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Photosynthetica

, Volume 56, Issue 1, pp 105–124 | Cite as

Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K

  • J. J. Lamb
  • G. Røkke
  • M. F. Hohmann-MarriottEmail author
Open Access
Review
First Online:

Abstract

Photosynthetic fluorescence emission spectra measurement at the temperature of 77 K (–196°C) is an often-used technique in photosynthesis research. At low temperature, biochemical and physiological processes that modulate fluorescence are mostly abolished, and the fluorescence emission of both PSI and PSII become easily distinguishable. Here we briefly review the history of low-temperature chlorophyll fluorescence methods and the characteristics of the acquired emission spectra in oxygen-producing organisms. We discuss the contribution of different photosynthetic complexes and physiological processes to fluorescence emission at 77 K in cyanobacteria, green algae, heterokont algae, and plants. Furthermore, we describe practical aspects for obtaining and presenting 77 K fluorescence spectra.

Additional key words

fluorescence low temperature photosynthesis 

Abbreviations

Chl

chlorophyll

LHC

light-harvesting complex

PSI

photosystem I

PSII

photosystem II

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References

  1. Alboresi A., Le Quiniou C., Yadav S.K.N. et al.: Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga Nannochloropsis gaditana.–New Phytol. 213: 714–726, 2017.PubMedCrossRefGoogle Scholar
  2. Allen J.F.: Protein phosphorylation in regulation of photosynthesis.–BBA-Bioenergetics 1098: 275–335, 1992.PubMedCrossRefGoogle Scholar
  3. Andrizhiyevskaya E.G., Chojnicka A., Bautista J.A. et al.: Origin of the F685 and F695 fluorescence in photosystem II.–Photosynth. Res. 84: 173–180, 2005.PubMedCrossRefGoogle Scholar
  4. Ben-Shem A., Frolow F., Nelson N.: Crystal structure of plant photosystem I.–Nature 426: 630–635, 2003.PubMedCrossRefGoogle Scholar
  5. Berkaloff C., Caron L., Rousseau B.: Subunit organization of PSI particles from brown algae and diatoms: polypeptide and pigment analysis.–Photosynth. Res. 23: 181–193, 1990.PubMedCrossRefGoogle Scholar
  6. Bibby T.S., Nield J., Barber J.: Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria.–Nature 412: 743–745, 2001a.PubMedCrossRefGoogle Scholar
  7. Bibby T.S., Nield J., Barber J.: Three-dimensional model and characterization of the iron stress-induced CP43′-photosystem I supercomplex isolated from the cyanobacterium Synechocystis PCC 6803.–J. Biol. Chem. 276: 43246–43252, 2001b.PubMedCrossRefGoogle Scholar
  8. Biggins J., Bruce D.: Regulation of excitation energy transfer in organisms containing phycobilins.–Photosynth. Res. 20: 1–34, 1989.PubMedCrossRefGoogle Scholar
  9. Bína D., Gardian Z., Herbstová M., Litvín R.: Modular antenna of photosystem I in secondary plastids of red algal origin: a Nannochloropsis oceanica case study.–Photosynth. Res. 131: 255–266, 2017.PubMedCrossRefGoogle Scholar
  10. Björkman O., Demmig B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins.–Planta 170: 489–504, 1987.PubMedCrossRefGoogle Scholar
  11. Boardman N., Thorne S., Anderson J.: Fluorescence properties of particles obtained by digitonin fragmentation of spinach chloroplasts.–P. Natl. Acad. Sci. USA 56: 586–593, 1966.CrossRefGoogle Scholar
  12. Boehm M., Romero E., Reisinger V. et al.: Investigating the early stages of Photosystem II assembly in Synechocystis sp. PCC 6803 isolation of CP47 and CP43 complexes.–J. Biol. Chem. 286: 14812–14819, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Boehm M., Yu J., Reisinger V. et al.: Subunit composition of CP43-less photosystem II complexes of Synechocystis sp. PCC 6803: implications for the assembly and repair of photosystem II.–Philos. T. R. Soc. B 367: 3444–3454, 2012.CrossRefGoogle Scholar
  14. Boekema E.J., Dekker J.P., van Heel M.G. et al.: Evidence for a trimeric organization of the photosystem I complex from the thermophilic cyanobacterium Synechococcus sp.–FEBS Lett. 217: 283–286, 1987.CrossRefGoogle Scholar
  15. Boekema E.J., Hifney A., Yakushevska A.E., Piotrowski M.: A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria.–Nature 412: 745–758, 2001.PubMedCrossRefGoogle Scholar
  16. Bonaventura C., Myers J.: Fluorescence and oxygen evolution from Chlorella pyrenoidosa.–BBA-Bioenergetics 189: 366–383, 1969.PubMedCrossRefGoogle Scholar
