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A unique supramolecular organization of photosystem I in the moss Physcomitrella patens

Nature Plants volume 4, pages 904–909 (2018)Cite this article

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Abstract

The photosynthesis machinery in chloroplast thylakoid membranes is comprised of multiple protein complexes and supercomplexes1,2. Here, we show a novel supramolecular organization of photosystem I (PSI) in the moss Physcomitrella patens by single-particle cryo-electron microscopy. The moss-specific light-harvesting complex (LHC) protein Lhcb9 is involved in this PSI supercomplex, which has been shown to have a molecular density similar to that of the green alga Chlamydomonas reinhardtii3. Our results show that the structural organization is unexpectedly different—two rows of the LHCI belt exist as in C. reinhardtii4, but the outer one is shifted toward the PsaK side. Furthermore, one trimeric LHC protein and one monomeric LHC protein position alongside PsaL/K, filling the gap between these subunits and the outer LHCI belt. We provide evidence showing that Lhcb9 is a key factor, acting as a linkage between the PSI core and the outer LHCI belt to form the unique supramolecular organization of the PSI supercomplex in P. patens.

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Fig. 1: Single-particle negative-stained electron microscopy analysis of PSI–LHCI supercomplexes from A. thaliana, C. reinhardtii and P. patens.
Fig. 2: The protein composition of the additional antenna complex of Pp-PSI-L.
Fig. 3: The supramolecular organization of Pp-PSI-L observed by single-particle cryo-electron microscopy analysis.

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Data availability

The 3D cryo-EM density map of Pp-PSI-L has been deposited in the Electron Microscopy Data Bank under accession code EMD-9107, and with the Protein Data Bank (PDB) under accession code 6MEM. The data are available from the corresponding authors (M.I. and K.K.N.) upon request.

References

  1. Dekker, J. P. & Boekema, E. J. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta 1706, 12–39 (2005).

    Article  CAS  Google Scholar 

  2. Nelson, N. & Yocum, C. F. Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57, 521–565 (2006).

    Article  CAS  Google Scholar 

  3. Iwai, M. et al. Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens. Nat. Plants 1, 14008 (2015).

    Article  CAS  Google Scholar 

  4. Drop, B. et al. Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J. Biol. Chem. 286, 44878–44887 (2011).

    Article  CAS  Google Scholar 

  5. Jansson, S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4, 236–240 (1999).

    Article  CAS  Google Scholar 

  6. Wobbe, L., Bassi, R. & Kruse, O. Multi-level light capture control in plants and green algae. Trends Plant Sci. 21, 55–68 (2016).

    Article  CAS  Google Scholar 

  7. Nelson, N. & Junge, W. Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu. Rev. Biochem. 84, 659–683 (2015).

    Article  CAS  Google Scholar 

  8. Büchel, C. Evolution and function of light harvesting proteins. J. Plant Physiol. 172, 62–75 (2015).

    Article  Google Scholar 

  9. Neilson, J. A. & Durnford, D. G. Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth. Res. 106, 57–71 (2010).

    Article  CAS  Google Scholar 

  10. Jensen, P. E. et al. Structure, function and regulation of plant photosystem I. Biochim. Biophys. Acta 1767, 335–352 (2007).

    Article  CAS  Google Scholar 

  11. Qin, X., Suga, M., Kuang, T. & Shen, J. R. Structural basis for energy transfer pathways in the plant PSI–LHCI supercomplex. Science 348, 989–995 (2015).

    Article  CAS  Google Scholar 

  12. Mazor, Y., Borovikova, A., Caspy, I. & Nelson, N. Structure of the plant photosystem I supercomplex at 2.6 Å resolution. Nat. Plants 3, 17014 (2017).

    Article  CAS  Google Scholar 

  13. Wientjes, E., Oostergetel, G. T., Jansson, S., Boekema, E. J. & Croce, R. The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J. Biol. Chem. 284, 7803–7810 (2009).

    Article  CAS  Google Scholar 

  14. Germano, M. et al. Supramolecular organization of photosystem I and light-harvesting complex I in Chlamydomonas reinhardtii. FEBS Lett. 525, 121–125 (2002).

    Article  CAS  Google Scholar 

  15. Kargul, J., Nield, J. & Barber, J. Three-dimensional reconstruction of a light-harvesting complex I-photosystem I (LHCI-PSI) supercomplex from the green alga Chlamydomonas reinhardtii. Insights into light harvesting for PSI. J. Biol. Chem. 278, 16135–16141 (2003).

    Article  CAS  Google Scholar 

  16. Rensing, S. A. et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64–69 (2008).

    Article  CAS  Google Scholar 

  17. Alboresi, A., Caffarri, S., Nogue, F., Bassi, R. & Morosinotto, T. In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS ONE 3, e2033 (2008).

