A theoretical investigation of the photophysical consequences of major plant light-harvesting complex aggregation within the photosynthetic membrane

Journal of Physical Chemistry B

Volumn 114, Issue 46, 2010, Pages 15244-15253

  Duffy, C D P ^a   Johnson, M P ^a   MacErnis, M ^b   Valkunas, L ^b   Barford, W ^c   Ruban, A V ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b VILNIUS UNIVERSITY   (Lithuania)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION; ABSORPTION SPECTROSCOPY; BINDING ENERGY; DIMERS; GEOMETRY; PHOTOSYNTHETIC MEMBRANES; PLANTS (BOTANY);

ABSORPTION CHANGES; ARABIDOPSIS LEAVES; BLUE SHIFT; ENERGY DEPENDENT; EXCITONIC COUPLING; EXCITONIC INTERACTION; HOMODIMERS; LIGHT-HARVESTING COMPLEX; LIGHT-HARVESTING COMPLEX II; MEMBRANE THICKNESS; NON-PHOTOCHEMICAL QUENCHING; PHOTOPHYSICAL; RED SHIFT; RELATIVE GEOMETRY; SPECTRAL SHIFT; SPECTROSCOPIC MEASUREMENTS; SPECTROSCOPIC SIGNATURES; THEORETICAL INVESTIGATIONS; TIME DEPENDENT DENSITY FUNCTIONAL THEORY; ZEAXANTHIN;

DENSITY FUNCTIONAL THEORY;

EID: 78649553229     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp106234e     Document Type: Article

References (64)

