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Photosynthesis Research

, 97:195 | Cite as

Protective dissipation of excess absorbed energy by photosynthetic apparatus of cyanobacteria: role of antenna terminal emitters

  • Navassard V. KarapetyanEmail author
Review

Abstract

Two mechanisms of photoprotective dissipation of the excessively absorbed energy by photosynthetic apparatus of cyanobacteria are described that divert energy from reaction centers. Energy dissipation, monitored as nonphotochemical fluorescence quenching, occurs at different steps of energy transfer within the phycobilisomes or core antenna of photosystem I. Although these mechanisms differ significantly, in both cases, energy dissipates mainly from terminal emitters: allophycocyanin B or core membrane linker protein (LCM) in phycobilisomes, or the longest-wavelength chlorophylls in photosystem I antenna. It is supposed that carotenoid-induced energy dissipation in phycobilisomes is triggered by light-induced transformation of the nonquenched state of antenna into quenched state due to conformation changes caused by orange carotinoid-binding protein (OCP)–phycobilisome interaction. Fluorescence of the longest-wavelength chlorophylls of photosystem I antenna is strongly quenched by P700 cation radical or by P700 triplet state, dependent on redox state of the acceptor side cofactors of photosystem I.

Keywords

Energy dissipation Fluorescence quenching Long-wavelength chlorophyll Phycobilisomes Photosystem I Terminal emitter 

Abbreviations

Chl

Chlorophyll

Chl710 (Chl740)

Chlorophyll with absorption band peaked at 710 nm (740 etc.)

LWC

Long-wavelength chlorophyll

OCP

Orange carotenoid-binding protein

PBS

Phycobilisome

P700

Primary electron donor of the PSI reaction center

P700+

P700 cation radical

3P700

P700 in triplet state

PSI (PSII)

Photosystem I (photosystem II)

TE

Terminal emitter

Notes

Acknowledgments

This work was supported by the Russian Academy of Sciences program “Molecular and Cell Biology” and the Russian Foundation of Basic Research, grant 08-04-00143a.

