Theory of optical spectra of photosystem II reaction centers: Location of the triplet state and the identity of the primary electron donor

Biophysical Journal

Volumn 88, Issue 2, 2005, Pages 986-998

  Raszewski, Grzegorz ^a   Saenger, Wolfram ^a   Renger, Thomas ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL;

ARTICLE; CIRCULAR DICHROISM; ELECTRON TRANSPORT; ENERGY; FLUORESCENCE; LOW TEMPERATURE; OPTICS; PHOTOSYSTEM II; STRUCTURE ANALYSIS; SYNECHOCOCCUS ELONGATUS; TEMPERATURE DEPENDENCE; THEORY; CHEMICAL MODEL; CHEMISTRY; COMPARATIVE STUDY; COMPUTER SIMULATION; ENERGY TRANSFER; EVALUATION; LIGHT; METHODOLOGY; RADIATION EXPOSURE; SPECTROFLUOROMETRY; STRUCTURE ACTIVITY RELATION; VALIDATION STUDY;

THERMOSYNECHOCOCCUS ELONGATUS;

COMPUTER SIMULATION; ELECTRON TRANSPORT; ENERGY TRANSFER; LIGHT; MODELS, CHEMICAL; PHOTOSYSTEM II PROTEIN COMPLEX; SPECTROMETRY, FLUORESCENCE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 21244494763     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.050294     Document Type: Article

References (60)

