Skip to main content

Modification of Energy Distribution Between Photosystems I and II by Spillover Revealed by Time-Resolved Fluorescence Spectroscopy

  • Chapter
  • First Online:
Photosynthesis: Molecular Approaches to Solar Energy Conversion

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 47))

  • 1313 Accesses

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akhtar P, Lingvay M, Kiss T, Deák R, Bóta A, Ughy B, Garab G, Lambrev PH (2016) Excitation energy transfer between light-harvesting complex II and photosystem I in reconstituted membranes. Biochim Biophys Acta 1857:462–472

    Article  CAS  PubMed  Google Scholar 

  • Akimoto S, Yokono M (2017) How light-harvesting and energy-transfer processes are modified under different light conditions: studies by time-resolved fluorescence spectroscopy. In: Hou HJM, Najafpour MM, Moore GF, Allakhverdiev SI (eds) Photosynthesis: Structures, Mechanisms, and Applications. Springer, Cham, pp 169–184

    Chapter  Google Scholar 

  • Akimoto S, Takaichi S, Ogata T, Nishimura Y, Yamazaki I, Mimuro M (1996) Excitation energy transfer in carotenoid–chlorophyll protein complexes probed by femtosecond fluorescence decays. Chem Phys Lett 260:147–152

    Article  CAS  Google Scholar 

  • Akimoto S, Yamazaki I, Takaichi S, Mimuro M (2000) Excitation relaxation dynamics of linear carotenoids. J Lumin 87–89:797–799

    Article  Google Scholar 

  • Akimoto S, Yokono M, Ohmae M, Yamazaki I, Tanaka A, Higuchi M, Tsuchiya T, …, Mimuro M (2005) Ultrafast excitation relaxation dynamics of lutein in solution and in the light-harvesting complexes II isolated from Arabidopsis thaliana. J Phys Chem B 109:12612–12619

    Google Scholar 

  • Akimoto S, Tomo T, Naitoh Y, Otomo A, Murakami A, Mimuro M (2007) Identification of a new excited state responsible for the in vivo unique absorption band of siphonaxanthin in the green alga Codium fragile. J Phys Chem B 111:9179–9181

    Article  CAS  PubMed  Google Scholar 

  • Akimoto S, Yokono M, Hamada F, Teshigahara A, Aikawa S, Kondo A (2012) Adaptation of light-harvsting systems of Arthrospira platensis to light conditions, probed by time-resolved fluorescence spectroscopy. Biochim Biophys Acta 1817:1483–1489

    Google Scholar 

  • Akimoto S, Yokono M, Aikawa S, Kondo A (2013) Modification of energy transfer processes in the cyanobacterium Arthrospira platensis to adapt to light conditions, probed by time-resolved fluorescence spectroscopy. Photosynth Res 117:235–243

    Article  CAS  PubMed  Google Scholar 

  • Akimoto S, Teshigahara A, Yokono M, Mimuro M, Nagao R, Tomo T (2014a) Excitation relaxation dynamics and energy transfer in fucoxanthin-chlorophyll a/c-protein complexes, probed by time-resolved fluorescence. Biochim Biophys Acta 1837:1514–1521

    Article  CAS  PubMed  Google Scholar 

  • Akimoto S, Yokono M, Yokono E, Aikawa S, Kondo A (2014b) Short-term light adaptation of a cyanobacterium, Synechocystis sp. PCC 6803, probed by time-resolved fluorescence spectroscopy. Plant Physiol Biochem 81:149–154

    Article  CAS  PubMed  Google Scholar 

  • Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, …, Aro EM (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci U S A 110:4111–4116

    Google Scholar 

  • Allorent G, Tokutsu R, Roach T, Peers G, Cardol P, Girard-Bascou J, Seigneurin-Berny D, …, Finazzi G (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557

    Google Scholar 

  • Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180

    Article  CAS  PubMed  Google Scholar 

  • Antoshvili M, Caspy I, Hippler M, Nelson N (2019) Structure and function of photosystem I in Cyanidioschyzon merolae. Photosynth Res 139:499–508

    Article  CAS  PubMed  Google Scholar 

  • Ballottari M, Alcocer MJP, D’Andrea C, Viola D, Ahn TK, Petrozza A, Polli D, …, Bassi R (2014) Regulation of photosystem I light harvesting by zeaxanthin. Proc Natl Acad Sci U S A 111:E2431–E2438

    Google Scholar 

  • Ballottari M, Truong TB, De Re E, Erickson E, Stella GR, Fleming GR, Bassi R, Niyogi KK (2016) Identification of pH-sensing sites in the light harvesting complex stress-related 3 protein essential for triggering non-photochemical quenching in Chlamydomonas reinhardtii. J Biol Chem 291:7334–7346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blankenship RE (2014) Molecular Mechanisms of Photosynthesis, 2nd edn. Wiley-Blackwell, Oxford

