Mechanisms of protein import into thylakoids of chloroplasts

Biological Chemistry

Volumn 388, Issue 9, 2007, Pages 907-915

  Schünemann, Danja ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Chloroplast; Protein transport; Sec; SRP; Tat; Thylakoid membrane

Indexed keywords

CARRIER PROTEIN; CHLOROPLAST SIGNAL RECOGNITION PARTICLE; GUANOSINE TRIPHOSPHATASE; PROTEIN CPSECY; PROTEIN CPSRP; PROTEIN CPTAT; SEC TRANSLOCASE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CHLOROPLAST; ENERGY CONSUMPTION; HYDROPHOBICITY; NONHUMAN; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; THYLAKOID; THYLAKOID MEMBRANE;

BIOSYNTHETIC PATHWAYS; CHLOROPLASTS; INTRACELLULAR MEMBRANES; MEMBRANE TRANSPORT PROTEINS; PLANT PROTEINS; PROTEIN PRECURSORS; PROTEIN TRANSPORT; THYLAKOIDS;

EID: 34547924871     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2007.111     Document Type: Review

References (91)

1. Abdallah, F., Salamini, F., and Leister, D. (2000). A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci. 5, 141-142.
2. Alder, N.N. and Theg, S.M. (2003). Energetics of protein transport across biological membranes. A study of the thylakoid DeltapH-dependent/cpTat pathway. Cell 112, 231-242.
3. Amin, P., Sy, D.A., Pilgrim, M.L., Parry, D.H., Nussaume, L., and Hoffman, N.E. (1999). Arabidopsis mutants lacking the 43-and 54-kilodalton subunits of the chloroplast signal recognition particle have distinct phenotypes. Plant Physiol. 121, 61-70.
4. Bellafiore, S., Ferris, P., Naver, H., Göhre, V., and Rochaix, J.D. (2002). Loss of Albino3 leads to the specific depletion of the light-harvesting system. Plant Cell 14, 2303-2314.
5. Berks, B.C., Palmer, T., and Sargent, F. (2005). Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr. Opin. Microbiol. 8, 174-181.
6. Bogsch, E., Brink, S., and Robinson, C. (1997). Pathway specificity for a delta pH-dependent precursor thylakoid lumen protein is governed by a 'Sec-avoidance' motif in the transfer peptide and a 'Sec-incompatible' mature protein. EMBO J. 16, 3851-3859.
7. Brink, S., Bogsch, E.G., Edwards, W.R., Hynds, P.J., and Robinson, C. (1998). Targeting of thylakoid proteins by the ΔpH-driven twin-arginine translocation pathway requires a specific signal in the hydrophobic domain in conjunction with the twin-arginine motif. FEBS Lett. 434, 425-430.
8. Chaddock, A.M., Mant, A., Karnauchov, I., Brink, S., Herrmann, R.G., Klösgen, R.B., and Robinson, C. (1995). A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase. EMBO J. 14, 2715-2722.
9. Clark, S.A. and Theg, S.M. (1997). A folded protein can be transported across the chloroplast envelope and thylakoid membranes. Mol. Biol. Cell 8, 923-934.
10. Cline, K. and Mori, H. (2001). Thylakoid DeltapH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 154, 719-729.
11. Cline, K., Ettinger, W.F., and Theg, S.M. (1992). Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP. J. Biol. Chem. 267, 2688-2696.
12. Dabney-Smith, C., Mori, H., and Cline, K. (2003). Requirement of a Tha4-conserved transmembrane glutamate in thylakoid Tat translocase assembly revealed by biochemical complementation. J. Biol. Chem. 278, 43027-43033.
13. Dabney-Smith, C., Mori, H., and Cline, K. (2006). Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J. Biol. Chem. 281, 5476-5483.
14. DeLille, J., Peterson, E.C., Johnson, T., Moore, M., Kight, A., and Henry, R. (2000). A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplasts. Proc. Natl. Acad. Sci. USA 97, 1926-1931.
15. Di Cola, A. and Robinson, C. (2005). Large-scale translocation reversal within the thylakoid Tat system in vivo. J. Cell Biol. 171, 281-289.
