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Photosynthesis Research

, Volume 35, Issue 3, pp 323–343 | Cite as

Properties of inactive Photosystem II centers

  • Jérôme Lavergne
  • Edlira Leci
Regular Paper

Abstract

A fraction (usually in the range of 10–25%) of PS II centers is unable to transfer electrons from the primary quinone acceptor QA to the secondary acceptor QB. These centers are inactive with respect to O2 evolution since their reopening after photochemical charge separation to the S2OA- state involves predominantly a back reaction to S1QA in the few seconds time range (slower phases are also occurring). Several properties of these centers are analyzed by fluorescence and absorption change experiments. The initial rise phase Fo-Fpl of fluorescence induction under weak illumination reflects both the closure of inactive centers and the modulation of the fluorescence yield by the S-states of the oxygen-evolving system: We estimate typical relative amplitudes of these contributions as, respectively, 65 and 35% of the Fo-Fpl amplitude. The half-rise time of this phase is significantly shorter than for the fluorescence induction in the presence of DCMU (in which all centers are involved). This finding is shown to be consistent with inactive centers sharing the same light-harvesting antenna as normal centers, a view which is also supported by comparing the dependence of the fluorescence yield on the amount of closed active or inactive centers estimated through absorption changes. It is argued that the exponential kinetics of the Fo-Fpl phase does not indicate absence of excitation energy transfer between the antennas of inactive and active centers. We show that the acceptor dichlorobenzoquinone does not restore electron transfer in inactive centers, in disagreement with previous suggestions. We confirm, however, the enhancement of steady-state electron flow caused by this quinone and suggest that it acts by relieving a blocking step involved in the reoxidation of a fraction of the plastoquinone pool. Part of the discrepancies between the present results and those from previous literature may arise from the confusion of inactive centers characterized on a single turnover basis and PS II centers that become blocked under steady-state conditions because of deficient reoxidation of their secondary acceptors.

Key words DCBQ Fluorescence induction inactive centers light-harvesting antenna Photosystem II centers oxygen evolving system 

