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.

The structure of a plant photosystem I supercomplex at 3.4 Å resolution

Abstract

All higher organisms on Earth receive energy directly or indirectly from oxygenic photosynthesis performed by plants, green algae and cyanobacteria. Photosystem I (PSI) is a supercomplex of a reaction centre and light-harvesting complexes. It generates the most negative redox potential in nature, and thus largely determines the global amount of enthalpy in living systems. We report the structure of plant PSI at 3.4 Å resolution, revealing 17 protein subunits. PsaN was identified in the luminal side of the supercomplex, and most of the amino acids in the reaction centre were traced. The crystal structure of PSI provides a picture at near atomic detail of 11 out of 12 protein subunits of the reaction centre. At this level, 168 chlorophylls (65 assigned with orientations for Qx and Qy transition dipole moments), 2 phylloquinones, 3 Fe4S4 clusters and 5 carotenoids are described. This structural information extends the understanding of the most efficient nano-photochemical machine in nature.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: The structural model of plant photosystem I at 3.4 Å resolution.
Figure 2: Position of β-carotenes in relation to the ETC.
Figure 3: The position of PsaN in relation to Lhca2 and Lhca3, and the unique fold of Lhca3.
Figure 4: Model for PSI–LHCII interactions.

References

  1. 1

    Barber, J. Engine of life and big bang of evolution: a personal perspective. Photosynth. Res. 80, 137–155 (2004)

    CAS  Article  Google Scholar 

  2. 2

    Nelson, N. & Ben-Shem, A. The complex architecture of oxygenic photosynthesis. Nature Rev. Mol. Cell Biol. 5, 971–982 (2004)

    CAS  Article  Google Scholar 

  3. 3

    Nelson, N. & Ben-Shem, A. The structure of photosystem I and evolution of photosynthesis. Bioessays 27, 914–922 (2005)

    CAS  Article  Google Scholar 

  4. 4

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

    ADS  CAS  Article  Google Scholar 

  5. 5

    Kurisu, G., Zhang, H., Smith, J. L. & Cramer, W. A. Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302, 1009–1014 (2003)

    ADS  CAS  Article  Google Scholar 

  6. 6

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

    ADS  CAS  Article  Google Scholar 

  7. 7

    Loll, B., Kern, J., Saenger, W., Zouni, A. & Biesiadka, J. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040–1044 (2005)

    ADS  CAS  Article  Google Scholar 

  8. 8

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

    CAS  Article  Google Scholar 

  9. 9

    Stroebel, D., Choquet, Y., Popot, J. L. & Picot, D. An atypical haem in the cytochrome b6f complex. Nature 426, 413–418 (2003)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Liu, Z. et al. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428, 287–292 (2004)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Standfuss, J., Terwisscha van Scheltinga, A. C., Lamborghini, M. & Kuhlbrandt, W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J. 24, 919–928 (2005)

    CAS  Article  Google Scholar 

  12. 12

    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 

  13. 13

    Ben-Shem, A., Frolow, F. & Nelson, N. The crystal structure of plant photosystem I. Nature 426, 630–635 (2003)

    ADS  CAS  Article  Google Scholar 

  14. 14

    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)

    CAS  Article  Google Scholar 

  15. 15

    Jensen, P. E., Haldrup, A., Zhang, S. & Scheller, H. V. The PSI-O subunit of plant photosystem I is involved in balancing the excitation pressure between the two photosystems. J. Biol. Chem. 279, 24212–24217 (2004)

    CAS  Article  Google Scholar 

  16. 16

    Khrouchtchova, A. et al. A previously found thylakoid membrane protein of 14 kDa (TMP14) is a novel subunit of plant photosystem I and is designated PSI-P. FEBS Lett. 579, 4808–4812 (2005)

    CAS  Article  Google Scholar 

  17. 17

    Zygadlo, A., Robinson, C., Scheller, H. V., Mant, A. & Jensen, P. E. The properties of the positively charged loop region in PSI-G are essential for its “spontaneous” insertion into thylakoids and rapid assembly into the photosystem I complex. J. Biol. Chem. 281, 10548–10554 (2006)

    CAS  Article  Google Scholar 

  18. 18

    Ben-Shem, A., Frolow, F. & Nelson, N. Evolution of Photosystem I—from symmetry through pseudosymmetry to asymmetry. FEBS Lett. 564, 274–280 (2004)

    CAS  Article  Google Scholar 

  19. 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)

    ADS  CAS  Article  Google Scholar 

  20. 20

    Dashdorj, N., Xu, W., Cohen, R. O., Golbeck, J. H. & Savikhin, S. Asymmetric electron transfer in cyanobacterial Photosystem I: charge separation and secondary electron transfer dynamics of mutations near the primary electron acceptor A0. Biophys. J. 88, 1238–1249 (2005)

    CAS  Article  Google Scholar 

  21. 21

    Joliot, P. & Joliot, A. In vivo analysis of the electron transfer within photosystem I: are the two phylloquinones involved? Biochemistry 38, 11130–11136 (1999)

    CAS  Article  Google Scholar 

  22. 22

    Jolley, C., Ben-Shem, A., Nelson, N. & Fromme, P. Structure of plant photosystem I revealed by theoretical modeling. J. Biol. Chem. 280, 33627–33636 (2005)

