Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Accessibility controls selective degradation of photosystem II subunits by FtsH protease

Nature Plants volume 1, Article number: 15168 (2015) Cite this article

Subjects

Abstract

The oxygen-evolving photosystem II (PSII) complex located in chloroplasts and cyanobacteria is sensitive to light-induced damage1 that unless repaired causes reduction in photosynthetic capacity and growth. Although a potential target for crop improvement, the mechanism of PSII repair remains unclear. The D1 reaction center protein is the main target for photodamage2, with repair involving the selective degradation of the damaged protein by FtsH protease3. How a single damaged PSII subunit is recognized for replacement is unknown. Here, we have tested the dark stability of PSII subunits in strains of the cyanobacterium Synechocystis PCC 6803 blocked at specific stages of assembly. We have found that when D1, which is normally shielded by the CP43 subunit, becomes exposed in a photochemically active PSII complex lacking CP43, it is selectively degraded by FtsH even in the dark. Removal of the CP47 subunit, which increases accessibility of FtsH to the D2 subunit, induced dark degradation of D2 at a faster rate than that of D1. In contrast, CP47 and CP43 are resistant to degradation in the dark. Our results indicate that protease accessibility induced by PSII disassembly is an important determinant in the selection of the D1 and D2 subunits to be degraded by FtsH.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structure and dark stability of wild-type and mutant PSII.
Figure 2: Structure of RC47 and dark stability of ΔCP43 mutants.
Figure 3: Structure of RCII and dark stability of ΔCP47 mutants.
Figure 4: Model of the selective degradation of the D1 and D2 proteins.

Similar content being viewed by others

References

  1. Adir, N., Zer, H., Shochat, S. & Ohad, I. Photoinhibition – a historical perspective. Photosynth. Res. 76, 343–370 (2003).

    Article  CAS  Google Scholar 

  2. Ohad, I., Kyle, D. J. & Arntzen, C. J. Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J. Cell Biol. 99, 481–485 (1984).

    Article  CAS  Google Scholar 

  3. Boehm, M. et al. Subunit organization of a Synechocystis hetero-oligomeric thylakoid FtsH complex involved in photosystem II repair. Plant Cell 24, 3669–3683 (2012).

    Article  CAS  Google Scholar 

  4. Bottomley, W., Spencer, D. & Whitfeld, P. R. Protein-synthesis in isolated spinach-chloroplasts – comparison of light-driven and ATP-driven synthesis. Arch. Biochem. Biophys. 164, 106–117 (1974).

    Article  CAS  Google Scholar 

  5. Eaglesham, A. R. & Ellis, R. J. Protein-synthesis in chloroplasts. 2. light-driven synthesis of membrane proteins by isolated pea chloroplasts. Biochim. Biophys. Acta 335, 396–407 (1974).

    Article  CAS  Google Scholar 

  6. Nagarajan, A. & Burnap, R. L. Parallel expression of alternate forms of psbA2 gene provides evidence for the existence of a targeted D1 repair mechanism in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta 1837, 1417–1426 (2014).

    Article  CAS  Google Scholar 

  7. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).

    Article  CAS  Google Scholar 

  8. Umena, Y., Kawakami, K., Shen, J. R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature 473, 55–60 (2011).

    Article  CAS  Google Scholar 

  9. Komenda, J. & Barber, J. Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicate that degradation of D1 protein is regulated by the QB site and is dependent on protein synthesis. Biochemistry 34, 9625–9631 (1995).

    Article  CAS  Google Scholar 

  10. Komenda, J., Knoppova, J., Krynicka, V., Nixon, P. J. & Tichy, M. Role of FtsH2 in the repair of photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster. Biochim. Biophys. Acta 1797, 566–575 (2010).

    Article  CAS  Google Scholar 

  11. Komenda, J. et al. The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp PCC 6803. J. Biol. Chem. 281, 1145–1151 (2006).

    Article  CAS  Google Scholar 

  12. Boehm, M. et al. Subunit composition of CP43-less photosystem II complexes of Synechocystis sp PCC 6803: implications for the assembly and repair of photosystem II. Phil. Trans. R. Soc. B 367, 3444–3454 (2012).

