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Plants lacking the main light-harvesting complex retain photosystem II macro-organization

Abstract

Photosystem II (PSII) is a key component of photosynthesis, the process of converting sunlight into the chemical energy of life. In plant cells, it forms a unique oligomeric macrostructure in membranes of the chloroplasts1. Several light-harvesting antenna complexes are organized precisely in the PSII macrostructure—the major trimeric complexes (LHCII)2 that bind 70% of PSII chlorophyll and three minor monomeric complexes3—which together form PSII supercomplexes4,5,6. The antenna complexes are essential for collecting sunlight and regulating photosynthesis7,8,9, but the relationship between these functions and their molecular architecture is unresolved. Here we report that antisense Arabidopsis plants lacking the proteins that form LHCII trimers10 have PSII supercomplexes with almost identical abundance and structure to those found in wild-type plants. The place of LHCII is taken by a normally minor and monomeric complex, CP26, which is synthesized in large amounts and organized into trimers. Trimerization is clearly not a specific attribute of LHCII. Our results highlight the importance of the PSII macrostructure: in the absence of one of its main components, another protein is recruited to allow it to assemble and function.

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Figure 1: PSII membrane composition.
Figure 2: PSII membrane spectra.
Figure 3: Average projections of the PSII complexes from Arabidopsis Lhcb2 plants.
Figure 4: Final result of image analysis of two-dimensional crystalline PSII complexes from Arabidopsis wild-type and Lhcb2 antisense plants.

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References

  1. Hankamer, B., Barber, J. & Boekema, E. J. Structure and membrane organisation of photosystem II in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 641–671 (1997)

    Article  CAS  Google Scholar 

  2. Kühlbrandt, W. & Wang, D. N. Three dimensional structure of plant light-harvesting complex by electron crystallography. Nature 350, 130–134 (1991)

    Article  ADS  Google Scholar 

  3. Peter, G. F. & Thornber, J. P. Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J. Biol. Chem. 266, 16745–16754 (1991)

    CAS  PubMed  Google Scholar 

  4. Boekema, E. J., Van Roon, H., Calkoen, F., Bassi, R. & Dekker, J. P. Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38, 2233 (1999)

    Article  CAS  Google Scholar 

  5. Boekema, E. J., Van Roon, H., Van Breemen, J. F. L. & Dekker, J. P. Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur. J. Biochem. 266, 444–452 (1999)

    Article  CAS  Google Scholar 

  6. Nield, J., Orlova, E. V., Morris, E. P., Gowen, B., Van Heel, M. & Barber, J. 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nature Struct. Biol. 7, 44–47 (2000)

    Article  CAS  Google Scholar 

  7. Jansson, S. The light-harvesting chlorophyll a/b-binding proteins. Biochim. Biophys. Acta 1184, 1–19 (1994)

    Article  CAS  Google Scholar 

  8. Paulsen, H. Chlorophyll a/b binding proteins. Photochem. Photobiol. 62, 367–382 (1995)

    Article  CAS  Google Scholar 

  9. Horton, P., Ruban, A. V. & Walters, R. G. Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655–684 (1996)

    Article  CAS  Google Scholar 

  10. Andersson, J. et al. Absence of the main light harvesting complex of photosystem II affects photosynthetic function. Plant J. (in the press)

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

    Article  CAS  Google Scholar 

  12. Zouni, A. Crystal structure of photosystem II from Synechoccus elongatus at 3.8 Å resolution. Nature 409, 739–743 (2001)

    Article  ADS  CAS  Google Scholar 

  13. Boekema, E. J., Van Breemen, J. F. L., Van Roon, H. & Dekker, J. P. Arrangement of photosystem II in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J. Mol. Biol. 301, 1123–1133 (2000)

    Article  CAS  Google Scholar 

  14. Hankamer, B. et al. Isolation and characterization of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. Eur. J. Biochem. 243, 422–429 (1997)

    Article  CAS  Google Scholar 

  15. Allen, J. F. & Forsberg, J. Molecular recognition in thylakoid structure and function. Trends Plant Sci. 6, 317–326 (2001)

    Article  CAS  Google Scholar 

  16. 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)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  18. Croce, R., Canino, G., Ros, F. & Bassi, R. Chromophore organisation in the higher plant photosystem II antenna protein CP26. Biochemistry 41, 7334–7343 (2002)

    Article  CAS  Google Scholar 

  19. Yakushevska, A. E. et al. Supramolecular organisation of photosystem II and its associated light harvesting antenna in Arabidopsis thaliana. Eur. J. Biochem. 268, 6020–6028 (2001)

    Article  CAS  Google Scholar 

  20. Caffrari, S., Croce, R., Cattivelli, L. & Bassi, R. The Lhcb1, 2 and 3 gene products, components of the trimeric antenna complex of higher plant photosystem II, have distinct biochemical and spectroscopic properties. Proc. 12th Int. Congr. Photosyn., S31–034 (CSIRO, Canberra, 2001)

  21. Hobe, S., Foster, R., Klingler, J. & Paulsen, H. N-proximal sequence motif in light-harvesting chlorophyll-a/b-binding protein is essential for trimerisation of the light harvesting chlorophyll a/b complex. Biochemistry 34, 10224–10228 (1995)

    Article  CAS  Google Scholar 

  22. Kuttkat, A., Kartmann, A., Hobe, S. & Paulsen, H. The C-terminal domain of light-harvesting chlorophyll-a/b-binding protein is involved in the stabilisation of trimeric light harvesting complex. Eur. J. Biochem. 242, 288–292 (1996)

    Article  CAS  Google Scholar 

  23. Garab, G. & Mustardy, L. Role of LHCII-containing macrodomains in the structure, function and dynamics of grana. Aust. J. Plant Physiol. 27, 648–658 (1999)

    Google Scholar 

  24. Bibby, T., 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 

  25. 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 

  26. Walters, R. G., Rogers, J. J. M., Shephard, F. & Horton, P. Acclimation of Arabidopsis thaliana to the light environment: the role of photoreceptors. Planta 209, 517–527 (1999)

    Article  CAS  Google Scholar 

  27. Berthold, D. A., Babcock, G. T. & Yocum, C. F. A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron transport properties. FEBS Lett. 134, 231–234 (1981)

    Article  CAS  Google Scholar 

  28. Ruban, A. V., Lee, P. J., Wentworth, M., Young, A. J. & Horton, P. Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes. J. Biol. Chem. 274, 10458–10465 (1999)

    Article  CAS  Google Scholar 

  29. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685 (1970)

    Article  ADS  CAS  Google Scholar 

  30. Andersson, J., Walters, R. G., Horton, P. & Jansson, S. Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13, 1193–1204 (2001)

    Article  CAS  Google Scholar 

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Acknowledgements

We wish to thank R. Walters for discussions. This work was supported by the UK Biotechnology and Biological Sciences Research Council, the UK Joint Infrastructure Fund, the Netherlands Foundation for Scientific Research (NWO) through the Foundation for Life and Earth Sciences (ALW), and the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning and the Foundation for Strategic Research.

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Correspondence to P. Horton.

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Ruban, A., Wentworth, M., Yakushevska, A. et al. Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421, 648–652 (2003). https://doi.org/10.1038/nature01344

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