References

  1. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85:15–32. doi: 10.1007/s11120-004-2143-y PubMedCrossRefGoogle Scholar
  2. Allen JF, Holmes NG (1986) A general model for regulation of photosynthetic unit function by protein phosphorylation. FEBS Lett 202:175–181. doi: 10.1016/0014-5793(86)80682-2 CrossRefGoogle Scholar
  3. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134. doi: 10.1016/0005-2728(93)90134-2 PubMedCrossRefGoogle Scholar
  4. Bailey S, Mann N, Robinson C, Scanlan DJ (2005) The occurrence of rapidly reversible non-photochemical quenching of chlorophyll fluorescence in cyanobacteria. FEBS Lett 579:275–280. doi: 10.1016/j.febslet.2004.11.091 PubMedCrossRefGoogle Scholar
  5. Bald D, Kruip J, Roegner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: How is the phycobilisome connected with the photosystems? Photosynth Res 49:103–118. doi: 10.1007/BF00117661 CrossRefGoogle Scholar
  6. Barber J, Nield J, Duncan J (2006) Accessory chlorophyll proteins in cyanobacteria. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin:ferredoxin oxydoreductase, Series Advances in photosynthesis and respiration, vol 24. Springer, Dordrecht, pp 99–117Google Scholar
  7. Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant, Cell Environ 24:163–176. doi: 10.1111/j.1365-3040.2001.00673.x CrossRefGoogle Scholar
  8. Biggins J, Bruce D (1989) Regulation of excitation energy transfer in organisms containing phycobilisomes. Photosynth Res 20:1–34. doi: 10.1007/BF00028620 CrossRefGoogle Scholar
  9. Bittersmann E, Vermaas WFJ (1991) Fluorescent lifetime studies of cyanobacterial photosystem II mutants. Biochim Biophys Acta 1098:105–116. doi: 10.1016/0005-2728(91)90014-F CrossRefGoogle Scholar
  10. Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33:91–111. doi: 10.1007/BF00039173 PubMedCrossRefGoogle Scholar
  11. Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll–protein complex induced by iron-deficiency in cyanobacteria. Nature 412:745–748. doi: 10.1038/35089104 PubMedCrossRefGoogle Scholar
  12. Bolychevtseva YV, Rakhimberdieva MG, Karapetyan NV, Popov VI, Moskalenko AA, Kuznetsova NY (1995) The development of carotenoid-deficient membranes in plastids of barley seedlings treated with norflurazon. J Photochem Photobiol 27B:153–160Google Scholar
  13. Byrdin M, Rimke I, Schlodder E, Stehlik D, Roelofs TA (2000) Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 reduced and oxidized state: Are the kinetics of excited state decay trap-limited or transfer-limited? Biophys J 79:992–1007PubMedGoogle Scholar
  14. Cadoret J-C, Demouliere R, Lavand J, van Gorkom H, Houmard J, Etienne A-L (2004) Dissipation of excess energy triggered by blue light in cyanobacteria with CP43′ (IsiA). Biochim Biophys Acta 1659:100–104. doi: 10.1016/j.bbabio.2004.08.001 PubMedCrossRefGoogle Scholar
  15. Castenholz RW (1997) Multiple strategies for UV tolerance in cyanobacteria. Spectrum 10:10–16Google Scholar
  16. Cogdell RJ, Howard TD, Bittl R, Schlodder E, Geisenheimer I, Lubitz W (2000) How carotenoids protect bacterial photosynthesis. Philos Trans R Soc Lond 355:1345–1349. doi: 10.1098/rstb.2000.0696 CrossRefGoogle Scholar
  17. Cometta A, Zucchelli G, Karapetyan NV, Engelmann E, Garlaschi FM, Jennings RC (2000) Thermal behavior of long wavelength absorption transitions in Spirulina platensis photosystem I trimers. Biophys J 79:3235–3243PubMedCrossRefGoogle Scholar
  18. Dorra D, Fromme P, Karapetyan NV, Holzwarth AR (1998) Fluorescence kinetics of photosystem I: multiple fluorescence components. In: Garab G (ed) Proc of the XIth Internat Photosynthesis Congress, vol 1. Kluwer Academic Publishers, Dordrecht, pp 587–590Google Scholar
