Azide-sensitive thylakoid membrane insertion of chimeric cytochrome f polypeptides imported by isolated pea chloroplasts

Plant Journal

Volumn 11, Issue 5, 1997, Pages 1051-1058

  Mould, Ruth M ^a   Knight, Jacqueline S ^a,b   Bogsch, Erik ^a,c   Gray, John C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AZIDE; CYTOCHROME; CYTOCHROME F; HYBRID PROTEIN; IONOPHORE; PROTEIN PRECURSOR; RIBULOSEBISPHOSPHATE CARBOXYLASE;

ARTICLE; CELL COMPARTMENTALIZATION; CHLOROPLAST; DRUG EFFECT; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; PEA; PHOTOSYNTHESIS; TRANSPORT AT THE CELLULAR LEVEL;

AZIDES; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CHLOROPLASTS; CYTOCHROMES; CYTOCHROMES F; INTRACELLULAR MEMBRANES; IONOPHORES; PEAS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN PRECURSORS; RECOMBINANT FUSION PROTEINS; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 0031149916     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1997.11051051.x     Document Type: Article

References (40)

1. Andersen, S. and 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. Anderson, C.M. and Gray, J.C. (1991) Cleavage of the precursor of pea chloroplast cytochrome f by leader peptidase from Escherichia coli. FEBS Lett. 280, 383-386.
3. Bartlett S., Grossman, A.R. and Chua, N.-H. (1982) In vitro synthesis and uptake of cytoplasmically-synthesized chloroplast proteins. In Methods in Chloroplast Molecular Biology (Edelman, M., Hallick, R. B., and Chua, N.-H., eds). Elsevier Biomedical Press: Amsterdam, pp. 1081-1091.
4. Betts, S.D., Hachigian, T.M., Pichersky, E. and Yocum, C.F. (1994) Reconstitution of the spinach oxygen-evolving complex with recombinant Arabidopsis manganese-stabilizing protein. Plant Mol. Biol. 26, 117-130.
5. Cline, K., Fulsom, D.R. and Viitanen, P.V. (1989) An imported thylakoid protein accumulates in the stroma when insertion into thylakoids is inhibited. J. Biol. Chem. 264, 14 225-14 232.
6. 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.
7. Cline, K., Henry, R., Li, C. and Yuan, J. (1993) Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J. 12, 4105-4114.
8. Cline, K. and Henry, R. (1996) Import and routing of nucleus encoded chloroplast proteins. Ann. Rev. Cell. Biol. Dev. Biol. 12, 1-26.
9. Franklin, A.E. and Hoffman, N.E. (1993) Characterization of a chloroplast homolog of the 54-kDa subunit of the signal recognition particle. J. Biol. Chem. 268, 22 175-22 180.
10. Friemann, A. and Hachtel, W. (1988) Chloroplast messenger RNAs of free and thylakoid-bound polysomes from Vicia faba L. Planta, 175, 50-59.
11. Gray, J.C., Phillips, A.L. and Smith, A.G. (1984) Protein synthesis by chloroplasts. In Chloroplast Biogenesis (Ellis, R.J., ed.). Cambridge: Cambridge University Press, pp 137-163.
12. Gray, J.C. (1992) Cytochrome f. structure, function and biosynthesis. Photosynth. Res. 34, 359-374.
13. Gray, J.C., Rochford, R.J. and Packman, L.C. (1994) Proteolytic removal of the C-terminal transmembrane region of cytochrome f during extraction from turnip and charlock leaves generates a water-soluble monomeric form of the protein. Eur. J. Biochem. 223, 481-488.
14. Hoffman, N.E. and Franklin, A.E. (1994) Evidence for a stromal GTP requirement for the integration of a chlorophyll a/b-binding polypeptide into thylakoid membranes. Plant Physiol. 105, 295-304.
15. Johnson, E.M., Schnabelrauch, L.S. and Sears, B.B. (1991) A plastome mutation affects processing of both chloroplast and nuclear DNA-encoded plastid proteins. Mol. Gen. Genet 225, 106-112.
16. Kuras, R., Wollman, F.-A. and Joliot, P. (1995a) Conversion of cytochrome f to a soluble form in vivo in Chlamydomonas reinhardtii. Biochemistry, 34, 7468-7475.
