Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Jan 29;358(1429):245–253. doi: 10.1098/rstb.2002.1186

Photosystem II: evolutionary perspectives.

A W Rutherford 1, P Faller 1
PMCID: PMC1693113  PMID: 12594932

Abstract

Based on the current model of its structure and function, photosystem II (PSII) seems to have evolved from an ancestor that was homodimeric in terms of its protein core and contained a special pair of chlorophylls as the photo-oxidizable cofactor. It is proposed that the key event in the evolution of PSII was a mutation that resulted in the separation of the two pigments that made up the special chlorophyll pair, making them into two chlorophylls that were neither special nor paired. These ordinary chlorophylls, along with the two adjacent monomeric chlorophylls, were very oxidizing: a property proposed to be intrinsic to monomeric chlorophylls in the environment provided by reaction centre (RC) proteins. It seems likely that other (mainly electrostatic) changes in the environments of the pigments probably tuned their redox potentials further but these changes would have been minor compared with the redox jump imposed by splitting of the special pair. This sudden increase in redox potential allowed the development of oxygen evolution. The highly oxidizing homodimeric RC would probably have been not only inefficient in terms of photochemistry and charge storage but also wasteful in terms of protein or pigments undergoing damage due to the oxidative chemistry. These problems would have constituted selective pressures in favour of the lop-sided, heterodimeric system that exists as PSII today, in which the highly oxidized species are limited to only one side of the heterodimer: the sacrificial, rapidly turned-over D1 protein. It is also suggested that one reason for maintaining an oxidizable tyrosine, TyrD, on the D2 side of the RC, is that the proton associated with its tyrosyl radical, has an electrostatic role in confining P(+) to the expendable D1 side.