    Google Scholar 

  • Bos I, Bland KM, Tian L, Croce R, Frankel LK, van Amerongen H, Bricker TM, Wientjes E (2017) Multiple LHCII antennae can transfer energy efficiently to a single photosystem I. Biochim Biophys Acta 1858:371–378

    Google Scholar 

  • Brown JS (1967) Fluorometric evidence for the participation of chlorophyll a-695 in systmem 2 of photosynthesis. Biochim Biophys Acta 143:391–398

    Article  CAS  PubMed  Google Scholar 

  • Bruce D, Biggins J, Steiner T, Thewalt M (1985) Mechanism of the light state transition in photosynthesis. IV. Picosecond fluorescence spectroscopy of Anacystis nidulans and Porphyridium cruentum in state 1 and state 2 at 77 K. Biochim Biophys Acta 806:237–246

    Google Scholar 

  • Bruce D, Brimble S, Bryant DA (1989) State transitons in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974:66–73

    Article  CAS  PubMed  Google Scholar 

  • Burton-Smith RN, Watanabe A, Tokutsu R, Song C, Murata K, Minagawa J (2019) Structural determination of the large photosystem II–light harvesting complex II supercomplex of Chlamydomonas reinhardtii using non-ionic amphipol. J Biol Chem 294:15003–15013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caffarri S, Broess K, Croce R, van Amerongen H (2011) Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys J 100:2094–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chisholm SW, Olson RJ, Zettler ER, Goericke R, Waterbury JB, Welschmeyer NA (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334:340–343

    Article  Google Scholar 

  • Chmeliov J, Gelzinis A, Songaila E, Augulis R, Duffy CDP, Ruban AV, Valkunas L (2016) The nature of self-regulation in photosynthetic light-harvesting antenna. Nat Plants 2:16045

    Article  CAS  PubMed  Google Scholar 

  • Christensen RL (1999) The electronic states of carotenoids. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The Photochemistry of Carotenoids. Kluwer Academic Publishers, Dordrecht, pp 137–157

    Google Scholar 

  • Correa-Galvis V, Poschmann G, Melzer M, Stühler K, Jahns P (2016) PsbS interactions involved in the activation of energy dissipation in Arabidopsis. Nat Plants 2:15225

    Article  CAS  PubMed  Google Scholar 

  • Crisafi E, Pandit A (2017) Disentangling protein and lipid interactions that control a molecular switch in photosynthetic light harvesting. Biochim Biophys Acta 1859:40–47

    Article  CAS  Google Scholar 

  • Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res 116:153–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croce R, Dorra D, Holzwarth AR, Jennings RC (2000) Fluorescence decay and spectral evolution in intact photosystem I of higher plants. Biochemistry 39:6341–6348

    Article  CAS  PubMed  Google Scholar 

  • Dall’Osto L, Caffarri S, Bassi R (2005) A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17:1217–1232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Demmig-Adams B, Garab G, Adams WIII, Govindjee (2014) Non-photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Springer, Dordrecht

    Book  Google Scholar 

  • Dinc E, Tian L, Roy LM, Roth R, Goodenough U, Croce R (2016) LHCSR1 induces a fast and reversible pH-dependent fluorescence quenching in LHCII in Chlamydomonas reinhardtii cells. Proc Natl Acad Sci U S A 113:7673–7678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drop B, Yadav KNS, Boekema EJ, Croce R (2014) Consequences of state transitions on the structural and functional organization of photosystem I in the green alga Chlamydomonas reinhardtii. Plant J 78:181–191

    Article  CAS  PubMed  Google Scholar 

  • Eads DD, Castner EW Jr, Alberte RS, Mets L, Fleming GR (1989) Direct observation of energy transfer in a photosynthetic membrane: chlorophyll b to chlorophyll a transfer in LHC. J Phys Chem 93:8271–8275

    Article  CAS  Google Scholar 

  • Fan M, Li M, Liu Z. Cao P. Pan X, Zhang H, Zhao X, …, Chang W (2015) Crystal structures of the PsbS protein essential for photoprotection in plants. Nat Struct Mol Biol 22:729–735

    Google Scholar 

  • Fleming GR (1986) Chemical Applications of Ultrafast Spectroscopy. Oxford Univ Press, Oxford

    Google Scholar 

  • Förster T (1965) Delocalized excitation and excitation transfer. In: Sinanoglu S (ed) Modern Quantum Chemistry Istanbul Lectures, vol 3. Academic, New York, pp 93–137

    Google Scholar 

  • Furukawa R, Aso M, Fujita T, Akimoto S, Tanaka R, Tanaka A, Yokono M, Takabayashi A (2019) Formation of a PSI–PSII megacomplex containing LHCSR and PsbS in the moss Physcomitrella patens. J Plant Res 132:867–880

