Trap-limited Charge Separation Kinetics in Higher Plant Photosystem I Complexes

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2008 Jan 29

PMID 18222996

Citations 33

Authors

Chavdar Slavov

Matteo Ballottari

Tomas Morosinotto

Roberto Bassi

Alfred R Holzwarth

Affiliations

Soon will be listed here.

Abstract

Time-resolved fluorescence measurements were performed on isolated core and intact Photosystem I (PS I) particles and stroma membranes from Arabidopsis thaliana to characterize the type of energy-trapping kinetics in higher plant PS I. Target analysis confirms the previously proposed "charge recombination" model. No bottleneck in the energy flow from the bulk antenna compartments to the reaction center has been found. For both particles a trap-limited kinetics is realized, with an apparent charge separation lifetime of approximately 6 ps. No red chlorophylls (Chls) are found in the PS I-core complex from A. thaliana. Rather, the observed red-shifted fluorescence (700-710 nm range) originates from the reaction center. In contrast, two red Chl compartments, located in the peripheral light-harvesting complexes, are resolved in the intact PS I particles (decay lifetimes 33 and 95 ps, respectively). These two red states have been attributed to the two red states found in Lhca 3 and Lhca 4, respectively. The influence of the red Chls on the slowing of the overall trapping kinetics in the intact PS I complex is estimated to be approximately four times larger than the effect of the bulk antenna enlargement.

Citing Articles

Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I.

Slama V, Cupellini L, Mascoli V, Liguori N, Croce R, Mennucci B J Phys Chem Lett. 2023; 14(37):8345-8352.

PMID: 37702053 PMC: 10518868. DOI: 10.1021/acs.jpclett.3c02091.

Energy transfer and trapping in photosystem I with and without chlorophyll-.

van Stokkum I, Muller M, Weissenborn J, Weigand S, Snellenburg J, Holzwarth A iScience. 2023; 26(9):107650.

PMID: 37680463 PMC: 10480676. DOI: 10.1016/j.isci.2023.107650.

Photosynthesis re-wired on the pico-second timescale.

K Baikie T, Wey L, Lawrence J, Medipally H, Reisner E, Nowaczyk M Nature. 2023; 615(7954):836-840.

PMID: 36949188 DOI: 10.1038/s41586-023-05763-9.

Light-induced changes of far-red excited chlorophyll fluorescence: further evidence for variable fluorescence of photosystem I in vivo.

Schreiber U Photosynth Res. 2023; 155(3):247-270.

PMID: 36598714 PMC: 9958156. DOI: 10.1007/s11120-022-00994-9.

Single chloroplast in folio imaging sheds light on photosystem energy redistribution during state transitions.

Verhoeven D, van Amerongen H, Wientjes E Plant Physiol. 2022; 191(2):1186-1198.

PMID: 36478277 PMC: 9922397. DOI: 10.1093/plphys/kiac561.

References

Savikhin S, Xu W, Soukoulis V, Chitnis P, Struve W . Ultrafast primary processes in photosystem I of the cyanobacterium Synechocystis sp. PCC 6803. Biophys J. 1999; 76(6):3278-88. PMC: 1300297. DOI: 10.1016/S0006-3495(99)77480-1. View

Morosinotto T, Ballottari M, Klimmek F, Jansson S, Bassi R . The association of the antenna system to photosystem I in higher plants. Cooperative interactions stabilize the supramolecular complex and enhance red-shifted spectral forms. J Biol Chem. 2005; 280(35):31050-8. DOI: 10.1074/jbc.M502935200. View

Sener M, Jolley C, Ben-Shem A, Fromme P, Nelson N, Croce R . Comparison of the light-harvesting networks of plant and cyanobacterial photosystem I. Biophys J. 2005; 89(3):1630-42. PMC: 1366667. DOI: 10.1529/biophysj.105.066464. View

Croce R, Mozzo M, Morosinotto T, Romeo A, Hienerwadel R, Bassi R . Singlet and triplet state transitions of carotenoids in the antenna complexes of higher-plant photosystem I. Biochemistry. 2007; 46(12):3846-55. DOI: 10.1021/bi602531k. View

