Phylogenetic transfer of organelle genes to the nucleus can lead to new mechanisms of protein integration into membranes

Plant Journal

Volumn 17, Issue 1, 1999, Pages 31-40

  Michl, Doris ^a   Karnauchov, Ivan ^a   Berghöfer, Jürgen ^a   Herrmann, Reinhold G ^a   Klösgen, Ralf Bernd ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS; CHLOROPLAST; CHROMOSOME; GENE TRANSFER; MEMBRANE PROTEIN; MEMBRANE STRUCTURE; MEMBRANE; PLASTID; PROTEIN; THYLAKOID;

ALGORITHMS; AMINO ACID SEQUENCE; CELL NUCLEUS; CHLOROPLASTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; INTRACELLULAR MEMBRANES; MACROMOLECULAR SUBSTANCES; MOLECULAR SEQUENCE DATA; ORGANELLES; PHYLOGENY; PLANT LEAVES; PROTON-TRANSLOCATING ATPASES; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SPINACIA OLERACEA;

EMBRYOPHYTA;

EID: 0033062001     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1999.00348.x     Document Type: Article

References (55)

1. Andersson, H. and von Heijne, G. (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.
2. Bartling, D., Clausmeyer, S., Oelmüller, R. and Herrmann, R.G. (1990) Towards epitope models for chloroplast transit sequences. Bot. Mag. Tokyo, (Special Issue) 2, 119-144.
3. Berzborn, R.J., Klein-Hitpaß, L., Otto, J., Schünemann, S. and Oworah-Nkruma, R. (1990) The 'additional subunit' CFoll of the photosynthetic ATP-synthase and the thylakoid polypeptide, binding ferredoxin NADP reductase: are they different? Zeitschr. Naturforsch. 45c, 772-784.
4. Bird, C.R., Koller, B., Auffret, A.D., Huttly, A.K., Howe, C.J., Dyer, T.A. and Gray, J.C. (1985) The wheat chloroplast gene for CFo subunit I of ATP synthase contains a large intron. EMBO J. 4, 1381-1388.
5. Bogsch, E., Brink, S. and Robinson, C. (1997) Pathway-specificity for a delta pH-dependent precursor thylakoidlumen protein is governed by a 'Sec-avoidance' motif in the transfer peptide and a 'Sec-incompatible' mature protein. EMBO J. 16, 3851-3859.
6. Cai, D., Herrmann, R.G. and Klösgen, R.B. (1993) The 20 kD apoprotein of the CP24 complex of photosystem II: an alternative model to study import and intraorganellar routing of nuclear-encoded thylakoid proteins. Plant J. 3, 383-392.
7. Cao, G., Cheng, S., Whitley, P., von Heijne, G., Kuhn, A. and Dalbey, R.E. (1994) Synergistic insertion of two hydrophobic regions drives Sec-independent membrane protein assembly. J. Biol. Chem. 269, 26898-26903.
8. Cao, G., Kuhn, A. and Dalbey, R.E. (1995) The translocation of negatively charged residues across the membrane is driven by the electrochemical potential: evidence for an electrophoresis-like membrane transfer mechanism. EMBO J. 14, 866-875.
9. 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 ΔpH-dependent thylakoidal protein translocase. EMBO J. 14, 2715-2722.
10. Chamberlain, J.P. (1979) Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor sodium salicylate. Anal. Biochem. 98, 132-135.
11. Clausmeyer, S., Klösgen, R.B. and Herrmann, R.G. (1993) Protein import into chloroplasts: the hydrophilic lumenal proteins exhibit unexpected import and sorting specificties in spite of structurally conserved transit peptides. J. Biol. Chem. 268, 13869-13876.
12. Cozens, A.L. and Walker, J.E. (1987) The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301. J. Mol. Biol. 194, 359-383.
13. Date, T., Goodman, J.M. and Wickner, W.T. (1980) Procoat, the precursor of M13 coat protein, requires an electrochemical potential for membrane insertion. Proc. Natl. Acad. Sci. USA, 77, 4669-4673.
14. von Heijne, G., Steppuhn, J. and Herrmann, R.G. (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biochem. 180, 535-545.
15. Hennig, J. and Herrmann, R.G. (1986) Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol. Gen. Genet. 203, 117-128.
16. Herrmann, R.G. (1997) Eukaryotism, towards a new interpretation. In Eukaryotism and Symbiosis (Schenk, H.E.A., Herrmann, R.G. Jeon, K.W. Müller, N.E. and Schwemmler, W., eds). Berln: Springer-Verlag, pp. 73-118.
17. Herrmann, R.G., Steppuhn, J., Herrmann, G.S. and Nelson, N. (1993) The nuclear-encoded polypeptide CFo-II from spinach is a real, ninth subunit of chloroplast ATP synthase. FEBS Lett. 326, 192-198.
18. +-ATP synthase complex and the ribosomal protein S2. J. Mol. Biol. 196, 283-298.
19. Hulford, A., Hazell, L., Mould, R.M. and Robinson, C. (1994) Two distinct mechanisms for the translocation of proteins across the thylakoid membrane, one requiring the presence of a stromal protein factor and nucleotide triphosphates. J. Biol. Chem. 269, 3251-3256.
20. Karnauchov, I., Herrmann, R.G., Pakrasi, H. and Klösgen, R.B. (1997) Transport of CtpA protein from the cyanobacterium Synechocystis 6803 across the thylakoid membrane in chloroplasts. Eur. J. Biochem. 249, 497-504.
21. 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.
