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Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis

Nature volume 464, pages 1210–1213 (2010)Cite this article

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Abstract

Photosynthetic light reactions establish electron flow in the chloroplast’s thylakoid membranes, leading to the production of the ATP and NADPH that participate in carbon fixation. Two modes of electron flow exist—linear electron flow (LEF) from water to NADP+ via photosystem (PS) II and PSI in series1 and cyclic electron flow (CEF) around PSI (ref. 2). Although CEF is essential for satisfying the varying demand for ATP, the exact molecule(s) and operational site are as yet unclear. In the green alga Chlamydomonas reinhardtii, the electron flow shifts from LEF to CEF on preferential excitation of PSII (ref. 3), which is brought about by an energy balancing mechanism between PSII and PSI (state transitions4). Here, we isolated a protein supercomplex composed of PSI with its own light-harvesting complex (LHCI), the PSII light-harvesting complex (LHCII), the cytochrome b6f complex (Cyt bf), ferredoxin (Fd)-NADPH oxidoreductase (FNR), and the integral membrane protein PGRL1 (ref. 5) from C. reinhardtii cells under PSII-favouring conditions. Spectroscopic analyses indicated that on illumination, reducing equivalents from downstream of PSI were transferred to Cyt bf, whereas oxidised PSI was re-reduced by reducing equivalents from Cyt bf, indicating that this supercomplex is engaged in CEF (Supplementary Fig. 1). Thus, formation and dissociation of the PSI–LHCI–LHCII–FNR–Cyt bf–PGRL1 supercomplex not only controlled the energy balance of the two photosystems, but also switched the mode of photosynthetic electron flow.

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Figure 1: State 2 transition induction of CEF.
Figure 2: Profiling the A4 supercomplex formed in State 2.
Figure 3: CEF activity in the A4 supercomplex.

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References

  1. Arnon, D. I., Whatley, F. R. & Allen, M. B. Assimilatory power in photosynthesis: photosynthetic phosphorylation by isolated chloroplasts is coupled with TPN reduction. Science 127, 1026–1034 (1958)

    Article  ADS  CAS  Google Scholar 

  2. Arnon, D. I., Allen, M. B. & Whatley, F. R. Photosynthesis by isolated chloroplasts. Nature 174, 394–396 (1954)

    Article  ADS  CAS  Google Scholar 

  3. Finazzi, G. et al. Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep. 3, 280–285 (2002)

    Article  CAS  Google Scholar 

  4. Rochaix, J. D. Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett. 581, 2768–2775 (2007)

    Article  CAS  Google Scholar 

  5. DalCorso, G. et al. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132, 273–285 (2008)

    Article  CAS  Google Scholar 

  6. Kramer, D. M., Avenson, T. J. & Edwards, G. E. Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci. 9, 349–357 (2004)

    Article  CAS  Google Scholar 

  7. Shikanai, T. Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant Biol. 58, 199–217 (2007)

    Article  CAS  Google Scholar 

  8. Ogawa, T. A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proc. Natl Acad. Sci. USA 88, 4275–4279 (1991)

    Article  ADS  CAS  Google Scholar 

  9. Bulté, L., Gans, P., Rebeille, F. & Wollman, F. A. ATP control on state transitions in vivo in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1020, 72–80 (1990)

    Article  Google Scholar 

  10. Takahashi, H., Iwai, M., Takahashi, Y. & Minagawa, J. Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 103, 477–482 (2006)

    Article  ADS  CAS  Google Scholar 

  11. Iwai, M., Takahashi, Y. & Minagawa, J. Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. Plant Cell 20, 2177–2189 (2008)

    Article  CAS  Google Scholar 

  12. Munekage, Y. et al. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110, 361–371 (2002)

    Article  CAS  Google Scholar 

  13. Gulis, G., Narasimhulu, K. V., Fox, L. N. & Redding, K. E. Purification of His6-tagged Photosystem I from Chlamydomonas reinhardtii. Photosynth. Res. 96, 51–60 (2008)

    Article  CAS  Google Scholar 

  14. Lam, E. & Malkin, R. Ferredoxin-mediated reduction of cytochrome b-563 in a chloroplast cytochrome b-563/f complex. FEBS Lett. 141, 98–101 (1982)

    Article  CAS  Google Scholar 

  15. Zhang, H., Whitelegge, J. P. & Cramer, W. A. Ferredoxin: NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. J. Biol. Chem. 276, 38159–38165 (2001)

    CAS  PubMed  Google Scholar 

  16. Rich, P. R., Heathcote, P. & Moss, D. A. Kinetic studies of electron transfer in a hybrid system constructed from the cytochrome bf complex and photosystem I. Biochim. Biophys. Acta 892, 138–151 (1987)

    Article  CAS  Google Scholar 

  17. Hippler, M., Drepper, F., Farah, J. & Rochaix, J. D. Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry 36, 6343–6349 (1997)

