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. 1997 Jun;9(6):957–965. doi: 10.1105/tpc.9.6.957

Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease.

O Ostersetzer 1, Z Adam 1
PMCID: PMC156970  PMID: 9212469

Abstract

Unassembled subunits of the cytochrome b6f complex as well as components of other unassembled chloroplastic complexes are rapidly degraded within the organelle. However, the mechanisms involved in these proteolytic processes are obscure. When the Rieske FeS protein (RISP) is imported into isolated chloroplasts in vitro, some of the protein does not property assemble with the cytochrome complex, as determined by its sensitivity to exogenous protease. When assayed in intact, lysed, or fractionated chloroplasts, the imported RISP was found to be sensitive to endogenous proteases as well. The activity responsible for degradation of the unassembled protein was localized to the thylakoid membrane and characterized as a metalloprotease requiring zinc ions for its activity. The degradation rate was stimulated by light, but no involvement of ATP or redox control was observed. Instead, when the RISP that was attached to thylakoid membranes was first illuminated on ice, degradation proceeded in either light or darkness at equal rates suggesting a light-induced conformational change making the protein prone to degradation. Antibodies raised against native FtsH, a bacterial, membrane-bound, ATP-dependent, zinc-stimulated protease, effectively inhibited degradation of the unassembled RISP, suggesting a role for the chloroplastic FtsH in this process.