    Article  CAS  PubMed  Google Scholar 

  • Gao S, Chi Z, Chen H, Zheng Z, Weng Y, Wang G (2019) A supercomplex, of approximately 720 kDa and composed of both photosystem reaction centers, dissipates excess energy by PSI in green macroalgae under salt stress. Plant Cell Physiol 60:166–175

    Article  CAS  PubMed  Google Scholar 

  • Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932

    Article  CAS  PubMed  Google Scholar 

  • Gillbro T, Andersson PO, Liu RSH, Asato AE, Takaichi S, Cogdell RJ (1993) Location of the carotenoid 2Ag state and its role in photosynthesis. Photochem Photobiol 57:44–48

    Article  CAS  Google Scholar 

  • Girolomoni L, Cazzaniga S, Pinnola A, Perozeni F, Ballottari M, Bassi R (2019) LHCSR3 is a nonphotochemical quencher of both photosystems in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 116:4212–4217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldschmidt-Clermont M, Bassi R (2015) Sharing light between two photosystems: mechanism of state transitions. Curr Opin Plant Biol 25:71–78

    Article  CAS  PubMed  Google Scholar 

  • Goodwin TW, Britton G (1988) Distribution and analysis of carotenoids. In: Goodwin TW (ed) Plant Pigments. Academic, London, pp 62–132

    Google Scholar 

  • Green BR, Anderson JM, Parson WW (2003) Photosynthetic membranes and their light-harvesting antennas. In: Green BR, Parson WW (eds) Light-Harvesting Antennas in Photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 1–28

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamada F, Murakami A, Akimoto S (2015) Comparative analysis of ultrafast excitation energy transfer pathways in three strains of divinyl chlorophyll a/b-containing cyanobacterium, Prochlorococcus marinus. J Phys Chem B 119:15593–15600

    Article  CAS  PubMed  Google Scholar 

  • Hamada F, Murakami A, Akimoto S (2017) Adaptation of divinyl chlorophyll a/b-containing cyanobacterium to different light conditions: three strains of Prochlorococcus marinus. J Phys Chem B 121:9081–9090

    Article  CAS  PubMed  Google Scholar 

  • Herbstová M, Bína D, Koník P, Gardian Z, Vácha F, Litvín R (2015) Molecular basis of chromatic adaptation in pennate diatom Phaeodactylum tricornutum. Biochim Biophys Acta 1847:534–543

    Article  PubMed  CAS  Google Scholar 

  • Hodges M, Barber J (1983) State 1-state 2 transitions in a unicellular green algae: analysis of in vivo chlorophyll fluorescence induction curves in the presence of 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea (DCMU). Plant Physiol 72:1119–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt NE, Kennis JTM, Dall’Osto L, Bassi R, Fleming GR (2003) Carotenoid to chlorophyll energy transfer in light harvesting complex II from Arabidopsis thaliana probed by femtosecond fluorescence upconversion. Chem Phys Lett 379:305–313

    Article  CAS  Google Scholar 

  • Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll–protein complex. FEBS Lett 292:1–4

    Article  CAS  PubMed  Google Scholar 

  • Ishihara T, Ifuku K, Yamashita E, Fukunaga Y, Nishino Y, Miyazawa A, Kashino Y, Inoue-Kashino N (2015) Utilization of light by fucoxanthin−chlorophyll-protein in a marine centric diatom, Chaetoceros gracilis. Photosynth Res 126:437–447

    Article  CAS  PubMed  Google Scholar 

  • Iwai M, Yokono M (2017) Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants. Curr Opin Plant Biol 37:94–101

    Article  CAS  PubMed  Google Scholar 

  • Johnson MP, Goral TK, Duffy CDP, Brain APR, Mullineaux CW, Ruban AV (2011) Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:1468–1479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato Y, Yokono M, Akimoto S, Takabayashi A, Tanaka A, Tanaka R (2017) Deficiency of the stroma-lamellar protein LIL8/PSB33 affects energy transfer around PSI in Arabidopsis. Plant Cell Physiol 58:2026–2039

    Article  CAS  PubMed  Google Scholar 

  • Katoh T, Nagashima U, Mimuro M (1991) Fluorescence properties of the allenic carotenoid fucoxanthin: implication for energy transfer in photosynthetic pigment systems. Photosynth Res 27:221–226

    Article  CAS  PubMed  Google Scholar 

  • Kim E, Akimoto S, Tokutsu R, Yokono M, Minagawa J (2017) Fluorescence lifetime analyses reveal how the high light-responsive protein LHCSR3 transforms PSII light-harvesting complexes into an energy-dissipative state. J Biol Chem 292:18951–18960

    Article  CAS  PubMed  PubMed Central  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 1817:158–166

