylation of the transit sequence of chloroplast precursor proteins. Journal of Biological Chemistry. (1996); 271 6545-6554
- 120 Wallas T. R., Smith M. D., Sanchez-Nieto S., Schnell D. J.. The roles of toc34 and toc75 in targeting the toc159 preprotein receptor to chloroplasts. Journal of Biological Chemistry. (2003); 278 44289-44297
- 121 Weeden N. F.. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. Journal of Molecular Evolution. (1981); 17 133-139
- 122 White S. H., Wimley W. C.. Hydrophobic interactions of peptide with membrane interfaces. Biochimica et Biophysica Acta. (1998); 1376 339-352
- 123 Wienk H. L. J., Czisch M., de Kruijff B.. The structural flexibility of the preferredoxin transit peptide. FEBS Letters. (1999); 453 318-326
- 124 Wienk H. L., Wechselberger R. W., Czisch M., de Kruijff B.. Structure, dynamics, and insertion of a chloroplast targeting peptide in mixed micelles. Biochemistry. (2000); 39 8219-8227
- 125 Wieprecht T., Apostolov M., Beyermann M., Seelig J.. Interaction of a mitochondrial presequence with lipid membranes: role of helix formation for membrane binding and pertubation. Journal of Molecular Biology. (1999); 294 785-794
- 126 Young M. E., Keegstra K., Froehlich J. E.. GTP promotes the formation of earlyimport intermediates but is not required during the translocation step of protein import into chloroplasts. Plant Physiology. (1999); 121 237-244
- 127 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
- 128 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 Physiology. (2001); 127 90-96
- 129 Zhang J., Nomura T., Yatsunami K., Honda A., Sugimoto Y., Moriwaki T., Yamamoto J., Ohta M., Fukui T., Ichikawa A.. Nucleotide sequence of the cDNA encoding nucleoside diphosphate kinase II from spinach leaves. Biochimica et Biophysica Acta. (1993); 1171 304-306
E. Schleiff
Botanisches Institut
Ludwig-Maximilian-Universität
Menzinger Straße 67
80368 München
Germany
eMail: schleiff@lrz.uni-muenchen.de
Editor: G. Thiel