Photosystem II Heterogeneity

  • Jérôme Lavergne
  • Jean-Marie Briantais
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 4)


Two main topics are addressed in this chapter:’ static heterogeneities’ of PS II, as they appear in standard dark-adapted material, and ‘dynamic heterogeneities’ possibly involved in the non-photochemical quenching processes that modulate the steady-state yield of PS II. Three types of static heterogeneities and possible correlations between them are discussed: (i) Granal and stromal PS II. A fraction, around 10–15%, of the PS II complex is found in stroma lamellae. (ii) PS II α and β. A fraction, around 35%, of PS II (β) appears to have a smaller antenna size and to be organized in isolated units, in contrast with the major part of PS II (α). (iii) A fraction, around 15%, of PS II centers are blocked on the acceptor side (non QE-transferring) and thus inactive with regard to oxygen evolution. A unifying model has been proposed by Melis (1985,1991), wherein stromal PS II, PS IIβ and inactive centers represent essentially the same sub-population of PS II, assumed to reflect a dynamic stock in the biosynthetic turnover of the PS II complex. The various correlations implied by this model are reexamined and evaluated in light of the currently available data, and alternative interpretations are discussed. It is argued that inactive centers belong to PS IIα and that, on the other hand, stromal PS II centers are active. The antenna size of stromal PS II is probably consistent with their belonging to PS IIβ but the amount of the latter exceeds significantly that of stromal PS II: it is suggested that a significant part of PS IIα may be located in the grana margins. The concept of non-photochemical quenching ‘qN’ covers three different contributions. ‘qT’, that appears at low irradiance levels, is interpreted as a ‘state 2 transition’, involving detachment of a fraction of LHCII from PS II α and thus probably increasing the β-fraction ‘qE’, controlled by the lumenal pH, is the major contribution to non-photochemical quenching at physiological irradiances. Most of the available evidence supports its interpretation as due to a dissipation pathway at the antenna level. The alternative mechanism of a formation of inactive centers of the quenching sink type does not account for the results obtained in vivo in normal materials, but seems to prevail in LHCII-deficient material. At over-saturating intensities, the ‘qI’ quenching reflects photoinhibition associated with inactivation of PS II centers in a quenching sink state. Significant formation of non QR-transferring centers does not take place as a result of photodegradation or of blocking the synthesis of the PS II complex. At physiological irradiances, there is no evidence that a sub-population of damaged PS II centers could be ascribed to insufficient synthetic turnover of the PS II complex.


BBY – granal membrane preparation according to Berthold et al. (1981) DCBQ – 2,6-dichloro-p-benzoquinone DCMU – 3-(3,4-dichlorophenyl)-1,1-dimethylurea DCIP – 2,6- dichlorophenol-indophenol DMBQ – 2,6-dimethyl-p-benzo-quinone F – level of chlorophyll fluorescence Fo: level with all centers open Fpl: plateau reached after the first phase of the induction kinetics (weak light, no DCMU) Fs: steady-state level Fm: level with all centers closed LHCII – light-harvesting chlorophyll-protein complex II PpBQ–phenyl-p-benzoquinone PS – Photosystem 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Albertsson PÅ, Andreasson E and Svensson P (1990) The domain organization of the plant thylakoid membrane. FEBS Lett 273: 36–40PubMedCrossRefGoogle Scholar
  2. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335PubMedGoogle Scholar
  3. Anderson JM and Melis A (1983) Localization of different photosystems in separate regions of chloroplast membranes. Proc Natl Acad Sci USA 80: 745–749PubMedGoogle Scholar
  4. Andersson B and Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 593:427–440PubMedGoogle Scholar
  5. Andreasson E, Svensson P, Weibull C and Albertsson PÅ (1988) Separation and characterization of stroma and grana membranes–evidence for heterogeneity in antenna size of both photosystem I and photosystem II. Biochim Biophys Acta 936: 339–350Google Scholar
  6. Arntzen CJ, Armond PA, Briantais JM, Burke JJ and Novitzky WP (1976) Dynamic interactions among structural components of the chloroplasts membrane, in chlorophyll proteins, reaction centers and photosynthetic membranes. Brookhaven Symposia in Biology 28: 316–337PubMedGoogle Scholar