    Article  CAS  PubMed  Google Scholar 

  • Klimov VV, Klevanik AV, Shuvalov VA, Kransnovsky AA (1977) Reduction of pheophytin in the primary light reaction of photosystem II. FEBS Lett 82:183–186

    Article  CAS  PubMed  Google Scholar 

  • Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004

    Article  CAS  PubMed  Google Scholar 

  • Kosuge K, Tokutsu R, Kim E, Akimoto S, Yokono M, Ueno Y, Minagawa J (2018) LHCSR1-dependent fluorescence quenching is mediated by excitation energy transfer from LHCII to photosystem I in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 115:3722–3727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouřil R, Zygadlo A, Arteni AA, de Wit CD, Dekker JP, Jensen PE, Scheller HV, Boekema EJ (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44:10935–10940

    Google Scholar 

  • Kowalczyk N, Rappaport F, Boyen C, Wollman FA, Collén J, Joliot P (2013) Photosynthesis in Chondrus crispus: the contribution of energy spill-over in the regulation of excitonic flux. Biochim Biophys Acta 1827:834–842

    Article  CAS  PubMed  Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis: An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574

    Article  CAS  Google Scholar 

  • Krause GH, Vernotte C, Briantais JM (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components. Biochim Biophys Acta 679:116–124

    Article  CAS  Google Scholar 

  • Kunugi M, Satoh S, Ihara K, Shibata K, Yamaguchi Y, Kogame K, Obokata J, …, Takabayashi A, Tanaka A (2016) Evolution of green plants accompanied changes in light-harvesting systems. Plant Cell Physiol 57:1231–1243

    Google Scholar 

  • Lakowicz JR (2006) Principles of Fluorescence Spectroscopy, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Lemeille S, Rochaix JD (2010) State transitions at the crossroad of thylakoid signalling pathways. Photosynth Res 106:33–46

    Article  CAS  PubMed  Google Scholar 

  • Ley AC, Butler WL (1977) Energy transfer from photosystem II to photosystem I in Porphyridium cruentum. Biochim Biophys Acta 462:290–294

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Lin Y, Garvey CJ, Birch D, Corkery RW, Loughlin PC, Scheer H, …, Chen M (2016) Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim Biophys Acta 1857:107–114

    Google Scholar 

  • Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292

    Article  CAS  PubMed  Google Scholar 

  • Liu LN, Elmalk AT, Aartsma TJ, Thomas JC, Lamers GEM, Zhou BC, Zhang YZ (2008) Light-induced energetic decoupling as a mechanism for phycobilisome-related energy dissipation in red algae: a single molecule study. PLoS One 3:e3134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342:1104–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Gao Z, Liu K, Sun R, Cui C, Holzwarth AR, Yang C (2016) Simultaneous refolding of denatured PsbS and reconstitution with LHCII into liposomes of thylakoid lipids. Photosynth Res 127:109–116

    Article  CAS  PubMed  Google Scholar 

  • Malnoë A (2018) Photoinhibition or photoprotection of photosynthesis? Update on the (newly termed) sustained quenching component qH. Environ Exp Bot 154:123–133

    Article  CAS  Google Scholar 

  • Malnoë A, Schultink A, Shahrasbi S, Rumeau D, Havaux M, Niyogi KK (2017) The plastid lipocalin LCNP is required for sustained photoprotective energy dissipation in Arabidopsis. Plant Cell 30:196–208

    Article  PubMed  PubMed Central  CAS  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 130:1201–1212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M, Garab G, Croce R, Holzwarth AR (2008) Far-red fluorescence: a direct spectroscopic marker for LHCII oligomers forming in non-photochemical quenching. FEBS Lett 582:3625–3631

    Article  CAS  PubMed  Google Scholar 

  • Mimuro M, Kikuchi H (2003) Antenna systems and energy tramsfer in cyanophyta and rhodophyta. In: Green BR, Parson WW (eds) Light-Harvesting Antennas in Photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 281–306

    Chapter  Google Scholar 

  • Mimuro M, Lipschultz C, Gantt E (1986) Energy flow in the phycobilisome core of Nostoc sp. (MAC): two independent terminal pigments. Biochim Biophys Acta 852:126–132

    Article  CAS  Google Scholar 

  • Mimuro M, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T (2007) Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta 1767:327–334

    Article  CAS  PubMed  Google Scholar 

  • Mimuro M, Yokono M, Akimoto S (2010) Variations in photosystem I properties in the primordial cyanobacterium Gloeobacter violaceus PCC 7421. Photochem Photobiol 86:62–69

    Article  CAS  PubMed  Google Scholar 

  • Mimuro M, Murakami A, Tomo T, Tsuchiya T, Watabe T, Yokono M, Akimoto S (2011) Molecular environments of divinyl chlorophylls in Prochlorococcus and Synechocystis: differences in fluorescence properties with chlorophyll replacement. Biochim Biophys Acta 1807:471–481

