Natural variants of photosystem II subunit D1 tune photochemical fitness to solar intensity

Journal of Biological Chemistry

Volumn 288, Issue 8, 2013, Pages 5451-5462

  Vinyard, David J ^a,b,c,e   Gimpel, Javier ^d   Ananyev, Gennady M ^a,b   Cornejo, Mario A ^b   Golden, Susan S ^d   Mayfield, Stephen P ^d   Dismukes, G Charles ^a,b  

^a Department of Chemistry and Chemical Biology ^*  (United States)

^b RUTGERS UNIVERSITY   (United States)

^c PRINCETON UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e U S ARMY RESEARCH OFFICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMASS ACCUMULATION; CHARGE RECOMBINATIONS; ENVIRONMENTAL CONDITIONS; HIGH LIGHTS; ISOFORMS; LOW LIGHT; PHOTOCHEMICAL EFFICIENCY; PHOTOSYSTEM II; SOLAR INTENSITIES; WATER OXIDATION;

BIOCHEMISTRY;

BIOLOGY;

MANGANESE DERIVATIVE; OXYGEN; WATER;

AMINO ACID SEQUENCE; ARTICLE; BIOMASS; CHLAMYDOMONAS REINHARDTII; CYANOBACTERIUM; ELECTRON SPIN RESONANCE; GENE; GENE EXPRESSION; GREEN ALGA; GROWTH RATE; ILLUMINATION; LIGHT INTENSITY; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; OXYGEN SATURATION; PHOTOCHEMISTRY; PHOTOSYSTEM II; PHOTOTROPH; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; PSBA GENE; SOLAR ENERGY; SYNECHOCOCCUS ELONGATUS; UPREGULATION; WATER OXIDATION;

BIOMASS; CHLAMYDOMONAS; CHLOROPHYLL; CYANOBACTERIA; ELECTRON SPIN RESONANCE SPECTROSCOPY; EVOLUTION, MOLECULAR; FOURIER ANALYSIS; GENETIC VARIATION; KINETICS; LIGHT; MUTATION; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN ISOFORMS; SOLAR ENERGY; THYLAKOIDS;

EID: 84874309410     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.394668     Document Type: Article

References (71)

