Trap-limited charge separation kinetics in higher plant photosystem i complexes

Biophysical Journal

Volumn 94, Issue 9, 2008, Pages 3601-3612

  Slavov, Chavdar ^a   Ballottari, Matteo ^b   Morosinotto, Tomas ^c   Bassi, Roberto ^b   Holzwarth, Alfred R ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^b UNIVERSITY OF VERONA   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARTICLE; CHEMISTRY; ENERGY TRANSFER; ENZYMOLOGY; FLUORESCENCE; KINETICS; LIGHT HARVESTING SYSTEM; METABOLISM; PHOTOSYSTEM I; TIME;

ARABIDOPSIS; ENERGY TRANSFER; FLUORESCENCE; KINETICS; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYSTEM I PROTEIN COMPLEX; TIME FACTORS;

EID: 43649104636     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.117101     Document Type: Article

References (68)

1. Ben-Shem, A., F. Frolow, and N. Nelson. 2003. Crystal structure of plant photosystem I. Nature. 426:630-635.
2. Amunts, A., O. Drory, and N. Nelson. 2007. The structure of a plant photosystem I supercomplex at 3.4 A ̊resolution. Nature. 447:58-63.
3. Fromme, P., E. Schlodder, and S. Jansson. 2003. Structure and function of the antenna system in photosystem I. In Light-Harvesting Antennas in Photosynthesis. B. R. Green and W. W. Parson, editors. Kluwer Academic, Dordrecht, The Netherlands. 253-279.
4. Jordan, P., P. Fromme, H. T. Witt, O. Klukas, W. Saenger, and N. Krauss. 2001. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature. 411:909-917.
5. Beddard, G. S. 1998. Excitations and excitons in photosystem I. Philos. Trans. R. Soc. Lond. A. 356:421-448.
6. Yang, M., A. Damjanovic, H. M. Vaswani, and G. R. Fleming. 2003. Energy transfer in photosystem I of cyanobacteria Synechococcus elongatus: model study with structure-based semi-empirical Hamiltonian and experimental spectral density. Biophys. J. 85:140-158.
7. Croce, R., G. Zucchelli, F. M. Garlaschi, R. Bassi, and R. C. Jennings. 1996. Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry. 35:8572-8579.
8. Gibasiewicz, K., V. M. Ramesh, A. N. Melkozernov, S. Lin, N. W. Woodbury, R. E. Blankenship, and A. N. Webber. 2001. Excitation dynamics in the core antenna of PS I from Chlamydomonas reinhardtii CC 2696 at room temperature. J. Phys. Chem. B. 105:11498-11506.
9. Muller, M. G., J. Niklas, W. Lubitz, and A. R. Holzwarth. 2003. Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 1. A new interpretation of the energy trapping and early electron transfer steps in photosystem I. Biophys. J. 85: 3899-3922.
10. Holzwarth, A. R., M. G. Müller, J. Niklas, and W. Lubitz. 2006. Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 2. Mutations around the P700 reaction center chlorophylls provide new insight into the nature of the primary electron donor. Biophys. J. 90:552-565.
11. Gibasiewicz, K., V. M. Ramesh, S. Lin, K. Redding, N. W. Woodbury, and A. N. Webber. 2003. Excitonic interactions in wild-type and mutant PSI reaction centers. Biophys. J. 85:2547-2559.
12. Stewart, D. H.,A. Cua,D.F.Bocian, andG. W.Brudvig.1999. Selective Raman scattering from the core chlorophylls in photosystem I via preresonant near-infrared excitation. J. Phys. Chem. B. 103:3758-3764.
13. Gibasiewicz, K., V. M. Ramesh, S. Lin, N. W. Woodbury, and A. N. Webber. 2002. Excitation dynamics in Eukaryotic PS I from Chlamydomonas reinhardtii CC 2696 at 10 K. Direct detection of the reaction center exciton states. J. Phys. Chem. B. 106:6322-6330.
14. Karapetyan, N. V., E. Schlodder, R. van Grondelle, and J. P. Dekker. 2006. The long-wavelength chlorophylls of photosystem I. In Advances in Photosynthesis and Respiration: The Light-Driven, Plasto- cyanin:Ferredoxin Oxydoreductase. J. H. Golbeck, editor. Springer, Dordrecht, The Netherlands. 177-192, CP9.