16. Di Cola, A., Bailey, S., and Robinson, C. (2005a). The thylakoid delta pH/delta psi are not required for the initial stages of Tat-dependent protein transport in tobacco protoplasts. J. Biol. Chem. 280, 41165-41170.
17. Di Cola, A., Klostermann, E., and Robinson, C. (2005b). The complexity of pathways for protein import into thylakoids: it's not easy being green. Biochem. Soc. Trans. 33, 1024-1027.
18. Finazzi, G., Chasen, C., Wollman, F.A., and de Vitry, C. (2003). Thylakoid targeting of Tat passenger proteins shows no delta pH dependence in vivo. EMBO J. 22, 807-815.
19. Fincher, V., Dabney-Smith, C., and Cline, K. (2003). Functional assembly of thylakoid deltapH-dependent/Tat protein transport pathway components in vitro. Eur. J. Biochem. 270, 4930-4941.
20. Franklin, A.E. and Hoffman, N.E. (1993). Characterization of a chloroplast homologue of the 54-kDa subunit of the signal recognition particle. J. Biol. Chem. 268, 22175-22180.
21. Funke, S., Knechten, T., Ollesch, J., and Schunemann, D. (2005). A unique sequence motif in the 54-kDa subunit of the chloroplast signal recognition particle mediates binding to the 43-kDa subunit. J. Biol. Chem. 280, 8912-8917.
22. Gerard, F. and Cline, K. (2006). Efficient twin arginine translocation (Tat) pathway transport of a precursor protein covalently anchored to its initial cpTatC binding site. J. Biol. Chem. 281, 6130-6135.
23. Gerard, F. and Cline, K. (2007). The thylakoid proton gradient promotes an advanced stage of signal peptide binding deep within the Tat pathway receptor complex. J. Biol. Chem. 282, 5263-5272.
24. Gerdes, L., Bals, T., Klostermann, E., Karl, M., Philippar, K., Hünken, M., Soll, J., and Schünemann, D. (2006). A second thylakoid membrane-localized Alb3/OxaI/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana. J. Biol. Chem. 281, 16632-16642.
25. Goforth, R.L., Peterson, E.C., Yuan, J., Moore, M.J., Kight, A.D., Lohse, M.B., Sakon, J., and Henry, R.L. (2004). Regulation of the GTPase cycle in post-translational signal recognition particle-based protein targeting involves cpSRP43. J. Biol. Chem. 279, 43077-43084.
26. Gohlke, U., Pullan, L., McDevitt, C.A., Porcelli, I., de Leeuw, E., Palmer, T., Saibil, H.R., and Berks, B.C. (2005). The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. USA 102, 10482-10486.
27. Göhre, V., Ossenbühl, F., Crevecoeur, M., Eichacker, L.A., and Rochaix, J.D. (2006). One of two Alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas. Plant Cell 18, 1454-1466.
28. Groves, M.R., Mant, A., Kuhn, A., Koch, J., Dubel, S., Robinson, C., and Sinning, I. (2001). Functional characterization of recombinant chloroplast signal recognition particle. J. Biol. Chem. 276, 27778-27786.
29. Gutensohn, M., Fan, E., Frielingsdorf, S., Hanner, P., Hou, B., Hust, B., and Klösgen, R.B. (2006). Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. J. Plant Physiol. 163, 333-347.
30. Hermkes, R., Funke, S., Richter, C., Kuhlmann, J., and Schünemann, D. (2006). The α-helix of the second chromodomain of the 43 kDa subunit of the chloroplast signal recognition particle facilitates binding to the 54 kDa subunit. FEBS Lett. 580, 3107-3111.
31. Hou, B., Frielingsdorf, S., Klösgen, R.B. (2006). Unassisted membrane insertion as the initial step in ΔpH/Tat-dependent protein transport. J. Mol. Biol. 355, 957-967.
32. Hutin, C., Havaux, M., Carde, J.P., Kloppstech, K., Meiherhoff, K., Hoffman, N., and Nussaume, L. (2002). Double mutation cpSRP43-/cpSRP54- is necessary to abolish the cpSRP pathway required for thylakoid targeting of the light-harvesting chlorophyll proteins. Plant J. 29, 531-543.
33. Hynds, P.J., Robinson, D., and Robinson, C. (1998). The sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane. J. Biol. Chem. 273, 34868-34874.