1. Muh, F., and Zouni, A. (2011) Light-induced water oxidation in photosystem II. Front. Biosci. 16, 3072-3132
2. Falkowski, P. G., and Raven, J. A. (2007) Aquatic Photosynthesis, 2nd Ed., pp. 81-117, Princeton University Press, Princeton, NJ
3. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55-60
4. Mulo, P., Sicora, C., and Aro, E.-M. (2009) Cyanobacterial psbA gene family. Optimization of oxygenic photosynthesis. Cell. Mol. Life Sci. 66, 3697-3710
5. Bouyoub, A., Vernotte, C., and Astier, C. (1993) Functional analysis of the two homologous psbA gene copies in Synechocystis PCC 6714 and PCC 6803. Plant Mol. Biol. 21, 249-258
6. Mohamed, A., Eriksson, J., Osiewacz, H. D., and Jansson, C. (1993) Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol. Gen. Genet. 238, 161-168
7. Summerfield, T. C., Toepel, J., and Sherman, L. A. (2008) Low-oxygen induction of normally cryptic psbA genes in cyanobacteria. Biochemistry 47, 12939-12941
8. Sicora, C. I., Ho, F. M., Salminen, T., Styring, S., and Aro, E.-M. (2009) Transcription of a "silent" cyanobacterial psbA gene is induced by microaerobic conditions. Biochim. Biophys. Acta 1787, 105-112
9. Golden, S. S., Brusslan, J., and Haselkorn, R. (1986) Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J. 5, 2789-2798
10. Boussac, A., Sugiura, M., and Rappaport, F. (2011) Probing the quinonebinding site of photosystem II from Thermosynechococcus elongatus containing either PsbA1 or PsbA3 as the D1 protein through the binding characteristics of herbicides. Biochim. Biophys. Acta 1807, 119-129
11. Hughes, J. L., Cox, N., Rutherford, A. W., Krausz, E., Lai, T.-L., Boussac, A., and Sugiura, M. (2010) D1 protein variants in photosystem II from Thermosynechococcus elongatus studied by low temperature optical spectroscopy. Biochim. Biophys. Acta 1797, 11-19
12. Kato, Y., Shibamoto, T., Yamamoto, S., Watanabe, T., Ishida, N., Sugiura, M., Rappaport, F., and Boussac, A. (2012) Influence of the PsbA1/PsbA3, Ca2+/Sr2+ and Cl-/Br-exchanges on the redox potential of the primary quinone QA in photosystem II from Thermosynechococcus elongatus as revealed by spectroelectrochemistry. Biochim. Biophys. Acta 1817, 1998-2004
13. Kato, Y., Sugiura, M., Oda, A., and Watanabe, T. (2009) Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in photosystem II. Proc. Natl. Acad. Sci. U.S.A. 106, 17365-17370
14. Ogami, S., Boussac, A., and Sugiura, M. (2012) Deactivation processes in PsbA1-photosystem II and PsbA3-photosystem II under photoinhibitory conditions in the cyanobacterium Thermosynechococcus elongatus. Biochim. Biophys. Acta 1817, 1322-1330
15. Shibamoto, T., Kato, Y., Sugiura, M., and Watanabe, T. (2009) Redox potential of the primary plastoquinone electron acceptorQAin photosystem II from Thermosynechococcus elongatus determined by spectroelectrochemistry. Biochemistry 48, 10682-10684
16. Sugiura, M., Iwai, E., Hayashi, H., and Boussac, A. (2010) Differences in the interactions between the subunits of photosystem II-dependent on D1 protein variants in the thermophilic cyanobacterium Thermosynechococcus elongatus. J. Biol. Chem. 285, 30008-30018
17. Schaefer, M. R., and Golden, S. S. (1989) Light availability influences the ratio of two forms of D1 in cyanobacterial thylakoids. J. Biol. Chem. 264, 7412-7417
18. Schaefer, M. R., and Golden, S. S. (1989) Differential expression of members of a cyanobacterial psbA gene family in response to light. J. Bacteriol. 171, 3973-3981
19. Bustos, S. A., Schaefer, M. R., and Golden, S. S. (1990) Different and rapid responses of four cyanobacterial psbA transcripts to changes in light intensity. J. Bacteriol. 172, 1998-2004
20. Campbell, D., Eriksson, M.-J., Oquist, G., Gustafsson, P., and Clarke, A. K. (1998) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc. Natl. Acad. Sci. U.S.A. 95, 364-369
21. Campbell, D., Zhou, G., Gustafsson, P., Oquist, G., and Clarke, A. K. (1995) Electron transport regulates exchange of two forms of photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J. 14, 5457-5466
22. Sippola, K., and Aro, E.-M. (1999) Thiol redox state regulates expression of psbA genes in Synechococcus sp. PCC 7942. Plant Mol. Biol. 41, 425-433
23. Merry, S. A., Nixon, P. J., Barter, L. M., Schilstra, M., Porter, G., Barber, J., Durrant, J. R., and Klug, D. R. (1998) Modulation of quantum yield of primary radical pair formation in photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry 37, 17439-17447