  7. Bassi R, Giacometti G and Simpson DJ (1988) Characterisation of stroma membranes from Zea Mays L. chloroplasts. Carlsberg Res Common 53: 221–232Google Scholar
  8. Bell DH and Hipkins MF (1985) Analysis of fluorescence induction curves from pea chloroplasts. Photosystem II reaction centre heterogeneity. Biochim Biophys Acta 807: 255–262Google Scholar
  9. Bennoun P and Li YS (1973) New results about the mode of action of DCMU in spinach chloroplasts. Biochim Biophys Acta 292: 162–168PubMedGoogle Scholar
  10. 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: 231–234CrossRefGoogle Scholar
  11. Bilger W and Björkman O (1990) Role of xanthophyll cycle in photoprotection elucidated by measurements of light induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25: 173–185Google Scholar
  12. Bilger W and Schreiber U (1986) Energy dependent quenching of dark level chlorophyll fluorescence in intact leaves. Photosynth Res 10: 303–308CrossRefGoogle Scholar
  13. Black MT, Brearley TH and Horton P (1986) Heterogeneity in chloroplast photosystem II. Photosynth Res 8: 193–207CrossRefGoogle Scholar
  14. Bradbury M and Baker NR (1984) A quantitative determination of photochemical and non-photochemical quenching during the slow phase of the chlorophyll fluorescence induction curve of bean leaves. Biochim Biophys Acta 765: 275–281Google Scholar
  15. Brearley T and Horton P (1984) Properties of photosystem IIα and photosystem IIβ in spinach chloroplasts. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol I, pp 433–436. Martinus Nijhoff/Dr W. Junk Publishers, The HagueGoogle Scholar
  16. Briantais JM (1994) Light-harvesting chlorophyll a–b complex requirement for regulation of photosystem II photochemistry by non-photochemical quenching. Photosynth Res 40: 287–294CrossRefGoogle Scholar
  17. Briantais JM, Vernotte C, Picaud M and Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138PubMedGoogle Scholar
  18. Briantais JM, Comic G and Hodges M (1988) The modification of chlorophyll fluorescence of Chlamydomonas reinhardtii by photoinhibition and chloramphenicol addition suggests a form of photosystem II less susceptible to degradation. FEBS Lett 236: 226–230CrossRefGoogle Scholar
  19. Briantais JM, Ducruet JM, Hodges M and Krause H (1992) The effects of low temperature acclimation and photoinhibitory treatments on photosystem 2 studied by thermoluminescence and fluorescence decay kinetics. Photosynth Res 31: 1–10CrossRefGoogle Scholar
  20. Butler WL, Visser JWM and Simons HL (1973) The kinetics of light-induced changes of C550, cytochrome b559 and fluorescence yield in chloroplasts at low temperature. Biochim Biophys Acta 292: 140–151PubMedGoogle Scholar
  21. Callahan FE, Becker DW and Cheniae GM (1986) Studies on the photoactivation of the water oxidizing enzyme II. Characterization of weak light photoinhibition of PS II and its light-induced recovery. Plant Physiol 82: 261–269PubMedGoogle Scholar
  22. Callahan FE, Wergin WP, Nelson N, Edelman M and Mattoo AK (1989) Distribution of thylakoid proteins between stromal and granal lamellae in Spirodela. Plant Physiol 91: 629–635PubMedGoogle Scholar
  23. 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
  24. Chow WS, Hope AB and Anderson JM (1990) A reassessment of the use of herbicide binding to measure photosystem II reaction centres in plant thylakoids. Photosynth Res 24: 109–113CrossRefGoogle Scholar
  25. 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
  26. Chylla RA and Whitmarsh J (1990) Light saturation response of inactive photosystem II reaction centers in spinach. Photosynth Res 25: 39–8CrossRefGoogle Scholar
  27. 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
  28. Cleland RE (1988) Molecular events of photoinhibitory inactivation in the reaction center of photosystem II. Aust J Plant Physiol 15: 135–150Google Scholar
  29. Cleland RE, Melis A and Neale PJ (1986) Mechanism of photoinhibition: Photochemical reaction center inactivation in system II of chloroplasts. Photosynth Res 9: 79–88CrossRefGoogle Scholar
  30. Critchley C (1988) The molecular mechanism of photoinhibition-facts and fiction. Aust J Plant Physiol 15: 27–41CrossRefGoogle Scholar
  31. Crofts J and Horton P (1991) Dissipation of excitation energy by photosystem II particles at low pH. Biochim Biophys Acta 1058: 187–193Google Scholar
  32. Dainese P, Marquardt J, Pineau B and Bassi R (1992a) Identification of violaxanthin and zeaxanthin binding proteins in maize photosystem II. In: Murata (ed) Research in Photosynthesis, Vol I, pp 287–290, Kluwer Academic Publishers, DordrechtGoogle Scholar