Abbreviations

DCBQ

2,6-dichloro-p-benzoquinone

DCMU

3-(3,4-dichlorophenyl)-1,1-dimethylurea

DMQ

2,5-dimethyl-p-benzoquinone

PS

photosystem

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References

  1. Bennoun P (1970) Réoxydation du quencher de fluorescence ‘Q’ en présence de 3-(3,4-dichlorophenyl)-1,1-dimethylurée. Biochim Biophys Acta 216: 357–363PubMedGoogle Scholar
  2. Berthold DA, Babcock GT and Yocum CF (1981) A highly resolved oxygen evolving Photosystem II preparation from spinach thylakoid membranes. EPR and electron transport properties. Febs Lett 134: 231–234Google Scholar
  3. Cao J and Govindjee (1990) Chlorophyll a fluorescence transient as an indicator of active and inactive Photosystem II in thylakoid membranes. Biochim Biophys Acta 1015: 180–188PubMedGoogle Scholar
  4. Chow WS, Hope AB and Anderson JM (1991) Further studies on quantifying Photosystem II in vivo by flash-induced oxygen yield from leaf discs. Aust J Plant Physiol 18: 397–410Google Scholar
  5. Chylla RA and Whitmarsh J (1990) Light saturation response of inactive Photosystem II reaction centers in spinach. Photosynth Res 25: 39–48Google Scholar
  6. Chylla RA, Garab G and Whitmarsh J (1987) Evidence for slow turnover in a fraction of Photosystem II complexes in thylakoid membranes. Biochim Biophys Acta 894: 562–571Google Scholar
  7. Dekker JP, vanGorkom HJ, Wensink J and Ouwehand L (1984) Absorbance difference spectra of the successive redox states of the oxygen-evolving apparatus of photosynthesis. Biochim Biophys Acta 767: 1–9Google Scholar
  8. Delosme R (1971) New results about chlorophyll fluorescence in vivo. In: Forti G, Avron M and Melandri A (eds) Proceedings of the IInd Int Cong on Photosynthesis, pp 187–195. Dr W Junk publishers, The HagueGoogle Scholar
  9. Delrieu MJ and Rosengard F (1988) Characterization of two types of oxygen-evolving Photosystem II reaction center by the flash-induced oxygen and fluorescence yield. Biochim Biophys Acta 936: 39–49Google Scholar
  10. Diner B and Joliot P (1976) Effect of the transmembrane electric field on the photochemical and quenching properties of Photosystem II in vivo. Biochim Biophys Acta 423: 479–498PubMedGoogle Scholar
  11. Etienne AL (1974) Effects of carbonyl cyanide m-chlorophenyl-hydrazone and hydroxylamine on the Photosystem II electron exchange mechanism in 3-(3,4-dichlorophenyl)-1,1-dimethylurea treated algae and chloroplasts. Biochim Biophys Acta 333: 497–508PubMedGoogle Scholar
  12. Graan T and Ort DR (1986) Detection of oxygen-evolving Photosystem II centers inactive in plastoquinone reduction. Biochim Biophys Acta 852: 320–330Google Scholar
  13. Guenther JE and Melis A (1990) The Physiological Significance of Photosystem II heterogeneity in chloroplasts. Photosynth Res 23: 105–109Google Scholar
  14. Hsu BD and Lee JY (1991) Characterization of the Photosystem II centers inactive in plastoquinone reduction by fluorescence induction. Photosynth Res 27: 143–150Google Scholar
  15. Joliot A and Joliot P (1964) Etude cinétique de la réaction photochimique libérant l'oxygène au cours de la photosynthèse. CR Acad Sc Paris 258: 3622–4625Google Scholar
  16. Joliot P and Joliot A (1977) Evidence for a double hit process in Photosystem II based on fluorescence studies. Biochim Biophys Acta 462: 558–574Google Scholar
  17. Joliot P and Joliot A (1984) Electron transfer between the two photosystems. I. Flash excitation under oxidizing conditions. Biochim Biophys Acta 765: 210–218Google Scholar
  18. Joliot P and Joliot A (1992) Electron transfer between Photosystem II and the cytochrome b/f complex: Mechanistic and structural implications. Biochim Biophys Acta 1102: 53–61Google Scholar
  19. Joliot P, Joliot A and Kok B (1968) Analysis of the interactions between the two photosystems in isolated chloroplasts. Biochim Biophys Acta 153: 635–652PubMedGoogle Scholar
  20. Joliot P, Joliot A, Bouges B and Barbieri G (1971) Studies of System II photocenters by comparative measurements of luminescence, fluorescence and oxygen emission. Photochem Photobiol 14: 287–305Google Scholar
  21. Joliot P, Béal D and Frilley B (1980) Une nouvelle méthode spectrophotométrique destinée à l'étude des réactions photosynthétiques. J Chimie Physique 77: 209–216Google Scholar
  22. Joliot P, Lavergne J and Béal D (1990) Organization of the plastoquinone pool in chloroplasts: Evidence for clusters of different sizes. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 2, pp 879–882. Kluwer Academic Publishers, DordrechtGoogle Scholar
