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Crystal structure of plant photosystem I

Nature volume 426, pages 630–635 (2003)Cite this article

Abstract

Oxygenic photosynthesis is the principal producer of both oxygen and organic matter on Earth. The conversion of sunlight into chemical energy is driven by two multisubunit membrane protein complexes named photosystem I and II. We determined the crystal structure of the complete photosystem I (PSI) from a higher plant (Pisum sativum var. alaska) to 4.4 Å resolution. Its intricate structure shows 12 core subunits, 4 different light-harvesting membrane proteins (LHCI) assembled in a half-moon shape on one side of the core, 45 transmembrane helices, 167 chlorophylls, 3 Fe–S clusters and 2 phylloquinones. About 20 chlorophylls are positioned in strategic locations in the cleft between LHCI and the core. This structure provides a framework for exploration not only of energy and electron transfer but also of the evolutionary forces that shaped the photosynthetic apparatus of terrestrial plants after the divergence of chloroplasts from marine cyanobacteria one billion years ago.

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Figure 1: The structural model of plant PSI at 4.4 Å represented as Cα backbone.
Figure 2: The arrangement of 167 chlorophyll molecules of plant PSI as seen from the stromal side.
Figure 3: Dimer formation between Lhca1 and Lhca4 and tight binding of Lhca1 to the reaction centre.
Figure 4: The structural model of Lhca monomers compared to LHCII.
Figure 5: Electron transfer chain and plastocyanin binding.
Figure 6: Loops altered during the evolution of plant PsaA and PsaB.

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References

  1. Chitnis, P. R. Photosystem I: Function and physiology. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 52, 593–626 (2001)

    Article  CAS  Google Scholar 

  2. Barber, J. Photosystem II: a multisubunit membrane protein that oxidises water. Curr. Opin. Struct. Biol. 12, 523–530 (2002)

    Article  CAS  Google Scholar 

  3. Junge, W. ATP synthase and other motor proteins. Proc. Natl Acad. Sci. USA 96, 4735–4737 (1999)

    Article  ADS  CAS  Google Scholar 

  4. Cramer, W. A. et al. Some new structural aspects and old controversies concerning the cytochrome b(6)f complex of oxygenic photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 477–508 (1996)

    Article  CAS  Google Scholar 

  5. Herrmann, R. G. Biogenesis and evolution of photosynthetic (thylakoid) membranes. Biosci. Rep. 19, 355–365 (1999)

    Article  CAS  Google Scholar 

  6. Trissl, H.-W. & Wilhelm, C. Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem. Sci. 18, 415–419 (1993)

    Article  CAS  Google Scholar 

  7. Bailey, S., Walters, R. G., Jansson, S. & Horton, P. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213, 794–801 (2001)

    Article  CAS  Google Scholar 

  8. Durnford, D. G. et al. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol. 48, 59–68 (1999)

    Article  ADS  CAS  Google Scholar 

  9. Croce, R., Morosinotto, T., Castelletti, S., Breton, J. & Bassi, R. The Lhca antenna complexes of higher plants photosystem I. Biochim. Biophys. Acta 1556, 29–40 (2002)

    Article  CAS  Google Scholar 

  10. Jordan, P. et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909–917 (2001)

    Article  ADS  CAS  Google Scholar 

  11. Ben-Shem, A., Nelson, N. & Frolow, F. Crystallization and initial X-ray diffraction studies of higher plant photosystem I. Acta Crystallogr. D 59, 1824–1827 (2003)

    Article  Google Scholar 

  12. Scheller, H. V., Jensen, P. E., Haldrup, A., Lunde, C. & Knoetzel, J. Role of subunits in eukaryotic Photosystem I. Biochim. Biophys. Acta 1507, 41–60 (2001)

    Article  CAS  Google Scholar 

  13. Jansson, S., Andersen, B. & Scheller, H. V. Nearest-neighbor analysis of higher-plant photosystem I holocomplex. Plant Physiol. 112, 409–420 (1996)

    Article  CAS  Google Scholar 

  14. 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 

  15. Ihalainen, J. A. et al. Pigment organization and energy transfer dynamics in isolated photosystem I (PSI) complexes from Arabidopsis thaliana depleted of the PSI-G, PSI-K, PSI-L, or PSI-N subunit. Biophys. J. 83, 2190–2201 (2002)

    Article  ADS  CAS  Google Scholar 

  16. Schmid, V. H., Paulsen, H. & Rupprecht, J. Identification of N- and C-terminal amino acids of Lhca1 and Lhca4 required for formation of the heterodimeric peripheral photosystem I antenna LHCI-730. Biochemistry 41, 9126–9131 (2002)

    Article  CAS  Google Scholar 

  17. Ganeteg, U., Strand, A., Gustafsson, P. & Jansson, S. The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition. Plant Physiol. 127, 150–158 (2001)

    Article  CAS  Google Scholar 

  18. Knoetzel, J., Mant, A., Haldrup, A., Jensen, P. E. & Scheller, H. V. PSI-O, a new 10-kDa subunit of eukaryotic photosystem I. FEBS Lett. 510, 145–148 (2002)

    Article  CAS  Google Scholar 

  19. Lunde, C. P., Jensen, P. E., Haldrup, A., Knoetzel, J. & Scheller, H. V. The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408, 613–615 (2000)