  17. Brewster D.: On the colours of natural bodies.–Earth Env. Sci. T. R. So. 12: 538–545, 1834.Google Scholar
  18. Brody S.: New excited state of chlorophyll.–Science 128: 838–839, 1958.PubMedCrossRefGoogle Scholar
  19. Burnap R.L., Troyan T., Sherman L.A.: The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43 [prime]) is encoded by the isiA gene.–Plant Physiol. 103: 893–902, 1993.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Busch A., Nield J., Hippler M.: The composition and structure of photosystem Iassociated antenna from Cyanidioschyzon merolae.–Plant J. 62: 886–897, 2010.PubMedCrossRefGoogle Scholar
  21. Butler W.L.: Chlorophyll fluorescence: a probe for electron transfer and energy transfer.–In: Trebst A., Avron M. (ed.): Photosynthesis I. Pp. 149–167. Springer, Berlin–Heidelberg 1977.CrossRefGoogle Scholar
  22. Cardona T.: Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution?–Front. Plant Sci. 7: 257, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cavalier Smith T.O.M.: Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree.–J. Eukaryot. Microbiol. 46: 347–366, 1999.PubMedCrossRefGoogle Scholar
  24. Chen M., Blankenship R.E.: Expanding the solar spectrum used by photosynthesis.–Trends Plant Sci. 16: 427–431, 2011.PubMedCrossRefGoogle Scholar
  25. Chen M., Li Y., Birch D., Willows R.D.: A cyanobacterium that contains chlorophyll f–a redabsorbing photopigment.–FEBS Lett. 586: 3249–3254, 2012.PubMedCrossRefGoogle Scholar
  26. Cho F., Spencer J.: Emission spectra of Chlorella at very low temperatures (−269° to −196°).–Biochim. Biophys. Acta 126: 174–176, 1966.PubMedCrossRefGoogle Scholar
  27. Cho F.: Low-temperature (4–77° K) spectroscopy of Anacystis; temperature dependence of energy transfer efficiency.–BBABioenergetics 216: 151–161, 1970a.CrossRefGoogle Scholar
  28. Cho F.: Low-temperature (4–77° K) spectroscopy of Chlorella; temperature dependence of energy transfer efficiency.–BBABioenergetics 216: 139–150, 1970b.CrossRefGoogle Scholar
  29. Clayton R.K.: Photosynthesis: Physical Mechanisms and Chemical Patterns. Vol. 4. Pp. 19–35. Cambridge University Press, Cambridge 1980.Google Scholar
  30. Cordón G.B., Lagorio M.G.: Re-absorption of chlorophyll fluorescence in leaves revisited. A comparison of correction models.–Photochem. Photobio. S. 5: 735–740, 2006.CrossRefGoogle Scholar
  31. Croce R., Zucchelli G., Garlaschi F.M., Jennings R.C.: A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core.–Biochemistry 37: 17355–17360, 1998.PubMedCrossRefGoogle Scholar
  32. Dau H.: Molecular mechanisms and quantitative models of variable photosystem II fluorescence.–Photochem Photobiol 60: 1–23, 1994a.CrossRefGoogle Scholar
  33. Dau H.: New trends in photobiology: Short-term adaptation of plants to changing light intensities and its relation to Photosystem II photochemistry and fluorescence emission.–J. Photoch. Photobio. B 26: 3–27, 1994b.CrossRefGoogle Scholar
  34. de Marsac N.T.: Phycobiliproteins and phycobilisomes: the early observations.–Photosynth. Res. 76: 193–205, 2003.CrossRefGoogle Scholar
  35. Dekker J., Hassoldt A., Petterson A. et al.: On the nature of the F695 and F685 emission of photosystem II.–In: Mathis P. (ed.): Photosynthesis: From Light to Biosphere, Vol III. Pp. 53–56. Kluwer, Dordrecht 1995.CrossRefGoogle Scholar
  36. Dietzel L., Bräutigam K., Steiner S. et al.: Photosystem II supercomplex remodeling serves as an entry mechanism for state transitions in Arabidopsis.–Plant Cell 23: 2964–2977, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dong C., Tang A., Zhao J. et al.: ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002.–BBA-Bioenergetics 1787: 1122–1128, 2009.PubMedCrossRefGoogle Scholar
  38. Drop B., Webber-Birungi M., Yadav S.K.N. et al.: Lightharvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii.–BBA-Bioenergetics 1837: 63–72, 2014.PubMedCrossRefGoogle Scholar
  39. Duysens L., Sweers H.: Mechanism of two photochemical reactions in algae as studied by means of fluorescence.–In: Tamiya H. (ed.): Studies on Microalgae and Photosynthetic Bacteria. Pp. 353–372. University of Tokyo Press, Tokyo 1963.Google Scholar
  40. Eaton-Rye J.J., Sobotka R.: Assembly of the photosystem II membrane-protein complex of oxygenic photosynthesis.–Front. Plant Sci. 8: 884, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  41. El Bissati K., Delphin E., Murata N. et al.: Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms.–BBABioenergetics 1457: 229–242, 2000.CrossRefGoogle Scholar