  33. Dainese P, Santini C, Ghiretti-Magaldi A, Marquardt J, Tidu V, Mauro S, Bergantino E and Bassi R (1992b) The organization of pigment-proteins within photosystem II. In Murata N (ed) Research in Photosynthesis, Vol II, pp 13–20. Kluwer Academic Publishers, DordrechtGoogle Scholar
  34. Dan H and Hansen UP (1990) A study of the energy-dependent quenching of chlorophyll fluorescence by means of photoacoustic measurements. Photosynth Res 25: 269–278Google Scholar
  35. Dau H (1994) Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60: 1–23Google Scholar
  36. Dekker JP, van Gorkom 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
  37. Delosme R (1967) Etude de lľinduction de fluorescence des algues vertes et des chloroplastes au début dďune illumination intense. Biochim Biophys Acta 143: 108–128PubMedGoogle Scholar
  38. Delrieu MJ and Rosengard F (1993) Events near the reaction center in O2 evolving PS II enriched thylakoid membranes: The presence of an electric field during the S2 state in a population of centers. Photosynth Res 37: 205–215CrossRefGoogle Scholar
  39. Demeter S, Rozza ZS, Vass I and Sallai A (1985) Thermo-luminescence study of charge recombination in photosystem II at low temperature. I Characterization of the Zv and A thermoluminescence bands. Biochim Biophys Acta 809: 369–378Google Scholar
  40. Demmig B and Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171: 171–184CrossRefGoogle Scholar
  41. Demmig-Adams B (1990) Carotenoids and photoprotection: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24Google Scholar
  42. Demmig-Adams B and Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626CrossRefGoogle Scholar
  43. Dennenberg RJ, Jursinic PA and McCarthy S (1986) Intactness of the oxygen-evolving system in thylakoids and photosystem II particles. Biochim Biophys Acta 852: 222–233Google Scholar
  44. Diner BA (1977) Dependence of the deactivation reactions of photosystem II on the redox state of plastoquinone pool A varied under anaerobic conditions. Equilibria on the acceptor side of photosystem II. Biochim Biophys Acta 460: 247–258PubMedGoogle Scholar
  45. Diner BA (1986) The reaction center of photosystem II. In Staehelin LA and Arntzen CJ (eds) Photosynthesis III, Encyclopedia of Plant Physiology, Vol 19, pp 422–436. Springer Verlag, BerlinGoogle Scholar
  46. Diner BA, Petrouleas V and Wendoloski JJ (1991) The ironquinone electron-acceptor complex of Photosystem II. Physiol Plant 81: 423–436CrossRefGoogle Scholar
  47. Doschek WW and Kok B (1972) Photon trapping in photosystem II of photosynthesis. Biophys J 12: 832–838PubMedCrossRefGoogle Scholar
  48. Edwards GE and Baker NR (1993) Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis? Photosynth Res 37: 89–102CrossRefGoogle Scholar
  49. Falkowski PG, Wyman K, Ley AC and Mauzerall DC (1986) Relationship of steady-state photosynthesis to fluorescence in eucaryotic algae. Biochim Biophys Acta 849: 183–192Google Scholar
  50. Forbush B and Kok B (1968) Reaction between primary and secondary electron acceptors of photosystem II of photo-synthesis. Biochim Biophys Acta 162: 243–253PubMedGoogle Scholar
  51. Genty B, Briantais JM and Baker NR (1989) The relationship between quantum yield of photosynthetic electron transfer and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92Google Scholar
  52. Genty B, Harbinson J, Briantais JM and Baker NR (1990a) The relationship between non-photochemical quenching of chlorophyll fluorescence and the rate of photosystem 2 photochemistry in leaves. Photosynth Res 25: 249–257CrossRefGoogle Scholar
  53. Genty B, Harbinson J, Briantais JM and Baker NR (1990b) The relationship between the relative quantum efficiencies of photosystems in leaves. Efficiency of PS2 in relation to nonphotochemical quenching. In: Baltcheffsky M (ed) Current Research in Photosynthesis, Vol IV, pp 365–368. Kluwer Academic Publishers, DordrechtGoogle Scholar
  54. Genty B, Wonders J and Baker NR (1990c) Non-photochemical quenching of Fo in leaves is emission wavelength dependent: Consequences for quenching analysis and its interpretation. Photosynth Res 26: 133–139CrossRefGoogle Scholar
  55. Genty B, Goulas Y, Dimon B, Peltier G, Briantais JM and Moya I (1992) Modulation of efficiency of primary conversion in leaves, mechanisms involved at PS2. In: Murata N (ed) Research in Photosynthesis, Vol IV, pp 603–610, Kluwer Acad Publishers, DordrechtGoogle Scholar
  56. Giardi MT, Rigoni F, Barbato R and Giacometti GM (1991) Relationship between heterogeneity of PS II in grana particles in vitro and phosphorylation. Biochem Biophys Res Comm 176: 1298–1305PubMedCrossRefGoogle Scholar
