Photosynthesis Research

, Volume 86, Issue 1–2, pp 251–262

Relevance of the Diastereotopic Ligation of Magnesium Atoms of Chlorophylls in the Major Light-harvesting Complex II (LHC II) of Green Plants

Regular Paper

Abstract

The recent high-resolution crystal structure of LHC II [Liu et al. (2004) Nature 428: 287–292] makes possible an unprecedented insight into the stereochemical features of how chlorophylls (Chl)s are bound. The diastereotopic ligation generates four structurally different pigment types, two Chl a and two Chl b, which are distinguished not only by the groups in the 7-position (methyl in Chl a and formyl in Chl b) but also by the face of the tetrapyrrole to which the fifth magnesium ligand is bound. Within a LHC II monomer, out of the eight Chl a six have a ‚normal’ α-coordination and two are β-coordinated while out of the six Chl b only one has the ‚special’ β-coordination. In Photosystem I where a more meaningful statistical analysis could be made, out of 96 Chl a only 14 are β-coordinated, again indicating a preference for the ‚normal’ α-coordination [Balaban et al. (2002) Biochim Biophys Acta Bioenerget 1556: 197–207; Oba and Tamiaki (2002a) Photosynth Res 74: 1–10]. Astonishingly, all the special β-Chls are part of the stromal ring of Chls within the LHC II trimers and occupy key positions for the excitation energy transfer. Sequential energy traps are engineered with one hetero- and three homo-dimers. A careful pairing of carotenoids with the special β-Chls, which could quench their triplet states efficiently, implies a functional relevance of this diastereotopic ligation.

Keywords

absorption carotenoid chlorophyll a chlorophyll b energy transfer fluorescence light-harvesting X-ray diffraction 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Balaban, TS 2003Are syn ligated (bacterio)chlorophyll dimers energetic traps in light-harvesting systems?FEBS Lett54597102 [Erratum FEBS Lett 547 In: 235]CrossRefPubMedGoogle Scholar
  2. Balaban, TS 2004

    Light-harvesting nanostructures

    Nalwa, HS eds. Encyclopedia of Nanoscience and NanotechnologyAmerican Scientific PublishersLos Angeles505559
    Google Scholar
  3. Balaban, TS, Holzwarth, AR, Schaffner, K 1995Circular dichroism study of the diastereoselective self-assembly of bacteriochlorophyll cSJ Mol Struct349183186CrossRefGoogle Scholar
  4. Balaban TS, Eichhöfer A and Lehn J-M (2000) Self-assembly by hydrogen bonding and π–π interactions in the crystal of a porphyrin – attempts to mimic bacteriochlorophyll c. Eur J Org Chem: 4047–4057Google Scholar
  5. Balaban, TS, Fromme, P, Holzwarth, AR, Krauß, N, Prokhorenko, VI 2002Relevance of the diastereotopic ligation of magnesium atoms of chlorophylls of Photosystem IBiochim Biophys Acta Bioenerget1556197207CrossRefGoogle Scholar
  6. Bassi, R, Croce, R, Cugini, D, Santona, D 1999Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sitesProc Natl Acad Sci USA961005610061CrossRefPubMedGoogle Scholar
  7. Ben-Shem, A, Frolow, F, Nelson, N 2003Crystal structure of plant Photosystem INature426630635PubMedGoogle Scholar
  8. Brabec, CJ, Sariciftci, NS, Hummelen, JC 2001Plastic solar cellsAdv Funct Mater111526CrossRefGoogle Scholar
  9. Collman, JP, Boulatov, R, Sutherland, CJ 2003

    Functional and structural analogs of the dioxygen reduction site in terminal oxidases