  42. Emerson R.: Dependence of yield of photosynthesis in long-wave red on wavelength and intensity of supplementary light.–Science 125: 746, 1957.CrossRefGoogle Scholar
  43. Erickson E., Wakao S., Niyogi K.K.: Light stress and photoprotection in Chlamydomonas reinhardtii.–Plant J. 82: 449–465, 2015.PubMedCrossRefGoogle Scholar
  44. Falk S., Samson G., Bruce D. et al.: Functional analysis of the iron-stress induced CP 43′ polypeptide of PS II in the cyanobacterium Synechococcus sp. PCC 7942.–Photosynth. Res. 45: 51–60, 1995.PubMedCrossRefGoogle Scholar
  45. Farkas D.L., Malkin S.: Cold storage of isolated class C chloroplasts optimal conditions for stabilization of photosynthetic activities.–Plant Physiol. 64: 942–947, 1979.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Förster T.: Delocalizing Excitation and Excitation Transfer. Modern Quantum Chemistry Istanbul Lectures. Pp. 93–137. Academic Press, New York 1965.Google Scholar
  47. Franck F., Juneau P., Popovic R.: Resolution of the photosystem I and photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature.–BBA-Bioenergetics 1556: 239–246, 2002.PubMedCrossRefGoogle Scholar
  48. Frank H.A., Cua A., Chynwat V. et al.: Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis.–Photosynth. Res. 41: 389–395, 1994.PubMedCrossRefGoogle Scholar
  49. Galka P., Santabarbara S., Khuong T.T.H. et al.: Functional analyses of the plant photosystem I–light-harvesting complex II supercomplex reveal that light-harvesting complex ii loosely bound to photosystem ii is a very efficient antenna for photosystem I in state II.–Plant Cell 24: 2963–2978, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Gan F., Shen G., Bryant D.A.: Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria.–Life 5: 4–24, 2015.CrossRefGoogle Scholar
  51. Garczarek L., van der Staay G.W.M., Thomas J.C., Partensky F.: Isolation and characterization of Photosystem I from two strains of the marine oxychlorobacterium Prochlorococcus.–Photosynth. Res. 56: 131–141, 1998.CrossRefGoogle Scholar
  52. Gardian Z., Bumba L., Schrofel A. et al.: Organisation of photosystem I and photosystem II in red alga Cyanidium caldarium: encounter of cyanobacterial and higher plant concepts.–BBA-Bioenergetics 1767: 725–731, 2007.PubMedCrossRefGoogle Scholar
  53. Goldschmidt-Clermont M., Bassi R.: Sharing light between two photosystems: mechanism of state transitions.–Curr. Opin. Plant. Biol. 25: 71–78, 2015.PubMedCrossRefGoogle Scholar
  54. Gouterman M., Wagnière G.H., Snyder L.C.: Spectra of porphyrins: Part II. Four orbital model.–J. Mol. Spectrosc. 11: 108–127, 1963.CrossRefGoogle Scholar
  55. Govindjee, Björn L.O.: Evolution of the Z-scheme of photosynthesis: a perspective.–Photosynth. Res. 133: 5–15, 2017.PubMedCrossRefGoogle Scholar
  56. Govindjee, Ichimura S., Cederstrand C., Rabinowitch E.: Effect of combining far-red light with shorter wave light in the excitation of fluorescence in Chlorella.–Arch. Biochem. Biophys. 89: 322–323, 1960.PubMedCrossRefGoogle Scholar
  57. Govindjee, Yang L.: Structure of the red fluorescence band in chloroplasts.–J. Gen. Physiol. 49: 763–780, 1966.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Govindjee: Emerson enhancement effect and two light reactions in photosynthesis.–In: Kok B., Jagendorf A.T. (ed.): Photosynthetic Mechanisms of Green Plants. Pp 318. National Academy of Science–National Research Council Publication, Washington DC 1963.Google Scholar
  59. Govindjee: Chlorophyll a fluorescence: a bit of basics and history.–In: Papageorgiou G.C., {ieGovindjee: Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 1–41. Springer, Dordrecht 2004.Google Scholar
  60. Govindjee: Sixty-three years since kautsky: chlorophyll a fluorescence.–Aust. J. Plant Physiol. 22: 131–160, 1995.CrossRefGoogle Scholar
  61. Grouneva I., Rokka A., Aro E.-M.: The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery.–J. Proteome Res. 10: 5338–5353, 2011.PubMedCrossRefGoogle Scholar
  62. Gundermann K., Büchel C.: Structure and functional heterogeneity of fucoxanthin-chlorophyll proteins in diatoms.–In: Hohmann-Marriott M.F. (ed.): The Structural Basis of Biological Energy Generation. Pp. 31–27. Springer, Dordrecht 2014.Google Scholar
  63. Havaux M., Guedeney G., Hagemann M. et al.: The chlorophyllbinding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress.–FEBS Lett. 579: 2289–2293, 2005.PubMedCrossRefGoogle Scholar