    CAS  Article  Google Scholar 

  23. 23

    Morosinotto, T., Ballottari, M., Klimmek, F., Jansson, S. & Bassi, R. The association of the antenna system to photosystem I in higher plants. Cooperative interactions stabilize the supramolecular complex and enhance red-shifted spectral forms. J. Biol. Chem. 280, 31050–31058 (2005)

    CAS  Article  Google Scholar 

  24. 24

    Ben-Shem, A., Frolow, F. & Nelson, N. Light-harvesting features revealed by the structure of plant photosystem I. Photosynth. Res 81, 239–250 (2004)

    CAS  Google Scholar 

  25. 25

    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)

    CAS  Article  Google Scholar 

  26. 26

    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)

    CAS  Article  Google Scholar 

  27. 27

    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)

    ADS  CAS  Article  Google Scholar 

  28. 28

    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)

    ADS  CAS  Article  Google Scholar 

  29. 29

    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)

    CAS  Article  Google Scholar 

  30. 30

    Anderson, J. M., Chow, W. S. & Park, Y.-I. The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth. Res 46, 129–139 (1995)

    CAS  Article  Google Scholar 

  31. 31

    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)

    CAS  Article  Google Scholar 

  32. 32

    Mozzo, M., Morosinotto, T., Bassi, R. & Croce, R. Probing the structure of Lhca3 by mutation analysis. Biochim. Biophys. Acta. 1757, 1607–1613 (2006).

    CAS  Article  Google Scholar 

  33. 33

    Ikeuchi, M. & Inoue, Y. Two new components of 9 and 14 kDa from spinach photosystem I complex. FEBS Lett. 280, 332–334 (1991)

    CAS  Article  Google Scholar 

  34. 34

    He, W. Z. & Malkin, R. Specific release of a 9-kDa extrinsic polypeptide of photosystem I from spinach chloroplasts by salt washing. FEBS Lett. 308, 298–300 (1992)

    CAS  Article  Google Scholar 

  35. 35

    Knoetzel, J. & Simpson, D. J. The primary structure of a cDNA for PsaN, encoding an extrinsic lumenal polypeptide of barley photosystem I. Plant Mol. Biol. 22, 337–345 (1993)

    CAS  Article  Google Scholar 

  36. 36

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

    CAS  Article  Google Scholar 

  37. 37

    Haldrup, A., Naver, H. & Scheller, H. V. The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem I. Plant J. 17, 689–698 (1999)

    CAS  Article  Google Scholar 

  38. 38

    Lucinski, R., Schmid, V.H., Jansson, S. & Klimmek, F. Lhca5 interaction with plant photosystem I. FEBS Lett. 580, 6485–6488 (2006); published online 7 November 2006.

    CAS  Article  Google Scholar 

  39. 39

    Bellafiore, S., Barneche, F., Peltier, G. & Rochaix, J. D. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892–895 (2005)

    ADS  CAS  Article  Google Scholar 

  40. 40

    Kyle, D. J., Staehelin, L. A. & Arntzen, C. J. Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch. Biochem. Biophys. 222, 527–541 (1983)

    CAS  Article  Google Scholar 

  41. 41

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

    CAS  Article  Google Scholar 

  42. 42

    Consoli, E., Croce, R., Dunlap, D. D. & Finzi, L. Diffusion of light-harvesting complex II in the thylakoid membranes. EMBO Rep. 6, 782–786 (2005)

    CAS  Article  Google Scholar 

  43. 43

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

    CAS  Article  Google Scholar 

  44. 44

    Haldrup, A., Jensen, P. E., Lunde, C. & Scheller, H. V. Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci. 6, 301–305 (2001)

    CAS  Article  Google Scholar 

  45. 45

    Kargul, J. et al. Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J. 272, 4797–4806 (2005)

    CAS  Article  Google Scholar 

  46. 46

    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)

    ADS  CAS  Article  Google Scholar 

  47. 47

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

    CAS  Article  Google Scholar 

  48. 48

    Sener, M. K. et al. Evolution of the excitation transfer network in photosystem I from cyanobacteria to plants. Biophys. J. 89, 1630–1642 (2005)

    ADS  CAS  Article  Google Scholar 

  49. 49

    Amunts, A., Ben-Shem, A. & Nelson, N. Solving the structure of plant photosystem I—biochemistry is vital. Photochem. Photobiol. Sci. 4, 1011–1015 (2005)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank the ESRF for synchrotron beam time, and staff scientists of the ID 14, ID 29 and ID 23 station clusters for their assistance. We also thank F. Frolow and J. Hirsh for valuable guidance and advice in crystallography. This work was supported by The Israel Science Foundation.

Atomic coordinates and structure factor files were deposited in the Protein Data Bank under accession number 2O01.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nathan Nelson.

Ethics declarations

Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Supplementary Tables S1-S2, Supplementary Figures S1-S3 with Legends and additional references. (PDF 10976 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Amunts, A., Drory, O. & Nelson, N. The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447, 58–63 (2007). https://doi.org/10.1038/nature05687

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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