  57. Gilmore A and Yamamoto HY (1991) Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplast under artificially mediated linear and cyclic electron transport. Plant Physiol 96: 635–643PubMedGoogle Scholar
  58. Gilmore AM and Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35: 67–78CrossRefGoogle Scholar
  59. Govindjee (1990) Photosystem II heterogeneity: The acceptor side. Photosynth Res 25: 151–160CrossRefGoogle Scholar
  60. Graan T and Ort DR (1986) Detection of oxygen-evolving photosystem II centers inactive in plastoquinone reduction. Biochim Biophys Acta 852: 320–330Google Scholar
  61. Greer DH and Laing WA (1988) Photoinhibition of photosynthesis in intact kiwifruit (Actinida deliciosa) leaves: Effect of light during growth on photoinhibition and recovery. Planta 175: 355–363CrossRefGoogle Scholar
  62. Henrysson T and Sundby C (1990) Characterization of photosystem II in stroma thylakoid membranes. Photosynth Res 25: 107–117CrossRefGoogle Scholar
  63. Hodges M and Barber J (1983) Analysis of chlorophyll fluorescence induction kinetics exhibited by DCMU-inhibited thylakoids and the origin of α and β centers. Biochim Biophys Acta 848: 239–248Google Scholar
  64. Hodges M and Barber J (1986) Analysis of chlorophyll fluorescence induction kinetics exhibited by DCMU-inhibited thylakoids and the origin of α and β centres. Biochim Biophys Acta 848: 239–246Google Scholar
  65. Hodges M, Boussac A and Briantais JM (1987) Thylakoid membrane protein phosphorylation modifies equilibrium between photosystem II quinone electron acceptors. Biochim Biophys Acta 894: 138–145Google Scholar
  66. Hodges M, Cornic G and Briantais JM (1989) Chlorophyll fluorescence from spinach leaves. Resolution of nonphotochemical quenching. Biochim Biophys Acta 974: 289–293Google Scholar
  67. Holzwarth AR (1991) Excited-state kinetics in chlorophyll systems and its relationship to the functional organization of the photosystems. In H Scheer (ed) Chlorophylls, pp 1125–1151, CRC Press, Boca RatonGoogle Scholar
  68. Hormann H, Neubauer C and Schreiber U (1994) On the relationship between chlorophyll fluorescence quenching and the quantum yield of electron transport in isolated thylakoids. Photosynth Res 40: 93–106CrossRefGoogle Scholar
  69. Horton P (1981) The effect of redox potential on the kinetics of fluorescence induction in pea chloroplasts. I. Removal of the slow phase. Biochim Biophys Acta 635: 105–110PubMedGoogle Scholar
  70. Horton P and Bowyer JR (1990) Chlorophyll fluorescence transients. In: Harwood JL and Bowyer JR (eds) Methods in Plant Biochemistry, Vol 4, pp 259–296. Acad Press, New YorkGoogle Scholar
  71. Horton P and Hague A (1988) Studies on the induction of chlorophyll fluorescence in barley protoplasts. IV Resolution of non-photochemical quenching. Biochim Biophys Acta 932: 107–115Google Scholar
  72. Horton P and Lee P (1984) Phosphorylation of chloroplast thylakoids decreases the maximum capacity of photosystem II electron transfer. Biochim Biophys Acta 767: 563–567Google Scholar
  73. Horton P and Lee P (1985) Phosphorylation of chloroplast membrane proteins partially protects against photoinhibition. Planta 165: 37–42CrossRefGoogle Scholar
  74. Horton P, Ruban AV, Rees D, Pascal AA, Noctor GD and Young AJ (1992) Control of the light-harvesting function of chloroplast membrane by aggregation of the LHCII chlorophyll protein complex. FEBS Let 292: 1–4Google Scholar
  75. Horvath G, Droppa M and Melis A (1984) Herbicide action on photosystem II in spinach chloroplasts: Concentration effect on PS II α and PS II β Photobiochem Photobiophys 7: 249–256Google Scholar
  76. Hsu BD (1992) The active photosystem II centers can make a significant contribution to the initial fluorescence rise from Fn to F1 Plant Science 81: 169–174CrossRefGoogle Scholar
  77. Hsu BD (1993) Evidence for the contribution of the S-state transitions of oxygen evolution to the initial phase of fluorescence induction, Photosynth Res 36: 81–88CrossRefGoogle Scholar
  78. Hsu BD and Lee JY (1991a) A study on the fluorescence induction curve of the DCMU-poisoned chloroplast. Biochim Biophys Acta 1056: 285–292Google Scholar
  79. Hsu BD and Lee JY (1991b) Characterization of the photosystem II centers inactive in plastoquinone reduction by fluorescence induction. Photosynth Res 27: 143–150CrossRefGoogle Scholar
  80. Hsu BD, Lee YS and Jang YR (1989) A method for analysis of fluorescence induction curve from DCMU-poisoned chloroplasts. Biochim Biophys Acta 975: 44–49Google Scholar
  81. Jegerschold C, Virgin I and Styring S (1990) Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction. Biochemistry 29: 6179–6186PubMedGoogle Scholar