  64. Herbstová M., Bína D., Koník P. et al.: Molecular basis of chromatic adaptation in pennate diatom Phaeodactylum tricornutum.–BBA-Bioenergetics 1847: 534–543, 2015.PubMedCrossRefGoogle Scholar
  65. Hillier W., Babcock G.T.: Photosynthetic reaction centers.–Plant Physiol. 125: 33–37, 2001.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hipkins M.F., Baker N.R.: Photosynthetic energy transduction: A practical approach.–In: Hipkins M.F., Baker N.R.: Photosynthesis: Energy Transduction, A Practical Approach. Pp 1. IRL Press, Arlington 1986.Google Scholar
  67. Hirsch R.E., Rich M., Govindjee: A tribute to Seymour Steven Brody: in memoriam (November 29, 1927 to May 25, 2010).–Photosynth. Res. 106: 191–199, 2010.PubMedCrossRefGoogle Scholar
  68. Hofstraat J.W., Rubelowsky K., Slutter S.: Corrected fluorescence excitation and emission spectra of phytoplankton: toward a more uniform approach to fluorescence measurements.–J. Plankton. Res. 14: 625–636, 1992.CrossRefGoogle Scholar
  69. Hohmann-Marriott M.F., Blankenship R.E.: Evolution of photosynthesis.–Plant. Physiol. 154: 434–438, 2011.Google Scholar
  70. Hohmann-Marriott M.F., Takizawa K., Eaton-Rye J.J. et al.: The redox state of the plastoquinone pool directly modulates minimum chlorophyll fluorescence yield in Chlamydomonas reinhardtii.–FEBS Lett. 584: 1021–1026, 2010.PubMedCrossRefGoogle Scholar
  71. Ikeda Y., Komura M., Watanabe M. et al.: Photosystem I complexes associated with fucoxanthin-chlorophyll-binding proteins from a marine centric diatom, Chaetoceros gracilis.–BBA-Bioenergetics 1777: 351–361, 2008.PubMedCrossRefGoogle Scholar
  72. Irrgang K.D., Boekema E.J., Vater J., Renger G.: Structural determination of the photosystem II core complex from spinach.–FEBS J. 178: 209–217, 1988.Google Scholar
  73. Iwai M., Takahashi Y., Minagawa J.: Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii.–Plant Cell 20: 2177–2189, 2008.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Järvi S., Suorsa M., Aro E.-M.: Photosystem II repair in plant chloroplasts–regulation, assisting proteins and shared components with photosystem II biogenesis.–BBABioenergetics 1847: 900–909, 2015.CrossRefGoogle Scholar
  75. Jordan P., Fromme P., Witt H.T., Klukas O.: Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution.–Nature 411: 909–917, 2001.PubMedCrossRefGoogle Scholar
  76. Joshua S., Mullineaux C.W.: Phycobilisome diffusion is required for light-state transitions in cyanobacteria.–Plant Physiol. 135: 2112–2119, 2004.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Juhas M., Büchel C.: Properties of photosystem I antenna protein complexes of the diatom Cyclotella meneghiniana.–J. Exp. Bot. 63: 3673–3681, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kaňa R., Kotabová E., Lukeš M. et al.: Phycobilisome mobility and its role in the regulation of light harvesting in red algae.–Plant Physiol. 165: 1618–1631, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Karapetyan N.V., Bolychevtseva Y.V., Yurina N.P. et al.: Longwavelength chlorophylls in photosystem I of cyanobacteria: origin, localization, and functions.–Biochemistry 79: 213, 2014.PubMedGoogle Scholar
  80. Kargul J., Nield J., Barber J.: Three-dimensional reconstruction of a light-harvesting complex I-photosystem I (LHCI-PSI) supercomplex from the green alga Chlamydomonas reinhardtii. Insights into light harvesting for PSI.–J. Biol. Chem. 278: 16135–16141, 2003.PubMedCrossRefGoogle Scholar
  81. Kautsky H., Hirsch A.: [New attempts for carbon dioxide assimilation.]–Naturwissenschaft 19: 964–964, 1931. [In German]CrossRefGoogle Scholar
  82. Keeling P.J.: The number, speed, and impact of plastid endosymbioses in eukaryotic evolution.–Annu. Rev. Plant Biol. 64: 583–607, 2013.PubMedCrossRefGoogle Scholar
  83. Komenda J., Sobotka R., Nixon P.J.: Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria.–Curr. Opin. Plant Biol. 15: 245–251, 2012.PubMedCrossRefGoogle Scholar
  84. Kondo K., Ochiai Y., Katayama M., Ikeuchi M.: The membraneassociated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna.–Plant Physiol. 144: 1200–1210, 2007.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Krause G.H., Briantais J.M., Vernotte C.: Characterization of chlorophyll fluorescence quenching in chloroplasts by fluorescence spectroscopy at 77 K I. ΔpH-dependent quenching.–BBA-Bioenergetics 723: 169–175, 1983.CrossRefGoogle Scholar