    Article  CAS  PubMed  Google Scholar 

  • Minagawa J (2011) State transitions–the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta 1807:897–905

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux CW, Pascal AA, Horton P, Holzwarth AR (1993) Excitation-energy quenching in aggregates of the LHCII chlorophyll-protein complex: a time-resolved fluorescence study. Biochim Biophys Acta 1141:23–28

    Article  CAS  Google Scholar 

  • Murao T, Yamazaki I, Yoshihara K (1982) Applicability of a microchannel plate photomultiplier to the time-correlated photon counting technique. Appl Opt 21:2297–2298

    Article  CAS  PubMed  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Satoh K (1986) Absorption and fluorescence emission by intact cells, chloroplasts, and chlorophyll–protein complexes. In: Govindjee, Amesz J, Fork DC (eds) Light Emission by Plants and Bacteria. Academic Press, Orlando, p 137–159

    Chapter  Google Scholar 

  • Nagae H, Kakitani T, Katoh T, Mimuro M (1993) Calculation of the excitation transfer matrix elements between the S2 or S1 state of carotenoid and the S2 or S1 state of bacteriochlorophyll. J Chem Phys 98:8012–8023

    Article  CAS  Google Scholar 

  • Nagao R, Yokono M, Tomo T, Akimoto S (2014) Control mechanism of excitation energy transfer in a complex consisting of photosystem II and fucoxanthin chlorophyll a/c-binding protein. J Phys Chem Lett 5:2983–2987

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Ueno Y, Yokono M, Shen J-R, Akimoto S (2018) Alterations of pigment composition and their interactions in response to different light conditions in the diatom Chaetoceros gracilis probed by time-resolved fluorescence spectroscopy. Biochim Biophys Acta 1859:524–530

    Article  CAS  Google Scholar 

  • Nagao R, Ueno Y, Yokono M, Shen J-R, Akimoto S (2019a) Effects of excess light energy on excitation-energy dynamics in a pennate diatom Phaeodactylum tricornutum. Photosynth Res 141:355–365

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Ueno Y, Shen J-R, Akimoto S (2019b) pH-sensing machinery of excitation energy transfer in diatom PSI–FCPI complexes. J Phys Chem Lett 10:3531–3535

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Ueno Y, Shen J-R, Akimoto S (2020) Excitation energy transfer and quenching in diatom PSI-FCPI upon P700 cation formation. J Phys Chem B 124:1481–1486

    Article  CAS  PubMed  Google Scholar 

  • Nakayama K, Mimuro M, Nishimura Y, Yamazaki I, Okada M (1994) Kinetic analysis of energy transfer processes in LHC II isolated from the siphonous green alga, Bryopsis maxima with use of picosecond fluorescence spectroscopy. Biochem Biophys Acta 1188:117–124

    CAS  Google Scholar 

  • Natali A, Gruber JM, Dietzel L, Stuart MCA, van Grondelle R, Croce R (2016) Light-harvesting complexes (LHCs) cluster spontaneously in membrane environment leading to shortening of their excited state lifetimes. J Biol Chem 291:16730–16739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura Y, Arai T (2005) Time-resolved fluorescence spectroscopy for excited state dynamics. In: Wada N, Mimuro M (eds) Recent Progress of Bio/Chemiluminescence and Fluorescence Analysis in Photosynthesis. Research Signpost, Kerala, pp 193–211

    Google Scholar 

  • O’Connor DV, Phillips D (1984) Time-Correlated Single Photon Counting. Academic, New York

    Google Scholar 

  • Oka K, Ueno Y, Yokono M, Shen JR, Nagao R, Akimoto S (2020) Adaptation of light-harvesting and energy-transfer processes of a diatom Phaeodactylum tricornutum to different light qualities. Photosynth Res 146:227–234

    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 208:308–312

    Article  CAS  Google Scholar 

  • Olive J, Aijani 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 

  • Ozawa SI, Bald T, Onishi T, Xue H, Matsumura T, Kubo R, Takahashi H, …, Takahashi Y (2018) Configuration of ten light-harvesting chlorophyll a/b complex I subunits in Chlamydomonas reinhardtii photosystem I. Plant Physiol 178:583–595

    Google Scholar 

  • Peterman EJG, Monshouwer R, van Stokkum IHM, van Grondelle R, van Amerongen H (1997) Ultrafast singlet excitation transfer from carotenoids to chlorophylls via different pathways in light-harvesting complex II of higher plants. Chem Phys Lett 264:279–284