  19. El-Bissati K, Delphin E, Murata N, Etienne A-L, Kirilovsky D (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis sp. PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457:229–242. doi: 10.1016/S0005-2728(00)00104-3 PubMedCrossRefGoogle Scholar
  20. Engelmann E, Tagliabue T, Karapetyan NV, Garlaschi FM, Zucchelli G, Jennings RC (2001) CD spectroscopy provides evidence for excitonic interactions involving red-shifted chlorophyll forms in photosystem I. FEBS Lett 499:112–115. doi: 10.1016/S0014-5793(01)02533-9 PubMedCrossRefGoogle Scholar
  21. Fujita J (1997) A study of the dynamic features of photosystem stoichiometry: accomplishments and problems for future studies. Photosynth Res 53:83–93. doi: 10.1023/A:1005870301868 CrossRefGoogle Scholar
  22. Funk C, Vermaas WFJ (1999) A cyanobacteria gene family coding for single-helix proteins resembling part of the light-harvesting proteins from higher plants. Biochemistry 38:9397–9404. doi: 10.1021/bi990545+ PubMedCrossRefGoogle Scholar
  23. Gobets B, van Stokkum IHM, Roegner M, Kruip J, Schlodder E, Karapetyan NV, Dekker JP, van Grondelle R (2001) Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophys J 81:407–424PubMedGoogle Scholar
  24. Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151. doi: 10.1016/S1360-1385(98)01200-X CrossRefGoogle Scholar
  25. Henderson JN, Zhang J, Evans B, Redding K (2003) Disassembly and degradation of photosystem I in an in vitro system are multievent, metal-dependent processes. J Biol Chem 278:39078–39086Google Scholar
  26. Holzwarth AR, Dorra D, Mueller MG, Karapetyan NV (1998) Structure–function relationship and excitation dynamics in photosystem I. In: Garab G (ed) Photosynthesis: mechanisms and effects, vol 1. Kluwer Academic Publishers, Dordrecht, pp 497–502Google Scholar
  27. Horton P, Ruban A, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684. doi: 10.1146/annurev.arplant.47.1.655 PubMedCrossRefGoogle Scholar
  28. Ihalainen JA, D’Haene S, Yeremenko N, van Roon H, Arteni AA, Boekema EJ, van Grondelle R, Matthijs HCP, Dekker JP (2005) Aggregates of the chlorophyll-binding protein IsiA (CP43′) dissipate energy in cyanobacteria. Biochemistry 44:10846–10853. doi: 10.1098/rstb.2000.0698 PubMedCrossRefGoogle Scholar
  29. Jansson S (1994) The light-harvesting chlorophyll a/b binding proteins. Biochim Biophys Acta 1184:1–19. doi: 10.1016/0005-2728(94)90148-1 PubMedCrossRefGoogle Scholar
  30. Jordan P, Fromme P, Klukas O, Witt HT, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Ǻ resolution. Nature 411:909–917. doi: 10.1038/35082000 PubMedCrossRefGoogle Scholar
  31. Joshua S, Bailey S, Mann NH, Mullineaux CW (2005) Involvement of phycobilisome diffusion in energy quenching in cyanobacteria. Plant Physiol 138:1577–1585. doi: 10.1104/pp.105.061168 PubMedCrossRefGoogle Scholar
  32. Karapetyan NV (1998) Organization and the role of longwave chlorophylls in the photosystem I of the cyanobacterium Spirulina. Membr Cell Biol 12:571–584PubMedGoogle Scholar
  33. Karapetyan NV (2004a) The dynamics of excitation energy in photosystem I of cyanobacteria: transfer in the antenna, capture by the reaction center, and dissipation. Biophysika Russ 49:212–226Google Scholar
  34. Karapetyan NV (2004b) Interaction of pigment–protein complexes within aggregates stimulates dissipation of excess energy. Biochemistry (Mosc) 69:1598–1605. doi: 10.1007/s10541-005-0075-6 Google Scholar
  35. Karapetyan NV (2007) Non-photochemical quenching of fluorescence in cyanobacteria. Biochemistry (Mosc) 72:1127–1135. doi: 10.1134/S0006297907100100 CrossRefGoogle Scholar
  36. Karapetyan NV, Klimov VV, Krasnovsky AA (1973) Light-induced changes in the fluorescence yield of particles obtained by digitonin fragmentation of chloroplasts. Photosynthetica 7:330–337Google Scholar
  37. Karapetyan NV, Dorra D, Schweitzer G, Bezsmertnaya IN, Holzwarth AR (1997) Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from cyanobacterium Spirulina platensis. Biochemistry 36:13830–13837. doi: 10.1021/bi970386z PubMedCrossRefGoogle Scholar