Croce R, Zucchelli G, Garlaschi F, Bassi R, Jennings R . Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry. 1996; 35(26):8572-9. DOI: 10.1021/bi960214m. View

Engelmann E, Zucchelli G, Casazza A, Brogioli D, Garlaschi F, Jennings R . Influence of the photosystem I-light harvesting complex I antenna domains on fluorescence decay. Biochemistry. 2006; 45(22):6947-55. DOI: 10.1021/bi060243p. View

Amunts A, Drory O, Nelson N . The structure of a plant photosystem I supercomplex at 3.4 A resolution. Nature. 2007; 447(7140):58-63. DOI: 10.1038/nature05687. View

Ihalainen J, van Stokkum I, Gibasiewicz K, Germano M, van Grondelle R, Dekker J . Kinetics of excitation trapping in intact Photosystem I of Chlamydomonas reinhardtii and Arabidopsis thaliana. Biochim Biophys Acta. 2005; 1706(3):267-75. DOI: 10.1016/j.bbabio.2004.11.007. View

Palsson L, Dekker J, Schlodder E, Monshouwer R, van Grondelle R . Polarized site-selective fluorescence spectroscopy of the long-wavelength emitting chlorophylls in isolated Photosystem I particles of Synechococcus elongatus. Photosynth Res. 2013; 48(1-2):239-46. DOI: 10.1007/BF00041014. View

10.

Holzwarth A, Schatz G, Brock H, Bittersmann E . Energy transfer and charge separation kinetics in photosystem I: Part 1: Picosecond transient absorption and fluorescence study of cyanobacterial photosystem I particles. Biophys J. 2009; 64(6):1813-26. PMC: 1262515. DOI: 10.1016/S0006-3495(93)81552-2. View

11.

Ihalainen J, Croce R, Morosinotto T, van Stokkum I, Bassi R, Dekker J . Excitation decay pathways of Lhca proteins: a time-resolved fluorescence study. J Phys Chem B. 2006; 109(44):21150-8. DOI: 10.1021/jp0519316. View

12.

Ben-Shem A, Frolow F, Nelson N . Crystal structure of plant photosystem I. Nature. 2003; 426(6967):630-5. DOI: 10.1038/nature02200. View

13.

Gobets B, van Grondelle R . Energy transfer and trapping in photosystem I. Biochim Biophys Acta. 2001; 1507(1-3):80-99. DOI: 10.1016/s0005-2728(01)00203-1. View

14.

Ihalainen J, Gobets B, Sznee K, Brazzoli M, Croce R, Bassi R . Evidence for two spectroscopically different dimers of light-harvesting complex I from green plants. Biochemistry. 2000; 39(29):8625-31. DOI: 10.1021/bi0007369. View

15.

Gobets B, van Stokkum I, Rogner M, Kruip J, Schlodder E, Karapetyan N . Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophys J. 2001; 81(1):407-24. PMC: 1301521. DOI: 10.1016/S0006-3495(01)75709-8. View

16.

Morosinotto T, Breton J, Bassi R, Croce R . The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J Biol Chem. 2003; 278(49):49223-9. DOI: 10.1074/jbc.M309203200. View

17.

Turconi S, Kruip J, Schweitzer G, Rogner M, Holzwarth A . A comparative fluorescence kinetics study of Photosystem I monomers and trimers from Synechocystis PCC 6803. Photosynth Res. 2013; 49(3):263-8. DOI: 10.1007/BF00034787. View

18.

Melkozernov A, Blankenship R . Structural and functional organization of the peripheral light-harvesting system in photosystem I. Photosynth Res. 2005; 85(1):33-50. DOI: 10.1007/s11120-004-6474-5. View

19.

Hastings G, Kleinherenbrink F, Lin S, Blankenship R . Time-resolved fluorescence and absorption spectroscopy of photosystem I. Biochemistry. 1994; 33(11):3185-92. DOI: 10.1021/bi00177a007. View

20.

Jordan P, Fromme P, Witt H, Klukas O, Saenger W, Krauss N . Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature. 2001; 411(6840):909-17. DOI: 10.1038/35082000. View