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Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions

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Abstract

Photosynthetic organisms tightly regulate the energy arriving to the reaction centers in order to avoid photodamage or imbalance between the photosystems. To this purpose, cyanobacteria have developed mechanisms involving relatively rapid (seconds to minutes) changes in the photosynthetic apparatus. In this review, two of these processes will be described: orange carotenoid protein(OCP)-related photoprotection and state transitions which optimize energy distribution between the two photosystems. The photoactive OCP is a light intensity sensor and an energy dissipater. Photoactivation depends on light intensity and only the red-active OCP form, by interacting with phycobilisome cores, increases thermal energy dissipation at the level of the antenna. A second protein, the “fluorescence recovery protein”, is needed to recover full antenna capacity under low light conditions. This protein accelerates OCP conversion to the inactive orange form and plays a role in dislodging the red OCP protein from the phycobilisome. The mechanism of state transitions is still controversial. Changes in the redox state of the plastoquinone pool induce movement of phycobilisomes and/or photosystems leading to redistribution of energy absorbed by phycobilisomes between PSII and PSI and/or to changes in excitation energy spillover between photosystems. The different steps going from the induction of redox changes to movement of phycobilisomes or photosystems remain to be elucidated.

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References

  • Allen JF, Holmes NG (1986) A general-model for regulation of photosynthetic unit function by protein-phosphorylation. FEBS Lett 202(2):175–181

    Article  CAS  Google Scholar 

  • Allen JF, Sanders CE, Holmes NG (1985) Correlation of membrane-protein phosphorylation with excitation-energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett 193(2):271–275

    Article  CAS  Google Scholar 

  • Aoki M, Katoh S (1982) Oxidation and reduction of plastoquinone by photosynthetic and respiratory electron transport in a cyanobacterium Synechococcus sp. Biochim Biophys Acta 682:307–314

    Article  CAS  Google Scholar 

  • Ashby MK, Mullineaux CW (1999) The role of ApcD and ApcF in energy transfer from phycobilisomes to PSI and PSII in a cyanobacterium. Photosynth Res 61(2):169–179

    Article  CAS  Google Scholar 

  • Aspinwall CL, Sarcina M, Mullineaux CW (2004) Phycobilisome mobility in the cyanobacterium Synechococcus sp. PCC7942 is influenced by the trimerisation of photosystem I. Photosynth Res 79(2):179–187

    Article  CAS  PubMed  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433(7028):892–895

    Article  CAS  PubMed  Google Scholar 

  • Berera R, Herrero C, van Stokkum IH, Vengris M, Kodis G, Palacios RE, van Amerongen H, van Grondelle R, Gust D, Moore TA, Moore AL, Kennis JT (2006) A simple artificial light-harvesting dyad as a model excess energy dissipation in oxygenic photosynthesis. Proc Natl Acad Sci USA 103(14):5343–5348

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berera R, van Stokkum IH, Gwizdala M, Wilson A, Kirilovsky D, van Grondelle R (2012) The photophysics of the orange carotenoid protein, a light-powered molecular switch. J Phys Chem 116(8):2568–2574

    Article  CAS  Google Scholar 

  • Berera R, Gwizdala M, van Stokkum IH, Kirilovsky D, van Grondelle R (2013) Excited States of the inactive and active forms of the orange carotenoid protein. J Phys Chem 117(31):9121–9128

    Article  CAS  Google Scholar 

  • Boulay C, Abasova L, Six C, Vass I, Kirilovsky D (2008) Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochim Biophys Acta 1777(10):1344–1354

    Article  CAS  PubMed  Google Scholar 

  • Boulay C, Wilson A, D’Haene S, Kirilovsky D (2010) Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria. Proc Natl Acad Sci USA 107(25):11620–11625

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Breyton C (2000) Conformational changes in the cytochrome b6f complex induced by inhibitor binding. J Biol Chem 275(18):13195–13201