  82. Joliot A (1974) Effect of low temperature (_30 to _60°C) on the reoxidation of the photosystem II primary acceptor in the presence and absence of DCMU. Biochim Biophys Acta 357: 439–448PubMedGoogle Scholar
  83. Joliot A and Joliot P (1964) Etude cinétique de la réaction photochimique libérant lľoxygène au cours de la photosynthèse. CR Acad Sci Paris 258: 4622–4625Google Scholar
  84. Joliot P (1965) Etudes simultanées des cinétiques de fluorescence et dďémission dďoxygène photosynthétique. Biochim Biophys Acta 102: 135–148PubMedGoogle Scholar
  85. Joliot P and Joliot A (1977) Evidence for a double hit process in photosystem II based on fluorescence studies. Biochim Biophys Acta 462: 559–574PubMedGoogle Scholar
  86. Joliot P and Joliot A (1979) Comparative study of the fluorescence yield and of the C550 absorption change at room temperature. Biochim. Biophys. Acta 546: 93–105PubMedGoogle Scholar
  87. Joliot P and Joliot A (1981a) Characterization of photosystem II centers by polarographic, spectroscopic and fluorescence methods. In Akoyunoglou G (ed) Photosynthesis III. Structure and Molecular Organization of the Photosynthetic Apparatus, pp 885–899. Balaban International Science Services, Philadelphia PAGoogle Scholar
  88. Joliot P and Joliot A (1981b) Double photoreactions induced by a laser flash as measured by oxygen emission. Biochim Biophys Acta 638: 132–140Google Scholar
  89. Joliot P, Joliot A, Bouges B and Barbieri B (1971) Studies of system II photocenters by comparative measurements of luminescence, fluorescence, and oxygen emission. Photochem Photobiol 14: 287–305Google Scholar
  90. Joliot P, Bennoun P and Joliot A (1973) New evidence supporting energy transfer between photosynthetic units. Biochim Biophys Acta 305: 317–328PubMedGoogle Scholar
  91. 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
  92. Jursinic PA and Dennenberg RJ (1989) Measurement of stoichiometry of photosystem II to photosystem I reaction centers. Photosynth Res 21: 197–200Google Scholar
  93. Keren N, Gong H and Ohad I (1995) Oscillation of reaction center II D1 protein degradation in vivo induced by repetitive light flashes: Correlation between the level of RC II QB and protein degradation in low light. J Biol Chem 270: 806–814PubMedCrossRefGoogle Scholar
  94. Kirilovsky DL, Vernotte C and Etienne AL (1990) Protection from photoinhibition by low temperature in Synechocystis 6714 and in Chlamydomonas reinhardtii: Detection of an intermediary state. Biochemistry 29: 8100–8106PubMedCrossRefGoogle Scholar
  95. Krause GH and Behrend U (1986) △pH-dependent chlorophyll fluorescence quenching indicates a mechanism of protection against photoinhibition of chloroplasts. FEBS Lett 200: 298–302CrossRefGoogle Scholar
  96. Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol 42: 313–349CrossRefGoogle Scholar
  97. Krieger A and Weis E (1990) pH-dependent quenching of chlorophyll fluorescence in isolated PS II particles: Dependence on the redox potential. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol VI, pp 563–566. Kluwer Academic Publishers, DordrechtGoogle Scholar
  98. Krieger A and Weis E (1993) The role of calcium in the pH dependent control of photosystem II. Photosynth Res 37: 117–130CrossRefGoogle Scholar
  99. Krieger A, Moya I and Weis E (1992) Energy-dependent quenching of chlorophyll a fluorescence: Effect of pH on stationary fluorescence and picosecond relaxation kinetics in thylakoid membranes and photosystem II preparations. Biochim Biophys Acta 1102: 167–176Google Scholar
  100. Kyle DJ (1987) The biochemical basis for photoinhibition of photosystem II. In: Kyle DJ, Osmond CB and Artnzen CJ (eds), Photoinhibition, pp 197–226. Elsevier Publishers, AmsterdamGoogle Scholar
  101. Lam E, Baltimore B, Ortiz W, Chollar S, Melis A and Malkin R (1983) Characterization of a resolved oxygen-evolving photosystem II preparation from spinach thylakoids. Biochim Biophys Acta 724: 201–211Google Scholar
  102. Lavergne J (1982a) Two types of primary acceptors in chloroplasts photosystem II. I. Different recombination properties. Photobiochem Photobiophys 3: 257–271Google Scholar
  103. Lavergne J (1982b) Two types of primary acceptors in chloroplasts photosystem II. II. Reduction in two successive photoacts. Photobiochem Photobiophys 3: 273–285Google Scholar
  104. Lavergne (1982c) Mode of action of diehlorophenyldimethylurea. Evidence that the inhibitor competes with plastoquinone for binding to a common site on the acceptor side of photosystem II. Biochim Biophys Acta 682: 345–353Google Scholar
  105. Lavergne J (1987) Optical difference spectra of the S-state transitions in the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 894: 91–107Google Scholar
  106. Lavergne J (1991) Improved UV-visible spectra of the Stransitions in the photosynthetic oxygen-evolving system. Biochim Biophys Acta 1060: 175–188Google Scholar
  107. Lavergne J and Leci E (1993) Properties of inactive photosystem II centers. Photosynth Res 35: 323–343CrossRefGoogle Scholar
  108. Lavergne J and Trissl HW (1995) Theory of fluorescence induction in Photosystem II: Derivation of analytical expressions in a model including exciton radical pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J 68: 2474–2492PubMedGoogle Scholar
  109. Lavorel J and Etienne AL (1977) In vivo chlorophyll fluorescence. In Barber J (ed) Primary Processes of Photosynthesis, pp 203–268, Elsevier, AmsterdamGoogle Scholar
  110. Le Gouallec JL, Cornic G and Briantais JM (1991) Chlorophyll fluorescence and photoinhibition in a tropical rainforest understory plant. Photosynth Res 27: 135–142CrossRefGoogle Scholar
  111. Lokstein H, Härtel H, Hoffmann P and Renger G (1993) Comparison of chlorophyll fluorescence quenching in leaves of wild type with a chlorophyll-b-less mutant of barley (Hordeum vulgare L.) J Photochem Photobiol B: Biol 19: 217–225Google Scholar
  112. Mäenpää P, Andersson B and Sundby C (1987) Difference in sensitivity to photoinhibition between photosystem II in the appressed and non-appressed thylakoid regions. FEES Lett 215: 31–36Google Scholar
  113. Malkin S and Kok B (1966) Fluorescence induction studies in isolated chloroplasts. I Number ofcomponents involved in the reaction and quantum yields. Biochim Biophys Acta 126: 413–432PubMedGoogle Scholar
  114. Mattoo AK, Hoffman-Falk H, Marder JB and Edelman M (1984) Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32 kilodalton protein of chloroplast membrane. Proc Natl Acad Sci USA 81: 1380–1384PubMedGoogle Scholar
  115. Mattoo AK, Marder JB and Edelman M (1989) Dynamics of the photosystem II reaction center. Cell 56: 241–246PubMedCrossRefGoogle Scholar
  116. McCarthy S, Jursinic P and Stemler A (1988) Atrazine binding sites of photosystem II. Plant Physiol 86S: 46Google Scholar
  117. Melis A (1985) Functional properties of photosystem IIβ in spinach chloroplasts. Biochim Biophys Acta 808: 334–342Google Scholar
  118. Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106Google Scholar
  119. Melis A and Anderson JM (1983) Structural and functional organization of the photosystem in spinach chloroplasts. Antenna size, relative electron-transport capacity, and chlorophyll composition. Biochim Biophys Acta 724: 473–484Google Scholar
  120. Melis A and Duysens LNM (1979) Biphasic energy conversion kinetics and absorbance difference spectra of photosystem II of chloroplasts. Evidence for two different PS II reaction centers. Photochem Photobiol 29: 373–382Google Scholar
  121. Melis A and Homann PH (1975) Kinetic analysis of the fluorescence induction in 3-(3,4-dichlorophenyl)-l, l-dimethylurea poisoned chloroplasts. Photochem Photobiol 21: 431–437Google Scholar
  122. Melis A and Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23: 343–350PubMedGoogle Scholar
  123. Melis A and Ow RA (1982) Photoconversion kinetics of chloroplast photosystems I and II. Effect of Ng2+, Biochim Biophys Acta 682: 1–10Google Scholar
  124. Melis A and Schreiber U (1979) The kinetic relationship between the C-550 absorbance change, the reduction of Q (ΔA2+ and the variable fluorescence yield change in chloroplasts at room temperature. Biochim Biophys Acta 547: 47–57PubMedGoogle Scholar
  125. Melis A and Thielen APMG (1980) The relative absorption cross-sections of photosystem I and photosystem II in chloroplasts from three types of Nicotiana tabacum. Biochim Biophys Acta 589: 275–286PubMedGoogle Scholar
  126. Michel H, Hunt DF, Shabanowitz J and Bennett J (1988) Tandem mass spectrometry reveals that three photosystem II proteins of spinach chloroplasts contain N-acetyl-O-phosphothreonine at their NH2 termini. J Biol Chem 263: 1123–1130PubMedGoogle Scholar
  127. Murata N, Nishimura M and Takamiya A (1966) Fluorescence of chlorophyll in photosynthetic systems. II Induction of fluorescence in isolated spinach chloroplasts. Biochim Biophys Acta 120: 20–33Google Scholar
  128. 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: 85–94CrossRefGoogle Scholar
  129. Noctor G, Rees D, Young A and Horton P (1991) The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence and the transthylakoid pH-gradient in isolated chloroplasts. Biochim Biophys Acta 1057: 320–330Google Scholar
  130. ögren E (1991) Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components. Planta 184: 538–544Google Scholar