34. Jarvis, P. and Robinson, C. (2004). Mechanisms of protein import and routing in chloroplasts. Curr. Biol. 14, R1064-R1077.
35. Jonas-Straube, E., Hutin, C., Hoffman, N.E., and Schunemann, D. (2001). Functional analysis of the protein-interacting domains of chloroplast SRP43. J. Biol. Chem. 276, 24654-24660.
36. Kessler, F. and Schnell, D.J. (2006). The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic 7, 248-257.
37. Kim, S.J., Robinson, C., and Mant, A. (1998). Sec/SRP-independent insertion of two thylakoid membrane proteins bearing cleavable signal peptides. FEBS Lett. 424, 105-108.
38. Kim, S.J., Jansson, S., Hoffman, N.E., Robinson, C., and Mant, A. (1999). Distinct 'assisted' and 'spontaneous' mechanisms for the insertion of polytopic chlorophyll-binding proteins into the thylakoid membrane. J. Biol. Chem. 274, 4715-4721.
39. Klimyuk, V.I., Persello-Cartieaux, F., Havaux, M., Contard-David, P., Schuenemann, D., Meiherhoff, K., Gouet, P., Jones, J.D., Hoffman, N.E., and Nussaume, L. (1999). A chromodomain protein encoded by the Arabidopsis CAO gene is a plant-specific component of the chloroplast signal recognition particle pathway that is involved in LHCP targeting. Plant Cell 11, 87-99.
40. Klösgen, R.B., Brock, I.W., Herrmann, R.G., and Robinson, C. (1992). Proton gradient-driven import of the 16 kDa oxygen-evolving complex protein as the full precursor protein by isolated thylakoids. Plant Mol. Biol. 18, 1031-1034.
41. Klostermann, E., Droste Gen Helling, I., Carde, J.P., and Schünemann, D. (2002). The thylakoid membrane protein ALB3 associates with the cpSecY-translocase in Arabidopsis thaliana. Biochem. J. 368, 777-781.
42. Kogata, N., Nishio, K., Hirohashi, T., Kikuchi, S., and Nakai, M. (1999). Involvement of a chloroplast homologue of the signal recognition particle receptor protein, FtsY, in protein targeting to thylakoids. FEBS Lett. 447, 329-333.
43. Laidler, V., Chaddock, A.M., Knott, T.G., Walker, D., and Robinson, C. (1995). A SecY homolog in Arabidopsis thaliana. Sequence of a full-length cDNA clone and import of the precursor protein into chloroplasts. J. Biol. Chem. 270, 17664-17667.
44. Lee, P.A., Tullman-Ercek, D., and Georgiou, G. (2006). The bacterial twin-arginine translocation pathway. Annu. Rev. Microbiol. 60, 373-395.
45. Li, X., Henry, R., Yuan, J., Cline, K., and Hoffman, N.E. (1995). A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc. Natl. Acad. Sci. USA 92, 3789-3793.
46. Luirink, J., von Heijne, G., Houben, E., and de Gier, J.W. (2005). Biogenesis of inner membrane proteins in Escherichia coli. Annu. Rev. Microbiol. 59, 329-355.
47. Mant, A., Woolhead, C.A., Moore, M., Henry, R., and Robinson, C. (2001). Insertion of PsaK into the thylakoid membrane in a 'horseshoe' conformation occurs in the absence of signal recognition particle, nucleoside triphosphates, or functional albino3. J. Biol. Chem. 276, 36200-36206.
48. Marques, J.P., Schattat, M.H., Hause, G., Dudeck, I., and Klösgen, R.B. (2004). In vivo transport of folded EGFP by the DeltapH/TAT- dependent pathway in chloroplasts of Arabidopsis thaliana. J. Exp. Bot. 55, 1697-1706.
49. Michl, D., Robinson, C., Shackleton, J.B., Herrmann, R.G., and Klösgen, R.B. (1994). Targeting of proteins to the thylakoids by bipartite presequences: CFoII is imported by a novel, third pathway. EMBO J. 13, 1310-1317.
50. Mitra, K., Frank, J., and Driessen, A. (2006). Co- and post-translational translocation through the protein-conducting channel: analogous mechanisms at work? Nat. Struct. Mol. Biol. 13, 957-964.
51. 6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J. Biol. Chem. 276, 42761-42766.
52. Moore, M., Harrison, M.S., Peterson, E.C., and Henry, R. (2000). Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J. Biol. Chem. 275, 1529-1532.
