Energetics in Photosystem II from Thermosynechococcus elongatus with a D1 protein encoded by either the psbA1 or psbA3 gene

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 8, 2010, Pages 1491-1499

  Sugiura, Miwa ^a   Kato, Yuki ^b   Takahashi, Ryouta ^c   Suzuki, Hiroyuki ^c   Watanabe, Tadashi ^b   Noguchi, Takumi ^c   Rappaport, Fabrice ^d   Boussac, Alain ^e  

^a EHIME UNIVERSITY   (Japan)

^b INSTITUTE OF INDUSTRIAL SCIENCE   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^e SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

Author keywords

D1 protein; Electron transfer; Pheophytin; Photosystem II; PsbA gene; Site directed mutagenesis; Thermosynechococcus elongatus

Indexed keywords

BACTERIAL PROTEIN; BROMOXYNIL; D1 PROTEIN; DIURON; NONHEME IRON PROTEIN; PROTEIN PSBA1; PROTEIN PSBA3; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BINDING SITE; CONTROLLED STUDY; CYANOBACTERIUM; ELECTROCHEMICAL ANALYSIS; ELECTRON TRANSPORT; GENE DELETION; GENETIC RECOMBINATION; HYDROGEN BOND; INFRARED SPECTROSCOPY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PHOTOSYSTEM II; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SYNECHOCYSTIS; TEMPERATURE SENSITIVITY; THERMOSYNECHOCOCCUS ELONGATUS; WILD TYPE;

CYANOBACTERIA; ELECTRON TRANSPORT; ENERGY METABOLISM; PHOTOSYSTEM II PROTEIN COMPLEX; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THERMODYNAMICS;

CYANOBACTERIA; SYNECHOCYSTIS SP. PCC 6803; THERMOSYNECHOCOCCUS ELONGATUS;

EID: 77953811055     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.03.022     Document Type: Article

References (57)