    Kadish, KMSmith, KMGuilard, R eds. The Porphyrin Handbook Vol. 11/Bioinorganic and Bioorganic ChemistryAcademic PressAmsterdam, The Netherlands149
    Google Scholar
  10. Croce, R, Müller, MG, Caffari, S, Bassi, R, Holzwarth, AR 2003Energy transfer pathways in the minor antenna complex CP29 of Photosystem II: a femtosecond study of carotenoid to chlorophyll transfer on mutant and WT complexesBiophys J8425172532PubMedGoogle Scholar
  11. Davidov, AS 1971Theory of Molecular ExcitonsPlenum PressNew YorkGoogle Scholar
  12. Ferreira, KN, Iverson, TN, Maghlaoui, K, Barber, J, Iwata, S 2004Architecture of the photosynthetic oxygen-evolving centerScience30318311838PubMedGoogle Scholar
  13. Förster, Th. 1948Zwischenmolekulare Energiewanderung und FluoreszenzAnn Phys (Leipzig)25575Google Scholar
  14. Frank, HA, Cogdell, RJ 1996Carotenoids in photosynthesis. PhotochemPhotobiol 3257264Google Scholar
  15. HyperChem® Release 7, (2002) Hypercube Inc. Gainesville, Florida, Publication HC70–00–01–00Google Scholar
  16. Jang, S, Newton, MD, Silbey, RJ 2004Multichromophoric Förster resonance energy transferPhys Rev Lett92218301-12183014Google Scholar
  17. Jordan, P, Fromme, P, Witt, H-T, Klukas, O, Saenger, W, Krauss, N 2001Three-dimensional structure of cyanobacterial Photosystem I at 2.5 Å resolutionNature411909917PubMedGoogle Scholar
  18. Kleima, FJ, Hobe, S, Calkoen, F, Urbanus, ML, Peterman, EJG, Grondelle, R, Paulsen, H, Amerongen, H 1999Decreasing the chlorophyll a/b ratio in reconstituted LHCII: structural and functional consequencesBiochemistry3865876596CrossRefPubMedGoogle Scholar
  19. Koepke, J, Hu, X, Muenke, C, Schulten, K, Michel, H 1996The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianumStructure4581597PubMedGoogle Scholar
  20. Kolb, HC, Nieuwenhze, MS, Sharpless, KB 1994Catalytic asymmetric dihydroxylationChem Rev9424832547CrossRefGoogle Scholar
  21. Kräutler B (1998) B12 Coenzymes, the central theme. In: Kräutler B, Arigoni D and Golding BT (eds) Vitamin B12 and B12)Proteins, Wiley-VCH, WeinheimGoogle Scholar
  22. Kühlbrandt, W, Wang, DN, Fujiyoshi, Y 1994Atomic model of plant light-harvesting complex by electron crystallographyNature367614621PubMedGoogle Scholar
  23. Liu, Z, Yan, H, Wang, K, Kuang, T, Zhang, J, Gui, L, An, X, Chang, W 2004Crystal structure of spinach major light-harvesting complex at 2.72 Å resolutionNature428287292PubMedGoogle Scholar
  24. McDermott, G, Prince, SM, Freer, AA, Hawthornthwaite-Lawless, AM, Papiz, MZ, Cogdell, RJ, Isaacs, NW 1995Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteriaNature374517521CrossRefGoogle Scholar
  25. McLuskey, K, Prince, SM, Cogdell, RJ, Isaacs, NW 2001The crystallographic structure of the B800–820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050Biochemistry4087838789PubMedGoogle Scholar
  26. Moss GP (1987) Nomenclature of tetrapyrroles. Pure Appl Chem 59: 779–832; Moss GP (1988) Eur J Biochem 178: 277–328; WWW edition: http://www.chem.qmul.ac.uk/iupac/ tetrapyr role, Sections TP−8.1 and TP−8.2
  27. Oba, T, Tamiaki, H 2002aWhich side of the π-macrocycle plane of (bacterio)chlorophylls is favored for binding the fifth ligand?Photosynth Res74110CrossRefGoogle Scholar
  28. Oba, T, Tamiaki, H. 2002bCoordination chemistry of chlorophylls: which side of the chlorin macrocycle is favored for the ligand coordination?J Photosci9362363Google Scholar
  29. Papiz, MZ, Prince, SM, Howard, T, Cogdell, RJ, Isaacs, NW 2003The structure and thermal motion of the B800–850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 100 K: new structural features and functionally relevant motionsJ Mol Biol32615231538CrossRefPubMedGoogle Scholar
  30. Pascal, A, Caffari, S, Croce, R, Sandona, D, Bassi, R, Robert, B 2002A structural investigation of the central chlorophyll a binding sites in the minor Photosystem II antennaprotein, Lhcb4Biochemistry4123052310CrossRefPubMedGoogle Scholar
  31. Remelli, R, Varotto, C, Sandonà, D, Croce, R, Bassi, R 1999Chlorophyll binding to monomeric light-harvesting complex. A mutation analysis of chromophore-binding residuesJ Biol Chem2743351033521CrossRefPubMedGoogle Scholar
  32. Roszak, AW, Howard, TD, Southall, J, Gardiner, AT, Law, CJ, Isaacs, NW, Cogdell, RJ 2003Crystal structure of the RC-LH 1 core complex from Rhodopseudomonas palustrisScience30219691972PubMedGoogle Scholar
  33. Schmidt, VHR, Thomé, P, Rühle, W, Paulsen, H, Kühlbrandt, W, Rogl, H 2001Chlorophyll b is involved in long-wavelength spectral properties of light-harvesting complexes LHC I and LHC IIFEBS Lett4992731CrossRefPubMedGoogle Scholar
  34. van Amerongen, H, van Grondelle, R 2001Understanding the energy transfer function of LHC II, the major light-harvesting complex of green plantsJ Phys Chem B105604617CrossRefGoogle Scholar
  35. Watanabe, T, Kobayashi, M, Hongu, A, Oba, T 1992Difference between chlorophylls a and a′ in the intermolecular association behavior. Visible absorption and circular dichroism spectral features in aqueous methanolChem Lett918471850Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  1. 1.Forschungszentrum KarlsruheInstitute for NanotechnologyKarlsruheGermany

Personalised recommendations