    Article  CAS  Google Scholar 

  • Pi X, Tian L, Dai HE, Qin X, Cheng L, Kuang T, Sen FS, Shen JR (2018) Unique organization of photosystem I–light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc Natl Acad Sci U S A 115:4423–4428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin XC, Pi X, Wang WD, Han G, Zhu L, Liu M, Cheng L, …, Sui SF (2019) Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits. Nat Plants 5:263–272

    Google Scholar 

  • Raszewski G, Renger T (2008) Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J Am Chem Soc 130:4431–4446

    Article  CAS  PubMed  Google Scholar 

  • Ricci M, Bradforth SE, Jimenez R, Fleming GR (1996) Internal conversion and energy transfer dyamics of spheroidene in solution and in the LH-1 and LH-2 light-harvesting complexes. Chem Phys Lett 259:381–390

    Article  CAS  Google Scholar 

  • Ruban AV (2013) The Photosynthetic Membrane: Molecular Mechanisms and Biophysics of Light Harvesting. Willy, Chichester

    Google Scholar 

  • Rüdiger W, Schoch S (1988) Chlorophylls. In: Goodwin TW (ed) Plant Pigments. Academic, London, pp 1–59

    Google Scholar 

  • Scheer H (2003) The pigments. In: Green BR, Parson WW (eds) Light-Harvesting Antennas in Photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 29–81

    Chapter  Google Scholar 

  • Schlodder E, Hussels M, Çetin M, Karapetyan NV, Brecht M (2011) Fluorescence of the various red antenna states in photosystem I complexes from cyanobacteria is affected differently by the redox state of P700. Biochim Biophys Acta 1807:1423–1431

    Article  CAS  PubMed  Google Scholar 

  • Shah J (1988) Ultrafast luminescence spectroscopy using sum frequency generation. IEEE J Quantum Electron 24:276–288

    Article  Google Scholar 

  • Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidr-Clemont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transtions in Arabidopsis. Proc Natl Acad Sci U S A 107:4782–4787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen L, Huang Z, Chang S, Wang W, Wang J, Kuang T, Han G, …, Zhang X (2019) Structure of a C2S2M2N2-type PSII–LHCII supercomplex from the green alga Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 116:21246–21255

    Google Scholar 

  • Sheng X, Watanabe A, Li A, Kim E, Song C, Murata K, Song D, …, Liu Z (2019) Structural insight into light harvesting for photosystem II in green algae. Nat Plants 5:1320–1330

    Google Scholar 

  • Shimura S, Fujita Y (1973) Some properties of the chlorophyll fluorescence of the diatom Phaeodactylum tricornutum. Plant Cell Physiol 14:341–352

    CAS  Google Scholar 

  • Shipman LL, Cotton TM, Norris JR, Katz JJ (1976) An analysis of the visible absorption spectrum of chlorophyll a monomer, dimer, and oligomers in solution. J Am Chem Soc 98:8222–8230

    Article  CAS  PubMed  Google Scholar 

  • Shubin VV, Bezsmertnaya IN, Karapetyan NV (1995) Efficient energy transfer from the long-wavelength antenna chlorophylls to P700 in photosystem I complexes from Spirulina platensis. J Photochem Photobiol B 30:153–160

    Article  CAS  Google Scholar 

  • Siefermann-Harms D (1985) Carotenoids in photosynthesis. I. Location in photosynthetic membranes and light-harvesting function. Biochem Biophys Acta 811:325–355

    CAS  Google Scholar 

  • Stowe-Evans EL, Kehoe DM (2004) Signal transduction during light-quality acclimation in cyanobacteria: a model system for understanding phytochrome-response pathways in prokaryotes. Photochem Photobiol Sci 3:495–502

    Article  CAS  PubMed  Google Scholar 

  • Su X, Ma J, Pan X, Zhao X, Chang W, Liu Z, Zhang X, Li M (2019) Antenna arrangement and energy transfer pathways of a green algal photosystem-I-LHCI supercomplex. Nat Plants 5:273–281

    Article  CAS  PubMed  Google Scholar 

  • Suga M, Ozawa SI, Yoshida-Motomura K, Akita F, Miyazaki N, Takahashi Y (2019) Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I. Nat Plants 5:626–636

    Article  PubMed  Google Scholar 

  • Suorsa M, Rantala M, Mamedov F, Lespinasse M, Trotta A, Grieco M, Vuorio E, …, Aro EM (2015) Light acclimation involves dynamic re-organization of the pigment–protein megacomplexes in non-appressed thylakoid domains. Plant J 84:360–373

    Google Scholar 

  • Tanabe M, Ueno Y, Yokono M, Shen JR, Nagao R, Akimoto S (2020) Changes in excitation relaxation of diatoms in response to fluctuating light, probed by fluorescence spectroscopies. Photosynth Res 146:143–150