Full Text

The Full Text of this article is available as a PDF (176.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ananyev G. M., Zaltsman L., Vasko C., Dismukes G. C. The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):52–68. doi: 10.1016/s0005-2728(00)00215-2. [DOI] [PubMed] [Google Scholar]
  2. Barber J., Nield J., Morris E. P., Hankamer B. Subunit positioning in photosystem II revisited. Trends Biochem Sci. 1999 Feb;24(2):43–45. doi: 10.1016/s0968-0004(98)01348-6. [DOI] [PubMed] [Google Scholar]
  3. Baymann F., Brugna M., Mühlenhoff U., Nitschke W. Daddy, where did (PS)I come from? Biochim Biophys Acta. 2001 Oct 30;1507(1-3):291–310. doi: 10.1016/s0005-2728(01)00209-2. [DOI] [PubMed] [Google Scholar]
  4. Beanland T. J. Evolutionary relationships between "Q-type" photosynthetic reaction centres: hypothesis-testing using parsimony. J Theor Biol. 1990 Aug 23;145(4):535–545. doi: 10.1016/s0022-5193(05)80487-4. [DOI] [PubMed] [Google Scholar]
  5. Bibby T. S., Nield J., Barber J. Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature. 2001 Aug 16;412(6848):743–745. doi: 10.1038/35089098. [DOI] [PubMed] [Google Scholar]
  6. Blankenship R. E., Hartman H. The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci. 1998 Mar;23(3):94–97. doi: 10.1016/s0968-0004(98)01186-4. [DOI] [PubMed] [Google Scholar]
  7. Blankenship R. E. Origin and early evolution of photosynthesis. Photosynth Res. 1992;33:91–111. [PubMed] [Google Scholar]
  8. Boerner R. J., Bixby K. A., Nguyen A. P., Noren G. H., Debus R. J., Barry B. A. Removal of stable tyrosine radical D+ affects the structure or redox properties of tyrosine Z in manganese-depleted photosystem II particles from Synechocystis 6803. J Biol Chem. 1993 Jan 25;268(3):1817–1823. [PubMed] [Google Scholar]
  9. Carrell G., Tyryshkin M., Dismukes C. An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J Biol Inorg Chem. 2001 Nov 8;7(1-2):2–22. doi: 10.1007/s00775-001-0305-3. [DOI] [PubMed] [Google Scholar]
  10. Davis M. S., Forman A., Fajer J. Ligated chlorophyll cation radicals: Their function in photosystem II of plant photosynthesis. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4170–4174. doi: 10.1073/pnas.76.9.4170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Debus R. J. Amino acid residues that modulate the properties of tyrosine Y(Z) and the manganese cluster in the water oxidizing complex of photosystem II. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):164–186. doi: 10.1016/s0005-2728(00)00221-8. [DOI] [PubMed] [Google Scholar]
  12. Debus R. J., Barry B. A., Babcock G. T., McIntosh L. Site-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci U S A. 1988 Jan;85(2):427–430. doi: 10.1073/pnas.85.2.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dekker J. P., Van Grondelle R. Primary charge separation in Photosystem II. Photosynth Res. 2000;63(3):195–208. doi: 10.1023/A:1006468024245. [DOI] [PubMed] [Google Scholar]
  14. Diner B. A., Schlodder E., Nixon P. J., Coleman W. J., Rappaport F., Lavergne J., Vermaas W. F., Chisholm D. A. Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry. 2001 Aug 7;40(31):9265–9281. doi: 10.1021/bi010121r. [DOI] [PubMed] [Google Scholar]
  15. Diner Bruce A., Rappaport Fabrice. Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol. 2002;53:551–580. doi: 10.1146/annurev.arplant.53.100301.135238. [DOI] [PubMed] [Google Scholar]
  16. Dorlet P., Rutherford A. W., Un S. Orientation of the tyrosyl D, pheophytin anion, and semiquinone Q(A)(*)(-) radicals in photosystem II determined by high-field electron paramagnetic resonance. Biochemistry. 2000 Jul 4;39(26):7826–7834. doi: 10.1021/bi000175l. [DOI] [PubMed] [Google Scholar]
  17. Durrant J. R., Klug D. R., Kwa S. L., van Grondelle R., Porter G., Dekker J. P. A multimer model for P680, the primary electron donor of photosystem II. Proc Natl Acad Sci U S A. 1995 May 23;92(11):4798–4802. doi: 10.1073/pnas.92.11.4798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goussias Charilaos, Boussac Alain, Rutherford A. William. Photosystem II and photosynthetic oxidation of water: an overview. Philos Trans R Soc Lond B Biol Sci. 2002 Oct 29;357(1426):1369–1420. doi: 10.1098/rstb.2002.1134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Guergova-Kuras M., Boudreaux B., Joliot A., Joliot P., Redding K. Evidence for two active branches for electron transfer in photosystem I. Proc Natl Acad Sci U S A. 2001 Mar 27;98(8):4437–4442. doi: 10.1073/pnas.081078898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hillmann B., Brettel K., van Mieghem F., Kamlowski A., Rutherford A. W., Schlodder E. Charge recombination reactions in photosystem II. 2. Transient absorbance difference spectra and their temperature dependence. Biochemistry. 1995 Apr 11;34(14):4814–4827. doi: 10.1021/bi00014a039. [DOI] [PubMed] [Google Scholar]
  21. Jordan P., Fromme P., Witt H. T., Klukas O., Saenger W., Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature. 2001 Jun 21;411(6840):909–917. doi: 10.1038/35082000. [DOI] [PubMed] [Google Scholar]