    Article  CAS  Google Scholar 

  13. Tyystjarvi, E. Photoinhibition of photosystem II. Int. Rev. Cell Mol. Biol. 300, 243–303 (2013).

    Article  CAS  Google Scholar 

  14. Kasson, T. M. D. & Barry, B. A. Reactive oxygen and oxidative stress: N-formyl kynurenine in photosystem II and non-photosynthetic proteins. Photosynth. Res. 114, 97–110 (2012).

    Article  CAS  Google Scholar 

  15. Komenda, J. & Masojidek, J. Structural changes of Photosystem II complex induced by high irradiance in cyanobacterial cells. Eur. J. Biochem. 233, 677–682 (1995).

    Article  CAS  Google Scholar 

  16. Knoppova, J. et al. Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis. Plant Cell 26, 1200–1212 (2014).

    Article  CAS  Google Scholar 

  17. Komenda, J. et al. Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J. Biol. Chem. 279, 48620–48629 (2004).

    Article  CAS  Google Scholar 

  18. Komenda, J. et al. Cleavage after residue Ala352 in the C-terminal extension is an early step in the maturation of the D1 subunit of photosystem II in Synechocystis PCC 6803. Biochim. Biophys. Acta 1767, 829–837 (2007).

    Article  CAS  Google Scholar 

  19. Williams, J. G. K. Construction of specific mutations in Photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol. 167, 766–778 (1988).

    Article  CAS  Google Scholar 

  20. Burnap, R. L. & Sherman, L. A. Deletion mutagenesis in Synechocystis sp. PCC6803 indicates that the Mn-stabilizing protein of photosystem II is not essential for oxygen evolution. Biochemistry 30, 440–446 (1991).

    Article  CAS  Google Scholar 

  21. Vermaas, W. F., Ikeuchi, M. & Inoue, Y. Protein composition of the photosystem II core complex in genetically engineered mutants of the cyanobacterium Synechocystis sp. PCC 6803. Photosynth. Res. 17, 97–113 (1988).

    Article  CAS  Google Scholar 

  22. Eaton-Rye, J. J. & Vermaas, W. F. J. Oligonucleotide – directed mutagenesis of psbB, the gene encoding CP47, employing a deletion mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol. Biol. 17, 1165–1177 (1991).

    Article  CAS  Google Scholar 

  23. Dobakova, M., Sobotka, R., Tichy, M. & Komenda, J. Psb28 protein is involved in the biogenesis of the Photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp PCC 6803. Plant Physiol. 149, 1076–1086 (2009).

    Article  CAS  Google Scholar 

  24. Wittig, I., Karas, M. & Schagger, H. High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell Proteomics 6, 1215–1225 (2007).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

V.K. and J.K. were supported by the National Programme of Sustainability I, ID: LO1416 and by the project P501/12/G055 of the Grant Agency of the Czech Republic, S.S. and P.J.N. by the BBSRC (grant BB/L003260/1) and S.S. by China Scholarship Council.

Author information

Authors and Affiliations

  1. Faculty of Science, University of South Bohemia, Branišovská 31, České Budějovice, 37005, Czech Republic

    Vendula Krynická & Josef Komenda

  2. Institute of Microbiology, Academy of Sciences of the Czech Republic, Center Algatech, Opatovický mlýn, Třeboň, 379 81, Czech Republic

    Vendula Krynická & Josef Komenda

  3. Department of Life Sciences, Sir Ernst Chain Building, Wolfson Laboratories, Imperial College London, S. Kensington campus, London, SW7 2AZ, UK

    Shengxi Shao & Peter J. Nixon

Authors
  1. Vendula Krynická
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shengxi Shao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter J. Nixon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josef Komenda
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

V.K. performed experiments and protein analyses under the supervision of J.K., J.K. designed the study, S.S. made model figures and P.J.N. and J.K. wrote the paper. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Josef Komenda.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krynická, V., Shao, S., Nixon, P. et al. Accessibility controls selective degradation of photosystem II subunits by FtsH protease. Nature Plants 1, 15168 (2015). https://doi.org/10.1038/nplants.2015.168

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.168

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing