Chloroplast SecA functions as a membrane-associated component of the Sec-like protein translocase of pea chloroplasts

European Journal of Biochemistry

Volumn 248, Issue 3, 1997, Pages 724-730

  Haward, Sam R ^a   Napier, Johnathan A ^b   Gray, John C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Chloroplast; Cross linking; SecA; Thylakoid membrane; Translocation

Indexed keywords

CARRIER PROTEIN;

ARTICLE; CHLOROPLAST; ENZYME ACTIVITY; PEA; PHOTOSYSTEM II; PRIORITY JOURNAL; THYLAKOID MEMBRANE;

PISUM SATIVUM;

EID: 0030817507     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00724.x     Document Type: Article

References (53)

1. Arkowitz, R. A. & Bassilana, M. (1994) Protein translocation in Escherichia coli, Biochim. Biophys. Acta 1197, 311-343.
2. Berghöfer, J., Karnauchov, I., Herrmann, R. G. & Klösgen, R. B. (1995) Isolation and characterisation of a cDNA encoding the SecA protein from spinach chloroplasts: evidence for azide resistance of Sec-dependent protein translocation across thylakoid membranes in spinach, J. Biol. Chem. 270, 18 341-18 346.
3. Cline, K., Ettinger, W. F. & 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.
4. 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.
5. Cline, K. & Henry, R. (1996) Import and routing of nucleus-encoded chloroplast proteins, Annu. Rev. Cell Dev. Biol. 12, 1-26.
6. Douglas, S. E. (1992) A secY homologue is found in the plastid genome of Cryptomonas Ø, FEBS Lett. 298, 93-96.
7. Douville, K., Price, A., Eichler, J., Economou, A. & Wickner, W. (1995) SecYEG and SecA are the stoichiometric components of preprotein translocase, J. Biol. Chem. 270, 20 106-20 111.
8. Driessen, A. J. M. (1992) Bacterial protein translocation: kinetic and thermodynamic role of ATP and the protonmotive force, Trends Biochem. Sci. 17, 219-223.
9. Economou, A. & Wickner, W. (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion, Cell 78, 835-843.
10. Economou, A., Pogliano, J. A., Beckwith, J., Oliver, D. B. & Wickner, W. (1995) SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF, Cell 83, 1171-1181.
11. Flachmann, R., Michlalowski, C. B., Löffelhardt, W. & Bohnert, H. J. (1993) SecY, an integral subunit of the bacterial preprotein translocase, is encoded by a plastid genome, J. Biol. Chem. 268, 7514-7519.
12. Hanada, M., Nishiyama, K., Mizushima, S. & Tokuda, H. (1994) Reconstitution of an efficient protein translocation machinery comprising SecA and the three membrane proteins, SecY, SecE, and SecG (p12), J. Biol. Chem. 269, 23 625-23 631.
13. Hartl, F.-U., Lecker, S., Schiebel, E., Hendrick, J. P. & Wickner, W. (1990) The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane, Cell 63, 269-279.
14. Hoffman, N. E. & 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. (Rockv.) 105, 295-304.
15. Hulford, A., Hazell, L., Mould, R. M. & Robinson, C. (1994) Two distinct mechanisms for the translocation of proteins across the thylakoid membrane, one requiring the presence of stromal factor and nucleotide triphosphates, J. Biol. Chem. 269, 3251-3256.
16. Joly, J. C. & Wickner, W. (1993) The SecA and SecY subunits of translocase are the nearest neighbours of a translocating preprotein, shielding it from phospholipids, EMBO J. 12, 255-263.
17. Kapazoglou, A. & Gray, J. C. (1995) Characterization of a cDNA for pea chloroplast SecA, in Photosynthesis: from light to biosphere (Mathis, P., ed.) vol. III, pp. 751-754. Kluwer Academic Publishers, Dordrecht.
18. Kapazoglou, A., Sagliocco, F. & Dure III, L. (1995) PSII-T, a new nuclear encoded lumenal protein from photosystem II, J. Biol. Chem. 270, 12 197- 12 202.
19. Karnauchov, I., Cai, D., Schmidt, I., Herrmann, R. G. & Klösgen, R. B. (1994) The thylakoid translocation of subunit 3 of photosystem I, the psaF gene product, depends on a bipartite transit peptide and proceeds along an azide-sensitive pathway, J. Biol. Chem. 269, 32871-32878.
20. Kirwin, P. M., Meadows, J. W., Shackleton, J. B., Musgrove, J. E., Elderfield, P. D., Mould, R. M., Hay, N. A. & Robinson, C. (1989) ATP-dependent import of a lumenal protein by isolated thylakoid vesicles, EMBO J. 8, 2251-2255.
21. Klösgen, R. B., Brock, I. W., Herrmann, R. G. & 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.
22. Knott, T. G. & Robinson, C. (1994) The secA inhibitor, azide, reversibly blocks the translocation of a subset of proteins across the chloroplast thylakoid membrane. J. Biol. Chem. 269, 7843-7846.
23. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4, Nature 227, 680-685.
24. Laidler, V., Chaddock, A. M., Knott, T. G., Walker, D. & Robinson, C. (1995) A SecY homologue in Arabidopsis thaliana. Sequence of a full-length cDN A clone and import of the precursor protein into chloroplasts, J. Biol. Chem. 270, 17 664-17 667.
25. Li, X., Henry, R., Yuan, J., Cline, K. & Holfman, 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.
26. Lill, R., Cunningham, K., Brundage, L. A., Ito, K., Oliver, D. & Wickner, W. (1989) SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli, EMBO J. 8, 961-966.