15. Byrdin, M., I. Rimke, E. Schlodder, D. Stehlik, and T. A. Roelofs. 2000. Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: are the kinetics of excited state decay trap-limited or transfer-limited? Biophys. J. 79:992-1007.
16. Gobets, B., and R. van Grondelle. 2001. Energy transfer and trapping in photosystem I. Biochim. Biophys. Acta. 1507:80-99.
17. Gobets,B., I. H. M. van Stokkum, M. Rögner, J. Kruip, E. Schlodder, N. V. Karapetyan, J. P. Dekker, and R. van Grondelle. 2001. Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophys. J. 81:407-124.
18. Gobets, B., I. H. M. van Stokkum, F. van Mourik, J. P. Dekker, and R. van Grondelle. 2003. Excitation wavelength dependence of the fluorescence kinetics in photosystem I particles from Synechocystis PCC 6803 and Synechococcus elongatus. Biophys. J. 85:3883-3898.
19. 1 electron transfer in photosystem I reaction centers. Biochemistry. 40:9282-9290.
20. Croce, R., D. Dorra, A. R. Holzwarth, and R. C. Jennings. 2000. Fluorescence decay and spectral evolution in intact photosystem I of higher plants. Biochemistry. 39:6341-6348.
21. Holzwarth, A. R., G. H. Schatz, H. Brock, and E. Bittersmann. 1993. Energy transfer and charge separation kinetics in photosystem I: 1. Picosecond transient absorption and fluorescence study of cyanobacterial photosystem I particles. Biophys. J. 64:1813-1826.
22. Melkozernov, A. N., S. Lin, and R. E. Blankenship. 2000. Excitation dynamics and heterogeneity of energy equilibration in the core antenna of photosystem I from the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry. 39:1489-1498.
23. Savikhin, S., W. Xu, V. Soukoulis, P. R. Chitnis, and W. S. Struve. 1999. Ultrafast primary processes in photosystem I of the cyanobacterium Synechocystis sp PCC 6803. Biophys. J. 76:3278-3288.
24. Holzwarth, A. R., M. G. Müller, J. Niklas, and W. Lubitz. 2005. Charge recombination fluorescence in photosystem I reaction centers from Chlamydomonas reinhardtii. J. Phys. Chem. B. 109:5903-5911.
25. Ihalainen, J. A., I. H. M. van Stokkum, K. Gibasiewicz, M. Germano, R. van Grondelle, and J. P. Dekker. 2005. Kinetics of excitation trapping in intact photosystem I of Chlamydomonas reinhardtii and Arabidopsis thaliana. Biochim. Biophys. Acta. 1706:267-275.
26. Engelmann, E., G. Zucchelli, A. P. Casazza, D. Brogioli, F. M. Garlaschi, and R. C. Jennings. 2006. Influence of the photosystem I-light harvesting complex I antenna domains on fluorescence decay. Biochemistry. 45:6947-6955.
27. Melkozernov, A. N., J. Kargul, S. Lin, J. Barber, and R. E. Blankenship. 2004. Energy coupling in the PSI-LHCI supercomplex from the green alga Chlamydomonas reinhardtii. J. Phys. Chem. B. 108:10547-10555.
28. Trissl, H.-W. 1993. Long-wavelength absorbing antenna pigments and heterogeneous absorption bands concentrate excitons and increase absorption cross section. Photosynth. Res. 35:247-263.
29. Karapetyan, N. V., A. R. Holzwarth, and M. Rogner. 1999. The photosystem I trimer of cyanobacteria: molecular organisation, excitation dynamics and physiological significance. FEBS Lett. 460:395-400.
30. Rivadossi, A., G. Zucchelli, F. M. Garlaschi, and R. C. Jennings. 1999. The importance of PSI chlorophyll red forms in light-harvesting by leaves. Photosynth. Res. 60:209-215.
31. Melkozernov, A. N., and R. E. Blankenship. 2005. Structural and functional organization of the peripheral light-harvesting system in photosystem I. Photosynth. Res. 85:33-50.
32. Karapetyan, N. V. 2004. The dynamics of excitation energy in photosystem I of cyanobacteria: transfer in the antenna, capture by the reaction site, and dissipation. Biophysics. 49:196-210.
33. Carbonera, D., G. Agostini, T. Morosinotto, and R. Bassi. 2005. Quenching of chlorophyll triplet states by carotenoids in reconstituted Lhca4 subunit of peripheral light-harvesting complex of photosystem I. Biochemistry. 44:8337-8346.