  86. Krause G.H., Weis E.: Chlorophyll fluorescence as a tool in plant physiology.–Photosynth. Res. 5: 139–157, 1984.PubMedCrossRefGoogle Scholar
  87. Krey A., Govindjee: Fluorescence studies on a red alga, Porphyridium cruentum.–Biochim. Biophys. Acta. 120: 1–18, 1966.PubMedCrossRefGoogle Scholar
  88. Kyle D.J., Ohad I., Arntzen C.J.: Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes.–P. Natl. Acad. Sci. USA 81: 4070–4074, 1984.CrossRefGoogle Scholar
  89. La Roche J., van der Staay G.W.M., Partensky F. et al.: Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins.–P. Natl. Acad. Sci. USA 93: 15244–15248, 1996.CrossRefGoogle Scholar
  90. Lakowicz J.R.: Fluorescence polarization.–In: Lakowicz J.R. (ed): Principles of Fluorescence Spectroscopy Pp. 111–153. Springer, Boston 1983a.CrossRefGoogle Scholar
  91. Lakowicz J.R.: Quenching of fluorescence.–In: Lakowicz J.R. (ed): Principles of Fluorescence Spectroscopy. Pp. 257–301. Springer, Boston 1983b.CrossRefGoogle Scholar
  92. Lamb J., Forfang K., Hohmann-Marriott M.: A practical solution for 77 K fluorescence measurements based on LED excitation and CCD array detector.–PLoS ONE 10: e0132258, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  93. Laudenbach D.E., Reith M.E., Straus N.A.: Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2.–J. Bacteriol. 170: 258–265, 1988.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Lavaud J., Lepetit B.: An explanation for the inter-species variability of the photoprotective non-photochemical chlorophyll fluorescence quenching in diatoms.–BBA-Bioenergetics 1827: 294–302, 2013.PubMedCrossRefGoogle Scholar
  95. Lepetit B., Volke D., Szabó M. et al.: Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum.–Biochemistry46: 9813–9822, 20PubMedCrossRefGoogle Scholar
  96. Ley A.C., Butler W.L.: Energy distribution in the photochemical apparatus of Porphyridium cruentum in state I and state II.–BBA-Bioenergetics 592: 349–363, 1980.PubMedCrossRefGoogle Scholar
  97. Li D., Xie J., Zhao J. et al.: Light-induced excitation energy redistribution in Spirulina platensis cells: “spillover” or “mobile PBSs”?–BBA-Bioenergetics 1608: 114–121, 2004.PubMedCrossRefGoogle Scholar
  98. Li H., Yang S., Xie J., Zhao J.: Probing the connection of PBSs to the photosystems in Spirulina platensis by artificially induced fluorescence fluctuations.–J. Lumin. 122-123: 294–296, 2007.CrossRefGoogle Scholar
  99. Li M., Semchonok D.A., Boekema E.J., Bruce B.D.: Characterization and evolution of tetrameric photosystem I from the thermophilic cyanobacterium Chroococcidiopsis sp TS-821.–Plant Cell 26: 1230–1245, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Li Y., Chen M.: Novel chlorophylls and new directions in photosynthesis research.–Funct. Plant Biol. 42: 493–501, 2015.CrossRefGoogle Scholar
  101. Litvin F.F., Krasnovsky A.A.: Investigation by fluorescence spectra of intermediate stages of chlorophyll biosynthesis in etiolated leaves.–Dokl. Acad. Nauk+ 117: 106–109, 1957.Google Scholar
  102. Litvín R., Bína D., Herbstová M., Gardian Z.: Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica.–Photosynth. Res. 130: 137–150, 20PubMedCrossRefGoogle Scholar
  103. Liu H., Roose J.L., Cameron J.C., Pakrasi H.B.: A genetically tagged Psb27 protein allows purification of two consecutive photosystem II (PSII) assembly intermediates in Synechocystis 6803, a cyanobacterium.–J. Biol. Chem. 286: 24865–24871, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  104. Liu H., Zhang H., Niedzwiedzki D.M. et al.: Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria.–Science 342: 1104–1107, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Marx A., David L., Adir N.: Piecing together the phycobilisome.–In: Hohmann-Marriott M.F. (ed): The Structural Basis of Biological Energy Generation. Pp. 59–76. Springer, Dordrecht 2014.CrossRefGoogle Scholar
  106. Maxwell K., Johnson G.N.: Chlorophyll fluorescence–a practical guide.–J. Exp. Bot. 51: 659–668, 2000.PubMedCrossRefGoogle Scholar
  107. Mazor Y., Borovikova A., Nelson N.: The structure of plant photosystem I super-complex at 2.8 Å resolution.–Elife 4: e07433, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  108. McConnell M.D., Koop R., Vasil’ev, S., Bruce D.: 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, 2002.PubMedPubMedCentralCrossRefGoogle Scholar
