FtsH2 and FtsH5: Two homologous subunits use different integration mechanisms leading to the same thylakoid multimeric complex

Plant Journal

Volumn 65, Issue 4, 2011, Pages 600-609

  Rodrigues, Ricardo A O ^a   Silva Filho, Marcio C ^a   Cline, Kenneth ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

chloroplast; protease; protein transport; SecY; Tat; twin arginine

Indexed keywords

CHLOROPLAST; PROTEASE; PROTEIN TRANSPORT; SECY; TAT; TWIN ARGININE;

AMINO ACIDS; ARGININE; CHLOROPHYLL; MACHINERY; PEPTIDES;

INTEGRATION;

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; ARABIDOPSIS PROTEIN; FTSH5 PROTEIN, ARABIDOPSIS; MEMBRANE PROTEIN; METALLOPROTEINASE; VAR2 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TRANSPORT; THYLAKOID;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-DEPENDENT PROTEASES; MEMBRANE PROTEINS; METALLOPROTEASES; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; THYLAKOIDS;

ARABIDOPSIS;

EID: 79551639846     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04448.x     Document Type: Article

References (30)

1. Adam, Z., Rudella, A., and, van Wijk, K.J., (2006) Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr. Opin. Plant Biol. 9, 234-240.
2. Arnon, D.I., (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol., 24, 1-15.
3. 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.
4. 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.
5. Cline, K., and, Dabney-Smith, C., (2008) Plastid protein import and sorting: different paths to the same compartments. Curr. Opin. Plant Biol. 11, 585-592.
6. Cline, K., and, Theg, S.M., (2007) The Sec and Tat protein translocation pathways in chloroplasts. In Molecular Machines Involved in Protein Transport across Cellular Membranes, Vol. XXV (, Dalbey, R.E., Tamanoi, F., and, Koehler, C.M., eds). London: Elsevier, pp. 463-492.
7. Cline, K., Henry, R., Li, C., and, Yuan, J., (1993a) Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J. 12, 4105-4114.
8. Driessen, A.J., and, Nouwen, N., (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 77, 643-667.
9. Ferro, M., Salvi, D., Brugiere, S., Miras, S., Kowalski, S., Louwagie, M., Garin, J., Joyard, J., and, Rolland, N., (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol. Cell Proteomics, 2, 325-345.
10. 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.
11. Hatzixanthis, K., Palmer, T., and, Sargent, F., (2003) A subset of bacterial inner membrane proteins integrated by the twin-arginine translocase. Mol. Microbiol. 49, 1377-1390.
12. Henry, R., Carrigan, M., McCaffrey, M., Ma, X., and, Cline, K., (1997) Targeting determinants and proposed evolutionary basis for the Sec and the Delta pH protein transport systems in chloroplast thylakoid membranes. J. Cell Biol. 136, 823-832.
13. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and, Pease, L.R., (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene, 77, 61-68.
14. 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.
15. Ito, K., and, Akiyama, Y., (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu. Rev. Microbiol. 59, 211-231.
16. Molik, S., Karnauchov, I., Weidlich, C., Herrmann, R.G., and, Klosgen, R.B., (2001) The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J. Biol. Chem. 276, 42761-42766.
17. Mori, H., and, Cline, K., (2001) Post-translational protein translocation into thylakoids by the Sec and DeltapH-dependent pathways. Biochim. Biophys. Acta, 1541, 80-90.
18. Mori, H., Summer, E.J., Ma, X., and, Cline, K., (1999) Component specificity for the thylakoidal Sec and Delta pH-dependent protein transport pathways. J. Cell Biol. 146, 45-56.
19. Niwa, H., Tsuchiya, D., Makyio, H., Yoshida, M., and, Morikawa, K., (2002) Hexameric ring structure of the ATPase domain of the membrane-integrated metalloprotease FtsH from Thermus thermophilus HB8. Structure, 10, 1415-1423.
20. Osborne, A.R., Rapoport, T.A., and, van den Berg, B., (2005) Protein translocation by the Sec61/SecY channel. Annu. Rev. Cell Dev. Biol. 21, 529-550.
21. Richter, S., Lindenstrauss, U., Lucke, C., Bayliss, R., and, Bruser, T., (2007) Functional Tat transport of unstructured, small, hydrophilic proteins. J. Biol. Chem. 282, 33257-33264.
22. Sakamoto, W., (2006) Protein degradation machineries in plastids. Annu. Rev. Plant Biol. 57, 599-621.
23. Sakamoto, W., Zaltsman, A., Adam, Z., and, Takahashi, Y., (2003) Coordinated regulation and complex formation of yellow variegated1 and yellow variegated2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell, 15, 2843-2855.
24. Stanley, N.R., Palmer, T., and, Berks, B.C., (2000) The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275, 11591-11596.
25. Summer, E.J., Mori, H., Settles, A.M., and, Cline, K., (2000) The thylakoid delta pH-dependent pathway machinery facilitates RR-independent N-tail protein integration. J. Biol. Chem. 275, 23483-23490.
26. Urantowka, A., Knorpp, C., Olczak, T., Kolodziejczak, M., and, Janska, H., (2005) Plant mitochondria contain at least two i-AAA-like complexes. Plant Mol. Biol. 59, 239-252.
27. Yu, F., Park, S., and, Rodermel, S.R., (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J., 37, 864-876.
28. Yu, F., Park, S., and, Rodermel, S.R., (2005) Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol. 138, 1957-1966.
29. 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.
30. Zaltsman, A., Ori, N., and, Adam, Z., (2005) Two types of FtsH protease subunits are required for chloroplast biogenesis and Photosystem II repair in Arabidopsis. Plant Cell, 17, 2782-2790.