Localization and integration of thylakoid protein translocase subunit cpTatC

Plant Journal

Volumn 58, Issue 5, 2009, Pages 831-842

  Martin, Jonathan R ^a   Harwood, Jessica H ^b,c   McCaffery, Michael ^a   Fernandez, Donna E ^b   Cline, Kenneth ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c Social Science Division   (United States)

Author keywords

Membrane protein integration; Protein translocation; SecY2; TatC; Thylakoid biogenesis; Twin arginine

Indexed keywords

ARABIDOPSIS PROTEIN; MEMBRANE PROTEIN; SECA PROTEIN, PLANT; SECY PROTEIN, ARABIDOPSIS; TATC PROTEIN, PLANT; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN TRANSPORT; THYLAKOID;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; MEMBRANE PROTEINS; PLANT PROTEINS; PROTEIN TRANSPORT; THYLAKOIDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 66249084873     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03816.x     Document Type: Article

References (50)

1. Anderson, S. Smith, S.M. (1986) Synthesis of the small subunit of ribulose-bisphosphate carboxylase from genes cloned into plasmids containing the SP6 promoter. Biochem. J. 240, 709 715.
2. Andersson, H. Heijne, G.v. (1993) Sec dependent and sec independent assembly of E. coli inner membrane proteins: the topological rules depend on chain length. EMBO J. 12, 683 691.
3. Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiol. 24, 1 15.
4. Asakura, Y., Hirohashi, T., Kikuchi, S., Belcher, S., Osborne, E., Yano, S., Terashima, I., Barkan, A. Nakai, M. (2004) Maize mutants lacking chloroplast FtsY exhibit Pleiotropic defects in the biogenesis of thylakoid membranes. Plant Cell, 16, 201 214.
5. Asakura, Y., Kikuchi, S. Nakai, M. (2008) Non-identical contributions of two membrane-bound cpSRP components, cpFtsY and Alb3, to thylakoid biogenesis. Plant J. 56, 1007 1017.
6. Benning, C., Xu, C. Awai, K. (2006) Non-vesicular and vesicular lipid trafficking involving plastids. Curr. Opin. Plant Biol. 9, 241 247.
7. Bloois, E.v., Haan, G.J., Gier, J.-W.d., Oudega, B. Luirink, J. (2004) F1F0 ATP synthase subunit c is targeted by the SRP to YidC in the E. coli inner membrane. FEBS Lett. 576, 97 100.
8. Brink, S., Fischer, K., Klosgen, R.-B. Flugge, U.-I. (1995) Sorting of nuclear-encoded chloroplast membrane proteins to the envelope and the thylakoid membrane. J. Biol. Chem. 270, 20808 20815.
9. Bruce, B.D. (2001) The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochemica et Biophysica Acta - Molecular Cell Research, 1541, 2 21.
10. Buchanan, G., Leeuw, E.d., Stanley, N.R., Wexler, M., Berks, B.C., Sargent, F. Palmer, T. (2002) Functional complexity of the twin-arginine translocase TatC component revealed by site-directed mutagenesis. Mol. Microbiol. 43, 1457 1470.
11. Carde, J.-P., Joyard, J. Douce, R. (1982) Electron microscopic studies of envelope membranes from Spinach plastids. Biol. Cell, 44, 315 324.
12. Cavalier-Smith, T. (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5, 174 182.
13. Cline, K. (1986) Import of proteins into chloroplasts: membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J. Biol. Chem. 261, 14804 14810.
14. Cline, K. Mori, H. (2001) Thylakoid δpH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 154, 719 730.
15. Cline, K. Theg, S.M. (2007) The Sec and Tat protein translocation pathways in chloroplasts. In The Enzymes, Vol. 25 (Dalbey, R., Koehler, C. Tamanoi, F., eds). London : Elsevier, pp. 1 25.
16. Cline, K., Henry, R., Li, C.-J. Yuan, J. (1992) Pathways and intermediates for the biogenesis of nuclear encoded thylakoid proteins. Res. Photosyn. III, 149 156.
17. Cline, K., Henry, R., Li, C. Yuan, J. (1993) Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J. 12, 4105 4114.
18. Cran, D. Possingham, J. (1972) Two forms of division profile in spinach chloroplasts. Nature New Biol. 235, 142.
19. Dalbey, R.E. Kuhn, A. (2000) Evolutionarily related insertion pathways of bacterial, mitochondrial, and thylakoid membrane proteins. Annu. Rev. Cell Dev. Biol., 16, 51 87.
20. Fandl, J.P., Cabelli, R., Oliver, D. Tai, P.C. (1988) SecA suppresses the temperature-sensitive SecY24 defect in protein translocation in Escherichia coli membrane vesicles. PNAS, 85, 8953 8957.
21. Fincher, V., Dabney-Smith, C. Cline, K. (2003) Functional assembly of thylakoid deltapH-dependent/Tat protein transport pathway components in vitro. Eur. J. Biochem. 270, 4930 4941.
22. Gerard, F. 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.
23. Gerdes, L., Bals, T., Klostermann, E., Karl, M., Philippar, K., Hünken, M., Soll, J. Schünemann, D. (2006) A second thylakoid membrane-associated Alb3/OxaI/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana. J. Biol. Chem. 281, 16632 16642.