1. Ferreira K.N., Iverson T.M., Maghlaoui K., Barber J., Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science 2004, 303:1831-1838.
2. Loll B., Kern J., Saenger W., Zouni A., Biesiadka J. Towards complete cofactor arrangement in the 3.0Å resolution structure of photosystem II. Nature 2005, 438:1040-1044.
3. Guskov A., Kern J., Gabdulkhakov A., Broser M., Zouni A., Saenger W. Cyanobacterial photosystem II at 2.9Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 2009, 16:334-342.
4. Diner B.A., Rappaport F. Structure, dynamics, and energetics of the primary photochemistry of Photosystem II of oxygenic photosynthesis. Annu. Rev. Plant. Biol. 2002, 53:551-580.
5. Groot M.L., Pawlowicz N.P., van Wilderen L.J., Breton J., van Stokkum I.H., van Grondelle R. Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13087-13092.
6. Holzwarth A.R., Muller M.G., Reus M., Nowaczyk M., Sander J., Rogner M. Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6895-6900.
7. 4Ca cluster and to the evolution of molecular oxygen in Photosystem II. Coord. Chem. Rev. 2008, 252:259-272.
8. Renger G. A.R. Holzwarth. Primary Electron Transfer in Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase 2005, Vol. 22:139-175. Springer, Dordrecht.
9. 2 evolution: I. A linear four step mechanism. Photochem. Photobiol. 1970, 11:457-475.
10. Joliot P., Kok B. Oxygen evolution in photosynthesis. Bioenergetics of Photosynthesis 1975, 387. Academic Press, New York. Govindjee (Ed.).
11. Nakamura Y., Kaneko T., Sato S., Ikeuchi M., Katoh H., Sasamoto S., Watanabe A., Iriguchi M., Kawashima K., Kimura T., Kishida Y., Kiyokawa C., Kohara M., Matsumoto M., Matsuno A., Nakazaki N., Shimpo S., Sugimoto M., Takeuchi C., Yamada M., Tabata S. Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res. 2002, 9:123-130.
12. Golden S.S., Brusslan J., Haselkorn R. Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J. 1986, 5:2789-2798.
13. Clarke A.K., Hurry V.M., Gustafsson P., Oquist G. Two functionally distinct forms of the photosystem-II reaction-center protein D1 in the cyanobacterium Synechococcus sp. PCC 7942. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11985-11989.
14. Clarke A.K., Soitamo A., Gustafsson P., Oquist G. Rapid interchange between two distinct forms of cyanobacterial photosystem-II reaction-center protein-D1 in response to photoinhibition. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:9973-9979.
15. Golden S.S. Light-responsive gene expression in cyanobacteria. J. Bacteriol. 1995, 177:1651-1654.
16. Campbell D., Zhou G., Gustafsson P., Oquist G., Clarke A.K. Electron transport regulates exchange of two forms of photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J. 1995, 14:5457-5466.
17. Oquist G., Campbell D., Clarke A.K., Gustafsson P. The cyanobacterium Synechococcus modulates Photosystem II function in response to excitation stress through D1 exchange. Photosynth. Res. 1995, 46:151-158.
18. Komenda J., Hassan H.A., Diner B.A., Debus R.J., Barber J., Nixon P.J. Degradation of the Photosystem II D1 and D2 proteins in different strains of the cyanobacterium Synechocytis PCC 6803 varying with respect to the type and level of psbA transcript. Plant Mol. Biol. 2000, 42:635-645.
19. Sicora C.I., Appleton S.E., Brown C.M., Chung J., Chandler J., Cockshutt A.M., Vass I., Campbell D.A. Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms. Biochim. Biophys. Acta 2006, 1757:47-56.
20. Kos P.B., Deak Z., Cheregi O., Vass I. Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim. Biophys. Acta 2008, 1777:74-83.
21. Loll B., Broser M., Kos P.B., Kern J., Biesiadka J., Vass I., Saenger W., Zouni A. Modeling of variant copies of subunit D1 in the structure of photosystem II from Thermosynechococcus elongatus. Biol. Chem. 2008, 389:609-617.
22. Sicora C.I., Brown C.M., Cheregi O., Vass I., Campbell D.A. The psbA gene family responds differentially to light and UVB stress in Gloeobacter violaceus PCC 7421, a deeply divergent cyanobacterium. Biochim. Biophys. Acta 2008, 1777:130-139.
23. Mulo P., Sicora C., Aro E.M. Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell. Mol. Life Sci. 2009, 66:3697-3710.
24. Mohamed A., Eriksson J., Osiewacz H.D., Jansson C. Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol. Gen. Genet. 1993, 238:161-168.
25. Schaefer M.R., Golden S.S. Light availability influences the ratio of two forms of D1 in cyanobacterial thylakoids. J. Biol. Chem. 1989, 264:7412-7417.
26. Kulkarni R.D., Golden S.S. Adaptation to high light intensity in Synechococcus sp. strain PCC 7942: regulation of three psbA genes and two forms of the D1 protein. J. Bacteriol. 1994, 176:959-965.
27. Mohamed A., Jansson C. Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol. Biol. 1989, 13:693-700.
28. Moënne-Loccoz P., Robert B., Lutz M. A resonance Raman characterization of the primary electron acceptor in Photosystem II. Biochemistry 1989, 28:3641-3645.
29. Dorlet P., Xiong L., Sayre R.T., Un S. High field EPR study of the pheophytin anion radical in wild type and D1-E130 mutants of photosystem II in Chlamydomonas reinhardtii. J. Biol. Chem. 2001, 276:22313-22316.