1. Barter, L. M. C., J. R. Dun-ant, and D. R. Klug. 2003. A quantitative structure-function relationship for the photosystem II reaction center: supermolecular behavior in natural photosynthesis. Proc. Natl. Acad. Sci. USA. 100:946-951.
2. Biesiadka, J., B. Loll, J. Kern, K. D. Irrgang, and A. Zouni. 2004. Crystal structure of cyanobacterial photosystem II at 3.2 A resolution: a closer look at the Mn-cluster. Phys. Ckem. Chem. Phys. 6:4733-4736.
3. Chang, J. C. 1977. Monopole effects on electronic excitation interactions between large molecules. I. Application to energy transfer in chlorophylls. J. Chem. Phys. 67:3901-3904.
4. Creemers, T. M. H., C. A. De Caro, R. W. Visschers, R. van Grondelle, and S. Völker. 1999. Spectral hole burning and fluorescence line narrowing in subunits of the light-harvesting complex LH1 of purple bacteria. J. Phys. Chem. B. 103:9770-9776.
5. Dekker, J. P., and R. van Grondelle. 2000. Primary charge separation in photosystem II. Photosynth. Res. 63:195-208.
6. Diner, B. A., and F. Rappaport. 2002. Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu. Rev. Plant Biol. 53:55-58.
7. 197 of photosystem II in Synechococcus PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry. 40:9265-9281.
8. Durrant, J. R., L. B. Giorgi, J. Barber, D. R. Klug, and G. Porter. 1990. Characterization of triplet states in isolated photosystem II reaction centres: oxygen quenching as a mechanism for photodamage. Biochemistry. 42:9205-9213.
9. Durrant, J. R., G. Hastings, D. M. Joseph, J. Barber, G. Porter, and D. R. Klug. 1992. Subpicosecond equilibration of excitation energy in isolated photosystem II reaction centers. Proc. Natl. Acad. Sci. USA. 89:11632-11636.
10. Durrant, J. R., D. R. Klug, S. L. S. Kwa, R. van Grondelle, G. Porter, and J. P. Dekker. 1995. A multimer model for P680, the primary electron donor of photosystem II. Proc. Natl. Acad. Sci. USA. 92:4798-4802.
11. Ferreira, K. N., T. M. Iverson, K. Maghlaoui, J. Barber, and S. Iwata. 2004. Architecture of photosynthetic oxygen-evolvine center. Science. 303:1831-1838.
12. Fetisova, Z., A. Freiberg, K. Mauring, V. Novoderezhkin, A. Taisova, and K. Timpmann. 1996. Excitation energy transfer in chlorosomes of green bacteria: theoretical and experimental studies. Biophys. J. 71:995-1010.
13. Frese, R. N., M. Germano, F. L. de Weerd, I. H. M. van Stokkum, A. Y. Shuropatov, V. A. Shuvalov, H. J. van Gorkom, R. van Grondelle, and J. P. Dekker. 2003. Electric field effects on the chlorophylls, pheophytins, and β-carotenes in the reaction center of photosystem II. Biochemistry. 42:9205-9213.
14. Germano, M., A. Y. Shkuropatov, H. Permentier, R. A. Khatypov, V. A. Shuvalov, A. J. Hoff, and H. J. van Gorkom. 2000. Selective replacement of the active and inactive pheophytin in reaction centers of photosystem II by 131-deoxo-131-hydroxy-pheophytin a and comparison of their 6 K absorption spectra. Photosyn. Res. 64:189-198.
15. Germano, M., A. Y. Shkuropatov, H. Permentier, R. WiJn de, A. J. Hoff, V. A. Shuvalov, and H. J. van Gorkom. 2001. Pigment organization and their interactions in reaction centers of photosystem II: optical spectroscopy at 6K of reaction centers with modified pheophytin composition. Biochemistry. 40:11472-11482.
16. Greenfield, S. R., M. Seibert, Govindjee, and M. R. Wasielewski. 1997. Direct measurements of the effective rate constant for primary charge separation in isolated photosystem II reaction centers. J. Phys. Chem. B. 101:2251-2255.
17. x band in isolated photosystem II reaction centers at 7 K: energy transfer and charge separation. J. Phys. Chem. B. 103:8364-8374.
18. Groot, M. L., J. P. Dekker, R. van Grondelle, F. T. H. Den Hartog, and S. Völker. 1996. Energy transfer and trapping in isolated photosystem II reaction centers of green plants at low temperature. A study by spectral hole burning. J. Phys. Chem. 100:11488-11495.
19. Groot, M. L., E. J. G. Peterman, P. J. M. van Kan, I. H. M. van Stokkum, J. P. Dekker, and R. van Grondelle. 1994. Temperature-dependent triplet and fluorescence quantum yields of the photosystem II reaction center described in a thermodynamic model. Biophys. J. 67:318-330.