  38. Karapetyan NV, Holzwarth AR, Roegner M (1999a) Photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and physiological significance. FEBS Lett 460:395–400. doi: 10.1016/S0014-5793(99)01352-6 PubMedCrossRefGoogle Scholar
  39. Karapetyan NV, Shubin VV, Strasser RJ (1999b) Energy exchange between the chlorophyll antennae of monomeric subunits within the photosystem I trimeric complex of cyanobacterium Spirulina. Photosynth Res 61:291–301. doi: 10.1023/A:1006385002635 CrossRefGoogle Scholar
  40. Karapetyan NV, Schlodder E, van Grondelle R, Dekker JP (2006) Long-wavelength chlorophylls of photosystem I. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin:ferredoxin oxydoreductase, series advances in photosynthesis and respiration, vol 24. Springer, Dordrecht, pp 177–192Google Scholar
  41. Kerfeld CA (2004) Water-soluble carotenoid proteins of cyanobacteria. Arch Biochem Biophys 430:2–9. doi: 10.1016/j.abb.2004.03.018 PubMedCrossRefGoogle Scholar
  42. Kerfeld CA, Sawaya MR, Brahmandam V, Cascio D, Ho KK, Trevithick-Sutton CC, Krogmann DW, Yeates TO (2003) The crystal structure of a cyanobacterial water-soluble protein. Structure 11:56–65. doi: 10.1016/S0969-2126(02)00936-X CrossRefGoogle Scholar
  43. Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7–16. doi: 10.1007/s11120-007-9168-y PubMedCrossRefGoogle Scholar
  44. Kruip J, Karapetyan NV, Terekhova IV, Roegner M (1999) In vitro oligomerisation of a membrane protein complex: liposome based reconstitution of trimeric photosystem I from isolated monomers. J Biol Chem 274:18181–18188. doi: 10.1074/jbc.274.26.18181 PubMedCrossRefGoogle Scholar
  45. McColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334. doi: 10.1006/jsbi.1998.4062 CrossRefGoogle Scholar
  46. McConnell MD, Koop R, Vasiliev S, Bruce D (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol 130:1201–1212. doi: 10.1104/pp.009845 PubMedCrossRefGoogle Scholar
  47. Mimuro M, Lipschultz CA, Gantt E (1986) Energy flow in the phycobilisomes of Nostoc sp. (Mac): two independent terminal pigments. Biochim Biophys Acta 852:126–132. doi: 10.1016/0005-2728(86)90065-4 CrossRefGoogle Scholar
  48. Moskalenko AA, Karapetyan NV (1996) Structural role of carotenoids in photosynthetic membranes. Z Naturforsch 51C:763–771Google Scholar
  49. Mulkidjanian AY, Junge W (1997) On the origin of photosynthesis as inferred from sequence analysis. Photosynth Res 51:27–42. doi: 10.1023/A:1005726809084 CrossRefGoogle Scholar
  50. Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium. Biochim Biophys Acta 1100:285–292Google Scholar
  51. Mullineaux CW (2008) Phycobilisome-reaction centre interaction in cyanobacteria. Photosynth Res 95:175–182. doi: 10.1007/s11120-007-9249-y PubMedCrossRefGoogle Scholar
  52. Mullineaux CW, Allen JF (1990) State 1–state 2 transitions in the cyanobacterium Synechocystis 6301 are controlled by the redox state of electron carriers between photosystems I and II. Photosynth Res 23:297–311. doi: 10.1007/BF00034860 CrossRefGoogle Scholar
  53. Mullineaux CW, Emplyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393. doi: 10.1093/jxb/eri064 PubMedCrossRefGoogle Scholar
  54. Mullineaux CW, Holzwarth AR (1991) Effect of photosystem II reaction centre closure on fluorescence decay kinetics in a cyanobacterium. Biochim Biophys Acta 1098:68–78. doi: 10.1016/0005-2728(91)90010-L CrossRefGoogle Scholar
  55. Mullineaux CW, Pascal AA, Horton P, Holzwarth AR (1993) Excitation-energy quenching in aggregates of the LHC-II chlorophyll-protein complex—a time-resolved fluorescence study. Biochim Biophys Acta 1141:23–28. doi: 10.1016/0005-2728(93)90184-H CrossRefGoogle Scholar
  56. Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390:421–424. doi: 10.1038/37157 CrossRefGoogle Scholar