24. Hutin, C., Havaux, M., Carde, J.-P., Kloppstech, K., Meiherhoff, K., Hoffman, N. 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.
25. 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 J. 34, 661 669.
26. Jackson, D.T., Froehlich, J.E. Keegstra, K. (1998) The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. J. Biol. Chem. 273, 16583 16588.
27. Knight, J.S. Gray, J.C. (1995) The N-terminal hydrophobic region of the mature phosphate translocator is sufficient for targeting to the chloroplast inner envelope membrane. The Plant Cell, 7, 1421 1432.
28. Kobayashi, K., Kondo, M., Fukuda, H., Nishimura, M. Ohta, H. (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. PNAS, 104, 17216 17221.
29. Koch, H.-G., Moser, M., Schimz, K.-L. Mueller, M. (2002) The integration of YidC into the cytoplasmic membrane of Escherichia coli requires the signal recognition particle, SecA and SecYEG. J. Biol. Chem., 277, 5715 5718.
30. Li, M. Schnell, D.J. (2006) Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. J. Cell Biol., 175, 249 259.
31. Moore, M., Harrison, M.S., Peterson, E.C. 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.
32. Mori, H., Summer, E.J. Cline, K. (2001) Chloroplast TatC plays a direct role in thylakoid δpH-dependent protein transport. FEBS Lett., 501, 65 68.
33. Nilsson, R. van Wijk, K.J.v. (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.
34. Reed, J.E., Cline, K., Stephens, L.C., Bacot, K.O. Viitanen, P.V. (1990) Early events in the import/assembly pathway of an integral thylakoid protein. Eur. J. Biochem., 194, 33 42.
35. Rhee, S.Y., Beavis, W., Berardini, T.Z. et al. (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res. 31, 224 228.
36. Richter, S. Lamppa, G.K. (1999) Stromal processing peptidase binds transit peptides and initiates their ATP-dependent turnover in chloroplasts. J. Cell Biol., 147, 33 44.
37. Schaller, G.E., Ladd, A.N., Lanahan, M.B., Spanbauer, J.M. Bleeker, A.B. (1995) The ethylene response mediator ETR1 from Arabidopsis form a disulfide-linked dimer. J. Biol. Chem. 270, 12526 12530.
38. Schuenemann, D. (2007) Mechanisms of protein import into thylakoids of chloroplasts. Biol. Chem. 388, 907 915.
39. Schuenemann, D., Amin, P., Hartmann, E. 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.
40. Scotti, P.A., Valent, Q.A., Manting, E.H., Urbanus, M.L., Driessen, A.J.M., Oudega, B. Luirink, J. (1999) SecA Is not required for signal recognition particle-mediated targeting and initial membrane insertion of a nascent inner membrane protein. J. Biol. Chem. 274, 29883 29888.
41. Siboo, I.R., Chaffin, D.O., Rubens, C.E. Sullam, P.M. (2008) Characterization of the accessory sec system of Staphylococcus aureus. J. Bacteriol. 190, 6188 6196.
42. Sirrenberg, C., Bauer, M.F., Guiard, B., Neupert, W. Brunner, M. (1996) Import of carrier proteins into the mitochondrial inner membrane mediated by Tim22. Nature, 384, 582 585.
43. Skalitzky, C.A. (2006) Genetic Analysis of SCY1 and SCY2 Function in Arabidopsis Thaliana, Master of Science. Botany, Madison : University of Wisconsin, 62.
44. Smith, M.D., Fitzpatrick, L., Keegstra, K. Schnell, D.J. (2003) In Vitro analysis of chloroplast protein import. In Current Protocols in Cell Biology (Bonifacino, J.S., Dasso, M., Harford, J.B., Lippincott-Schwartz, J. Yamada, K., eds). Hoboken : John Wiley and Sons, Inc., pp. 16.11 16.21.
45. Steiner, J.M., Kocher, T., Nagy, C. Loffelhardt, W. (2002) Chloroplast SecE: evidence for spontaneous insertion into the thylakoid membrane. Biochem. Biophys. Res. Commun. 293, 747 752.
46. Sundberg, E., Slagter, J., Fridborg, I., Cleary, S., Robinson, C. 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.
47. Valent, Q.A., Scotti, P.A., High, S., Gier, J.-W.L.d., Heijne, G.v., Lentzen, G., Wintermeyer, W., Oudega, B. Luirink, J. (1998) The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J. 17, 2504 2512.
48. Voelker, R., Mendel-Hartvig, J. Barkan, A. (1997) Transposon-disruption of a maize nuclear Gene, tha1, encoding a chloroplast SecA homologue: In Vivo role of cp-SecA in Thylakoid protein targeting. Genetics, 145, 467 478.
49. Yi, L., Jiang, F., Chen, M., Cain, B., Bolhuis, A. Dalbey, R.E. (2003) YidC Is strictly required for membrane insertion of subunits a and c of the F1F0ATP synthase and SecE of the SecYEG translocase. Biochemistry, 42, 10537 10544.
50. Zhang, L., Paakkarinen, V., Suorsa, M. Aro, E.-M. (2001) A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis. J. Biol. Chem. 276, 37809 37814.