20. Groot, M., F. van Mourik, C. Eijckelhoff, I. H. M. van Stokkum, J. P. Dekker, and R. van Grondelle. 1997. Charge separation in the reaction center of photosystem II studied as a function of temperature. Proc. Natl. Acad. Sci. USA. 94:4389-4394.
21. Huber, H., M. Meyer, H. Scheer, W. Zinth, and J. Wachtveitl. 1998. Temperature-dependence of the primary electron transfer reaction in pigment-modified bacterial reaction centers. Photosyn. Res. 55:153-162.
22. Jankowiak, R., M. Ratsep, M. Picorel, M. Seibert, and G. J. Small. 1999. Excited states of the 5-chlorophyll photosystem II reaction center. J. Phys. Chem. B. 103:9759-9769.
23. Jankowiak, R., D. Tang, G. J. Small, and M. Seibert. 1989. Transient and persistent hole-burning of the reaction center of photosystem-II. J. Phys. Chem. 93:1649-1654.
24. 559-complex of photosystem II. Ber. Bunsenges. Phys. Chem. 100:2045-2051.
25. Konermann, L., and A. R. Holzwarth. 1996. Analysis of the absorption spectrum of photosystem II reaction centers: temperature-dependence, pigment assignment and inhomogeneous broadening. Biochemistry. 35:829-842.
26. Konermann, L., I. Yruela, and A. R. Holzwarth. 1997. Pigment assignment in the absorption spectrum of the photosystem II reaction center by site-selection fluorescence spectroscopy. Biochemistry. 36:7498-7502.
27. Krawczyk, S. 1991. Electrochromism of chlorophyll-a monomer and special-pair dimer. Biochim. Biophys. Acta. 1056:64-70.
28. Kwa, S. L. S., C. Eijckelhoff, v. Grondelle, and J. P. Dekker. 1994. Site-selection spectroscopy of the reaction center complex of photosystem II. 1. Triplet-minus-singlet absorption difference: search for a second exciton band of P-680y. J. Phys. Chem. 98:7702-7711.
29. Lax, M. 1952. The Franck-Condon principle and its application to crystals. J. Chem. Phys. 20:1752-1760.
30. May, V., and O. Kühn. 2000. Charge and Energy Transfer Dynamics in Molecular Systems: A Theoretical Introduction. Wiley-VCH. Berlin, Germany. 103-113, 137, 203, 233.
31. Merry, S. A. P., S. Kumazaki, Y. Tachibana, D. M. Joseph, G. Porter, K. Yoshihara, J. Barber, J. P. Durrant, and D. R. Klug. 1996. Subpicosecond equilibration of excitation energy in isolated photosystem II reaction centers revisited: time-dependent anisotropy. J. Phys. Chem, 100:10469-10478.
32. Noguchi, T. 2002. Dual role of triplet localization on the accessory chlorophyll in the photosystem II reaction center: photoprotection and photodamage of the D1 protein. Plant Cell Physiol. 43:1112-1116.
33. Noguchi, T., Y. Inoue, and K. Satoh. 1993. FT-IR studies on the triplet state of P680 in the photosystem II reaction center: triplet equilibrium within a chlorophyll dimer. Biochemistry. 32:7186-7195.
34. 680 in the photosystem II reaction center: evidence for charge delocalization on the chlorophyll dimer. Biochemistry. 37:13614-13625.
35. Noguchi, T., T. Tomo, and C. Kato. 2001. Triplet formation on a monomeric chlorophyll in the photosystem II reaction center as studied by time-resolved infrared spectroscopy. Biochemistry. 40:2176-2185.
36. Ohta, K., M. Yang, and G. R. Fleming. 2001. Ultrafast exciton dynamics of J-aggregates in room temperature solution studied by third-order nonlinear optical spectroscopy and numerical simulation based on exciton theory. J. Chem. Phys. 115:7609-7621.
37. Peterman, E. J. G., H. van Amerongen, R. van Grondelle, and J. P. Dekker. 1998. The nature of the excited state of the reaction center of photosystem II of green plants: a high resolution fluorescence spectroscopy study. Proc. Natl. Acad. Sci. USA. 95:6128-6133.
38. Prokhorenko, V., and A. R. Holzwarth. 2000. Primary processes and structure of the photosystem II reaction center: a photon echo study. J. Phys. Chem. B. 104:11563-11578.
39. Renger, T. 2004. Theory of optical spectra involving charge transfer states: dynamic localization predicts a temperature-dependent optical band shift. Phys. Rev. Lett. 93:188101.
40. Renger, T., and R. A. Marcus. 2002a. On the relation of protein dynamics and exciton relaxation in pigment-protein complexes: an estimation of the spectral density and a theory for the calculation of optical spectra. J. Chem. Phys. 116:9997-10019.