  22. Koulougliotis D., Tang X. S., Diner B. A., Brudvig G. W. Spectroscopic evidence for the symmetric location of tyrosines D and Z in photosystem II. Biochemistry. 1995 Mar 7;34(9):2850–2856. doi: 10.1021/bi00009a015. [DOI] [PubMed] [Google Scholar]
  23. Krauss N., Schubert W. D., Klukas O., Fromme P., Witt H. T., Saenger W. Photosystem I at 4 A resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nat Struct Biol. 1996 Nov;3(11):965–973. doi: 10.1038/nsb1196-965. [DOI] [PubMed] [Google Scholar]
  24. Matysik J., Alia, Gast P., van Gorkom H. J., Hoff A. J., de Groot H. J. Photochemically induced nuclear spin polarization in reaction centers of photosystem II observed by 13C-solid-state NMR reveals a strongly asymmetric electronic structure of the P680(.+) primary donor chlorophyll. Proc Natl Acad Sci U S A. 2000 Aug 29;97(18):9865–9870. doi: 10.1073/pnas.170138797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mulkidjanian AY. Photosystem II of green plants: on the possible role of retarded protonic relaxation in water oxidation1 . Biochim Biophys Acta. 1999 Jan 27;1410(1):1–6. doi: 10.1016/s0005-2728(98)00174-1. [DOI] [PubMed] [Google Scholar]
  26. Nanba O., Satoh K. Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci U S A. 1987 Jan;84(1):109–112. doi: 10.1073/pnas.84.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nitschke W., Rutherford A. W. Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem Sci. 1991 Jul;16(7):241–245. doi: 10.1016/0968-0004(91)90095-d. [DOI] [PubMed] [Google Scholar]
  28. Noguchi T., Inoue Y., Satoh K. FT-IR studies on the triplet state of P680 in the photosystem II reaction center: triplet equilibrium within a chlorophyll dimer. Biochemistry. 1993 Jul 20;32(28):7186–7195. doi: 10.1021/bi00079a016. [DOI] [PubMed] [Google Scholar]
  29. Nugent J. H., Bratt P. J., Evans M. C., MacLachlan D. J., Rigby S. E., Ruffle S. V., Turconi S. Photosystem II electron transfer: the manganese complex to P680. Biochem Soc Trans. 1994 May;22(2):327–331. doi: 10.1042/bst0220327. [DOI] [PubMed] [Google Scholar]
  30. Olson J. M., Pierson B. K. Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol. 1987;108:209–248. doi: 10.1016/s0074-7696(08)61439-4. [DOI] [PubMed] [Google Scholar]
  31. Peloquin J. M., Britt R. D. EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):96–111. doi: 10.1016/s0005-2728(00)00219-x. [DOI] [PubMed] [Google Scholar]
  32. Rhee K. H., Morris E. P., Barber J., Kühlbrandt W. Three-dimensional structure of the plant photosystem II reaction centre at 8 A resolution. Nature. 1998 Nov 19;396(6708):283–286. doi: 10.1038/24421. [DOI] [PubMed] [Google Scholar]
  33. Robblee J. H., Cinco R. M., Yachandra V. K. X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):7–23. doi: 10.1016/s0005-2728(00)00217-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rutherford A. W., Faller P. The heart of photosynthesis in glorious 3D. Trends Biochem Sci. 2001 Jun;26(6):341–344. doi: 10.1016/s0968-0004(01)01874-6. [DOI] [PubMed] [Google Scholar]
  35. Rutherford A. W., Krieger-Liszkay A. Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci. 2001 Nov;26(11):648–653. doi: 10.1016/s0968-0004(01)01953-3. [DOI] [PubMed] [Google Scholar]
  36. Rutherford A. W., Paterson D. R., Mullet J. E. A light-induced spin-polarized triplet detected by EPR in photosystem II reaction centers. Biochim Biophys Acta. 1981 Apr 13;635(2):205–214. doi: 10.1016/0005-2728(81)90020-7. [DOI] [PubMed] [Google Scholar]
  37. Rutherford A. W. Photosystem II, the water-splitting enzyme. Trends Biochem Sci. 1989 Jun;14(6):227–232. doi: 10.1016/0968-0004(89)90032-7. [DOI] [PubMed] [Google Scholar]
  38. Schubert W. D., Klukas O., Saenger W., Witt H. T., Fromme P., Krauss N. A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J Mol Biol. 1998 Jul 10;280(2):297–314. doi: 10.1006/jmbi.1998.1824. [DOI] [PubMed] [Google Scholar]
  39. Stewart D. H., Brudvig G. W. Cytochrome b559 of photosystem II. Biochim Biophys Acta. 1998 Oct 5;1367(1-3):63–87. doi: 10.1016/s0005-2728(98)00139-x. [DOI] [PubMed] [Google Scholar]
  40. Telfer Alison. What is beta-carotene doing in the photosystem II reaction centre? Philos Trans R Soc Lond B Biol Sci. 2002 Oct 29;357(1426):1431-39; discussion 1439-40, 1469-70. doi: 10.1098/rstb.2002.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vermaas W. F. Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth Res. 1994;41:285–294. [PubMed] [Google Scholar]
  42. Vermass W. F., Rutherford A. W., Hansson O. Site-directed mutagenesis in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: Donor D is a tyrosine residue in the D2 protein. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8477–8481. doi: 10.1073/pnas.85.22.8477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zech S. G., Kurreck J., Eckert H. J., Renger G., Lubitz W., Bittl R. Pulsed EPR measurement of the distance between P680+. and Q(A)-. in photosystem II. FEBS Lett. 1997 Sep 8;414(2):454–456. doi: 10.1016/s0014-5793(97)01054-5. [DOI] [PubMed] [Google Scholar]
  44. Zouni A., Witt H. T., Kern J., Fromme P., Krauss N., Saenger W., Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature. 2001 Feb 8;409(6821):739–743. doi: 10.1038/35055589. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES