Photosynthetica 2018, 56(1):105-124 | DOI: 10.1007/s11099-018-0791-y

Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K

J. J. Lamb1, G. Røkke2, M. F. Hohmann-Marriott2,*
1 Department of Electronic Systems & ENERSENSE, NTNU, Trondheim, Norway
2 Department of Biotechnology & CenTroN for Synthetic Biology, NTNU, Trondheim, Norway

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

Received: October 27, 2017; Accepted: January 10, 2018; Published: March 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Lamb, J.J., Røkke, G., & Hohmann-Marriott, M.F. (2018). Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. Photosynthetica, 56(SPECIAL ISSUE), 105-124. doi: 10.1007/s11099-018-0791-y
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    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. Go to original source...
    2. Allen J.F.: Protein phosphorylation in regulation of photosynthesis.-BBA-Bioenergetics 1098: 275-335, 1992. Go to original source...
    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. Go to original source...
    4. Ben-Shem A., Frolow F., Nelson N.: Crystal structure of plant photosystem I.-Nature 426: 630-635, 2003. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    8. Biggins J., Bruce D.: Regulation of excitation energy transfer in organisms containing phycobilins.-Photosynth. Res. 20: 1-34, 1989. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    16. Bonaventura C., Myers J.: Fluorescence and oxygen evolution from Chlorella pyrenoidosa.-BBA-Bioenergetics 189: 366-383, 1969. Go to original source...
    17. Brewster D.: On the colours of natural bodies.-Earth Env. Sci. T. R. So. 12: 538-545, 1834. Go to original source...
    18. Brody S.: New excited state of chlorophyll.-Science 128: 838-839, 1958. Go to original source...
    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. Go to original source...
    20. Busch A., Nield J., Hippler M.: The composition and structure of photosystem Iassociated antenna from Cyanidioschyzon merolae.-Plant J. 62: 886-897, 2010. Go to original source...
    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. Go to original source...
    22. Cardona T.: Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution?-Front. Plant Sci. 7: 257, 2016. Go to original source...
    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. Go to original source...
    24. Chen M., Blankenship R.E.: Expanding the solar spectrum used by photosynthesis.-Trends Plant Sci. 16: 427-431, 2011. Go to original source...
    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. Go to original source...
    26. Cho F., Spencer J.: Emission spectra of Chlorella at very low temperatures (-269° to -196°).-Biochim. Biophys. Acta 126: 174-176, 1966. Go to original source...
    27. Cho F.: Low-temperature (4-77° K) spectroscopy of Anacystis; temperature dependence of energy transfer efficiency.-BBABioenergetics 216: 151-161, 1970a. Go to original source...
    28. Cho F.: Low-temperature (4-77° K) spectroscopy of Chlorella; temperature dependence of energy transfer efficiency.-BBABioenergetics 216: 139-150, 1970b. Go to original source...
    29. Clayton R.K.: Photosynthesis: Physical Mechanisms and Chemical Patterns. Vol. 4. Pp. 19-35. Cambridge University Press, Cambridge 1980.
    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. Go to original source...
    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. Go to original source...
    32. Dau H.: Molecular mechanisms and quantitative models of variable photosystem II fluorescence.-Photochem Photobiol 60: 1-23, 1994a. Go to original source...
    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. Go to original source...
    34. de Marsac N.T.: Phycobiliproteins and phycobilisomes: the early observations.-Photosynth. Res. 76: 193-205, 2003. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    40. Eaton-Rye J.J., Sobotka R.: Assembly of the photosystem II membrane-protein complex of oxygenic photosynthesis.-Front. Plant Sci. 8: 884, 2017. Go to original source...
    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. Go to original source...
    42. Emerson R.: Dependence of yield of photosynthesis in long-wave red on wavelength and intensity of supplementary light.-Science 125: 746, 1957.
    43. Erickson E., Wakao S., Niyogi K.K.: Light stress and photoprotection in Chlamydomonas reinhardtii.-Plant J. 82: 449-465, 2015. Go to original source...
    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. Go to original source...
    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. Go to original source...
    46. Förster T.: Delocalizing Excitation and Excitation Transfer. Modern Quantum Chemistry Istanbul Lectures. Pp. 93-137. Academic Press, New York 1965.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    50. Gan F., Shen G., Bryant D.A.: Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria.-Life 5: 4-24, 2015. Go to original source...
    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. Go to original source...
    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. Go to original source...
    53. Goldschmidt-Clermont M., Bassi R.: Sharing light between two photosystems: mechanism of state transitions.-Curr. Opin. Plant. Biol. 25: 71-78, 2015. Go to original source...
    54. Gouterman M., Wagnière G.H., Snyder L.C.: Spectra of porphyrins: Part II. Four orbital model.-J. Mol. Spectrosc. 11: 108-127, 1963. Go to original source...
    55. Govindjee, Björn L.O.: Evolution of the Z-scheme of photosynthesis: a perspective.-Photosynth. Res. 133: 5-15, 2017. Go to original source...
    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. Go to original source...
    57. Govindjee, Yang L.: Structure of the red fluorescence band in chloroplasts.-J. Gen. Physiol. 49: 763-780, 1966. Go to original source...
    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.
    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. Go to original source...
    60. Govindjee: Sixty-three years since kautsky: chlorophyll a fluorescence.-Aust. J. Plant Physiol. 22: 131-160, 1995. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    65. Hillier W., Babcock G.T.: Photosynthetic reaction centers.-Plant Physiol. 125: 33-37, 2001. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    69. Hohmann-Marriott M.F., Blankenship R.E.: Evolution of photosynthesis.-Plant. Physiol. 154: 434-438, 2011. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    73. Iwai M., Takahashi Y., Minagawa J.: Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii.-Plant Cell 20: 2177-2189, 2008. Go to original source...