24. Sugiura, M., Kato, Y., Takahashi, R., Suzuki, H., Watanabe, T., Noguchi, T., Rappaport, F., and Boussac, A. (2010) Energetics in Photosystem II from Thermosynechococcus elongatus with a D1 protein encoded by either the psbA1 or psbA3 gene. Biochim. Biophys. Acta 1797, 1491-1499
25. Clarke, A. K., Hurry, V. M., Gustafsson, P., and Oquist, G. (1993) 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. 90, 11985-11989
26. Sander, J., Nowaczyk, M., Buchta, J., Dau, H., Vass, I., Deák, Z., Dorogi, M., Iwai, M., and Rögner, M. (2010) Functional characterization and quantification of the alternative psbA copies in Thermosynechococcus elongatus and their role in photoprotection. J. Biol. Chem. 285, 29851-29856
27. Clarke, A. K., Soitamo, A., Gustafsson, P., and Oquist, G. (1993) 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. 90, 9973-9977
28. Kulkarni, R. D., and Golden, S. S. (1994) 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. 176, 959-965
29. Tichý, M., Lupínková, L., Sicora, C., Vass, I., Kuviková, S., Prásil, O., and Komenda, J. (2003) Synechocystis 6803 mutants expressing distinct forms of the photosystem II D1 protein from Synechococcus 7942. Relationship between the psbA coding region and sensitivity to visible and UV-B radiation. Biochim. Biophys. Acta 1605, 55-66
30. Schreiber, U. (2004) in Chlorophyll a Fluorescence: A Signature of Photosynthesis (Papageorgiou, G. C., and Govindjee, eds) pp. 279-319, Springer, Dordrecht, The Netherlands
31. Manuell, A. L., Beligni, M. V., Elder, J. H., Siefker, D. T., Tran, M., Weber, A., McDonald, T. L., and Mayfield, S. P. (2007) Robust expression of a bioactive mammalian protein in Chlamydomonas chloroplast. Plant Biotechnol. J. 5, 402-412
32. Rasala, B. A., Muto, M., Sullivan, J., and Mayfield, S. P. (2011) Improved heterologous protein expression in the chloroplast of Chlamydomonas reinhardtii through promoter and 5'-untranslated region optimization. Plant Biotechnol. J. 9, 674-683
33. Sueoka, N. (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U.S.A. 46, 83-91
34. Zwietering, M. H., Jongenburger, I., Rombouts, F. M., and van 't Riet, K. (1990) Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56, 1875-1881
35. Porra, R. J., Thompson, W. A., and Kriedemann, P. E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384-394
36. Chen, R., Gyokusen, M., Nakazawa, Y., and Gyokusen, K. (2010) Selection of housekeeping genes for transgene expression analysis in Eucommia ulmoides Oliver using real time RT-PCR. J. Bot. 2010
37. Mayfield, S. P., Cohen, A., Danon, A., and Yohn, C. B. (1994) Translation of the psbA mRNA of Chlamydomonas reinhardtii requires a structured RNA element contained within the 5'-untranslated region. J. Cell Biol. 127, 1537-1545
38. Schuster, G., Timberg, R., and Ohad, I. (1988) Turnover of thylakoid photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. Eur. J. Biochem. 177, 403-410
39. Shim, H., Cao, J., Govindjee, and Debrunner, P. G. (1990) Purification of highly active oxygen-evolving photosystem II from Chlamydomonas reinhardtii. Photosynth. Res. 26, 223-228
40. Gokhale, Z., and Sayre, R. T. (2009) in The Chlamydomonas Sourcebook (Stern, D. B., ed) pp. 573-602, Academic Press, Amsterdam
41. Berthold, D. A., Babcock, G. T., and Yocum, C. F. (1981)Ahighly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett. 134, 231-234
42. Mason, C. B., Bricker, T. M., and Moroney, J. V. (2006)Arapid method for chloroplast isolation from the green alga Chlamydomonas reinhardtii. Nat. Protoc. 1, 2227-2230
43. Babcock, G. T., Ghanotakis, D. F., Ke, B., and Diner, B. A. (1983) Electron donation to photosystem II in reaction center preparations. Biochim. Bio-phys. Acta 723, 276-286
44. Ananyev, G. M., and Dismukes, G. C. (1996) Assembly of the tetra-Mn site of photosynthetic water oxidation by photoactivation. Mn stoichiometry and detection of a new intermediate. Biochemistry 35, 4102-4109
45. Ananyev, G., and Dismukes, G. C. (2005)Howfast can photosystem II split water? Kinetic performance at high and low frequencies. Photosynth. Res. 84, 355-365