17. Kuras, R., Büschlen, S. and Wollman, F.-A. (1995b) Maturation of pre-apocytochrome f in vivo. A site-directed mutagenesis study in Chlamydomonas reinhardtii. J. Biol. Chem. 270, 27 797-27 803.
18. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685
19. Li, X., Henry, R., Yuan, J., Cline, K. and Hoffman, N. (1995) A chloroplast homolog 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.
20. Lorkovic, Z.J., Schröder, W.P., Pakrasi, H.B., Irrgang, K.-D., Herrmann, R.G. and Oelmüller, R. (1995) Molecular characterization of PsbW, a nuclear-encoded component of the photosystem II reaction center complex in spinach. Proc. Natl Acad. Sci. USA, 92, 8930-8934.
21. Maduen̈o, F., Napier, J.A. and Gray, J.C. (1993) Newly imported Rieske iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell, 5, 1865-1876.
22. Michl, D., Robinson, C., Shackleton, J.B., Herrmann, R.G. and Klösgen, R.B. (1994) Targeting of proteins to the thylakoids by bipartite presequences: CFoll is imported by a novel, third pathway. EMBO J. 13, 1310-1317.
23. 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. 266, 31338-31341.
24. + reductase. Plant Mol. Biol. 10, 511-520.
25. Nohara, T., Asai, T., Nakai, M., Sugiura, M. and Endo, T. (1996) Cytochrome f encoded by the chloroplast genome is imported into thylakoids via the SecA-dependent pathway. Biochem. Biophys. Res. Commun. 224, 474-478.
26. Oliver, D.B., Cabelli, R.J., Dolan, K.M. and Jarosik, G.P. (1990) Azide resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl Acad. Sci. USA, 87, 8227-8231.
27. Paulsen, H., Rümler, U. and Rüdiger, W. (1990) Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed in Escherichia coli. Planta, 181, 204-211.
28. Rothstein, S.J., Gatenby, A.A., Willey, D.L. and Gray, J.C. (1985) Binding of pea cytochrome f to the inner membrane of Escherichia coli requires the bacterial secA gene-product. Proc. Natl Acad. Sci. USA, 82, 7955-7959.
29. Saiki, R.K., Schart, S., Faloona, F., Mullis, K.B., Horn, G.T., Erlich, H.A. and Arnheim, N. (1985) Enzymatic amplification of betaglobin genomic sequences and restriction site analysis for diagnosis of sickle-cell anemia. Science, 230, 1350-1352.
30. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
31. Schatz, G. and Dobberstein, B. (1996) Common principles of protein translocation across membranes. Science, 271, 1519-1526.
32. Smeekens, S., Bauerle, C, Hageman, J., Keegstra, K. and Weisbeek, P. (1986) The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell, 46, 365-375.
33. Smith, T.A. and Kohorn, B.D. (1994) Mutations in a signal sequence for the thylakoid membrane identify multiple protein transport pathways and nuclear suppressors. J. Cell Biol. 126, 365-374.
34. Voelker, R. and Barkan, A. (1995) Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J. 16, 3905-3914.
35. Willey, D.L., Auffret, A.D. and Gray, J.C. (1984a) Structure and topology of cytochrome f in pea chloroplast membranes. Cell, 36, 555-562.
36. Willey, D.L., Howe, C.J., Auffret, A.D., Bowman, C.M., Dyer, T.A. and Gray, J.C. (1984b) Location and nucleotide sequence of the gene for cytochrome f in wheat chloroplast DNA. Mol. Gen. Genet. 194, 416-422.
37. Wu, N.-H., Côté, J.C. and Wu, R. (1986) Nucleotide sequence of the rice cytochrome f gene and the presence of sequence variation near this gene. Gene, 50, 271-278.
38. Yuan, J., Henry, R. and Cline, K. (1993) Stromal factor plays an essential role in protein integration into thylakoids that cannot be replaced by unfolding or by heat-shock protein Hsp70. Proc. Natl Acad. Sci. USA, 90, 8552-8556.
39. Yuan, J. and Cline, K. (1994) Plastocyanin and the 33-kDa subunit of the oxygen-evolving complex are transported into thylakoids with similar requirements as predicted from pathway specificity. J. Biol. Chem. 269, 18463-18467.
40. 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.