22. Kim, S.J., Robinson, D. and Robinson, C. (1996) An Arabidopsis thaliana cDNA encoding PSII-X, a 4.1 kDa component of photosystem II: a bipartite presequence mediates SecA/ΔpH-independent targeting into thylakoids. FEBS Lett. 390, 175-178.
23. Kirwin, P.M., Elderfield, P.D., Williams, R.S. and Robinson, C. (1988) Transport of proteins into chloroplasts: organization, orientation and lateral distribution of the plastocyanin processing peptidase in the thylakoid network. J. Biol. Chem. 263, 18128-18132.
24. Klösgen, R.B. (1997) Protein transport into and across the thylakoid membrane. J. Photochem. Photobiol. B: Biology, 38, 1-9.
25. Knott, T. and 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.
26. Kowallik, K.V. (1997) Origin and evolution of chloroplasts: current status and future perspectives. In Eukaryotism and Symbiosis (Schenk, H.E.A., Herrmann, R.G., Jeon, K.W., Müller, N.E. and Schwemmler, W., eds). Berlin: Springer-Verlag, pp. 3-23.
27. Kuhn, A. (1988) Alterations in the extracellular matrix domain of M13 procoat protein makes its membrane insertion dependent on secA and secY. Eur. J. Biochem. 177, 267-271.
28. Kuhn, A., Kreil, G. and Wickner, W. (1987) Recombinant forms of M13 procoat with an OmpA leader sequence or a large carboxyterminal extension retain their independence of secY function. EMBO J. 6, 501-505.
29. Kuhn, A., Wickner, W. and Kreil, G. (1986) The cytoplasmic carboxy terminus of M13 procoat is required for the membrane insertion of its central domain. Nature, 322, 335-339.
30. Kyte, J. and Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
31. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
32. 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.
33. Lill, H. and Nelson, N. (1991) The atp1 and atp2 operons of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol. Biol. 17, 641-652.
34. Lipman, D.J. and Pearson, W.R. (1985) Rapid and sensitive protein similarity searches. Science, 227, 1435-1441.
35. 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. Proceedings Natl Acad. Sci. USA, 92, 8930-8934.
36. Mant, A., Schmidt, I., Herrmann, R.G., Robinson, C. and Klösgen, R.B. (1995) Sec-dependent thylakoid protein translocation: ΔpH-requirement is dictated by passenger protein and ATP concentration. J. Biol. Chem. 270, 23275-23281.
37. Martin, W. and Müller, M. (1998) The hydrogen hypothesis for the first eukaryote. Nature, 392, 37-41.
38. Martin, W. and Schnarrenberger, C. (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32, 1-18.
39. 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.
40. Mould, R.M., Knight, J.S., Bogsch, E. and Gray, J.C. (1997) Azide-sensitive thylakoid membrane insertion of chimeric cytochrome f polypeptides imported into isolated pea chloroplasts. Plant J. 11, 1051-1058.
41. 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.
42. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57, 50-108.
43. 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 CFo-II integration. Plant J. 10, 149-155.
44. Rohrer, J. and Kuhn, A. (1990) The function of a leader peptide in translocating charged amino acyl residues across a membrane. Science, 250, 1418-1421.
45. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
46. Sanger, F., Nicklen, S. and Coulsen, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
47. Schägger, H. and von Jagow, G. (1987) Tricine-sodium dodecylsulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379.
48. Schmidt G., Rodgers, A.J.W., Howitt, S.M., Munn, A.L., Hudson, G.S., Holten, T.A., Whitfeld, P.R., Bottomley, W., Gibson, F. and Cox, G.B. (1990) The chloroplast CFol subunit can replace the b-subunit of the FoF1-ATPase in a mutant strain of Escherichia coli K12. Biochim. Biophys. Acta, 1015, 195-199.
49. 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.
50. Van den Broeck, G., Timko, M.P., Kausch, A.P., Cashmore, A.R., van Montagu, M. and Herrera-Estrella, L. (1985) Targeting of a foreign protein to chloroplasts by fusion to the transit peptide from the small subunit of ribulose-1,5-bisphosphate carboxylase. Nature, 313, 358-363.
51. Walker, J.E., Saraste, M. and Gay, N.J. (1984) The unc operon: nucleotide sequence, regulation and structure of ATP-synthase. Biochim. Biophys. Acta, 768, 164-200.
52. Westhoff, P., Alt, J., Nelson, N. and Herrmann, R.G. (1985) Genes and transcripts for the ATP synthase CFo subunits I and II from spinach thylakoid membranes. Mol. Gen. Genet. 199, 290-299.
53. 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.
54. 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.
55. Zak, E., Sokolenko, A., Unterholzner, G., Altschmied, L. and Herrmann, R.G. (1997) On the mode of integration of plastid-encoded components of the cytochrome bf complex into thylakoid membranes. Planta, 201, 334-341.