46. Kolling, D. R., Brown, T. S., Ananyev, G., and Dismukes, G. C. (2009) Photosynthetic oxygen evolution is not reversed at high oxygen pressures. Mechanistic consequences for the water-oxidizing complex. Biochemistry 48, 1381-1389
47. Kok, B., Forbush, B., and McGloin, M. (1970) Cooperation of charges in photosyntheticO2 evolution-I.Alinear four-step mechanism. Photochem. Photobiol. 11, 457-475
48. Forbush, B., Kok, B., and McGloin, M. P. (1971) Cooperation of charges in photosynthetic O2 evolution-II. Damping of flash yield oscillation, deactivation. Photochem. Photobiol. 14, 307-321
49. Lavorel, J. (1976) Matrix analysis of the oxygen evolving system of photosynthesis. J. Theor. Biol. 57, 171-185
50. Delrieu, M. J., and Rosengard, F. (1987) Fundamental differences between period-4 oscillations of the oxygen and fluorescence yield induced by flash excitation in inside-out thylakoids. Biochim. Biophys. Acta 892, 163-171
51. Shinkarev, V. P. (2005) Flash-induced oxygen evolution in photosynthesis: Simple solution for the extended S-state model that includes misses, double-hits, inactivation, and backward-transitions. Biophys. J. 88, 412-421
52. Powell, M. J. D. (2009) The BOBYQA Algorithm for Bound Constrained Optimization Without Derivatives. Technical Report NA2009/06, Cambridge, UK
53. Johnson, S. G. (2011) The NLopt Nonlinear Optimization Package, Version 2.2.4, Massachusetts Institute of Technology, Cambridge, MA
54. Joliot, P., and Kok, B. (1975) in Bioenergetics of Photosynthesis (Govindjee, ed) pp. 387-412, Academic Press, New York
55. Messinger, J., Schröder, W. P., and Renger, G. (1993) Structure-function relations in photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution. Biochemistry 32, 7658-7668
56. Vass, I., and Styring, S. (1991) pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry 30, 830-839
57. Sugiura, M., and Inoue, Y. (1999) Highly purified thermo-stable oxygenevolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol. 40, 1219-1231
58. Kulkarni, R., and Golden, S. (1995) Form II of D1 is important during transition from standard to high light intensity in Synechococcus sp. strain PCC 7942. Photosynth. Res. 46, 435-443
59. Morton, B. R. (1996) Selection on the codon bias of Chlamydomonas reinhardtii chloroplast genes and the plant psbA gene. J. Mol. Evol. 43, 28-31
60. Mayfield, S. P., Manuell, A. L., Chen, S., Wu, J., Tran, M., Siefker, D., Muto, M., and Marin-Navarro, J. (2007) Chlamydomonas reinhardtii chloroplasts as protein factories. Curr. Opin. Biotechnol. 18, 126-133
61. Rutherford, A. W., Osyczka, A., and Rappaport, F. (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer. Redox tuning to survive life in O2. FEBS Lett. 586, 603-616
62. Vass, I., and Cser, K. (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci. 14, 200-205
63. Prasil, O., Kolber, Z., Berry, J. A., and Falkowski, P. G. (1996) Cyclic electron flow around photosystem II in vivo. Photosynth. Res. 48, 395-410
64. Whitmarsh, J., and Cramer, W. A. (1978) A pathway for the reduction of cytochrome b-559 by photosystem II in chloroplasts. Biochim. Biophys. Acta 501, 83-93
65. Buser, C. A., Diner, B. A., and Brudvig, G. W. (1992) Photooxidation of cytochrome b559 in oxygen-evolving photosystem II. Biochemistry 31, 11449-11459
66. Shinopoulos, K. E., and Brudvig, G. W. (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim. Biophys. Acta 1817, 66-75
67. Sane, P. V., Ivanov, A. G., Sveshnikov, D., Huner, N. P., and Oquist, G. (2002) A transient exchange of the photosystem II reaction center protein D1:1 with D1:2 during low temperature stress of Synechococcus sp. PCC 7942 in the light lowers the redox potential of QB. J. Biol. Chem. 277, 32739-32745
68. Chen, G., Han, G., Göransson, E., Mamedov, F., and Styring, S. (2012) Stability of the S3 and S2 state intermediates in photosystem II directly probed by EPR spectroscopy. Biochemistry 51, 138-148
69. Dyer, B. D. (2003) A Field Guide to Bacteria, pp. 232-263, Cornell University Press, Ithaca, NY
70. Stambler, N., and Dubinsky, Z. (2007) in Algae and Cyanobacteria in Extreme Environments (Seckbach, J., ed) pp. 81-97, Springer, Dordrecht, The Netherlands
71. Loll, B., Broser, M., Kós, P. B., Kern, J., Biesiadka, J., Vass, I., Saenger, W., and Zouni, A. (2008) Modeling of variant copies of subunit D1 in the structure of photosystem II from Thermosynechococcus elongatus. Biol. Chem. 389, 609-617