    Article  CAS  PubMed  Google Scholar 

  • Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62(3):667–683

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chábera P, Durchan M, Shih PM, Kerfeld CA, Polívka T (2010) Excited-state properties of the 16 kDa red carotenoid protein from Arthrospira maxima. Biochim Biophysic Acta 1807(1):30–35

    Article  CAS  Google Scholar 

  • Depege N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299(5612):1572–1575

    Article  CAS  PubMed  Google Scholar 

  • Dong C, Zhao J (2008) ApcD is required for state transition but not involved in blue-light induced quenching in the cyanobacterium Anabaena sp. PCC7120. Chin Sci Bull 53:3422–3424

    Article  CAS  Google Scholar 

  • Dong C, Tang A, Zhao J, Mullineaux CW, Shen G, Bryant DA (2009) ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 1787(9):1122–1128

    Article  CAS  PubMed  Google Scholar 

  • El Bissati K, Delphin E, Murata N, Etienne A, Kirilovsky D (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457(3):229–242

    Article  PubMed  Google Scholar 

  • Emlyn-Jones D, Ashby MK, Mullineaux CW (1999) A gene required for the regulation of photosynthetic light harvesting in the cyanobacterium Synechocystis 6803. Mol Microbiol 33(5):1050–1058

    Article  CAS  PubMed  Google Scholar 

  • Finazzi G, Zito F, Barbagallo RP, Wollman FA (2001) Contrasted effects of inhibitors of cytochrome b6f complex on state transitions in Chlamydomonas reinhardtii: the role of Qo site occupancy in LHCII kinase activation. J Biol Chem 276(13):9770–9774

    Article  CAS  PubMed  Google Scholar 

  • Folea IM, Zhang P, Aro EM, Boekema EJ (2008) Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett 582(12):1749–1754

    Article  CAS  PubMed  Google Scholar 

  • Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, Hagemann M (2006) Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 6(9):2733–2745

    Article  CAS  PubMed  Google Scholar 

  • Gantt E, Conti SF (1966a) Granules associated with the chloroplast lamellae of Porphyridium cruentum. J Cell Biol 29(3):423–434

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gantt E, Conti SF (1966b) Phycobiliprotein localization in algae. Brookhaven Symp Biol 19:393–405

    CAS  PubMed  Google Scholar 

  • Gindt YM, Zhou J, Bryant DA, Sauer K (1992) Core mutations of Synechococcus sp. PCC 7002 phycobilisomes: a spectroscopic study. J Photochem Photobiol 15(1–2):75–89

    Article  CAS  Google Scholar 

  • Glazer AN (1984) Phycobilisome—a macromolecular complex optimized for light energy-transfer. Biochim Biophys Acta 768(1):29–51

    Article  CAS  Google Scholar 

  • Gorbunov MY, Kuzminov FI, Fadeev VV, Kim JD, Falkowski PG (2011) A kinetic model of non-photochemical quenching in cyanobacteria. Biochim Biophys Acta 1807(12):1591–1599

    Article  CAS  PubMed  Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental-conditions. Microbiol Rev 57(3):725–749

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gwizdala M, Wilson A, Kirilovsky D (2011) In vitro reconstitution of the cyanobacterial photoprotective mechanism mediated by the orange carotenoid protein in Synechocystis PCC 6803. Plant Cell 23(7):2631–2643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gwizdala M, Wilson A, Omairi-Nasser A, Kirilovsky D (2013) Characterization of the Synechocystis PCC 6803 fluorescence recovery protein involved in photoprotection. Biochim Biophys Acta 1827:348–354

    Article  CAS  PubMed  Google Scholar 

  • Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13(4):793–806

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang C, Yuan X, Zhao J, Bryant DA (2003) Kinetic analyses of state transitions of the cyanobacterium Synechococcus sp. PCC 7002 and its mutant strains impaired in electron transport. Biochim Biophys Acta 1607(2–3):121–130

    Article  CAS  PubMed  Google Scholar 

  • Jallet D, Gwizdala M, Kirilovsky D (2012) ApcD, ApcF and ApcE are not required for the Orange Carotenoid Protein related phycobilisome fluorescence quenching in the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta 1817(8):1418–1427

    Article  CAS  PubMed  Google Scholar 

  • Jallet D, Thurotte A, Leverenz RL, Perreau F, Kerfeld CA, Kirilovsky D (2014) Specificity of the cyanobacterial orange carotenoid protein: influences of orange carotenoid protein and phycobilisome structures. Plant Physiol 164(2):790–804

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411(6840):909–917

    Article  CAS  PubMed  Google Scholar 

  • Joshua S, Mullineaux CW (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135(4):2112–2119

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Joshua S, Mullineaux CW (2005) The rpaC gene product regulates phycobilisome-photosystem II interaction in cyanobacteria. Biochim Biophys Acta 1709(1):58–68

    Article  CAS  PubMed  Google Scholar 

  • Kana R (2013) Mobility of photosynthetic proteins. Photosynth Res 116(2–3):465–479

    Article  CAS  PubMed  Google Scholar 

  • Kana R, Kotabova E, Komarek O, Sediva B, Papageorgiou GC, Govindjee, Prasil O (2012) The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta 1817(8):1237–1247

    Article  CAS  PubMed  Google Scholar 

  • Karapetyan NV (2007) Non-photochemical quenching of fluorescence in cyanobacteria. Biochemistry 72(10):1127–1135

    CAS  PubMed  Google Scholar 

  • Kerfeld CA, Kirilovsky D (2013) Structural, mechanistic and genomic insights into OCP-mediated photoprotection. In: Chauvat F, Cassier-Chauvat C (eds) Advances in botanical research: genomics in cyanobacteria, vol 65. Elsevier, UK, pp 1–26

    Chapter  Google Scholar 

  • 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 carotenoid binding protein. Structure 11(1):55–65

    Article  CAS  PubMed  Google Scholar 

  • Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7–16

    Article  CAS  PubMed  Google Scholar 

  • Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817(1):158–166

    Article  CAS  PubMed  Google Scholar 

  • Kondo K, Geng XX, Katayama M, Ikeuchi M (2005) Distinct roles of CpcG1 and CpcG2 in phycobilisome assembly in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 84(1–3):269–273

    Article  CAS  PubMed  Google Scholar 

  • Kondo K, Ochiai Y, Katayama M, Ikeuchi M (2007) The membrane-associated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna. Plant Physiol 144(2):1200–1210

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kondo K, Mullineaux CW, Ikeuchi M (2009) Distinct roles of CpcG1-phycobilisome and CpcG2-phycobilisome in state transitions in a cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 99(3):217–225

    Article  CAS  PubMed  Google Scholar 

  • Kruip J, Bald D, Boekema E, Rogner M (1994) Evidence for the existence of trimeric and monomeric photosystem-I complexes in thylakoid membranes from cyanobacteria. Photosynth Res 40(3):279–286

    Article  CAS  PubMed  Google Scholar 

  • Kuzminov FI, Karapetyan NV, Rakhimberdieva MG, Elanskaya IV, Gorbunov MY, Fadeev VV (2012) Investigation of OCP-triggered dissipation of excitation energy in PSI/PSII-less Synechocystis sp. PCC 6803 mutant using non-linear laser fluorimetry. Biochim Biophys Acta 1817(7):1012–1021

    Article  CAS  PubMed  Google Scholar 

  • Leverenz RL, Jallet D, Li MD, Mathies RA, Kirilovsky D, Kerfeld CA (2014) Structural and functional modularity of the orange carotenoid protein: distinct roles for the N- and C-terminal domains in cyanobacterial photoprotection. Plant Cell 26:426–437

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li D, Xie J, Zhao Y, Zhao J (2003) Probing connection of PBS with photosystems in intact cells of Spirulina platensis by temperature-induced fluorescence fluctuations. Biochim Biophys Acta 1557:35–40