  57. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421. doi: 10.1016/j.bbabio.2006.11.019 PubMedCrossRefGoogle Scholar
  58. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359. doi: 10.1146/annurev.arplant.50.1.333 PubMedCrossRefGoogle Scholar
  59. Oliveberg M, Tan Y-J, Fersht AR (1995) Negative activation enthalpies in the kinetics of protein folding. Proc Natl Acad Sci USA 92:8926–8929. doi: 10.1073/pnas.92.19.8926 PubMedCrossRefGoogle Scholar
  60. Polivka T, Kerfeld CA, Pascher T, Sundstroem V (2005) Spectroscopic properties of the carotenoid 3′-hydroxyechinenone in the orange carotenoif protein from the cyanobacterium Arthrospira maxima. Biochemistry 44:3994–4003. doi: 10.1021/bi047473t PubMedCrossRefGoogle Scholar
  61. Rakhimberdieva MG, Boichenko VA, Karapetyan NV, Stadnichuk IN (2001) Interaction of phycobilisomes with photosystem 2 dimers and photosystem 1 monomers and trimers of the cyanobacterium Spirulina platensis. Biochemistry 40:15780–15788. doi: 10.1021/bi010009t PubMedCrossRefGoogle Scholar
  62. Rakhimberdieva MG, Stadnichuk IN, Elanskaya IV, Karapetyan NV (2004) Carotenoid-induced quenching of the phycobilisome fluorescence in photosystem II-deficient mutant of Synechocystis sp. FEBS Lett 574:85–88. doi: 10.1016/j.febslet.2004.07.087 PubMedCrossRefGoogle Scholar
  63. Rakhimberdieva MG, Elanskaya IV, Vavilin DV, Vermaas WFJ, Karapetyan NV (2006) Blue light-induced fluorescence quenching of phycobilisomes in the cyanobacterium Synechocystis sp. PCC 6803 in the absence of the IsiA protein. Biochim Biophys Acta 1757(Suppl 1):286–287Google Scholar
  64. Rakhimberdieva MG, Bolychevtseva YV, Elanskaya IV, Karapetyan NV (2007a) Protein–protein interactions in carotenoid triggered quenching of phycobilisome fluorescence in Synechocystis sp PCC 6803. FEBS Lett 581:2429–2433. doi: 10.1016/j.febslet.2007.04.056 PubMedCrossRefGoogle Scholar
  65. Rakhimberdieva MG, Vavilin DV, Vermaas WFJ, Elanskaya IV, Karapetyan NV (2007b) Phycobilin/chlorophyll excitation equilibration upon carotenoid-induced non-photochemical fluorescence quenching in phycobilisomes of the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1767:757–765PubMedCrossRefGoogle Scholar
  66. Ruban AB, Berera R, Ilioaia C, van Stockkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Indentification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578PubMedCrossRefGoogle Scholar
  67. Sarcina M, Tobin MJ, Mullineaux CW (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942: effect of phycobilisome size, temperature, and membrane lipid composition. J Biol Chem 276:46830–46834. doi: 10.1074/jbc.M107111200 PubMedCrossRefGoogle Scholar
  68. Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5–8. doi: 10.1007/s00425-005-1507-7 PubMedCrossRefGoogle Scholar
  69. Schlodder E, Paul A, Cetin M (2001) Triplet states in photosystem I complexes from Synechococcus elongatus. In: Proceedings of the 12th International Congress on Photosynthesis. CSIRO Publishing: Melbourne, Australia. www.publishcsiro.au/ps2001; contribution S6-015
  70. Schlodder E, Cetin M, Byrdin M, Terekhova IN, Karapetyan NV (2005) P700+-and 3P700-induced quenching of the fluorescence at 760 nm in trimeric photosytem I complexes from the cyanobacterium Arthrospira platensis. Biochim Biophys Acta 1706:53–67. doi: 10.1016/j.bbabio.2004.08.009 PubMedCrossRefGoogle Scholar
  71. Schlodder E, Shubin VV, El-Mohsnawy E, Roegner M, Karapetyan NV (2007) Steady-state and transient polarized absorption spectroscopy of photosytem I complexes from the cyanobacteria Arthrospira platensis and Thermosynechococcus elongatus. Biochim Biophys Acta 1767:732–741. doi: 10.1016/j.bbabio.2007.01.013 PubMedCrossRefGoogle Scholar