    Article  ADS  CAS  Google Scholar 

  20. Hippler, M. et al. The plastocyanin binding domain of photosystem I. EMBO J. 15, 6374–6384 (1996)

    Article  CAS  Google Scholar 

  21. Raymond, J., Zhaxybayeva, O., Gogarten, J. P., Gerdes, S. Y. & Blankenship, R. E. Whole-genome analysis of photosynthetic prokaryotes. Science 298, 1616–1620 (2002)

    Article  ADS  CAS  Google Scholar 

  22. Xiong, J. & Bauer, C. E. Complex evolution of photosynthesis. Annu. Rev. Plant Biol. 53, 503–521 (2002)

    Article  CAS  Google Scholar 

  23. Kuhlbrandt, W., Wang, D. N. & Fujiyoshi, Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367, 614–621 (1994)

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Morosinotto, T., Castelletti, S., Breton, J., Bassi, R. & Croce, R. Mutation analysis of Lhca1 antenna complex. Low energy absorption forms originate from pigment–pigment interactions. J. Biol. Chem. 277, 36253–36261 (2002)

    Article  CAS  Google Scholar 

  26. Moseley, J. L. et al. Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J. 21, 6709–6720 (2002)

    Article  CAS  Google Scholar 

  27. Schmid, V. H. et al. Pigment binding of photosystem I light-harvesting proteins. J. Biol. Chem. 277, 37307–37314 (2002)

    Article  CAS  Google Scholar 

  28. Croce, R., Zucchelli, G., Garlaschi, F. M. & Jennings, R. C. A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core. Biochemistry 37, 17355–17360 (1998)

    Article  CAS  Google Scholar 

  29. Rivadossi, A., Zucchelli, G., Garlaschi, F. M. & Jennings, R. C. The importance of PSI chlorophyll red forms in light-harvesting by leaves. Photosynth. Res. 60, 209–215 (1999)

    Article  CAS  Google Scholar 

  30. Jennings, R. C., Zucchelli, G., Croce, R. & Garlaschi, F. M. The photochemical trapping rate from red spectral states in PSI-LHCI is determined by thermal activation of energy transfer to bulk chlorophylls. Biochim. Biophys. Acta 1557, 91–98 (2003)

    Article  CAS  Google Scholar 

  31. Bengis, C. & Nelson, N. Subunit structure of chloroplast photosystem I reaction center. J. Biol. Chem. 252, 4564–4569 (1977)

    CAS  PubMed  Google Scholar 

  32. Xue, Y., Okvist, M., Hansson, O. & Young, S. Crystal structure of spinach plastocyanin at 1.7 Å resolution. Protein Sci. 7, 2099–2105 (1998)

    Article  CAS  Google Scholar 

  33. Sommer, F., Drepper, F. & Hippler, M. The luminal helix l of PsaB is essential for recognition of plastocyanin or cytochrome c6 and fast electron transfer to photosystem I in Chlamydomonas reinhardtii. J. Biol. Chem. 277, 6573–6581 (2002)

    Article  CAS  Google Scholar 

  34. Chitnis, P. R., Purvis, D. & Nelson, N. Molecular cloning and targeted mutagenesis of the gene psaF encoding subunit III of photosystem I from the cyanobacterium Synechocystis sp PCC 6803. J. Biol. Chem. 266, 20146–20151 (1991)

    CAS  PubMed  Google Scholar 

  35. Hippler, M., Drepper, F., Haehnel, W. & Rochaix, J. D. The N-terminal domain of PsaF: precise recognition site for binding and fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 95, 7339–7344 (1998)

    Article  ADS  CAS  Google Scholar 

  36. Bibby, T. S., Nield, J. & Barber, J. Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412, 743–745 (2001)

    Article  ADS  CAS  Google Scholar 

  37. Boekema, E. J. et al. A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria. Nature 412, 745–748 (2001)

    Article  ADS  CAS  Google Scholar 

  38. Nield, J., Morris, E. P., Bibby, T. S. & Barber, J. Structural analysis of the photosystem I supercomplex of cyanobacteria induced by iron deficiency. Biochemistry 42, 3180–3188 (2003)

    Article  CAS  Google Scholar 

  39. Melkozernov, A. N., Lin, S., Bibby, T. S., Barber, J. & Blankenship, R. E. Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed Synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core. Biochemistry 42, 3893–3903 (2003)

    Article  CAS  Google Scholar 

  40. Nelson, N. & Ben-Shem, A. Photosystem I reaction center: Past and future. Photosynth. Res. 73, 193–206 (2002)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the ESRF for synchrotron beam time, and staff scientists of the ID14 stations cluster for their assistance. We thank W. Kuhlbrandt for LHCII coordinates. A.B. is a recipient of a Charles Clore Foundation Ph.D. student scholarship. This work was supported by a grant from The Israel Science Foundation to N.N. and F.F.

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Authors and Affiliations

  1. Department of Biochemistry, The George S. Wise Faculty of Life Sciences, Tel Aviv University, 69978, Tel Aviv, Israel

    Adam Ben-Shem & Nathan Nelson

  2. Molecular Microbiology and Biotechnology, The George S. Wise Faculty of Life Sciences, Tel Aviv University, 69978, Tel Aviv, Israel

    Felix Frolow

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Correspondence to Nathan Nelson.

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Ben-Shem, A., Frolow, F. & Nelson, N. Crystal structure of plant photosystem I. Nature 426, 630–635 (2003). https://doi.org/10.1038/nature02200

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