  109. McCormac D.J., Marwood C.A., Bruce D., Greenberg B.M.: Assembly of Photosystem I and II during the early phases of lightinduced development of chloroplasts from proplastids in Spirodela oligorrhiza.–Photochem. Photobiol. 63: 837–845, 19CrossRefGoogle Scholar
  110. Miloslavina Y., Grouneva I., Lambrev P.H. et al.: Ultrafast fluorescence study on the location and mechanism of nonphotochemical quenching in diatoms.–BBA-Bioenergetics 1787: 1189–1197, 2009.PubMedCrossRefGoogle Scholar
  111. Minagawa J.: State transitions–the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast.–BBA-Bioenergetics 1807: 897–905, 2011.PubMedCrossRefGoogle Scholar
  112. Miyashita H., Ikemoto H., Kurano N. et al.: Chlorophyll d as a major pigment.–Nature 383: 402, 1996.CrossRefGoogle Scholar
  113. Morosinotto T., Breton J., Bassi R., Croce R.: The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I.–J. Biol. Chem. 278: 49223–49229, 2003.PubMedCrossRefGoogle Scholar
  114. Mukerji I., Sauer K.: Temperature Dependent Steady State and Picosecond Kinetic Fluorescence Measurements of a Photosystem I Preparation from Spinach. Pp. 30. Lawrence Berkeley Laboratory, Berkeley, 1988.Google Scholar
  115. Müller N.: [Relationships between assimilation, absorption and fluorescence in the chlorophyll of the living leaf.]–Jahrb. Wiss. Bot. 9: 42–49, 1887. [In German]Google Scholar
  116. Mullet J., Burke J., Arntzen C.: A developmental study of photosystem I peripheral chlorophyll proteins.–Plant Physiol. 65: 823–827 1980a.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Mullet J., Burke J., Arntzen C.: Chlorophyll proteins of photosystem I.–Plant Physiol. 65: 814–822, 1980b.PubMedPubMedCentralCrossRefGoogle Scholar
  118. Mullineaux C.W., Allen J.F.: State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystems I and II.–Photosynth. Res. 23: 297–311, 1990.PubMedCrossRefGoogle Scholar
  119. Mullineaux C.W.: Electron transport and light-harvesting switches in cyanobacteria.–Front. Plant Sci. 5: 7, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Mullineaux C.W.: Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterial mutant lacking photosystem II.–BBA-Bioenergetics 1184: 71–77, 1994.CrossRefGoogle Scholar
  121. Mullineaux C.W.: Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium.–BBABioenergetics 1100: 285–292, 1992.CrossRefGoogle Scholar
  122. Mullineaux C.W.: Phycobilisome-reaction centre interaction in cyanobacteria.–Photosynth. Res. 95: 175–182, 2008.PubMedCrossRefGoogle Scholar
  123. Mulo P., Sakurai I., Aro E.-M.: Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair.–BBA-Bioenergetics 1817: 247–257, 2012.PubMedCrossRefGoogle Scholar
  124. Murakami A.: Quantitative analysis of 77K fluorescence emission spectra in Synechocystis sp. PCC 6714 and Chlamydomonas reinhardtii with variable PS I/PS II stoichiometries.–Photosynth. Res. 53: 141–148, 1997.CrossRefGoogle Scholar
  125. Murata N., Nishimura M., Takamiya A.: Fluorescence of chlorophyll in photosynthetic systems. III. Emission and action spectra of fluorescence–three emission bands of chlorophyll a and the energy transfer between two pigment systems.–Biochim. Biophys. Acta 126: 234–243, 1966.PubMedCrossRefGoogle Scholar
  126. Murata N.: Control of excitation transfer in photosynthesis I. Light-induced change of chlorophyll a fluoresence in Porphyridium cruentum.–BBA-Bioenergetics 172: 242–251, 19PubMedCrossRefGoogle Scholar
  127. Murata N.: Control of excitation transfer in photosynthesis. IV. Kinetics of chlorophyll a fluorescence in Porphyra yezoensis.–BBA-Bioenergetics 205: 379–389, 1970.PubMedCrossRefGoogle Scholar
  128. Mysliwa-Kurdziel B., Barthélemy X., Strzalka K., Franck F.: The early stages of photosystem II assembly monitored by measurements of fluorescence lifetime, fluorescence induction and isoelectric focusing of chlorophyll-proteins in barley etiochloroplasts.–Plant Cell Physiol. 38: 1187–1196, 1997.CrossRefGoogle Scholar
  129. Nagao R., Takahashi S., Suzuki T. et al.: Comparison of oligomeric states and polypeptide compositions of fucoxanthin chlorophyll a/c-binding protein complexes among various diatom species.–Photosynth. Res. 117: 281–288, 2013.PubMedCrossRefGoogle Scholar
  130. Nagao R., Tomo T., Noguchi E. et al.: Purification and characterization of a stable oxygen-evolving Photosystem II complex from a marine centric diatom, Chaetoceros gracilis.–BBABioenergetics 1797: 160–166, 2010.CrossRefGoogle Scholar