  72. Schopf JW (1993) Microfossils of the early archean apex chert: new evidence of the antiquity of life. Science 260:640–646. doi: 10.1126/science.260.5108.640 PubMedCrossRefGoogle Scholar
  73. Scott M, McCollum C, Vasiliev S, Croizer C, Espie GS, Krol M, Huner NPA, Bruce D (2006) Mechanism of the down regulation of photosynthesis by blue light in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 45:8952–8958. doi: 10.1021/bi060767p PubMedCrossRefGoogle Scholar
  74. Shen G, Boussiba S, Vermaas WFJ (1993) Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5:1853–1863PubMedCrossRefGoogle Scholar
  75. Shubin VV, Murthy SDS, Karapetyan NV, Mohanty P (1991) Origin of the 77 K variable fluorescence at 758 nm in cyanobacterium Spirulina platensis. Biochim Biophys Acta 1060:28–36. doi: 10.1016/S0005-2728(05)80115-X CrossRefGoogle Scholar
  76. Shubin VV, Bezsmertnaya IN, Karapetyan NV (1992) Isolation from Spirulina membranes of two photosystem I-type complexes one of which contains chlorophyll responsible for the 77 K fluorescence band at 760 nm. FEBS Lett 30:340–342CrossRefGoogle Scholar
  77. Shubin VV, Tsuprun VL, Bezsmertnaya IN, Karapetyan NV (1993) Trimeric forms of the photosystem I reaction center complex pre-exist in the membranes of the cyanobacterium Spirulina platensis. FEBS Lett 334:79–82. doi: 10.1016/0014-5793(93)81685-S PubMedCrossRefGoogle Scholar
  78. Shubin VV, Bezsmertnaya IN, Karapetyan NV (1995) Efficient energy transfer from the longwave antenna chlorophylls to P700 in photosystem I complexes from Spirulina. J Photochem Photobiol 30B:153–160Google Scholar
  79. Shubin VV, Terekhova IV, Kirillov BA, Karapetyan NV (2008) Quantum yield of P700+ photodestruction in isolated photosystem I complexes of the cyanobacterium Arthrospira platensis. Photochem Photobiol Sci . doi: 10.1039/b719122g PubMedGoogle Scholar
  80. Sonoike K (2006) Photoinhibition and protection of photosystem I. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin:ferredoxin oxydoreductase, series advances in photosynthesis and respiration, vol 24. Springer, Dordrecht, pp 657–668Google Scholar
  81. van der Weij-de Wit CD, Ihalainen JA, van der Vijver E, D’Haene S, Matthijs HCP, van Grondelle R, Dekker JP (2007) Fluorescence quenching of IsiA in early stage of iron deficiency and at cryogenic temperatues. Biochim Biophys Acta 1767:1393–1400PubMedCrossRefGoogle Scholar
  82. Vavilin DV, Hu S, Lin S, Vermaas WFJ (2003) Energy and electron transfer in photosystem II of a chlorophyll b-containing Synechocystis sp. 6803 mutant. Biochemistry 42:1731–1746. doi: 10.1021/bi026853g PubMedCrossRefGoogle Scholar
  83. Wang Q, Jantaro S, Lu B, Majeed W, Bailey M, He Q (2008) The high light-inducible polypeptides (HLIP) stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol 147:1239–1250Google Scholar
  84. Wentworth M, Ruban AV, Horton P (2003) Thermodynamic investigation into the mechanism of the chlorophyll fluorescence quenching in isolated photosystem II light-harvesting complex. J Biol Chem 278:21845–21850. doi: 10.1074/jbc.M302586200 PubMedCrossRefGoogle Scholar
  85. Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007. doi: 10.1105/tpc.105.040121 PubMedCrossRefGoogle Scholar
  86. Wilson A, Boulay C, Wilde A, Kerfeld CA, Kirilovsky D (2007) Light-induced energy dissipation in iron-starved cyanobacteria: roles of OCP and IsiA proteins. Plant Cell 19:656–672. doi: 10.1105/tpc.106.045351 PubMedCrossRefGoogle Scholar
  87. Young AJ, Frank HA (1996) Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence. J Photochem Photobiol 36B:3–15Google Scholar
  88. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Ǻ resolution. Nature 409:739–743. doi: 10.1038/35055589 PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.A.N. Bakh Institute of BiochemistryRussian Academy of SciencesMoscowRussia

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