1. Liu, Z.; Yan, H.; Wang, K.; Kuang, T.; Zhang, J.; Gui, L.; An, X.; Chang, W. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 2004, 428, 287-292
2. Standfuss, J.; Terwisscha van Sceltinga, A. C.; Lamborghini, M.; Kuhlbrandt, W. Mechanisms of photoprotection and non-photochemical quenching in pea light-harvesting complex at 2.5 Å resolution EMBO J. 2005, 24, 919-928
3. Niyogi, K.; Li, X.; Li, Z.; Anwaruzzanman, M.; Ledford, H.; Chin, B.; Wakao, S.; Fischer, B. Sensing and responding to high light stress Photosynth. Res. 2007, 91, 284
4. Horton, P.; Ruban, A. V.; Walters, R. G. Regulation of Light Harvesting in Green Plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47, 655-684
5. Holt, N. E.; Fleming, G. R.; Niyogi, K. K. Toward an understanding of the mechanism of nonphotochemical quenching in green plants Biochem. 2004, 43, 8281-8289
6. Horton, P.; Ruban, A. V. Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection J. Exp. Bot. 2005, 56, 365-373
7. Ma, Y. Z.; Holt, N. E.; Li, X. P.; Niyogi, K. K.; Fleming, G. R. Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 4377-4382
8. Holt, N. E.; Zigmantas, D.; Valkunas, L.; Li, X. P.; Niyogi, K. K.; Fleming, G. R. Carotenoid cation formation and the regulation of photosynthetic light harvesting Science 2005, 307, 433-436
9. Ahn, T. K.; Avenson, T. J.; Ballottari, M.; Cheng, Y. C.; Niyogi, K. K.; Bassi, R.; Fleming, G. R. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein Science 2008, 320, 794-797
10. Ruban, A. V.; Berera, R.; Ilioaia, C.; van Stokkum, I. H.; Kennis, J. T.; Pascal, A. A.; van Amerongen, H.; Robert, B.; Horton, P.; van Grondelle, R. Identification of a mechanism of photoprotective energy dissipation in higher plants Nature 2007, 450, 575-578
11. Bode, S.; Quentmeier, C. C.; Liao, P. N.; Hafi, N.; Barros, T.; Wilk, L.; Bittner, F.; Walla, P. J. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 12311-12316
12. Muller, M. G.; Lambrev, P.; Reus, M.; Wientjes, E.; Croce, R.; Holzwarth, A. R. Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids ChemPhysChem. 2010, 11, 1289-1296
13. Briantais, J. M.; Vernotte, C.; Picaud, M.; Krause, G. H. Quantitative Study of the Slow Decline of Chlorophyll α-Fluorescence in Isolated-Chloroplasts Biochim. Biophys. Acta 1979, 548, 128-138
14. Li, X. P.; Gilmore, A. M.; Caffarri, S.; Bassi, R.; Golan, T.; Kramer, D.; Niyogi, K. K. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein J. Biol. Chem. 2004, 279, 22866-22874
15. Walters, R. G.; Ruban, A. V.; Horton, P. Higher-Plant Light-Harvesting Complexes LHCIIa and LHCIIc Are Bound by Dicyclohexylcarbodiimide during Inhibition of Energy-Dissipation Eur. J. Biochem. 1994, 226, 1063-1069
16. Walters, R. G.; Ruban, A. V.; Horton, P. Identification of proton-active residues in a higher plant light-harvesting complex Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 14204-14209
17. Jahns, P.; Latowski, D.; Strzalka, K. Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids Biochim. Biophys. Acta 2009, 1787, 3-14
18. Horton, P.; Ruban, A. V.; Rees, D.; Pascal, A. A.; Noctor, G.; Young, A. J. Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex FEBS Lett. 1991, 292, 1-4
19. Horton, P.; Wentworth, M.; Ruban, A. V. Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching FEBS Lett. 2005, 579, 4201-4206
20. Bilger, W.; Bjorkman, O.; Thayer, S. S. Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves Plant Physiol. 1989, 91, 542-551
21. Bilger, W.; Bjorkman, O. Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and nonphotochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.) Planta 1994, 193, 238-246
22. Ruban, A. V.; Young, A. J.; Horton, P. Induction of Nonphotochemical Energy Dissipation and Absorbance Changes in Leaves (Evidence for Changes in the State of the Light-Harvesting System of Photosystem II in Vivo) Plant Physiol. 1993, 102, 741-750
23. Johnson, M. P.; Perez-Bueno, M. L.; Zia, A.; Horton, P.; Ruban, A. V. The zeaxanthin-independent and zeaxanthin-dependent qE components of nonphotochemical quenching involve common conformational changes within the photosystem II antenna in Arabidopsis Plant Physiol. 2009, 149, 1061-1075
24. Pascal, A. A.; Liu, Z.; Broess, K.; van Oort, B.; van Amerongen, H.; Wang, C.; Horton, P.; Robert, B.; Chang, W.; Ruban, A. Molecular basis of photoprotection and control of photosynthetic light-harvesting Nature 2005, 436, 134-137
25. Horton, P.; Johnson, M. P.; Perez-Bueno, M. L.; Kiss, A. Z.; Ruban, A. V. Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states FEBS J. 2008, 275, 1069-1079
26. Murakami, S.; Packer, L. Protonation and Chloroplast Membrane Structure J. Cell Biol. 1970, 47, 332-351
27. Ruban, A. V.; Horton, P.; Young, A. J. Aggregation of higher plant xanthophylls: differences in absorption spectra and in the dependency on solvent polarity J. Photochem. Photobiol., B 1993, 21, 229-234
28. Ruban, A. V.; Pascal, A. A.; Robert, B.; Horton, P. Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting J. Biol. Chem. 2002, 277, 7785-7789
29. Li, X. P.; Bjorkman, O.; Shih, C.; Grossman, A. R.; Rosenquist, M.; Jansson, S.; Niyogi, K. K. A pigment-binding protein essential for regulation of photosynthetic light harvesting Nature 2000, 403, 391-395
30. Bonente, G.; Howes, B. D.; Caffarri, S.; Smulevich, G.; Bassi, R. Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro J. Biol. Chem. 2008, 283, 8434-8445
31. Johnson, M. P.; Ruban, A. V. Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation Plant J. 2010, 61, 283-289