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Selected References

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  1. Adam Z., Hoffman N. E. Biogenesis of a photosystem I light-harvesting complex. Evidence for a membrane intermediate. Plant Physiol. 1993 May;102(1):35–43. doi: 10.1104/pp.102.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adam Z. Protein stability and degradation in chloroplasts. Plant Mol Biol. 1996 Dec;32(5):773–783. doi: 10.1007/BF00020476. [DOI] [PubMed] [Google Scholar]
  3. Arlt H., Tauer R., Feldmann H., Neupert W., Langer T. The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell. 1996 Jun 14;85(6):875–885. doi: 10.1016/s0092-8674(00)81271-4. [DOI] [PubMed] [Google Scholar]
  4. Berthold D. A., Schmidt C. L., Malkin R. The deletion of petG in Chlamydomonas reinhardtii disrupts the cytochrome bf complex. J Biol Chem. 1995 Dec 8;270(49):29293–29298. doi: 10.1074/jbc.270.49.29293. [DOI] [PubMed] [Google Scholar]
  5. Breyton C., de Vitry C., Popot J. L. Membrane association of cytochrome b6f subunits. The Rieske iron-sulfur protein from Chlamydomonas reinhardtii is an extrinsic protein. J Biol Chem. 1994 Mar 11;269(10):7597–7602. [PubMed] [Google Scholar]
  6. Bruce B. D., Malkin R. Biosynthesis of the chloroplast cytochrome b6f complex: studies in a photosynthetic mutant of Lemna. Plant Cell. 1991 Feb;3(2):203–212. doi: 10.1105/tpc.3.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cramer W. A., Soriano G. M., Ponomarev M., Huang D., Zhang H., Martinez S. E., Smith J. L. SOME NEW STRUCTURAL ASPECTS AND OLD CONTROVERSIES CONCERNING THE CYTOCHROME b6f COMPLEX OF OXYGENIC PHOTOSYNTHESIS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):477–508. doi: 10.1146/annurev.arplant.47.1.477. [DOI] [PubMed] [Google Scholar]
  8. Haley J., Bogorad L. A 4-kDa maize chloroplast polypeptide associated with the cytochrome b6-f complex: subunit 5, encoded by the chloroplast petE gene. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1534–1538. doi: 10.1073/pnas.86.5.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Halperin T., Adam Z. Degradation of mistargeted OEE33 in the chloroplast stroma. Plant Mol Biol. 1996 Mar;30(5):925–933. doi: 10.1007/BF00020804. [DOI] [PubMed] [Google Scholar]
  10. Hugueney P., Bouvier F., Badillo A., d'Harlingue A., Kuntz M., Camara B. Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5630–5634. doi: 10.1073/pnas.92.12.5630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kihara A., Akiyama Y., Ito K. FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4532–4536. doi: 10.1073/pnas.92.10.4532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Leonhard K., Herrmann J. M., Stuart R. A., Mannhaupt G., Neupert W., Langer T. AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J. 1996 Aug 15;15(16):4218–4229. [PMC free article] [PubMed] [Google Scholar]
  13. Levy M., Adam Z. Mutations in the processing site of the precursor of ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit: effects on import, processing, assembly and stability. Plant Mol Biol. 1995 Oct;29(1):53–61. doi: 10.1007/BF00019118. [DOI] [PubMed] [Google Scholar]
  14. Lindahl M., Tabak S., Cseke L., Pichersky E., Andersson B., Adam Z. Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. J Biol Chem. 1996 Nov 15;271(46):29329–29334. doi: 10.1074/jbc.271.46.29329. [DOI] [PubMed] [Google Scholar]
  15. Madueno F., Napier J. A., Gray J. C. Newly Imported Rieske Iron-Sulfur Protein Associates with Both Cpn60 and Hsp70 in the Chloroplast Stroma. Plant Cell. 1993 Dec;5(12):1865–1876. doi: 10.1105/tpc.5.12.1865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Madueño F., Bradshaw S. A., Gray J. C. The thylakoid-targeting domain of the chloroplast Rieske iron-sulfur protein is located in the N-terminal hydrophobic region of the mature protein. J Biol Chem. 1994 Jul 1;269(26):17458–17463. [PubMed] [Google Scholar]
  17. Madueño F., Napier J. A., Cejudo F. J., Gray J. C. Import and processing of the precursor of the Rieske FeS protein of tobacco chloroplasts. Plant Mol Biol. 1992 Oct;20(2):289–299. doi: 10.1007/BF00014496. [DOI] [PubMed] [Google Scholar]
  18. Pajic A., Tauer R., Feldmann H., Neupert W., Langer T. Yta10p is required for the ATP-dependent degradation of polypeptides in the inner membrane of mitochondria. FEBS Lett. 1994 Oct 17;353(2):201–206. doi: 10.1016/0014-5793(94)01046-3. [DOI] [PubMed] [Google Scholar]
  19. Rep M., van Dijl J. M., Suda K., Schatz G., Grivell L. A., Suzuki C. K. Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast Lon. Science. 1996 Oct 4;274(5284):103–106. doi: 10.1126/science.274.5284.103. [DOI] [PubMed] [Google Scholar]
  20. Salter A. H., Newman B. J., Napier J. A., Gray J. C. Import of the precursor of the chloroplast Rieske iron-sulphur protein by pea chloroplasts. Plant Mol Biol. 1992 Nov;20(3):569–574. doi: 10.1007/BF00040617. [DOI] [PubMed] [Google Scholar]
  21. Schmidt G. W., Mishkind M. L. Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci U S A. 1983 May;80(9):2632–2636. doi: 10.1073/pnas.80.9.2632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tomoyasu T., Gamer J., Bukau B., Kanemori M., Mori H., Rutman A. J., Oppenheim A. B., Yura T., Yamanaka K., Niki H. Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J. 1995 Jun 1;14(11):2551–2560. doi: 10.1002/j.1460-2075.1995.tb07253.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tomoyasu T., Yamanaka K., Murata K., Suzaki T., Bouloc P., Kato A., Niki H., Hiraga S., Ogura T. Topology and subcellular localization of FtsH protein in Escherichia coli. J Bacteriol. 1993 Mar;175(5):1352–1357. doi: 10.1128/jb.175.5.1352-1357.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Voelker R., Barkan A. Nuclear genes required for post-translational steps in the biogenesis of the chloroplast cytochrome b6f complex in maize. Mol Gen Genet. 1995 Dec 15;249(5):507–514. doi: 10.1007/BF00290576. [DOI] [PubMed] [Google Scholar]
  25. Wickner S., Gottesman S., Skowyra D., Hoskins J., McKenney K., Maurizi M. R. A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12218–12222. doi: 10.1073/pnas.91.25.12218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. de Vitry C., Breyton C., Pierre Y., Popot J. L. The 4-kDa nuclear-encoded PetM polypeptide of the chloroplast cytochrome b6f complex. Nucleic acid and protein sequences, targeting signals, transmembrane topology. J Biol Chem. 1996 May 3;271(18):10667–10671. doi: 10.1074/jbc.271.18.10667. [DOI] [PubMed] [Google Scholar]

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