    Article  CAS  PubMed  Google Scholar 

  • Li D, Xie J, Zhao J, Xia A, Li D, Gong Y (2004) Light-induced excitation energy redistribution in Spirulina platensis cells: “spillover” or “mobile PBSs”? Biochim Biophys Acta 1608(2–3):114–121

    Article  CAS  PubMed  Google Scholar 

  • Li H, Li D, Yang S, Xie J, Zhao J (2006) The state transition mechanism—simply depending on light-on and -off in Spirulina platensis. Biochim Biophys Acta 1757(11):1512–1519

    Article  CAS  PubMed  Google Scholar 

  • MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124(2–3):311–334

    Article  CAS  PubMed  Google Scholar 

  • Maksimov EG, Schmitt FJ, Shirshin EA, Svirin MD, Elanskaya IV, Friedrich T, Fadeev VV, Paschenko VZ, Rubin AB (2014) The time course of non-photochemical quenching in phycobilisomes of Synechocystis sp. PCC6803 as revealed by picosecond time-resolved fluorimetry. Biochim Biophys Acta. doi:10.1016/j.bbabio.2014.01.010

  • Mao HB, Li GF, Ruan X, Wu QY, Gong YD, Zhang XF, Zhao NM (2002) The redox state of plastoquinone pool regulates state transitions via cytochrome b6f complex in Synechocystis sp. PCC 6803. FEBS Lett 519(1–3):82–86

    Article  CAS  PubMed  Google Scholar 

  • McConnell MD, Koop R, Vasil’ev 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(3):1201–1212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Minagawa J (2010) State transitions—the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta 1807(8):897–905

    Article  PubMed  CAS  Google Scholar 

  • Minagawa J, Takahashi Y (2004) Structure, function and assembly of Photosystem II and its light-harvesting proteins. Photosynth Res 82(3):241–263

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to photosystem-I and photosystem-II in a cyanobacterium. Photosynth Res 34(1):114

    Google Scholar 

  • Mullineaux CW (2014) Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1837(4):503–511

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux C, Allen J (1986) The state 2 transition in the cyanobacterium Synechococcus 6301 can be driven by respiratory electron flow into the plastoquinone pool. FEBS Lett 205:155–160

    Article  CAS  Google Scholar 

  • Mullineaux CW, Allen JF (1990) State 1-state 2 transitions in the Cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystem I and Photosystem II. Photosynth Res 23(3):297–311

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56(411):389–393

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390(6658):421–424

    Article  CAS  Google Scholar 

  • Olive J, Mbina I, Vernotte C, Astier C, Wollman FA (1986) Randomization of the Ef particles in thylakoid membranes of Synechocystis 6714 upon transition from State-I to State-II. FEBS Lett 208(2):308–312

    Article  CAS  Google Scholar 

  • Olive J, Ajlani G, Astier C, Recouvreur M, Vernotte C (1997) Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis PCC 6803. Biochim Biophys Acta 1319:275–282

    Article  CAS  Google Scholar 

  • Polivka T, Kerfeld CA, Pascher T, Sundström V (2005) Spectroscopic properties of the carotenoid 3′-hydroxyechinenone in the orange carotenoid protein from the cyanobacterium Arthrospira maxima. Biochemistry 44(10):3994–4003

    Article  CAS  PubMed  Google Scholar 

  • Polivka T, Chabera P, Kerfeld CA (2013) Carotenoid-protein interaction alters the S(1) energy of hydroxyechinenone in the orange carotenoid protein. Biochim Biophys Acta 1827(3):248–254

    Article  CAS  PubMed  Google Scholar 

  • Punginelli C, Wilson A, Routaboul JM, Kirilovsky D (2009) Influence of zeaxanthin and echinenone binding on the activity of the orange carotenoid protein. Biochim Biophys Acta 1787(4):280–288