    Google Scholar 

  • Tanaka K, Iida S, Takaichi S, Mimuro M, Murakami A, Akimoto S (2016) Excitation relaxation dynamics and energy transfer in pigment–protein complexes of a dinoflagellate, revealed by ultrafast fluorescence spectroscopy. Photosynth Res 130:183–191

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Farooq S, van Amerongen H (2013) Probing the picosecond kinetics of the photosystem II core complex in vivo. Phys Chem Chem Phys 15:3146–3154

    Article  CAS  PubMed  Google Scholar 

  • Tikkanen M, Grieco M, Kangasjärvi S, Aro EM (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152:723–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tikkanen M, Rantala S, Aro EM (2015) Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. Front Plant Sci 6:521

    Article  PubMed  PubMed Central  Google Scholar 

  • Tiwari A, Mamedov F, Grieco M, Suorsa M, Jajoo A, Styring S, Tikkanen M, Aro EM (2016) Photodamage of iron–Sulphur clusters in photosystem I induces non-photochemical energy dissipation. Nat Plants 2:16035

    Article  CAS  PubMed  Google Scholar 

  • Tokutsu R, Kato N, Bui KH, Ishikawa T, Minagawa J (2012) Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 287:31574–31581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 110:10016–10021

    Google Scholar 

  • Ueno Y, Aikawa S, Kondo A, Akimoto S (2015) Light adaptation of the unicellular red alga Cyanidioschyzon merolae, probed by time-resolved fluorescence spectroscopy. Photosynth Res 125:211–218

    Article  CAS  PubMed  Google Scholar 

  • Ueno Y, Aikawa S, Kondo A, Akimoto S (2016) Energy transfer in cyanobacteria and red algae: confirmation of spillover in intact megacomplexes of phycobilisome and both photosystems. J Phys Chem Lett 7:3567–3571

    Article  CAS  PubMed  Google Scholar 

  • Ueno Y, Aikawa S, Niwa K, Abe T, Murakami A, Kondo A, Akimoto S (2017) Variety in excitation energy transfer processes from phycobilisomes to photosystems I and II. Photosynth Res 133:235–243

    Article  CAS  PubMed  Google Scholar 

  • Ueno Y, Shimakawa G, Miyake C, Akimoto S (2018) Light-harvesting strategy during CO2-dependent photosynthesis in the green alga Chlamydomonas reinhardtii. J Phys Chem Lett 9:1028–1033

    Article  CAS  PubMed  Google Scholar 

  • Ueno Y, Aikawa S, Kondo A, Akimoto S (2019a) Adaptation of light-harvesting functions of unicellular green algae to different light qualities. Photosynth Res 139:145–154

    Article  CAS  PubMed  Google Scholar 

  • Ueno Y, Nagao R, Shen J-R, Akimoto S (2019b) Spectral properties and excitation relaxation of novel fucoxanthin chlorophyll a/c–binding protein complexes. J Phys Chem Lett 10:5148–5152

    Article  CAS  PubMed  Google Scholar 

  • van Amerongen H, Valkunas L, van Grondelle R (2000) Photosynthetic Excitons. World Scientific, London

    Book  Google Scholar 

  • van Grondelle R (1985) Excitation energy transfer, trapping and annihilation in photosynthetic systems. Biochim Biophys Acta 811:147–195

    Article  Google Scholar 

  • Vasil’ev S, Irrgang KD, Schrötter T, Bergmann A, Eichler HJ, Renger G (1997) Quenching of chlorophyll a fluorescence in the aggregates of LHCII: steady state fluorescence and picosecond relaxation kinetics. Biochemistry 36:7503–7512

    Article  PubMed  Google Scholar 

  • Vernotte C, Astier C, Olive J (1990) State 1−state 2 adaptation in the cyanobacteria Synechocystis PCC 6714 wild type and Synechocystis PCC 6803 wild type and phycocyanin-less mutant. Photosynth Res 26:203–212

    Article  CAS  PubMed  Google Scholar 

  • Walla PJ, Yom J, Krueger BP, Fleming GR (2000) Two-photon excitation spectrum of light-harvesting complex II and fluorescence upconversion after one- and two-photon excitation of the carotenoids. J Phys Chem B 104:4799–4806

    Article  CAS  Google Scholar 

  • Ware MA, Giovagnetti V, Belgio E, Ruban AV (2015) PsbS protein modulates non-photochemical chlorophyll fluorescence quenching in membranes depleted of photosystems. J Photochem Photobiol B 152:301–307

    Article  CAS  PubMed  Google Scholar 

  • Wasielewski MR, Kispert LD (1986) Direct measurement of the lowest excited singlet state lifetime of all-trans-β-carotene and related carotenoids. Chem Phys Lett 128:238–243

    Article  CAS  Google Scholar 

  • Wientjes E, van Amerongen H, Croce R (2013) LHCII is an antenna of both photosystems after long-term acclimation. Biochim Biophys Acta 1827:420–426