53. Moore, M., Goforth, R.L., Mori, H., and Henry, R. (2003). Functional interaction of chloroplast SRP/FtsY with the ALB3 translocase in thylakoids: substrate not required. J. Cell Biol. 162, 1245-1254.
54. Mori, H. and Cline, K. (2002). A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid ΔpH/Tat translocase. J. Cell Biol. 157, 205-210.
55. Mori, H., Summer, E.J., Ma, X., and Cline, K. (1999). Component specificity for the thylakoidal Sec and ΔpH-dependent protein transport pathways. J. Cell Biol. 146, 45-56.
56. Mori, H., Summer, E.J., and Cline, K. (2001). Chloroplast TatC plays a direct role in thylakoid ΔpH-dependent protein transport. FEBS Lett. 501, 65-68.
57. Mould, R.M. and Robinson, C. (1991). A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. J. Biol. Chem. 266, 12189-12193.
58. Müller, M. and Klösgen, R.B. (2005). The Tat pathway in bacteria and chloroplasts. Mol. Membr. Biol. 22, 113-121.
59. Musser, S.M. and Theg, S.M. (2000). Characterization of the early steps of OE17 precursor transport by the thylakoid ΔpH/Tat machinery. Eur. J. Biochem. 267, 2588-2598.
60. Nakai, M., Goto, A., Nohara, T., Sugita, D., and Endo, T. (1994). Identification of the SecA protein homolog in pea chloroplasts and its possible involvement in thylakoidal protein transport. J. Biol. Chem. 269, 31338-31341.
61. Nilsson, R. and van Wijk, K.J. (2002). Transient interaction of cpSRP54 with elongating nascent chains of the chloroplast-encoded D1 protein; 'cpSRP54 caught in the act'. FEBS Lett. 524, 127-133.
62. Nilsson, R., Brunner, J., Hoffman, N.E., and van Wijk, K.J. (1999). Interactions of ribosome nascent chain complexes of the chloroplast-encoded D1 thylakoid membrane protein with cpSRP54. EMBO J. 18, 733-742.
63. Ossenbühl, F., Göhre, V., Meurer, J., Krieger-Liszkay, A., Rochaix, J.D., and Eichacker, L.A. (2004). Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. Plant Cell 16, 1790-1800.
64. Palmer, T. and Berks, B.C. (2003). Moving folded proteins across the bacterial cell membrane. Microbiology 149, 547-556.
65. Pasch, J.C., Nickelsen, J., and Schünemann, D. (2005). The yeast split-ubiquitin system to study chloroplast membrane protein interactions. Appl. Microbiol. Biotechnol. 69, 440-447.
66. Robinson, D., Karnauchov, I., Herrmann, R.G., Klösgen, R.B., and Robinson, C. (1996). Protease-sensitive thylakoidal import machinery for the Sec-, ΔpH- and signal recognition particle-dependent protein targeting pathways, but not for CFoII integration. Plant J. 10, 149-155.
67. Robson, A. and Collinson, I. (2006). The structure of the Sec complex and the problem of protein translocation. EMBO Rep. 7, 1099-1103.
68. Rohl, T. and van Wijk, K.J. (2001). In vitro reconstitution of insertion and processing of cytochrome f in a homologous chloroplast translation system. J. Biol. Chem. 276, 35465-35472.
69. Roy, L.M. and Barkan, A. (1998). A SecY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J. Cell Biol. 141, 385-395.
70. Sargent, F., Gohlke, U., De Leeuw, E., Stanley, N.R., Palmer, T., Saibil, H.R., and Berks, B.C. (2001). Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268, 3361-3367.
71. Schubert, M., Petersson, U.A., Haas, B.J., Funk, C., Schroder, W.P., and Kieselbach, T. (2002). Proteome map of the chloroplast lumen of Arabidopsis thaliana. J. Biol. Chem. 277, 8354-8365.
72. Schuenemann, D., Gupta, S., Persello-Cartieaux, F., Klimyuk, V.I., Jones, J.D.G., Nussaume, L., and Hoffman, N.E. (1998). A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc. Natl. Acad. Sci. USA 95, 10312-10316.
73. Schuenemann, D., Amin, P., Hartmann, E., and Hoffman, N.E. (1999). Chloroplast SecY is complexed to SecE and involved in the translocation of the 33-kDa but not the 23-kDa subunit of the oxygen-evolving complex. J. Biol. Chem. 274, 12177-12182.