  131. Nakatani H., Ke B., Dolan E., Arntzen C.: Identity of the photosystem II reaction center polypeptide.–BBABioenergetics 765: 347–352, 1984.CrossRefGoogle Scholar
  132. Natali A., Croce R.: Characterization of the major lightharvesting complexes (LHCBM) of the green alga Chlamydomonas reinhardtii.–PLoS ONE 10: e0119211, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  133. Nickelsen J., Rengstl B.: Photosystem II assembly: from cyanobacteria to plants.–Annu. Rev. Plant Biol. 64: 609–635, 2013.PubMedCrossRefGoogle Scholar
  134. Nixon P.J., Barker M., Boehm M. et al.: FtsH-mediated repair of the photosystem II complex in response to light stress.–J. Exp. Bot. 56: 357–363, 2005.PubMedCrossRefGoogle Scholar
  135. Novoderezhkin V.I., Palacios M.A., van Amerongen H., van Grondelle R.: Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Å crystal structure.–J. Phys. Chem. B 109: 10493–10504, 2005.PubMedCrossRefGoogle Scholar
  136. Owens T.G.: Dynamics and mechanism of singlet energytransfer between carotenoids and chlorophylls-light harvesting and nonphotochemical fluorescence quenching.–In: Murata N. (ed.): Research in Photosynthesis. Pp. 179–186. Kluwer Acad. Publ., Dordrecht 1992.Google Scholar
  137. Pakrasi H.B., Goldenberg A., Sherman L.A.: Membrane development in the cyanobacterium, Anacystis nidulans, during recovery from iron starvation.–Plant Physiol. 79: 290–295, 1985a.PubMedPubMedCentralCrossRefGoogle Scholar
  138. Pakrasi H.B., Riethman H.C., Sherman L.A.: Organization of pigment proteins in the photosystem II complex of the cyanobacterium Anacystis nidulans R2.–P. Natl. Acad. Sci. USA 82: 6903–6907, 1985b.CrossRefGoogle Scholar
  139. Park Y.I., Sandström S., Gustafsson P., Öquist G.: Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting photosystem II from excess light under iron limitation.–Mol. Microbiol. 32: 123–129, 1999.PubMedCrossRefGoogle Scholar
  140. Passarini F., Wientjes E., Hienerwadel R., Croce R.: Molecular basis of light harvesting and photoprotection in CP24 unique features of the most recent antenna complex.–J. Biol. Chem. 284: 29536–29546, 2009.PubMedPubMedCentralCrossRefGoogle Scholar
  141. Pfundel E., Pfeffer M.: Modification of photosystem I light harvesting of bundle-sheath chloroplasts occurred during the evolution of NADP-malic enzyme C4 photosynthesis.–Plant Physiol. 114: 145–152, 1997.PubMedPubMedCentralCrossRefGoogle Scholar
  142. Qin X., Suga M., Kuang T., Shen J.-R.: Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex.–Science 348: 989–995, 2015.PubMedCrossRefGoogle Scholar
  143. Rabinowitch E., Govindjee: Photosynthesis. Pp. 273. John Wiley & Sons, Inc, New York 1969.Google Scholar
  144. Riethman H.C., Sherman L.A.: Purification and characterization of an iron stress-induced chlorophyll-protein from the cyanobacterium Anacystis nidulans R2.–BBA-Bioenergetics 935: 141–151, 1988.PubMedCrossRefGoogle Scholar
  145. Rijgersberg C.P., Amesz J., Thielen A., Swager J.A.: Fluorescence emission spectra of chloroplasts and subchloroplast preparations at low temperature.–BBA-Bioenergetics 545: 473–482, 1979.PubMedCrossRefGoogle Scholar
  146. Ruban A.V., Calkoen F., Kwa S.L.S. et al.: Characterisation of LHC II in the aggregated state by linear and circular dichroism spectroscopy.–BBA-Bioenergetics 1321: 61–70, 1997.CrossRefGoogle Scholar
  147. Ruban A.V., Johnson M.P., Duffy C.D.P.: The photoprotective molecular switch in the photosystem II antenna.–BBABioenergetics 1817: 167–181, 2012.CrossRefGoogle Scholar
  148. Şener M., Strümpfer J., Hsin J. et al.: Förster energy transfer theory as reflected in the structures of photosynthetic lightharvesting systems.–ChemPhysChem. 12: 518–531, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  149. Sétif P., Mathis P., Vänngård T.: Photosystem I photochemistry at low temperature. Heterogeneity in pathways for electron transfer to the secondary acceptors and for recombination processes.–BBA-Bioenergetics 767: 404–414, 1984.CrossRefGoogle Scholar
  150. Schlodder E., Falkenberg K., Gergeleit M., Brettel K.: Temperature dependence of forward and reverse electron transfer from A1-, the reduced secondary electron acceptor in photosystem I.–Biochemistry 37: 9466–9476, 1998.PubMedCrossRefGoogle Scholar
  151. Sjöback R., Nygren J., Kubista M.: Absorption and fluorescence properties of fluorescein.–Spectrochim. Acta A 51: 7–21, 1995.CrossRefGoogle Scholar