30. Shibuya Y., Takahashi R., Okubo T., Suzuki H., Sugiura M., Noguchi T. Hydrogen bond interaction of the pheophytin electron acceptor and its radical anion in Photosystem II as revealed by Fourier Transform Infrared Difference Spectroscopy. Biochemistry 2010, 49:493-501.
31. Merry S.A.P., Nixon P.J., Barter L.M.C., Schilstra M.J., Porter G., Barber J., Durrant J.R., Klug D. Modulation of quantum yield of primary radical pair formation in photosystem II by site directed mutagenesis affecting radical cations and anions. Biochemistry 1998, 37:17439-17447.
32. Rappaport F., Guergova-Kuras M., Nixon P.J., Diner B.A., Lavergne J. Kinetics and pathways of charge recombination in Photosystem II. Biochemistry 2002, 41:8518-8527.
33. Cuni A., Xiong L., Sayre R.T., Rappaport F., Lavergne J. Modification of the pheophytin midpoint potential in Photosystem II: modulation of the quantum yield of charge separation and of charge recombination pathways. Phys. Chem. Chem. Phys. 2004, 6:4825-4831.
34. Cser K., Vass I. Radiative and non-radiative charge recombination pathways in Photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6803. Biochim. Biophys. Acta 2007, 1767:233-243.
35. 680, of Photosystem II in Thermosynechococcus elongatus. Biochim. Biophys. Acta 2008, 1777:331-342.
36. Sugiura M., Inoue Y. Highly purified thermo-stable oxygen-evolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol. 1999, 40:1219-1231.
37. Hughes J.L., Cox N., Rutherford A.W., Krausz E., Lai T.L., Boussac A., Sugiura M. D1 protein variants in Photosystem II from Thermosynechococcus elongatus studied by low temperature optical spectroscopy. Biochim. Biophys. Acta 2010, 1797:11-19.
38. Beal D., Rappaport F., Joliot P. A new high-sensitivity 10-ns time-resolution spectrophotometric technique adapted to in vivo analysis of the photosynthetic apparatus. Rev. Sci. Instrum. 1999, 70:202-207.
39. • state of Photosystem II from Thermosynechococcus elongatus. Biochemistry 2007, 46:3138-3150.
40. Noguchi T., Katoh M., Inoue Y. A new system for detection of thermoluminescence and delayed fluorescence from photosynthetic apparatus with precise temperature control. Spectroscopy 2002, 16:89-94.
41. Takahashi R., Boussac A., Sugiura M., Noguchi T. Structural coupling of a tyrosine side chain with the non-heme iron center in photosystem II as revealed by light-induced Fourier transform infrared difference spectroscopy. Biochemistry 2009, 48:8994-9001.
42. Kato Y., Sugiura M., Oda A., Watanabe T. Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in photosystem II. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17365-17370.
43. van Gorkom H.J. Electron transfer in photosystem II. Photosynth. Res. 1985, 6:97-112.
44. Alric J., Cuni A., Maki H., Nagashima K.V., Verméglio A., Rappaport F. Electrostatic interaction between redox cofactors in photosynthetic reaction centers. J. Biol. Chem. 2004, 279:47849-47855.
45. Rappaport F., Lavergne J. Thermoluminescence: theory. Photosynth. Res. 2009, 101:205-216.
46. Krieger A., Rutherford A.W., Johnson G.N. On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in photosystem II. Biochim. Biophys. Acta 1995, 1229:193-201.
47. Krieger-Liszkay A., Rutherford A.W. Influence of herbicide binding on the redox potential of the quinone acceptor of photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 1998, 37:17339-17344.
48. Socrates G. Infrared Characteristic Group Frequencies 1994, 54. John Wiley & Sons, Chichester, U.K.
49. Takano A., Takahashi R., Suzuki H., Noguchi T. Herbicide effect on the hydrogen-bonding interaction of the primary quinone electron acceptor QA in photosystem II as studied by Fourier transform infrared spectroscopy. Photosynth. Res. 2008, 98:159-167.
50. Trebst A. The three-dimensional structure of the herbicide binding on the reaction center polypeptides of photosystem II. Z. Naturforsch. 1987, 42c:742-750.
51. Sobolev V., Edelman M. Modeling the quinone-B binding site of the photosystem-II reaction center using notions of complementarity and contact-surface between atoms. Proteins 1995, 21:214-225.
52. Rappaport F., Boussac A., Force D.A., Peloquin J., Brynda M., Sugiura M., Un S., Britt R.D., Diner B.A. Probing the coupling between proton and electron transfer in photosystem II core complexes containing a 3-fluorotyrosine. J. Am. Chem. Soc. 2009, 131:4425-4433.
53. Rappaport F., Lavergne J. Coupling of electron and proton transfer in the photosynthetic water oxidase. Biochim. Biophys. Acta 2001, 1503:246-259.
54. Renger G., Wolff C. Existence of a high photochemical turnover rate at reaction centers of system-2 in tris-washed chloroplasts. Biochim. Biophys. Acta 1976, 423:610-614.
55. Haveman J., Mathis P. Flash-induced absorption changes of primary donor of photosystem-ii at 820nm in chloroplasts inhibited by low ph or tris-treatment. Biochim. Biophys. Acta 1976, 440:346-355.
56. Giorgi L.B., Nixon P.J., Merry S.A.P., Joseph D.M., Durrant J.R., Rivas J.D., Barber J., Porter G., Klug D.R. Comparison of primary charge separation in the photosystem II reaction center complex isolated from wild-type and D1-130 mutants of the cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 1996, 271:2093-2101.
57. Vass I., Cser K. Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci. 2009, 14:200-205.