27. Lill, R., Dowhan, W. & Wickner, W. (1990) The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins, Cell 60, 271-280.
28. Mant, A., Nielsen, V. S., Knott, T. G., Møller, B. L. & Robinson, C. (1994) Multiple mechanisms for the targeting of photosystem I subunits F, H, K, L, and N into and across the thylakoid membrane, J. Biol. Chem. 269, 27 303-27 309.
29. Mant, A., Schmidt, I., Herrmann, R. G., Robinson, C. & Klösgen, R. B. (1995) Sec-dependent thylakoid protein translocation: ΔpH requirement is dictated by passenger protein and ATP concentration, J. Biol. Chem. 270, 23 275-23 281.
30. Michl, D., Robinson, C., Shackleton, J. B., Herrmann, R. G. & Klösgen, R. B. (1994) Targeting of proteins by bipartite presequences: CFoll is imported by a novel, third pathway, EMBO J. 13, 1310-1317.
31. Mould, R. M. & 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, 12 189-12 193.
32. Mould, R. M., Shackleton, J. B. & Robinson, C. (1991) Transport of proteins into chloroplasts: requirements for the efficient import of two lumenal oxygen-evolving complex proteins into isolated thylakoids, J. Biol. Chem. 266, 17 286-17 289.
33. Mould, R. M., Knight, J. S., Bogsch, E. & Gray, J. C. (1997) Azide-sensitive thylakoid membrane insertion of chimeric cytochrome ∫ polypeptides imported by isolated pea chloroplasts, Plant J. 11, 1051-1058.
34. Nakai, M., Goto, A., Nohara, T., Sugita, D. & Endo, T. (1994) Identification of the SecA protein homolog in pea chloroplasts and its possible involvement in thylakoidal protein transport, J. Biol. Chem. 269, 31 338-31 341.
35. Nielsen, V. S., Mant, A., Knoetzel, J., Møller, B. L. & Robinson, C. (1994) Import of barley photosystem I subunit N into the thylakoid lumen is mediated by a bipartite presequence lacking an intermediate processing site: role of the delta pH in translocation across the thylakoid membrane, J. Biol. Chem. 269, 3762-3766.
36. Nohara, T., Nakai, M., Goto, A. & Endo, T. (1995) Isolation and characterization of the cDNA for pea chloroplast SecA. Evolutionary conservation of the bacterial-type SecA-dependent protein transport within chloroplasts, FEBS Lett. 364, 305-308.
37. Nohara, T., Asai, T., Nakai, M., Sugiura, M. & Endo, T. (1996) Cytochrome ∫ encoded by the chloroplast genome is imported into thylakoids via the SecA-dependent pathway. Biochem. Biophys. Res. Commun. 224, 474-478.
38. Oliver, D. B., Cabelli, R. J., Dolan, K. M. & 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.
39. Oliver, D. B. (1993) SecA protein: autoregulated ATPase catalysing preprotein insertion and translocation across the Escherichia coli inner membrane, Mol. Microbiol. 7, 159-165.
40. Partis, M. D., Griffiths, D. G., Roberts, G. C. & Beechey, R. B. (1983) Cross-linking of protein by ω-malcimido alkanoyl N-hydroxysuccinimido esters, J. Protein Chem. 2, 263-277.
41. Payan, L. A. & Cline, K. (1991) A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane protein, J. Cell Biol. 112, 603-613.
42. Rajapandi, T. & Oliver, D. (1996) Integration of SecA protein into the Escherichia coli inner membrane is regulated by its amino-terminal ATP-binding domain. Mol. Microbiol. 20, 43-51.
43. Rothstein, S. J., Gatenby, A. A., Willey, D. L. & Gray, J. C. (1985) Binding of pea cytochrome ∫ to the inner membrane of Escherichia coli requires the bacterial SecA gene product. Proc. Natl Acad. Sci. USA 82, 7455-7459.
44. Scaramuzzi, C. D., Hiller, R. G. & Stokes, H. W. (1992a) Identification of a chloroplast-encoded secA gene homologue in a chromophytic alga: possible role in chloroplast protein translocation, Curr. Genet. 22, 421-427.
45. Scaramuzzi, C. D., Stokes, M. W. & Hiller, R. G. (1992b) Characterisation of a chloroplast-encoded secY homologue and atpH from a chromophytic alga, FEBS Lett. 304, 119-123.
46. H and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64, 927-439.
47. Söllner, T., Rassow, J., Wiedmann, M., Schlossmann, J., Keil, P., Neupert, W. & Pfanner, N. (1992) Mapping of the protein mport machinery in the mitochondrial outer membrane by cross-linking of translocation intermediates. Nature 355, 84-87.
48. Swidersky, U. E., Hoffschulte, H. K. & Müller, M. (1990) Determinants of membrane-targeting and transmembrane translocation during bacterial protein export, EMBO J. 9, 1777-1785.
49. Valentin, K. (1993) SecA is plastid-encoded in a red alga: implications for the evolution of plastid genomes and the thylakoid protein import apparatus, Mol. Gen. Genet. 236, 245-250.
50. Voelker, R., Mendel-Hartvig, J. & Barkan, A. (1997) Transposon-disruption of a maize nuclear gene, thal, encoding a chloroplast SecA homologue: in vivo role of chloroplast SecA in thylakoid protein targeting. Genetics 145, 467-478.
51. Wickner, W. & Leonard, M. R. (1996) Escherichia coli preprotein translocase, J. Biol. Chem. 271, 29514- 29516.
52. Yuan, J. & 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, 18 463-18 467.
53. Yuan, J., Henry, R., McCaffery, M. & Cline, K. (1994) SecA hemolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting, Science 266, 796-798.