Photosynthesis Research

, Volume 61, Issue 1, pp 77–90

Structural and functional heterogeneity in the major light-harvesting complexes of higher plants

Article

Abstract

The major light-harvesting complex (LHC IIb) of higher plants plays a crucial role in capturing light energy for photosynthesis and in regulating the flow of energy within the photosynthetic apparatus. Multiple isoforms of the protein bind chlorophyll and xanthophyll chromophores, but it is commonly believed that the pigment-binding properties of different LHC IIb complexes are conserved within and between species. We have investigated the structure and function of different LHC IIb complexes isolated from Arabidopsis thaliana grown under different light conditions. LHC IIb isolated from low light-grown plants shows increased amounts of the Lhcb2 gene product, increased binding of chlorophyll a, and altered energy transfer characteristics. We suggest that Lhcb2 specifically binds at least one additional chlorophyll a compared to the Lhcb1 gene product, and that differences in the functioning of LHC IIb from high and low light-grown plants are a direct consequence of the change in polypeptide composition. We show that changes in LHC IIb composition are accompanied by changes in photosynthetic function in vivo and discuss the possible functional significance of LHC IIb heterogeneity.

acclimation chlorophyll fluorescence LHC II energy dissipation 

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References

  1. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys Acta 1098: 275–335PubMedGoogle Scholar
  2. Anderson JM and Osmond CB (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 1–38. Elsevier, AmsterdamGoogle Scholar
  3. Beauregard M, Martin I and Holzwarth AR (1991) Kinetic modelling of exciton migration in photosynthetic systems: 1. Effects of pigment heterogeneity and antenna topography on exciton kinetics and charge separation yields. Biochim Biophys Acta 1060: 271–283Google Scholar
  4. Burke JJ, Ditto CL and Arntzen CJ (1978) Involvement of the lightharvesting complex in cation regulation of energy distribution in chloroplasts. Arch Biochem Biophys 187: 252–263PubMedGoogle Scholar
  5. Dau H and Sauer K (1996) Exciton equilibration and Photosystem II exciton dynamics – a fluorescence study on Photosystem II membrane particles of spinach. Biochim Biophys Acta 1273: 175–190Google Scholar
  6. Flachmann R and Kühlbrandt W (1995) Accumulation of plant antenna complexes is regulated by post-transcriptional mechanisms in tobacco. Plant Cell 7: 149–160PubMedGoogle Scholar
  7. Flachmann R and Kühlbrandt W (1996) Crystallisation and identification of an assembly defect of recombinant antenna complexes produced in transgenic tobacco plants. Proc Natl Acad Sci USA 93: 14966–14971PubMedGoogle Scholar
  8. Genetics Computer Group (1994) Program Manual for the Wisconsin Package (Genetics Computer Group, Madison, WI), Version 8Google Scholar
  9. Giuffra E, Zucchelli G, Sandona D, Croce R, Cugini D, Garlaschi FM, Bassi R and Jennings RC (1997) Analysis of some optical properties of a native and reconstituted Photosystem II antenna complex, CP29: Pigment binding sites can be occupied by chlorophyll a or chlorophyll b and determine spectral forms. Biochemistry 36: 12984–12993PubMedGoogle Scholar
  10. Hankamer B, Barber J and Boekema EJ (1997) Structure and membrane organisation of Photosystem II in green plants. Annu Rev Plant Physiol Plant Mol Biol 48: 641–671PubMedGoogle Scholar
  11. Hare PE, St John PA and Engel MH (1985) Ion exchange separation of amino acids. In: Barrett GC (ed) Chemistry and Biochemistry of the Amino Acids, pp 414–425. Chapman & Hall, LondonGoogle Scholar
  12. Hobe S, Foster R, Klingler J and Paulsen H (1995) N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34: 10224–10228PubMedGoogle Scholar
  13. Horton P, Ruban AV and Walters RG (1996) Regulation of lightharvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47: 655–684PubMedGoogle Scholar
  14. Hunt S (1985) Degradation of amino acids accompanying in vitro protein hydrolysis. In: Barrett GC (ed) Chemistry and Biochemistry of the Amino Acids, pp 376–398. Chapman & Hall, LondonGoogle Scholar
  15. Hunter CN, Artymiuk PJ and van Amerongen H (1994) Many chlorophylls make light work. Curr Biol 4: 344–346PubMedGoogle Scholar
  16. Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184: 1–19PubMedGoogle Scholar
  17. Jansson S and Gustafsson P (1990) Type I and Type II genes for the chlorophyll a/b-binding protein in the gymnosperm Pinus Sylvestris (Scots Pine) – cDNA cloning and sequence analysis. Plant Mol Biol 14: 287–296PubMedGoogle Scholar