34. Croce, R., M. Mozzo, T. Morosinotto, A. Romeo, R. Hienerwadel, and R. Bassi. 2007. Singlet and triplet state transitions of carotenoids in the antenna complexes of higher-plant photosystem I. Biochemistry. 46: 3846-3855.
35. Palsson, L.-O., J. P. Dekker, E. Schlodder, R. Monshouwer, and R. van Grondelle. 1996. Polarized site-selective fluorescence spectroscopy of the long- wavelength emitting chlorophylls in isolated photosystem I particles of Synechococcus elongatus. Photosynth. Res. 48:239-246.
36. Zazubovich, V., S. Matsuzaki, T. W. Johnson, J. M. Hayes, P. R. Chitnis, and G. J. Small. 2002. Red antenna states of photosystem I from cyanobacterium Synechococcus elongatus: a spectral hole burning study. Chem. Phys. 275:47-59.
37. Ratsep, M., T. W. Johnson, P. R. Chitnis, and G. J. Small. 2000. The red-absorbing chlorophyll a antenna states of photosystem. I: A hole-burning study of Synechocystis sp PCC 6803 and its mutants. J. Phys. Chem. B. 104:836-847.
38. Jelezko, F., C. Tietz, U. Gerken, J. Wrachtrup, and R. Bittl. 2000. Single-molecule spectroscopy on photosystem I pigment-protein complexes. J. Phys. Chem. B. 104:8093-8096.
39. Ihalainen, J. A., M. Rätsep, P. E. Jensen, H. V. Scheller, R. Croce, R. Bassi, J. E. I. Korppi-Tommola, and A. Freiberg. 2003. Red spectral forms of chlorophylls in green plant PSI-a site-selective and high-pressure spectroscopy study. J. Phys. Chem. B. 107:9086-9093.
40. Melkozernov, A. N., S. Lin, and R. E. Blankenship. 2000. Femtosecond transient spectroscopy and excitonic interactions in photosystem I. J. Phys. Chem. B. 104:1651-1656.
41. Palsson, L.-O., C. Flemming, B. Gobets, R. van Grondelle, J. P. Dekker, and E. Schlodder. 1998. Energy transfer and charge separation in photosystem I P700 oxidation upon selective excitation of the long-wavelength antenna chlorophylls of Synechococcus elongatus. Biophys. J. 74:2611-2622.
42. Mullet, J. E., J. J. Burke, and C. J. Arntzen. 1980. Chlorophyll proteins of photosystem I. Plant Physiol. 65:814-822.
43. Croce, R., G. Zucchelli, F. M. Garlaschi, and R. C. Jennings. 1998. A thermal broadening study of the antenna chlorophylls in PSI- 200, LHCI, and PSI core. Biochemistry. 37:17355-17360.
44. Jennings, R. C., G. Zucchelli, E. Engelmann, and F. M. Garlaschi. 2004. The long-wavelength chlorophyll states of plant LHCI at room temperature: a comparison with PSI-LHCI. Biophys. J. 87:488-497.
45. Melkozernov, A. N., J. Kargul, S. Lin, J. Barber, and R. E. Blankenship. 2005. Spectral and kinetic analysis of the energy coupling in the PSI-LHC I supercomplex from the green alga Chlamydomonas reinhardtii at 77 K. Photosynth. Res. 86:203-215.
46. Morosinotto, T., M. Ballottari, F. Klimmek, S. Jansson, and R. Bassi. 2005. The association of the antenna system to photosystem I in higher plants. J. Biol. Chem. 280:31050-31058.
47. Castelletti, S., T. Morosinotto, B. Robert, S. Caffarri, R. Bassi, and R. Croce. 2003. Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry. 42:4226-4234.
48. Morosinotto, T., J. Breton, R. Bassi, and R. Croce. 2003. The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J. Biol. Chem. 278:49223 49229.
49. Hastings, G., F. A. M. Kleinherenbrink, S. Lin, and R. E. Blankenship. 1994. Time-resolved fluorescence and absorption spectroscopy of photosystem I. Biochemistry. 33:3185-3192.
50. Turconi, S., J. Kruip, G. Schweitzer, M. Rögner, and A. R. Holzwarth. 1996. A comparative fluorescence kinetics study of photosystem I monomers and trimers from Synechocystis PCC 6803. Photosynth. Res. 49:263-268.
51. Karapetyan, N. V., D. Dorra, G. Schweitzer, I. N. Bezsmertnaya, and A. R. Holzwarth. 1997. Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis. Biochemistry. 36:13830-13837.