    Article  Google Scholar 

  18. Iwai, M. & Yokono, M. Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants. Curr. Opin. Plant Biol. 37, 94–101 (2017).

    Article  CAS  Google Scholar 

  19. Alboresi, A., Gerotto, C., Cazzaniga, S., Bassi, R. & Morosinotto, T. A red-shifted antenna protein associated with photosystem II in Physcomitrella patens. J. Biol. Chem. 286, 28978–28987 (2011).

    Article  CAS  Google Scholar 

  20. Busch, A. et al. Composition and structure of photosystem I in the moss Physcomitrella patens. J. Exp. Bot. 64, 2689–2699 (2013).

    Article  CAS  Google Scholar 

  21. Drop, B., Yadav, K. N. S., Boekema, E. J. & Croce, R. Consequences of state transitions on the structural and functional organization of photosystem I in the green alga Chlamydomonas reinhardtii. Plant J. 78, 181–191 (2014).

    Article  CAS  Google Scholar 

  22. Kouřil, R. et al. Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44, 10935–10940 (2005).

    Article  Google Scholar 

  23. Olsson, T., Thelander, M. & Ronne, H. A novel type of chloroplast stromal hexokinase is the major glucose-phosphorylating enzyme in the moss Physcomitrella patens. J. Biol. Chem. 278, 44439–44447 (2003).

    Article  CAS  Google Scholar 

  24. Thelander, M., Olsson, T. & Ronne, H. Effect of the energy supply on filamentous growth and development in Physcomitrella patens. J. Exp. Bot. 56, 653–662 (2005).

    Article  CAS  Google Scholar 

  25. Schumaker, K. S. & Dietrich, M. A. Programmed changes in form during moss development. Plant Cell 9, 1099–1107 (1997).

    Article  CAS  Google Scholar 

  26. Sugiyama, T. et al. Involvement of PpDof1 transcriptional repressor in the nutrient condition-dependent growth control of protonemal filaments in Physcomitrella patens. J. Exp. Bot. 63, 3185–3197 (2012).

    Article  CAS  Google Scholar 

  27. Pinnola, A. et al. A LHCB9-dependent photosystem I megacomplex induced under low light in Physcomitrella patens. Nat. Plants https://doi.org/10.1038/s41477-018-0270-2 (2018).

    Article  Google Scholar 

  28. 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  CAS  Google Scholar 

  29. Nishiyama, T., Hiwatashi, Y., Sakakibara, I., Kato, M. & Hasebe, M. Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis. DNA Res. 7, 9–17 (2000).

    Article  CAS  Google Scholar 

  30. 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 

  31. Porra, R. J., Thompson, W. A. & Kriedemann, P. E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384–394 (1989).

    Article  CAS  Google Scholar 

  32. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334–347 (2003).

    Article  Google Scholar 

  33. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).

    Article  CAS  Google Scholar 

  34. Tan, Y. Z. et al. Addressing preferred specimen orientation in single-particle cryo-EM through tilting. Nat. Methods 14, 793–796 (2017).

    Article  CAS  Google Scholar 

  35. Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    Article  CAS  Google Scholar 

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Acknowledgements

The QB3/Chemistry Mass Spectrometry Facility at the University of California, Berkeley receives support from the National Institutes of Health (grant 1S10OD020062-01). This work was supported by the US Department of Energy, Office of Science, through the Photosynthetic Systems programme in the Office of Basic Energy Sciences. E.N. and K.K.N. are investigators of the Howard Hughes Medical Institute.

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Author notes

  1. These authors contributed equally: M. Iwai, P. Grob.

Authors and Affiliations

  1. Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA

    Masakazu Iwai & Krishna K. Niyogi

  2. Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Masakazu Iwai, Patricia Grob, Eva Nogales & Krishna K. Niyogi

  3. Howard Hughes Medical Institute, University of California, Berkeley, CA, USA

    Patricia Grob, Eva Nogales & Krishna K. Niyogi

  4. QB3/Chemistry Mass Spectrometry Facility, University of California, Berkeley, CA, USA

    Anthony T. Iavarone

  5. Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA

    Eva Nogales

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Contributions

M.I. designed the research and performed the sample preparation and protein analysis. P.G. performed electron microscopy analysis and image processing. M.I. and P.G. wrote the paper. A.T.I. performed mass spectrometry analysis. E.N. and K.K.N. provided resources and supervision. All authors analysed the data, discussed the results and edited the manuscript.

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Correspondence to Masakazu Iwai or Krishna K. Niyogi.

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Iwai, M., Grob, P., Iavarone, A.T. et al. A unique supramolecular organization of photosystem I in the moss Physcomitrella patens. Nature Plants 4, 904–909 (2018). https://doi.org/10.1038/s41477-018-0271-1

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