    Article  CAS  PubMed  Google Scholar 

  • Wlodarczyk LM, Dinc E, Croce R, Dekker JP (2016) Excitation energy transfer in Chlamydomonas reinhardtii deficient in the PSI core or the PSII core under conditions mimicking state transitions. Biochim Biophys Acta 1857:625–633

    Article  CAS  PubMed  Google Scholar 

  • Wolfe GR, Cunningham FX, Durnford D, Green BR, Gantt E (1994) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367:566–568

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wood WHJ, Barnett SFH, Flannery S, Hunter CN, Johnson MP (2019) Dynamic thylakoid stacking is regulated by LHCII phosphorylation but not its interaction with PSI. Plant Physiol 180:2152–2166

    Article  CAS  PubMed Central  Google Scholar 

  • Xue H, Tokutsu R, Bergner SV, Scholz M, Minagawa J, Hippler M (2015) PHOTOSYSTEM II SUBUNIT R is required for efficient binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to photosystem II-light-harvesting supercomplexes in Chlamydomonas reinhardtii. Plant Physiol 167:1566–1578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav KNS, Semchonok DA, Nosek L, Kouřil R, Fucile G, Boekema EJ, Eichacker LA (2017) Supercomplexes of plant photosystem I with cytochrome b6f, light-harvesting complex II and NDH. Biochim Biophys Acta 1858:12–20

    Article  CAS  Google Scholar 

  • Yamazaki I, Mimuro M, Murao T, Yamazaki T, Yoshihara K, Fujita Y (1984) Excitation energy transfer in the light harvesting antenna system of the red alga Phorphyridium cruentum and the blue-green alga Anacystis nidulans: analysis of time-resolved fluorescence spectra. Photochem Photobiol 39:233–240

    Article  CAS  Google Scholar 

  • Yamazaki I, Tamai N, Yamazaki T, Murakami A, Mimuro M, Fujita Y (1988) Sequential excitation energy transport in stacking multilayers: comparative study between photosynthetic antenna and Langmuir-Blodgett multilayers. J Phys Chem 92:5035–5044

    Article  CAS  Google Scholar 

  • Yamazaki T, Nishimura Y, Yamazaki I, Hirano M, Matsuura K, Shimada K, Mimuro M (1994) Energy migration in allophycocyanin-B trimer with a linker polypeptide: analysis by the principal multi-component spectral estimation (PMSE) method. FEBS Lett 353:43–47

    Article  CAS  PubMed  Google Scholar 

  • Yamori W, Kondo E, Sugiura D, Terashima I, Suzuki Y, Makino A (2016) Enhanced leaf photosynthesis as a target to increase grain yield: insights from transgenic rice lines with variable Rieske FeS protein content in the cytochrome b6/f complex. Plant Cell Environ 39:80–87

    Article  CAS  PubMed  Google Scholar 

  • Yokono M, Akimoto S (2018) Energy transfer and distribution in photosystem super/megacomplexes of plants. Curr Opin Biotech 54:50–56

    Article  CAS  PubMed  Google Scholar 

  • Yokono M, Murakami A, Akimoto S (2011) Excitation energy transfer between photosystem II and photosystem I in red algae: larger amounts of phycobilisome enhance spillover. Biochim Biophys Acta 1807:847–853

    Article  CAS  PubMed  Google Scholar 

  • Yokono M, Uchida H, Suzawa Y, Akimoto S, Murakami A (2012) Stabilization and modulation of the phycobilisome by calcium in the calciphilic freshwater red alga Bangia atropurpurea. Biochim Biophys Acta 1817:306–311

    Article  CAS  PubMed  Google Scholar 

  • Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675

    Article  CAS  PubMed  Google Scholar 

  • Yokono M, Umetani I, Takabayashi T, Akimoto S, Tanaka A (2019a) Regulation of excitation energy in Nannochloropsis photosystem II. Photosynth Res 139:155–161

    Article  CAS  PubMed  Google Scholar 

  • Yokono M, Takabayashi A, Kishimoto J, Fujita T, Iwai M, Murakami A, Akimoto S, Tanaka A (2019b) The PS–PSII megacomplex in green plants. Plant Cell Physiol 60:1098–1108

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seiji Akimoto .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Yokono, M., Ueno, Y., Akimoto, S. (2021). Modification of Energy Distribution Between Photosystems I and II by Spillover Revealed by Time-Resolved Fluorescence Spectroscopy. In: Shen, JR., Satoh, K., Allakhverdiev, S.I. (eds) Photosynthesis: Molecular Approaches to Solar Energy Conversion. Advances in Photosynthesis and Respiration, vol 47. Springer, Cham. https://doi.org/10.1007/978-3-030-67407-6_10

Download citation

Publish with us

Policies and ethics