  18. Jansson S, Selstam E and Gustafsson P (1990) The rapidly phosphorylated 25 kDa polypeptide of the light-harvesting complex of Photosystem II is encoded by the Type 2 cab-II genes. Biochim Biophys Acta 1019: 110–114PubMedGoogle Scholar
  19. Johnson GN, Young AJ, Scholes JD and Horton P (1993) The dissipation of excess excitation energy in British plant species. Plant Cell Environ 16: 673–679Google Scholar
  20. Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621CrossRefPubMedGoogle Scholar
  21. Leutwiler LS, Meyerowitz EM and Tobin EM (1986) Structure and expression of 3 light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res 14: 4051–4064PubMedGoogle Scholar
  22. Mäenpää P and Andersson B (1989) Photosystem II heterogeneity and long-term acclimation of light-harvesting. Z Naturforsch 44C: 403–406Google Scholar
  23. McGrath JM, Terzghi WB, Sridhar P, Cashmore AR and Pichersky E (1992) Sequence of the 4th and 5th Photosystem II Type I chlorophyll a/b-binding protein genes of Arabidopsis thaliana and evidence for the presence of a full complement of the extended cab gene family. Plant Mol Biol 19: 725–733PubMedGoogle Scholar
  24. Mullineaux CW, Pascal AA, Horton P and Holzwarth AR (1993) Excitation-energy quenching in aggregates of the LHC II chlorophyll-protein complex: A time-resolved fluorescence study. Biochim Biophys Acta 1141: 23–28Google Scholar
  25. Murchie EH and Horton P (1997) Acclimation of photosynthesis to irradiance and spectral quality in British plant species: Chlorophyll content, photosynthetic capacity and habitat preference. Plant Cell Environ 20: 438–448Google Scholar
  26. Nussberger S, Dörr K, Wang DN and Kühlbrandt W (1993) Lipidprotein interactions in crystals of plant light-harvesting complex. J Mol Biol 234: 347–356PubMedGoogle Scholar
  27. Nussberger S, Dekker JP, Kühlbrandt W, van Bolhuis BM, van Grondelle R and van Amerongen H (1994) Spectroscopic characterisation of three different monomeric forms of the main chlorophyll a/b binding protein from chloroplast membranes. Biochemistry 33: 14775–14783PubMedGoogle Scholar
  28. Porra RJ, Thompson WA and Kriedemann PE (1989) 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: 384–394Google Scholar
  29. Ruban AV and Horton P (1992) Mechanism of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes. I. Spectroscopic analysis of isolated light-harvesting complexes. Biochim Biophys Acta 1102: 30–38Google Scholar
  30. Ruban AV, Rees D, Noctor G, Young AJ and Horton P (1991) Long wavelength chlorophyll species are associated with amplification of high-energy-state excitation quenching in higher plants. Biochim Biophys Acta 1059: 355–360Google Scholar
  31. Ruban AV, Young AJ, Pascal AA and Horton P (1994) The effects of illumination on the xanthophyll composition of the Photosystem II light-harvesting complexes of spinach thylakoid membranes. Plant Physiol 104: 227–234PubMedGoogle Scholar
  32. Schatz GH, Brock H and Holzwarth AR (1988) Kinetic and energetic model for the primary processes in Photosystem II. Biophys J 54: 397–405Google Scholar
  33. Singrist M and Staehlin LA (1992) Identification of type 1 and type 2 light-harvesting chlorophyll a/b-binding proteins using monospecific antibodies. Biochim Biophys Acta 1098: 191–200PubMedGoogle Scholar
  34. Spangfort M and Andersson B (1989) Subpopulations of the main chlorophyll a/b light-harvesting complex of Photosystem II – isolation and biochemical characterization. Biochim Biophys Acta 977: 163–170Google Scholar
  35. Walters RG and Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27: 121–133Google Scholar
  36. Walters RG and Horton P (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PS2 fluorescence in barley leaves. Photosynth Res 36: 119–139Google Scholar
  37. Walters RG and Horton P (1994) Acclimation of Arabidopsis thaliana to the light environment: Changes in composition of the photosynthetic apparatus. Planta 195: 248–256Google Scholar
  38. Walters RG and Horton P (1995) Acclimation of Arabidopsis thaliana to the light environment: Changes in photosynthetic function. Planta 197: 306–312PubMedGoogle Scholar
  39. Walters RG, Ruban AV and Horton P (1994) Higher plant lightharvesting complexes LHC IIa and LHC IIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur J Biochem 226: 1063–1069PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  1. 1.Robert Hill Institute, Department of Molecular Biology and BiotechnologyUniversity of SheffieldWestern Bank, SheffieldUK

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