    Article  CAS  Google Scholar 

  18. Joliot, P. & Joliot, A. Cyclic electron transfer in plant leaf. Proc. Natl Acad. Sci. USA 99, 10209–10214 (2002)

    Article  ADS  CAS  Google Scholar 

  19. Laisk, A. Mathematical modelling of free-pool and channelled electron transport in photosynthesis: evidence for a functional supercomplex around photosystem 1. Proc. Biol. Sci. 251, 243–251 (1993)

    Article  CAS  Google Scholar 

  20. Breyton, C., Nandha, B., Johnson, G. N., Joliot, P. & Finazzi, G. Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 45, 13465–13475 (2006)

    Article  CAS  Google Scholar 

  21. Hamel, P., Olive, J., Pierre, Y., Wollman, F.-A. & de Vitry, C. A new subunit of cytochrome b6f complex undergoes reversible phosphorylation upon state transition. J. Biol. Chem. 275, 17072–17079 (2000)

    Article  CAS  Google Scholar 

  22. Tagawa, K., Tsujimoto, H. Y. & Arnon, D. I. Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc. Natl Acad. Sci. USA 49, 567–572 (1963)

    Article  ADS  CAS  Google Scholar 

  23. Bendall, D. S. & Manasse, R. S. Cyclic photophosphorylation and electron transport. Biochim. Biophys. Acta 1229, 23–38 (1995)

    Article  Google Scholar 

  24. Allen, J. F. Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 8, 15–19 (2003)

    Article  CAS  Google Scholar 

  25. Vallon, O. et al. Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc. Natl Acad. Sci. USA 88, 8262–8266 (1991)

    Article  ADS  CAS  Google Scholar 

  26. Pesaresi, P. et al. Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21, 2402–2423 (2009)

    Article  CAS  Google Scholar 

  27. Gorman, D. S. & Levine, R. P. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 54, 1665–1669 (1965)

    Article  ADS  CAS  Google Scholar 

  28. Lemaire, C., Girard-Bascou, J., Wollman, F. A. & Bennoun, P. Studies on the cytochrome b6/f complex. I. Characterization of the complex subunits in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 851, 229–238 (1986)

    Article  CAS  Google Scholar 

  29. Avenson, T. J., Cruz, J. A. & Kramer, D. M. Modulation of energy-dependent quenching of excitons in antennae of higher plants. Proc. Natl Acad. Sci. USA 101, 5530–5535 (2004)

    Article  ADS  CAS  Google Scholar 

  30. Sacksteder, C. A., Jacoby, M. E. & Kramer, D. M. A portable, non-focusing optics spectrophotometer (NoFOSpec) for measurements of steady-state absorbance changes in intact plants. Photosynth. Res. 70, 231–240 (2001)

    Article  CAS  Google Scholar 

  31. Metzger, S. U., Cramer, W. A. & Whitmarsh, J. Critical analysis of the extinction coefficient of chloroplast cytochrome f. Biochim. Biophys. Acta 1319, 233–241 (1997)

    Article  CAS  Google Scholar 

  32. Markwell, J. P., Thornber, J. P. & Skrdla, M. P. Effect of detergents on the reliability of a chemical assay for P-700. Biochim. Biophys. Acta 591, 391–399 (1980)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank S. Ozawa and M. Kuwano for technical help with MS/MS analysis, D. Kramer for valuable discussions, T. Shikanai, D. Leister and T. Hase for providing antibodies, and K. Redding for providing the PSI-His mutant. This study was supported by the Research Fellowship for Young Scientists from the Japan Society for the Promotion of Science (M.I., R.T.), Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (Y.T., 18GS0318; J.M.,18GS0318, 2120006309, 2157003109), the Strategic International Cooperative Program by Japan Science and Technology Agency (J.M.), and a Research Grant in the Natural Sciences by the Mitsubishi Foundation (J.M.).

Author Contributions M.I. and R.T. purified supercomplexes and Pc, and performed biochemical analyses; K.T. performed spectroscopic analyses; A.O. purified Fd under the supervision of Y.T.; M.I., K.T. and J.M. designed the study, analysed data, and wrote the paper. M.I. and K.T. contributed equally to the study. The whole study was supervised by J.M. All authors discussed the results and commented on the manuscript.

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  1. Masakazu Iwai

    Present address: Present address: Real-Time Bio-Imaging Research Team, Extreme Photonics Research Group, RIKEN Advanced Science Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan.,

  2. Masakazu Iwai and Kenji Takizawa: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Low Temperature Science, Hokkaido University, Sapporo 060-0819, Japan

    Masakazu Iwai, Kenji Takizawa, Ryutaro Tokutsu & Jun Minagawa

  2. Department of Biology, Faculty of Science, Okayama University, 3-1-1 Tsushima-naka, Okayama 700-8530, Japan,

    Akira Okamuro & Yuichiro Takahashi

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Correspondence to Jun Minagawa.

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Iwai, M., Takizawa, K., Tokutsu, R. et al. Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464, 1210–1213 (2010). https://doi.org/10.1038/nature08885

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