41. Renger, T., and R. A. Marcus. 2002b. Photophysical properties of PS-2 reaction centers and a discrepancy in exciton relaxation times. J. Phys. Chem. B. 106:1809-1819.
42. Renger, T., and R. A. Marcus. 2003. Variable-range hopping electron transfer through disordered bridge states: application to DNA. J. Phys. Chem. A. 107:8404-8419.
43. Renger, T., and V. May. 2000. Simulations of frequency-domain spectra: structure-function relationships in photosynthetic pigment-protein complexes. Phys. Rev. Lett. 84:5228-5231.
44. Renger T., V. May, and O. Kühn. 2001. Ultrafast excitation energy transfer dynamics in photosynthetic piement protein complexes. Phys. Rep. 343:137-254.
45. Shkuropatov, A. Y., R. A. Khatypov, V. A. Shkuropatova, M. G. Zvereva, T. G. Owens, and V. A. Shuvalov. 1999. Reaction centers of photosystem II with a chemically modified pigment composition: exchange of pheophytins with 131-deoxo-131-hydroxy-pheophytin a. FEBS Lett. 450:163-167.
46. Shkuropatov, A. Y., R. A. Khatypov, T. S. Volshchukova, V. A. Shkuropatova, T. G. Owens, and V. A. Shuvalov. 1997. Spectral and photochemical properties of borohydride-treated D1-D2-cytochrome b-559 complex of photosystem II. FEBS Lett. 420:171-174.
47. Steifen, M. A., K. Lao, and S. G. Boxer. 1994. Dielectric asymmetry in the photosynthetic reaction center. Science. 264:810-816.
48. Sumi, H. 1999. Theory on rates of excitation-energy transfer between molecular aggregates through distributed transition dipoles with application to the antenna system in bacterial photosynthesis. J. Phys. Chem. B. 103:252-260.
49. Tang, D., R. Jankowiak, M. Seibert, C. F. Yocum. and G. J. Small. 1990. Excited-state structure and energy-transfer dynamics of two different preparations of the reaction center of photosystem II: a hole-burning study. J. Phys. Chem. 94:6519-6522.
50. Vacha, F., M. Durchan, and P. Siffel. 2002. Excitonic interactions in the reaction centre of photosystem II studied by using circular dichroism. Biochim. Biophys. Acta. 1554:147-152.
51. Vacha, F., D. M. Joseph, J. R. Durrant, A. Telfer, D. R. Klug, G. Porter, and J. Barber. 1995. Photochemistry and spectroscopy of a five-chlorophyll reaction center of photosystem II isolated by using a Cu affinity column. Proc. Natl. Acad. Sci. USA. 92:2929-2933.
52. van Brederode, M. E., M. R. Jones, F. van Mourik, I. H. M. van Stokkum, and R. van Grondelle. 1997. A new pathway for transmembrane electron transfer in photosynthetic reaction centers of Rhodobacrer sphaeroides not involving the excited special-pair. Biochemistry. 36:6855-6861.
53. van Brederode, M. E., M. E. van Brederode, and R. van Grondelle. 1999a. New and unexpected routes for ultrafast electron transfer in photosynthetic reaction centers. FEBS Lett. 455:1-7.
54. van Brederode, M. E., F. van Mourik, I. H. M. van Stokkum, M. R. Jones, and R. van Grondelle. 1999b. Multiple pathways for ultrafast transduction of light energy in the photosynthetic reaction center of Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. USA. 96:2054-2059.
55. van Kan, P. J. M., S. C. M. Otte, F. A. M. Kleinherenbrink, M. C. Nieveen, T. J. Aartsma, and H. J. van Gorkom. 1990. Time-resolved spectroscopy at 10 K of the photosystem II reaction center; deconvolution of the red absorption band. Biochim. Biophys. Acta. 1020:146-152.
56. van Mieghem, F., K. Brettel, B. Hillmann, A. Kamlowski, A. W. Rutherford, and E. Schlodder. 1995. Charge recombination reactions in photosystem II. 1. Yields, recombination pathways, and kinetics of the primary pair. Biochemistry. 34:4789-4813.
57. van Mieghem, F. J. E., K. Satoh, and A. W. Rutherford. 1991. A chlorophyll tilted 30° relative to the membrane in the photosystem II reaction center. Biochim. Biophys. Acta. 1058:379-385.
58. Zhang, W. M., T. Meier, V. Chemyak, and S. Mukamel. 1998a. Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J. Chem. Phys. 108:763-774.
59. Zhang, W. M., T. Meier, V. Chemyak, and S. Mukamel. 1998b. Simulation of three-pulse-echo and fluorescence depolarization in photosynthetic aggregates. Philos. Trans. R. Soc. London. Ser. A. 356:405-419.
60. Zouni, A., H. T. Witt, J. Kern, P. Fromme, N. Krauss, W. Saenger, and P. Orth. 2001. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature. 409:739-743.