  131. Ohad I, Koike H, Shochat S and Inoue Y (1988) Changes in the properties of reaction centers during the initial stages of photoinhibition as revealed by thermoluminescence measurements. Biochim Biophys Acta 993: 288–298Google Scholar
  132. Ohad I, Keren N, Zer H, Gong H, Mor TS, Gal A, Tal S and Domovich Y (1994) Light-induced degradation of the photosystem II reaction centre D1 protein in vivo: An integrative approach. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, From Molecular Mechanisms to the Field, pp 161–178. Environmental Plant Biology series, Davies (ed), Bios Scientific Publishers, OxfordGoogle Scholar
  133. Olive J, Vallon O, Wollman F-A, Recouvreur M and Bennoun P (1986) Studies b 6/f complex. II. Localization of the complex in the thylakoid membranes from spinach and Chlamydomonas reinhardtii by immunocytochemistry and freeze-fracture analysis of b 6-f mutants. Biochim Biophys Acta 851: 239–248Google Scholar
  134. Oxborough K and Horton P (1987) Characterization of the effects of antimycin A upon the high energy state quenching of chlorophyll fluorescence (qE) in spinach and pea chloroplasts. Photosynth Res 12: 119–128CrossRefGoogle Scholar
  135. Percival MP, Webber AN and Baker NR (1984) Evidence for the role of the light-harvesting chlorophyll a/b protein complex in photosystem II heterogeneity. Biochim Biophys Acta 767: 582–589Google Scholar
  136. Peter GF and Thornber JP (1991a) Biochemical evidence that the higher plant photosystem II core complex is organized as a dimer. Plant Cell Physiol 32: 1237–1250Google Scholar
  137. Peter GF and Thornber JP (1991b) Biochemical composition and organization of higher plant photosystem II light harvesting pigment proteins. J Biol Chem 266: 16745–16754PubMedGoogle Scholar
  138. Ramm D and Hansen UP (1993) Can charge recombination as caused by pH dependent donor side limitation in PS2 account for high-energy state quenching? Photosynth Res 35: 97–100CrossRefGoogle Scholar
  139. Rees D, Noctor GD and Horton P (1990) The effect of highenergy-state excitation quenching on maximum and dark level chlorophyll fluorescence yield. Photosynth Res 25: 199–211CrossRefGoogle Scholar
  140. Rees D, Noctor GD, Ruban AV, Crofts J, Young AJ and Horton P (1992) pH dependent chlorophyll fluorescence quenching in spinach thylakoids from light treated or dark adapted leaves. Photosynth Res 31: 11–19CrossRefGoogle Scholar
  141. Robinson HH and Crofts AR (1983) Kinetics of the oxidationreduction reactions of the photosystem II quinone acceptor complex, and the pathway for deactivation. FEBS Lett 151: 221–226Google Scholar
  142. Robinson HH and Crofts AR (1984) Kinetics of proton uptake and the oxidation-reduction reactions of quinone acceptor complex of PS II from pea chloroplasts. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol 1, pp 477–480. Martinus Nijhoff/Dr W Junk Publishers, The HagueGoogle Scholar
  143. Roelofs TA, Lee CH and Holzwarth AR (1992) Global target analysis of picosecond chlorophyll fluorescence kinetics from pea chloroplasts. A new approach to the characterization of the primary process in photosystem II α-and β-units. Biophys J 61: 1147–1163CrossRefPubMedGoogle Scholar
  144. Ruban AV and Horton P (1992) Mechanism of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes. I–Spectroscopic analysis of isolated light-harvesting complexes. Biochim Biophys Acta 1102: 30–38Google Scholar
  145. Ruban AV and Horton P (1995) An investigation of the sustained component of nonphotochemical quenching of chlorophyll fluorescence in isolated chloroplasts and leaves of spinach. Plant Physiol 108: 721–726PubMedGoogle Scholar
  146. Ruban AV, Young AJ and Horton P (1993) Induction of nonphotochemical energy dissipation and absorbance changes in leaves. Plant Physiol 102: 741–750PubMedGoogle Scholar
  147. Schreiber U and Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: Partial control by the photosystem II donor side and possible ways of interpretation. Z Naturforsch 42C: 1255–1264Google Scholar
  148. Schreiber U and Neubauer C (1990) O-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25: 279–293CrossRefGoogle Scholar
  149. Schreiber U and Pfister K (1982) Kinetic analysis of the light-induced chlorophyll fluorescence rise curve in the presence of. dichlorophenyldimethylurea. Dependence of the slow-rise component on the degree of chloroplast intactness. Biochim Biophys Acta 680: 60–68Google Scholar
  150. Schreiber U, Schliwa U and Bilger W (1986) Continuous recording of photochemical and non photochemical chlorophyll fluorescence quenching with a new type of modulation fluorimeter. Photosynth Res 10: 51–62CrossRefGoogle Scholar