  23. Joliot P, Lavergne J and Béal D (1992) Plastoquinone compartmentation in chloroplasts. I. Evidence for domains with different rates of photoreduction. Biochim Biophys Acta 1101: 1–12Google Scholar
  24. Jursinic PA and Dennenberg RJ (1988) Enhanced oxygen yields caused by double turnovers of Photosystem II induced by dichlorobenzoquinone. Biochim Biophys Acta 934: 177–185Google Scholar
  25. Kyle DJ, Ohad I and Arntzen CJ (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplasts membranes. Proc Natl Acad Sci USA 81: 4070–4074Google Scholar
  26. Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74: 566–574Google Scholar
  27. Lacambra M, Larsen U, Olive J, Bennoun P and Wollman FA (1984) Mutants of Chlorella Sorokiniana: A new material for photosynthesis studies. I. Characterization of the thylakoid membranes of wild type and mutant strains. Photobiochem Photobiophys 8: 191–205Google Scholar
  28. Lavergne J (1982a) Two types of primary acceptor in chloroplasts Photosystem II. I. Different recombination properties. Photobiochem Photobiophys 3: 257–271Google Scholar
  29. Lavergne J (1982b) Two types of primary acceptor in chloroplasts Photosystem II. II. Reduction in two successive Photoacts. Photobiochem Photobiophys 3: 273–285Google Scholar
  30. Lavergne J (1987) Optical difference spectra of the S-state transitions in the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 894: 91–107Google Scholar
  31. Lavergne J (1991) Improved UV-visible spectra of the S-transitions in the photosynthetic oxygen-evolving systems. Biochim Biophys Acta 1060: 175–188Google Scholar
  32. Lavergne J and Etienne AL (1980) Prompt and delayed fluorescence of chloroplasts upon mixing with dichlorophenyldimethylurea Biochim Biophys Acta 593: 136–148PubMedGoogle Scholar
  33. Lavergne J and Joliot P (1991) Restricted diffusion in photosynthetic membranes. Trends Bio Sci 16: 129–134CrossRefGoogle Scholar
  34. Lavergne J, Delosme R, Larsen U and Bennoun P (1984) Mutants of Chlorella Sorokiniana: A new material for photosynthesis studies. II. Improved spectroscopic analysis of electron transfer in mutant strains. Photobiochem Photobiophys 8: 207–219Google Scholar
  35. Lavergne J, Bouchaud JP and Joliot P (1992) Plastoquinone compartmentation in chloroplasts. II. Theoretical aspects. Biochim Biophys Acta 1101: 13–22Google Scholar
  36. Malkin S and Kok B (1966) Fluorescence induction studies in isolated chloroplasts. I, Number of components involved in the reaction and quantum yields. Biochim Biophys Acta 126: 413–432PubMedGoogle Scholar
  37. Melis A (1985) Functional properties of Photosystem IIβ in spinach chloroplasts. Biochim Biophys Acta 808: 334–342Google Scholar
  38. Melis A and Homann PH (1976) Heterogeneity of the photochemical centers in System II of chloroplasts. Photochem Photobiol 23: 343–350PubMedGoogle Scholar
  39. Nedbal L, Gibas C and Whitmarsh J (1991) Light saturation curves show competence of the water splitting complex in inactive Photosystem II reaction centers. Photosynth Res 30: 85–94Google Scholar
  40. Paillotin G (1976) Movement of excitations in the photosynthetic domains of Photosystem II. J Theor Biol 58: 237–252Google Scholar
  41. Rappaport F and Lavergne J (1991) Proton release during successive oxidation steps of the photosynthetic water oxidation process: Stoichiometries and pH dependence. Biochemistry 30: 10004–10012PubMedGoogle Scholar
  42. Saygin Ö and Witt HT (1985) Evidence for the electrochromic identification of the change of charges in the four oxidation steps of the photo-induced water cleavage in photosynthesis. FEBS Lett 187: 224–226CrossRefGoogle Scholar
  43. Velthuys BR and Amesz J (1974) Charge accumulation at the reducing side of System 2 of photosynthesis. Biochim Biophys Acta 333: 85–94Google Scholar
  44. Vos MH, vanGorkom HJ and vanLeeuwen PJ (1991) An electroluminescence study of stabilization reactions in the oxygen-evolving complex of Photosystem II. Biochim Biophys Acta 1056: 27–39Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Jérôme Lavergne
    • 1
  • Edlira Leci
    • 2
  1. 1.Institut de Biologie Physico-ChimiqueParisFrance
  2. 2.Fakulteti i Shkencave te Natyres, Katedra e BiofizikesUniversiteti i TiranesTiranaAlbania

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