    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. Go to original source...
    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. Go to original source...
    76. Joshua S., Mullineaux C.W.: Phycobilisome diffusion is required for light-state transitions in cyanobacteria.-Plant Physiol. 135: 2112-2119, 2004. Go to original source...
    77. Juhas M., Büchel C.: Properties of photosystem I antenna protein complexes of the diatom Cyclotella meneghiniana.-J. Exp. Bot. 63: 3673-3681, 2012. Go to original source...
    78. Kaòa R., Kotabová E., Luke¹ M. et al.: Phycobilisome mobility and its role in the regulation of light harvesting in red algae.-Plant Physiol. 165: 1618-1631, 2014. Go to original source...
    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. Go to original source...
    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. Go to original source...
    81. Kautsky H., Hirsch A.: [New attempts for carbon dioxide assimilation.]-Naturwissenschaft 19: 964-964, 1931. [In German] Go to original source...
    82. Keeling P.J.: The number, speed, and impact of plastid endosymbioses in eukaryotic evolution.-Annu. Rev. Plant Biol. 64: 583-607, 2013. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    86. Krause G.H., Weis E.: Chlorophyll fluorescence as a tool in plant physiology.-Photosynth. Res. 5: 139-157, 1984. Go to original source...
    87. Krey A., Govindjee: Fluorescence studies on a red alga, Porphyridium cruentum.-Biochim. Biophys. Acta. 120: 1-18, 1966. Go to original source...
    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. Go to original source...
    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. Go to original source...
    90. Lakowicz J.R.: Fluorescence polarization.-In: Lakowicz J.R. (ed): Principles of Fluorescence Spectroscopy Pp. 111-153. Springer, Boston 1983a. Go to original source...
    91. Lakowicz J.R.: Quenching of fluorescence.-In: Lakowicz J.R. (ed): Principles of Fluorescence Spectroscopy. Pp. 257-301. Springer, Boston 1983b. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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, 20
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    100. Li Y., Chen M.: Novel chlorophylls and new directions in photosynthesis research.-Funct. Plant Biol. 42: 493-501, 2015. Go to original source...
    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.
    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, 20
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    106. Maxwell K., Johnson G.N.: Chlorophyll fluorescence-a practical guide.-J. Exp. Bot. 51: 659-668, 2000. Go to original source...
    107. Mazor Y., Borovikova A., Nelson N.: The structure of plant photosystem I super-complex at 2.8 Å resolution.-Elife 4: e07433, 2015. Go to original source...
    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. Go to original source...
    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, 19
    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. Go to original source...
    111. Minagawa J.: State transitions-the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast.-BBA-Bioenergetics 1807: 897-905, 2011. Go to original source...
    112. Miyashita H., Ikemoto H., Kurano N. et al.: Chlorophyll d as a major pigment.-Nature 383: 402, 1996. Go to original source...
    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. Go to original source...
    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.
    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]
    116. Mullet J., Burke J., Arntzen C.: A developmental study of photosystem I peripheral chlorophyll proteins.-Plant Physiol. 65: 823-827 1980a. Go to original source...
    117. Mullet J., Burke J., Arntzen C.: Chlorophyll proteins of photosystem I.-Plant Physiol. 65: 814-822, 1980b. Go to original source...
    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. Go to original source...
    119. Mullineaux C.W.: Electron transport and light-harvesting switches in cyanobacteria.-Front. Plant Sci. 5: 7, 2014. Go to original source...
    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. Go to original source...
    121. Mullineaux C.W.: Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium.-BBABioenergetics 1100: 285-292, 1992. Go to original source...
    122. Mullineaux C.W.: Phycobilisome-reaction centre interaction in cyanobacteria.-Photosynth. Res. 95: 175-182, 2008. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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, 19
    127. Murata N.: Control of excitation transfer in photosynthesis. IV. Kinetics of chlorophyll a fluorescence in Porphyra yezoensis.-BBA-Bioenergetics 205: 379-389, 1970. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    131. Nakatani H., Ke B., Dolan E., Arntzen C.: Identity of the photosystem II reaction center polypeptide.-BBABioenergetics 765: 347-352, 1984. Go to original source...
    132. Natali A., Croce R.: Characterization of the major lightharvesting complexes (LHCBM) of the green alga Chlamydomonas reinhardtii.-PLoS ONE 10: e0119211, 2015. Go to original source...
    133. Nickelsen J., Rengstl B.: Photosystem II assembly: from cyanobacteria to plants.-Annu. Rev. Plant Biol. 64: 609-635, 2013. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    143. Rabinowitch E., Govindjee: Photosynthesis. Pp. 273. John Wiley & Sons, Inc, New York 1969.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    148. ªener 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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    151. Sjöback R., Nygren J., Kubista M.: Absorption and fluorescence properties of fluorescein.-Spectrochim. Acta A 51: 7-21, 1995. Go to original source...
    152. Sobiechowska-Sasim M., Stoñ-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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    157. Takahashi S., Badger M.R.: Photoprotection in plants: a new light on photosystem II damage.-Trends Plant Sci. 16: 53-60, 2011. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    163. Walters R.G., Horton P.: Resolution of components of nonphotochemical chlorophyll fluorescence quenching in barley leaves.-Photosynth. Res. 27: 121-133, 1991. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    170. Young A.J., Frank H.A.: Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence.-J. Photoch. Photobio. B 36: 3-15, 1996. Go to original source...

    Return to the content