  151. Sinclair J and Spence SM (1990) Heterogeneous photosystem 2 activity in isolated spinach chloroplasts. Photosynth Res 24: 209–220CrossRefGoogle Scholar
  152. Somersalo S and Krause GH (1989) Photoinhibition at chilling temperature, fluorescence characteristics of unharded and cold acclimated spinach leaves. Planta 177: 409–416CrossRefGoogle Scholar
  153. Styring S, Virgin I, Ehrenberg A and Andersson B (1990) Strong light photoinhibition of electron transport in photosystem II. Impairment of the function of the first quinone acceptor, QA Biochim Biophys Acta 1015: 269–278Google Scholar
  154. Thayer SS and Björkman O (1992) Carotenoid distribution and deepoxidation in thylakoids pigment-protein complexes from cotton leaves and bundle sheath cells of maize. Photosynth Res 33: 213–226CrossRefGoogle Scholar
  155. Theg SM, Filar LJ and Dilley RA (1986) Photoinactivation of chloroplasts already inhibited on the oxidizing side of photosystem II. Biochim Biophys Acta 849: 104–111Google Scholar
  156. Thielen AMPG and van Gorkom HJ (1981a) Energy transfer and quantum yield in photosystem II. Biochim Biophys Acta 637: 439–446Google Scholar
  157. Thielen AMPG and van Gorkom HJ (1981b) Redox potentials of electron acceptors in photosystems II α and II β, FEES Lett 129: 205–209CrossRefGoogle Scholar
  158. Thielen AMPG, van Gorkom HJ and Rijgersberg CP (1981) Chlorophyll composition of photosystems IIα, IIβ and I in tobacco chloroplasts. Biochim Biophys Acta 635: 121–123PubMedGoogle Scholar
  159. Vallon O, Wollman FA and Olive J (1985) Distribution of intrinsic and extrinsic subunits of the PS II protein complex between appressed and non-appressed regions of the thylakoid membrane: An immunocytochemical study. FEBS Lett 183: 245–250CrossRefGoogle Scholar
  160. Vallon O, Hoyer-Hansen G and Simpson DJ (1987) Photosystem II and cytochrome b-559 in the stroma lamellae of barley chloroplasts. Carlsberg Res Com 52: 405–421Google Scholar
  161. Vallon O, Bulté L, Dainese P, Olive J, Bassi R and Wollman F-A (1991) Lateral redistribution of cytochrome b 6-f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci 88: 8262–8266PubMedGoogle Scholar
  162. Van Wijk KJ and Van Hasselt PR (1990) The quantum efficiency of photosystem II and its relation to non-photochemical quenching of chlorophyll fluorescence: The effect of measuring and growth temperature. Photosynth Res 25: 233–240CrossRefGoogle Scholar
  163. Van Wijk KJ and Van Hasselt PR (1993) Photoinhibition of photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: Consequence for the mechanism of photoinhibition in vivo. Planta 189: 359–368Google Scholar
  164. Vass I, Gatzen G and Holzwarth AR (1993) Picosecond timeresolved fluorescence studies on photoinhibition and double reduction of QA in photosystem II. Biochim Biophys Acta 1183: 388–396Google Scholar
  165. Vernotte C, Etienne AL and Briantais JM (1979) Quenching of the system II chlorophyll fluorescence by the plastoquinone pool. Biochim Biophys Acta 545: 519–527PubMedGoogle Scholar
  166. Walter RG and Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27: 121–133Google Scholar
  167. Walter RG and Horton P (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PS II fluorescence in barley leaves. Photosynth Res 36: 119–139Google Scholar
  168. Weis E and Berry J (1987) Quantum efficiency of PS II in relation to energy dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 283: 259–267Google Scholar
  169. Weis E and Lechtenberg D (1989) Fluorescence analysis during steady state photosynthesis. Philos Trans R Soc London Biol Sci 233: 253–268Google Scholar
  170. Wettern M (1986) Localization of the 32,000 Dalton chloroplast protein pools in thylakoids: Significance in atrazine binding. Plant Science 43: 173–177CrossRefGoogle Scholar
  171. Wollenberger L, Stefansson H, Yu SG and Albertsson Pè (1994) Isolation and characterization of vesicles originating from the chloroplast grana margins. Biochim Biophys Acta 1184: 93–102Google Scholar
  172. Wollman FA (1978) Determination and modification of th redox state of the secondary acceptor of photosystem II in the dark. Biochim Biophys Acta 503: 263–273PubMedGoogle Scholar
  173. Yu SG, Bjorn G and Albertsson Pè (1993) Characterization of a non-detergent PS II-cytochrome b/f preparation (BS) Photosynth Res 37: 227–236CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Jérôme Lavergne
    • 1
  • Jean-Marie Briantais
    • 2
  1. 1.Institut de Biologie Physico-ChimiqueParisFrance
  2. 2.Laboratoire ďEcologie VégétaleUniversité de Paris-SudOrsayFrance

Personalised recommendations