    Article  CAS  PubMed  Google Scholar 

  • Rakhimberdieva MG, Boichenko VA, Karapetyan NV, Stadnichuk IN (2001) Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis. Biochemistry 40(51):15780–15788

    Article  CAS  PubMed  Google Scholar 

  • 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(1–3):85–88

    Article  CAS  PubMed  Google Scholar 

  • 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(13):2429–2433

    Article  CAS  PubMed  Google Scholar 

  • Rakhimberdieva MG, Vavilin DV, Vermaas WF, 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(6):757–765

    Article  CAS  PubMed  Google Scholar 

  • Rakhimberdieva MG, Elanskaya IV, Vermaas WFJ, Karapetyan NV (2010) Carotenoid-triggered energy dissipation in phycobilisomes of Synechocystis sp. PCC 6803 diverts excitation away from reaction centers of both photosystems. Biochim Biophys Acta 1797(2):241–249

    Article  CAS  PubMed  Google Scholar 

  • Redlinger T, Gantt E (1982) A M(r) 95,000 polypeptide in Porphyridium cruentum phycobilisomes and thylakoids: possible function in linkage of phycobilisomes to thylakoids and in energy transfer. Proc Natl Acad Sci USA 79(18):5542–5546

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sarcina M, Tobin MJ, Mullineaux CW (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942. Effects of phycobilisome size, temperature, and membrane lipid composition. J Biol Chem 276(50):46830–46834

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U, Endo T, Mi HL, Asada K (1995) Quenching analysis of chlorophyll fluorescence by the saturation pulse method—particular aspects relating to the study of eukaryotic algae and cyanobacteria. OP Skrin 36(5):873–882

    CAS  Google Scholar 

  • Scott M, McCollum C, Vasil’ev S, Crozier C, Espie GS, Krol M, Huner NP, Bruce D (2006) Mechanism of the down regulation of photosynthesis by blue light in the Cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 45(29):8952–8958

    Article  CAS  PubMed  Google Scholar 

  • Stadnichuk IN, Yanyushin MF, Maksimov EG, Lukashev EP, Zharmukhamedov SK, Elanskaya IV, Paschenko VZ (2012) Site of non-photochemical quenching of the phycobilisome by orange carotenoid protein in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1917:1436–1445

    Article  CAS  Google Scholar 

  • Stadnichuk IN, Yanyushin MF, Bernat G, Zlenko DV, Krasilnikov PM, Lukashev EP, Maksimov EG, Paschenko VZ (2013) Fluorescence quenching of the phycobilisome terminal emitter LCM from the cyanobacterium Synechocystis sp. PCC 6803 detected in vivo and in vitro. J Photochem Photobiol 125:137–145

    Article  CAS  Google Scholar 

  • Su X, Fraenkel PG, Bogorad L (1992) Excitation energy transfer from phycocyanin to chlorophyll in an apcA-defective mutant of Synechocystis sp. PCC 6803. J Biol Chem 267(32):22944–22950

    CAS  PubMed  Google Scholar 

  • Sutter M, Wilson A, Leverenz RL, Lopez-Igual R, Thurotte A, Salmeen AE, Kirilovsky D, Kerfeld CA (2013) Crystal structure of the FRP and identification of the active site for modulation of OCP-mediated photoprotection in cyanobacteria. Proc Natl Acad Sci USA 110(24):10022–10027

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tandeau de Marsac N (2003) Phycobiliproteins and phycobilisomes: the early observations. Photosynth Res 76(1–3):197–205

    CAS  Google Scholar 

  • Tian L, van Stokkum IH, Koehorst RB, Jongerius A, Kirilovsky D, van Amerongen H (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133(45):18304–18311

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Gwizdala M, van Stokkum IH, Koehorst RB, Kirilovsky D, van Amerongen H (2012) Picosecond kinetics of light harvesting and photoprotective quenching in wild-type and mutant phycobilisomes isolated from the cyanobacterium Synechocystis PCC 6803. Biophys J 102(7):1692–1700