  152. Sobiechowska-Sasim M., Stoń-Egiert J., Kosakowska A.: Quantitative analysis of extracted phycobilin pigments in cyanobacteria–an assessment of spectrophotometric and spectrofluorometric methods.–J. Appl. Phycol. 26: 2065–2074, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  153. Standfuss J., Kühlbrandt W.: The three isoforms of the lightharvesting complex II spectroscopic features, trimer formation, and functional roles.–J. Biol. Chem. 279: 36884–36891, 2004.PubMedCrossRefGoogle Scholar
  154. Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the Chlorophyll a Fluorescence Transient.–In: Papageorgiou G.C., {ieGovindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 321–362. Springer, Dordrecht 2004.CrossRefGoogle Scholar
  155. Sugiura M., Inoue Y.: Highly purified thermo-stable oxygenevolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43.–Plant Cell Physiol. 40: 1219–1231, 1999.PubMedCrossRefGoogle Scholar
  156. Swingley W.D., Iwai M., Chen Y. et al.: Characterization of photosystem I antenna proteins in the prasinophyte Ostreococcus tauri.–BBA-Bioenergetics 1797: 1458–1464, 2010.PubMedCrossRefGoogle Scholar
  157. Takahashi S., Badger M.R.: Photoprotection in plants: a new light on photosystem II damage.–Trends Plant Sci. 16: 53–60, 2011.PubMedCrossRefGoogle Scholar
  158. Tang K., Ding W.-L., Höppner A. et al.: LCM: A light-harvesting pigment with a phytochrome chromophore.–P. Natl. Acad. Sci. USA 112: 15880–15885, 2015.CrossRefGoogle Scholar
  159. Tokutsu R., Minagawa J.: Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii.–P. Natl. Acad. Sci. USA 110: 10016–10021, 2013.CrossRefGoogle Scholar
  160. Umena Y., Kawakami K., Shen J.-R., Kamiya N.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.–Nature 473: 55–60, 2011.PubMedCrossRefGoogle Scholar
  161. van Wijk K.J., Bingsmark S., Aro E.-M., Andersson B.: In vitro synthesis and assembly of photosystem II core proteins. the D1 protein can be incorporated into photosystem II in isolated chloroplasts and thylakoids.–J. Biol. Chem. 270: 25685–25695, 1995.PubMedCrossRefGoogle Scholar
  162. Veith T., Büchel C.: The monomeric photosystem I-complex of the diatom Phaeodactylum tricornutum binds specific fucoxanthin chlorophyll proteins (FCPs) as light-harvesting complexes.–BBA-Bioenergetics 1767: 1428–1435, 2007.PubMedCrossRefGoogle Scholar
  163. Walters R.G., Horton P.: Resolution of components of nonphotochemical chlorophyll fluorescence quenching in barley leaves.–Photosynth. Res. 27: 121–133, 1991.PubMedCrossRefGoogle Scholar
  164. Watanabe M., Semchonok D.A., Webber-Birungi M.T. et al.: Attachment of phycobilisomes in an antenna–photosystem I supercomplex of cyanobacteria.–P. Natl. Acad. Sci. USA 111: 2512–2517, 2014.CrossRefGoogle Scholar
  165. Wei X., Su X., Cao P. et al.: Structure of spinach photosystem IILHCII supercomplex at 3.2 Å resolution.–Nature 534: 69–87, 2016.PubMedCrossRefGoogle Scholar
  166. Weis E.: Chlorophyll fluorescence at 77 K in intact leaves: characterization of a technique to eliminate artifacts related to self-absorption.–Photosynth. Res. 6: 73–86, 1985.PubMedCrossRefGoogle Scholar
  167. Wientjes E., van Stokkum I.H.M., van Amerongen H., Croce R.: The role of the individual Lhcas in photosystem I excitation energy trapping.–Biophys. J. 101: 745–754, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  168. Yamamoto Y., Hori H., Kai S. et al.: Quality control of Photosystem II: reversible and irreversible protein aggregation decides the fate of Photosystem II under excessive illumination.–Front. Plant Sci. 4: 433, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  169. Yokono M., Nagao R., Tomo T., Akimoto S.: Regulation of excitation energy transfer in diatom PSII dimer: How does it change the destination of excitation energy?–BBABioenergetics 1847: 1274–1282, 2015.CrossRefGoogle Scholar
  170. Young A.J., Frank H.A.: Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence.–J. Photoch. Photobio. B 36: 3–15, 1996.CrossRefGoogle Scholar

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Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

Authors and Affiliations

  • J. J. Lamb
    • 1
  • G. Røkke
    • 2
  • M. F. Hohmann-Marriott
    • 2
    Email author
  1. 1.Department of Electronic Systems & ENERSENSENTNUTrondheimNorway
  2. 2.Department of Biotechnology & CenTroN for Synthetic BiologyNTNUTrondheimNorway

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