74. Schünemann, D. (2004). Structure and function of the chloroplast signal recognition particle. Curr. Genet. 44, 295-304.
75. Sivaraja, V., Kumar, T.K., Leena, P.S., Chang, A.N., Vidya, C., Goforth, R.L., Rajalingam, D., Arvind, K., Ye, J.L., Chou, J., et al. (2005). Three-dimensional solution structures of the chromodomains of cpSRP43. J. Biol. Chem. 280, 41465-41471.
76. Soll, J. and Schleiff, E. (2004). Protein import into chloroplasts. Nat. Rev. Mol. Cell. Biol. 5, 198-208.
77. Steiner, J.M., Kocher, T., Nagy, C., and Loffelhardt, W. (2002). Chloroplast SecE: evidence for spontaneous insertion into the thylakoid membrane. Biochem. Biophys. Res. Commun. 293, 747-752.
78. Summer, E.J., Mori, H., Settles, A.M., and Cline, K. (2000). The thylakoid ΔpH-dependent pathway machinery facilitates RR-independent N-tail protein integration. J. Biol. Chem. 275, 23483-23490.
79. Sundberg, E., Slagter, J.G., Fridborg, I., Cleary, S.P., Robinson, C., and Coupland, G. (1997). ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9, 717-730.
80. Theg, S.M., Cline, K., Finazzi, G., and Wollman, F.A. (2005). The energetics of the chloroplast Tat protein transport pathway revisited. Trends Plant Sci. 10, 153-154.
81. Thompson, S.J., Kim, S.J., and Robinson, C. (1998). Sec-independent insertion of thylakoid membrane proteins. Analysis of insertion forces and identification of a loop intermediate involving the signal peptide. J. Biol. Chem. 273, 18979-18983.
82. Thompson, S.J., Robinson, C., and Mant, A. (1999). Dual signal peptides mediate the signal recognition particle/Sec-independent insertion of a thylakoid membrane polyprotein, PsbY. J. Biol. Chem. 274, 4059-4066.
83. Tu, C.J., Schuenemann, D., and Hoffman, N.E. (1999). Chloroplast FtsY, chloroplast signal recognition particle, and GTP are required to reconstitute the soluble phase of light-harvesting chlorophyll protein transport into thylakoid membranes. J. Biol. Chem. 274, 27219-27224.
84. Tu, C.J., Peterson, E.C., Henry, R., and Hoffman, N.E. (2000). The L18 domain of light-harvesting chlorophyll proteins binds to chloroplast signal recognition particle 43. J. Biol. Chem. 275, 13187-13190.
85. van der Laan, M., Nouwen, N.P., and Driessen, A.J. (2005). YidC - an evolutionary conserved device for the assembly of energy-transducing membrane protein complexes. Curr. Opin. Microbiol. 8, 182-187.
86. Woolhead, C.A., Thompson, S.J., Moore, M., Tissier, C., Mant, A., Rodger, A., Henry, R., and Robinson, C. (2001). Distinct Albino3-dependent and -independent pathways for thylakoid membrane protein insertion. J. Biol. Chem. 276, 40841-40846.
87. Yi, L. and Dalbey, R.E. (2005). Oxa1/Alb3/YidC system for insertion of membrane proteins in mitochondria, chloroplasts and bacteria. Mol. Membr. Biol. 22, 101-111.
88. Yuan, J., Henry, R., McCaffery, M., and Cline, K. (1994). SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting. Science 266, 796-798.
89. Yuan, J., Kight, A., Goforth, R.L., Moore, M., Peterson, E.C., Sakon, J., and Henry, R. (2002). ATP stimulates signal recognition particle (SRP)/FtsY-supported protein integration in chloroplasts. J. Biol. Chem. 277, 32400-32404.
90. Zhang, L.X., Paakkarinen, V., Suorsa, M., and Aro, E.M. (2001). A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis. J. Biol. Chem. 276, 37809-37814.
91. Zygadlo, A., Robinson, C., Scheller, H.V., Mant, A., and Jensen, P.E. (2006). The properties of the positively charged loop region in PSI-G are essential for its 'spontaneous' insertion into thylakoids and rapid assembly into the photosystem I complex. J. Biol. Chem. 281, 10548-10554.