52. Gobets, B., J. T. M. Kennis, J. A. Ihalainen, M. Brazzoli, R. Croce, I. H. M. van Stokkum, R. Bassi, J. P. Dekker, H. van Amerongen, G. R. Fleming, and R. van Grondelle. 2001. Excitation energy transfer in dimeric light harvesting complex I: a combined streak-camera/fluorescence upconversion study. J. Phys. Chem. B. 105:10132-10139.
53. Ihalainen, J. A., R. Croce, T. Morosinotto, I. H. M. van Stokkum, R. Bassi, J. P. Dekker, and R. van Grondelle. 2005. Excitation decay pathways of Lhca proteins: a time-resolved fluorescence study. J. Phys. Chem. B. 109:21150-21158.
54. Koehne, B., and H.-W. Trissl. 1998. The cyanobacterium Spirulina platensis contains a long wavelength absorbing pigment C738(F760/77K) at room temperature. Biochemistry. 37:5494-5500.
55. Bassi, R., G. M. Giacometti, and D. J. Simpson. 1988. Changes in the organization of stroma membranes induced by in vivo state 1-state 2 transition. Biochim. Biophys. Acta. 935:152-165.
56. Holzwarth, A. R. 1996. Data analysis of time-resolved measurements. In Biophysical Techniques in Photosynthesis. Advances in Photosynthesis Research. J. Amesz and A. J. Hoff, editors. Kluwer Academic, Dordrecht, The Netherlands. 75-92.
57. van Stokkum, I. H. M., D. S. Larsen, and R. van Grondelle. 2004. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta. 1657:82-104.
58. Turconi, S., N. Weber, G. Schweitzer, H. Strotmann, and A. R. Holzwarth. 1994. Energy transfer and charge separation kinetics in photosystem I. 2. Picosecond fluorescence study of various PSI particles and light-harvesting complex isolated from higher plants. Biochim. Biophys. Acta. 1187:324-334.
59. Holzwarth, A. R. 2004. Light absorption and harvesting. In Molecular to Global Photosynthesis. M. D. Archer and J. Barber, editors. Imperial College Press, London. 43-115.
60. Gobets, B., H. van Amerongen, R. Monshouwer, J. Kruip, M. Rögner, R. van Grondelle, and J. P. Dekker. 1994. Polarized site-selected fluorescence spectroscopy of isolated photosystem I particles. Biochim. Biophys. Acta. 1188:75-85.
61. Kennard, E. H. 1918. On the thermodynamics of fluorescence. Phys. Rev. 11:29-38.
62. Stepanov, B. I. 1957. A universal relation between the absorption and luminescence spectra of complex molecules. Dokl. Akad. Nauk. SSSR. 112:839-841.
63. Ihalainen, J. A., B. Gobets, K. Sznee, M. Brazzoli, R. Croce, R. Bassi, R. van Grondelle, J. E. I. Korppi-Tommola, and J. P. Dekker. 2000. Evidence for two spectroscopically different dimers of light-harvesting complex I from green plants. Biochemistry. 39:8625-8631.
64. Holzwarth, A. R., M. G. Müller, C. Slavov, R. Luthra, and K. Redding. 2007. Ultrafast energy and electron transfer in photosystem I. Direct evidence for two-branched electron transfer. In Ultrafast Phenomena XV. P. B. Corkum, D. Jonas, R. J. D. Miller, and A. M. Weiner, editors. 471-473.
65. van Grondelle, R., and B. Gobets. 2004. Transfer and trapping of excitations in plant photosystems. In Chlorophyll a Fluorescence: A Signature of Photosynthesis. G. C. Papageorgiou and Govindjee, editors. Springer, Dordrecht, The Netherlands. 107-132.
66. Miloslavina, Y., M. Szczepaniak, M. G. Müller, J. Sander, M. Nowaczyk, M. Rögner, and A. R. Holzwarth. 2006. Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry. 45:2436-2442.
67. Sener, M. K., C. Jolley, A. Ben-Shem, P. Fromme, N. Nelson, R. Croce, and K. Schulten. 2005. Comparison of the light-harvesting networks of plant and cyanobacterial photosystem I. Biophys. J. 89:1630-1642.
68. Liu, Z., H. Yan, K. Wang, T. Kuang, J. Zhang, L. Gui, X. An, and W. Chang. 2004. Crystal structure of spinach major light-harvesting complex at 2.72 angstrom resolution. Nature. 428:287-292.