32. Ruban, A. V. Identification of carotenoids in photosynthetic proteins: Xanthophylls of the light harvesting antenna. In Carotenoids: Physical, Chemical, and Biological Functions and Properties; CRC Press: Boca Raton, FL, 2009.
33. Davydov, A. S. The theory of molecular excitons Sov. Phys. Usp. 1964, 7, 145
34. Heisenberg, W. Mehrkörperproblem und Resonanz in der Quantenmechanik Z. Phys. 1926, 38, 411-426
35. Dirac, P. A. M. On the Theory of Quantum Mechanics Proc. R. Soc. London A 1926, 112, 661-677
36. Rabi, I. I.; Millman, S.; Kusch, P.; Zacharias, J. R. A new method of measuring nuclear magnetic moments Phys. Rev. 1938, 53, 318
37. Rabi, I. I.; Millman, S.; Kusch, P.; Zacharias, J. R. The molecular beam resonance method for measuring nuclear magnetic moments. The magnetic moments of Li6, Li7 and F19 Phys. Rev. 1939, 55, 526
38. Altshuler, B. L.; Aronov, A. G.; Khmelnitsky, D. E. Effects of electron-electron collisions with small energy transfers on quantum localization J. Phys. C 1982, 15, 7367-7386
39. Redfield, A. G. On the theory of relaxation processes IBM J. Res. Dev. 1957, 1, 19-31
40. Förster, T. Zwischenmolekulare Energiewanderung und Fluoreszenz Ann. Phys. 1948, 437, 55
41. Chang, J. C. Monopole effects on electronic excitation interactions between large molecules. 1. Application to energy transfer in chlorophylls J. Chem. Phys. 1977, 67, 3901-3909
42. Krueger, B. P.; Scholes, G. D.; Flemming, G. R. Calculation of couplings and energy-transfer pathways between the pigments of LH2 by the ab initio transition density cube method J. Phys. Chem. B 1998, 102, 5378-5386
43. Dreuw, A.; Harbach, P. H. P.; Mewes, J. M.; Wormit, M. Quantum chemical excited state calculations on pigment-protein complexes require thorough geometry re-optimization of experimental crystal structures Theor. Chem. Acc. 2010, 125, 419-426]
44. Curutchet, C.; Munoz-Losa, A.; Monti, S.; Kongsted, J.; Scholes, D. G. Electronic energy transfer in condensed phase studied by a polarisable QM/MM model J. Chem. Theor. Comput. 2009, 5, 1838
45. Neugebauer, J.; Curuchet, C.; Munos-Losa, A.; Mennucci, B. A subsystem TDDFT approach for solvent screening effects on excitation energy transfer couplings J. Chem. Theor. Comput. 2010, 6, 1843
46. Hohenberg, P.; Kohn, W. Inhomogeneous electron gas Phys. Rev. 1964, 136, 864-871
47. Kohn, W.; Sham, L. J. Self-consistent equations including exchange and correlation effects Phys. Rev. 1965, 140, 1133-1138
48. Becke, A. D. A new mixing of Hartree-Fock and local density-functional theories J. Chem. Phys. 1993, 98, 1372-1377
49. Haharan, P. C.; Pople, J. A. The Influence of Polarization Functions on Molecular Orbital Hydrogenation Energies Theor. Chim. Acta 1973, 28, 213
50. Schulten, K.; Ohmine, I.; Karplus, M. Correlation effects in the spectra of polyenes J. Chem. Phys. 1976, 64, 4422-4441
51. Barford, W. Electronic and optical properties of conjugated polymers. International series of monographs on physics, Vol. 129; Oxford Science Publications: New York, 2005.
52. Foresman, J. B.; Head-Gordon, M.; Pople, J. A. Toward a systematic molecular orbital theory for excited states J. Phys. Chem. 1992, 96, 135-149
53. Runge, E.; Gross, E. K. U. Density-functional theory for time-dependent systems Phys. Rev. Lett. 1984, 52, 997-1000
54. Gross, E. K. U.; Kohn, W. Local density functional theory of frequency-dependent linear response Phys. Rev. Lett. 1985, 55, 2850
55. Roos, B. O.; Taylor, P. R.; Siegbhan, P. E. M. A complete active space SCF method (CASSCF) using a density matrix formulated super-CI approach Chem. Phys. 1980, 48, 157-173
56. Casida, M. E. Time-dependent density-functional response theory for molecules. In Recent advances in density functional methods, Part I; Chong, D. P., Ed.; World Scientific: Singapore, 1995.
57. Yanai, T.; Tew, D. P.; Handy, N. C. A new exchange-correlation functional using the Coulomb attenuated method (CAM-B3LYP) Chem. Phys. Lett. 2004, 393, 51-57
58. Dunning, T. H., Jr. Gaussian Basis Sets for Use in Correlated Molecular Calculations. I. The Atoms Boron through Neon and Hydrogen Chem. Phys. 1989, 90, 1007-1023
59. Ruban, A. V.; Pascal, A. A.; Robert, B.; Horton, P. Configuration and dynamics of xanthophylls in light-harvesting antennae of higher plants. Spectroscopic analysis of isolated light-harvesting complex of photosystem II and thylakoid membranes J. Biol. Chem. 2001, 276, 24862-24870
60. Gradinaru, C. C.; van Stokkum, I. H. M.; Pascal, A. A.; van Grondelle, R.; van Amerongen, H. Identifying the pathways of energy transfer between carotenoids and chlorophylls in LHCII and CP29. A multi-color, femtosecond pump-probe study J. Phys. Chem. B 2000, 104, 9330-9342
61. Novoderezhkin, V. I.; Palacios, M. A.; van Amerongen, H.; van Grondelle, R. Excitation dynamics in the LHCII complex of higher plants: Modeling based on the 2.72 Å crystal structure J. Phys. Chem. B 2005, 109, 10493-10504
62. Ruban, A. V.; Calkoen, F.; Kwa, S. L. S.; van Grondelle, R.; Horton, P.; Dekker, J. P. Characterisation of LHC II in the aggregated state by linear and circular dichroism spectroscopy Biochim. Biophys. Acta 1997, 1321, 61-70
63. Ruban, A. V.; Pascal, A. A.; Lee, P. J.; Robert, B.; Horton, P. Molecular configuration of xanthophyll cycle carotenoids in photosystem II antenna complexes J. Biol. Chem. 2002, 277, 42937-42942
64. 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. 1999, 274, 10458-10465