DOI: 10.1098/rstb.2002.1134. Photosystem II and photosynthetic oxidation of water: an overview

Photosystem II and photosynthetic oxidation of water: an overview

10.1098/rstb.2002.1134

Crossref journal-article

The Royal Society

Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences (175)

Abstract

Conceptually, photosystem II, the oxygen–evolving enzyme, can be divided into two parts: the photochemical part and the catalytic part. The photochemical part contains the ultra–fast and ultra–efficient light–induced charge separation and stabilization steps that occur when light is absorbed by chlorophyll. The catalytic part, where water is oxidized, involves a cluster of Mn ions close to a redox–active tyrosine residue. Our current understanding of the catalytic mechanism is mainly based on spectroscopic studies. Here, we present an overview of the current state of knowledge of photosystem II, attempting to delineate the open questions and the directions of current research.

Bibliography

Goussias, C., Boussac, A., & Rutherford, A. W. (2002). Photosystem II and photosynthetic oxidation of water: an overview. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1426), 1369â1381.

Authors 3

Charilaos Goussias (first)
Alain Boussac (additional)
A. William Rutherford (additional)

References 97 Referenced 150

10.1021/bi00028a010
10.1021/ja981471c
10.1016/S0005-2728(00)00215-2
10.1098/rstb.2002.1144
10.1016/S1010-6030(01)00503-2
10.1016/S0968-0004(98)01348-6
10.1021/bi00500a014
10.1039/a703381h
10.1016/0014-5793(88)80071-1
10.1021/bi00409a052
10.1021/bi00449a005
10.1021/bi00119a036
10.1021/bi001159r
Britt R. D. 1996 Oxygen evolution. In Oxygenic photosysnthesis: the light reactions (ed. D. R. Ort & C. F. Yocum) pp. 137-164. Dordrecht The Netherlands: Kluwer. (10.1007/0-306-48127-8_9)
10.1073/pnas.83.13.4586
10.1021/ja991402d
10.1007/s00775-001-0305-3
10.1016/S0005-2728(00)00230-9
10.1016/0005-2728(92)90133-M
Debus R. J. 2000 The polypeptides of photosystem II and their influence on manganotyrosyl-based oxygen evolution. In Metals in biological systems vol. 37 (ed. H. Sigel & A. Sigel) p. 65. New York: Marcel Dekker.
10.1016/S0005-2728(00)00221-8
Dekker J. P. 1992 Optical studies on the oxygen evolving complex of photosystem II. In Manganese redox enzymes (ed. V. L. Pecoraro) pp. 85-101. New York: VCH Publishers.
10.1023/A:1006468024245
10.1016/S0005-2728(00)00220-6
Diner B. A. & Babcock G. T. 1996 Structure dynamics and energy conversion efficiency in photosystem II. In Oxygenic photosysnthesis: the light reactions (ed. D. R. Ort & C. F. Yocum) pp. 213-247. Dordrecht The Netherlands: Kluwer. (10.1007/0-306-48127-8_12)
10.1021/bi010121r
10.1073/pnas.78.1.274
10.1073/pnas.92.21.9545
10.1021/bi962899w
10.1146/annurev.arplant.48.1.641
10.1016/S0014-5793(01)02766-1
10.1021/bi990633u
10.1021/bi973057f
10.1016/S0005-2728(99)00045-6
10.1016/S0005-2728(00)00225-5
10.1126/science.277.5334.1953
Hoganson C. W. & Babcock G. T. 2000 Mechanistic aspects of the tyrosyl radical-manganese complex in photosynthetic water oxidation. In Metals in biological systems vol. 37 (ed. H. Sigel & A. Sigel) pp. 613-656. New York: Marcel Dekker.
10.1021/bi9710885