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tian L, van Stokkum IH, Koehorst RB, van Amerongen H (2013) Light harvesting and blue-green light induced non-photochemical quenching in two different C-phycocyanin mutants of Synechocystis PCC 6803. J Phys Chem 117(38):11000–11006

    Article  CAS  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature 473(7345):55–60

    Article  CAS  PubMed  Google Scholar 

  • Unlu C, Drop B, Croce R, van Amerongen H (2014) State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proc Natl Acad Sci USA 111(9):3460–3465

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • van Thor JJ, Mullineaux CW, Matthijs HCP, Hellingwert KJ (1998) Light harvesting and state transitions in cyanobacteria. Bot Acta 111(6):430–443

    Article  Google Scholar 

  • Vener AV, Van Kan PJ, Gal A, Andersson B, Ohad I (1995) Activation/deactivation cycle of redox-controlled thylakoid protein phosphorylation. Role of plastoquinol bound to the reduced cytochrome bf complex. J Biol Chem 270(42):25225–25232

    Article  CAS  PubMed  Google Scholar 

  • Vener AV, van Kan PJ, Rich PR, Ohad I, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci USA 94(4):1585–1590

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Watanabe M, Ikeuchi M (2013) Phycobilisome: architecture of a light-harvesting supercomplex. Photosynth Res 116(2–3):265–276

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Semchonok DA, Webber-Birungi MT, Ehira S, Kondo K, Narikawa R, Ohmori M, Boekema EJ, Ikeuchi M (2014) Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc Natl Acad Sci USA 111(7):2512–2517

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18(4):992–1007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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(2):656–672

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson A, Punginelli C, Gall A, Bonetti C, Alexandre M, Routaboul JM, Kerfeld CA, van Grondelle R, Robert B, Kennis JT, Kirilovsky D (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci USA 105(33):12075–12080

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson A, Kinney JN, Zwart PH, Punginelli C, D’Haene S, Perreau F, Klein MG, Kirilovsky D, Kerfeld CA (2010) Structural determinants underlying photoprotection in the photoactive orange carotenoid protein of cyanobacteria. J Biol Chem 285(24):18364–18375

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson A, Punginelli C, Couturier M, Perrau F, Kirilovsky D (2011) Essential role of two tyrosines and two tryptophans on photoprotection activity of the Orange Carotenoid Protein. Biochim Biophys Acta 1807:293–301

    Article  CAS  PubMed  Google Scholar 

  • Wilson A, Gwizdala M, Mezzetti A, Alexandre M, Kerfeld CA, Kirilovsky D (2012) The essential role of the N-terminal domain of the orange carotenoid protein in cyanobacterial photoprotection: importance of a positive charge for phycobilisome binding. Plant Cell 24(5):1972–1983

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20(14):3623–3630

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wollman FA, Lemaire C (1988) Studies on kinase-controlled state transitions in Photosystem II and b6f mutants from Chlamydomonas Reinhardtii which lack quinone-binding proteins. Biochim Biophys Acta 933(1):85–94

    Article  CAS  Google Scholar 

  • Yang S, Su Z, Li H, Feng J, Xie J, Xia A, Gong Y, Zhao J (2007) Demonstration of phycobilisome mobility by the time- and space-correlated fluorescence imaging of a cyanobacterial cell. Biochim Biophys Acta 1767(1):15–21

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Zhang R, Hu C, Xie J, Zhao J (2009) The dynamic behavior of phycobilisome movement during light state transitions in cyanobacterium Synechocystis PCC6803. Photosynth Res 99(2):99–106

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA, Kim SH (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392(6677):677–684

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Liu H, Niedzwiedzki DM, Prado M, Jiang J, Gross ML, Blankenship RE (2013) Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein. Biochemistry 53(1):13–19

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA (1999) The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J 18(11):2961–2969

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Kirilovsky, D. Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions. Photosynth Res 126, 3–17 (2015). https://doi.org/10.1007/s11120-014-0031-7

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