10.1021/bi000131c
10.1007/PL00010664
10.1021/bi9817360
10.1111/j.1751-1097.1969.tb05696.x
10.1111/j.1751-1097.1970.tb06017.x
10.1016/0005-2728(86)90107-6
10.1016/S0005-2728(00)00218-8
10.1126/science.283.5407.1524
10.1021/bi961244s
10.1021/ja981494r
10.1021/bi9818570
10.1016/S0005-2728(00)00187-0
10.1021/bi00245a027
10.1021/ja004307
10.1021/bi00401a001
10.1002/anie.199418391
10.1016/0005-2728(86)90125-8
10.1016/0014-5793(86)80745-1
Pecoraro V. L. & Hsieh W. Y. 2000 The use of model complexes to elucidate the structure and function of manganese redox enzymes. In Metals in biological systems vol. 37 (ed. H. Sigel & A. Sigel) pp. 429-504. New York: Marcel Dekker.
10.1021/cr00027a012
10.1351/pac199870040925
10.1016/S0005-2728(00)00219-X
10.1021/ja981196u
10.1021/ja002104f
10.1021/jp002323n
10.1021/bi00105a027
10.1016/S0005-2728(00)00228-0
10.1016/S0005-2728(00)00227-9
10.1016/0014-5793(92)80092-U
10.1038/24421
10.1016/S0005-2728(00)00217-6
Rutherford A. W. 1988 Phototsystem II the oxygen evolving photoystem. In Light-energy transduction in photosynthesis: higher plant and bacterial models (ed. S. E. Stevens Jr & D. A. Bryant) pp. 163-177. Rockville MD: American Society of Plant Physiologists.
10.1016/0968-0004(89)90032-7
Rutherford A. W. & Nitschke W. 1996 Photosystem II and the quinone-iron-containing reaction centers/comparisons and evolutionary perspectives. In Origin and evolution of biological energy conversion (ed. H. Baltscheffsky) pp. 143-175. New York: VCH Publishers Inc.
10.1016/0005-2728(82)90061-5
10.1021/bi972828c
10.1021/bi015903z
10.1074/jbc.274.43.30387
10.1006/jmbi.1998.1824
Sharp R. R. 1992 Proton NMR relaxation due to the photosynthetic oxygen evolving center. In Magnetic redox enzymes (ed. V. L. Pecoraro) pp. 177-196. New York: VCH Publishers Inc.
10.1021/bi971676i
10.1016/S0005-2728(98)00139-X
10.1021/bi00383a001
10.1021/bi00413a049
10.1021/bi960764k
10.1016/0005-2728(87)90019-3
10.1016/S0005-2728(00)00069-4
10.1021/bi9514471
10.1007/BF02184169
10.1016/0005-2728(84)90028-8
10.1016/S0020-1693(00)81142-1
10.1016/0005-2728(87)90069-7
10.1098/rstb.2002.1136
10.1016/S0005-2728(00)00214-0
10.1021/bi982295n
10.1098/rstb.2002.1133
10.1021/cr950052k
10.1021/ic9512340
10.1038/35055589

Dates

Type	When
Created	22 years, 9 months ago (Nov. 18, 2002, 5:42 p.m.)
Deposited	4 years, 6 months ago (Feb. 18, 2021, 11:32 p.m.)
Indexed	1 day ago (Aug. 29, 2025, 6:04 a.m.)
Issued	22 years, 10 months ago (Oct. 29, 2002)
Published	22 years, 10 months ago (Oct. 29, 2002)
Published Online	22 years, 10 months ago (Oct. 29, 2002)
Published Print	22 years, 10 months ago (Oct. 29, 2002)

Funders 0

None

BibTeX

@article{Goussias_2002, title={Photosystem II and photosynthetic oxidation of water: an overview}, volume={357}, ISSN={1471-2970}, url={http://dx.doi.org/10.1098/rstb.2002.1134}, DOI={10.1098/rstb.2002.1134}, number={1426}, journal={Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences}, publisher={The Royal Society}, author={Goussias, Charilaos and Boussac, Alain and Rutherford, A. William}, editor={Barber, J. and Anderson, J. M}, year={2002}, month=oct, pages={1369–1381} }

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