Evolution and function of light harvesting proteins

Journal of Plant Physiology

Volumn 172, Issue , 2015, Pages 62-75

  Büchel, Claudia ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Chlorophyll c; Chromalveolatae; Lhcx; Non photochemical quenching; Thylakoid structure

Indexed keywords

LIGHT HARVESTING SYSTEM;

GENE EXPRESSION REGULATION; GENETICS; LIGHT HARVESTING SYSTEM; METABOLISM; MOLECULAR EVOLUTION; PLANT;

EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; LIGHT-HARVESTING PROTEIN COMPLEXES; PLANTS;

EID: 84911374114     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2014.04.018     Document Type: Review

References (188)

1. Ahn T.K., Avenson T.J., Ballottari M., Cheng Y.-C., Niyogi K.K., Bassi R., et al. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 2008, 320:794-797.
2. Alberte R.S., Friedman A.L., Gustafson D.L., Rudnick M.S., Lyman H. Light-harvesting systems of brown algae and diatoms. Isolation and characterization of chlorophyll a/c and chlorophyll a/fucoxanthin pigment-protein complexes. Biochim Biophys Acta 1981, 635:304-316.
3. Alboresi A., Caffarri S., Nogue F., Bassi R., Morosinotto T. In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS One 2008, 3:e2033.
4. Archibald J.M., Keeling P.J. Recycled plastids: a 'green movement' in eukaryotic evolution. Trends Genet 2002, 18:577-584.
5. Armbrust E.V., Berges J.A., Bowler C., Green B.R., Martinez D., Putnam N.H., et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 2004, 306:79-86.
6. Aspinall-O'Dea M., Wentworth M., Pascal A., Robert B., Ruban A., Horton P. In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc Natl Acad Sci USA 2002, 99:16331-16335.
7. Bailleul B., Rogato A., de Martino A., Coesel S., Cardol P., Bowler C., et al. An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc Natl Acad Sci USA 2010, 107:18214-18219.
8. Ballottari M., Girardon J., Dall'Osto L., Bassi R. Evolution and functional properties of Photosystem II light harvesting complexes in eukaryotes. Biochim Biophys Acta 2012, 1817:143-157.
9. Barber J. Regulation of energy transfer by cations and protein phosphorylation in relation to thylakoid membrane organization. Photosynth Res 1986, 10:243-253.
10. Bassi R., Croce R., Cugini D., Sandona D. Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc Natl Acad Sci USA 1999, 96:10056-10061.
11. Bathke L., Rhiel E., Krumbein W.E., Marquardt J. Biochemical and Immunochemical Investigations on the light-harvesting system of the cryptophyte Rhodomonas sp.: evidence for a photosystem I specific antenna. Plant Biol 1999, 1:516-523.
12. Bautista J.A., Hiller R.G., Sharples F.P., Gosztola D., Wasielewski M., Frank H.A. Singlet and triplet energy transfer in the peridinin-chlorophyll a protein from Amphidinium carterae. J Phys Chem A 1999, 103:2267-2273.
13. Becker B., Hoef-Emden K., Melkonian M. Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol Biol 2008, 8:203.
14. Becker F., Rhiel E. Immuno-electron microscopic quantification of the fucoxanthin chlorophyll a/c binding polypeptides Fcp2, Fcp4, and Fcp6 of Cyclotella cryptica grown under low- and high-light intensities. Int Microbiol 2006, 9:29-36.
15. Beer A., Gundermann K., Beckmann J., Büchel C. Subunit composition and pigmentation of fucoxanthin-chlorophyll proteins in diatoms: evidence for a subunit involved in diadinoxanthin and diatoxanthin binding. Biochemistry 2006, 45:13046-13053.
16. Beer A., Juhas M., Büchel C. Influence of different light intensities and different iron nutrition on the photosynthetic apparatus in the diatom Cyclotella meneghiniana (Bacillariophyceae). J Phycol 2011, 47:1266-1273.
17. Ben-Shem A., Frolow F., Nelson N. Crystal structure of plant photosystem I. Nature 2003, 426:630-635.
18. Bergantino E., Segalla A., Brunetta A., Teardo E., Rigoni F., Giacometti G.M., et al. Light- and pH dependent structural changes in the psbS subunit of photosystem II. Proc Natl Acad Sci USA 2003, 100:15265-15270.
19. Berkaloff C., Caron L., Rousseau B. Subunit organization of PS I particles from brown algae and diatoms: polypeptide and pigment analysis. Photosynth Res 1990, 23:181-193.
20. Betterle N., Ballottari M., Zorzan S., de Bianchi S., Cazzaniga S., Dall'Osto L., et al. Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 2009, 284:15255-15266.
21. Bhaya D., Grossman A.R. Characterization of gene clusters encoding the fucoxanthin chlorophyll proteins of the diatom Phaeodactylum tricornutum. Nucleic Acids Res 1993, 21:4458-4466.
22. Bibby T.S., Nield J., Barber J. Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 2001, 412:743-745.
23. Boekema E.J., Hankamer B., Bald D., Kruip J., Boonstra A.F., Barber J., et al. Supramolecular structure of photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 1995, 92:175-179.
24. Boekema E.J., Hifney A., Yakushevska A.E., Piotrowlski M., Keegstra W., Berry S., et al. A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 2001, 412:745-748.
25. Bonente G., Ballottari M., Truong T.B., Morosinotto T., Ahn T.K., Fleming G.R., et al. Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 2011, 9:1000577.
26. Bonente G., Passarini F., Cazzaniga S., Mancone C., Buia M.C., Tripodi M., et al. The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 2008, 84:1359-1370.
27. Bowler C., Allen A.E., Badger J.H., Grimwood J., Jabbari K., Kuo A., et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456:239-244.
28. Brakemann T., Schlörmann W., Marquardt J., Nolte M., Rhiel E. Association of fucoxanthin chlorophyll a/c-binding polypeptides with photosystems and phosphorylation in the centric diatom Cyclotella cryptica. Protist 2006, 157:463-475.
29. Brown J.S. Photosynthetic pigment organization in diatoms (Bacillariophyceae). J Phycol 1988, 24:96-102.
30. Bruce D., Brimble S., Bryant D.A. State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 1989, 974:66-73.
31. Büchel C. Fucoxanthin-chlorophyll proteins in diatoms: 18 and 19kDa subunits assemble into different oligomeric states. Biochemistry 2003, 42:13027-13034.
32. Büchel C., Wilhelm C. Wavelength independent state transitions and light regulated chlororespiration as mechanisms to control the energy status in the chloroplast of Pleurochloris meiringensis. Plant Physiol Biochem 1990, 28:307-317.
33. Büchel C., Wilhelm C. Isolation and characterization of a photosystem I-associated antenna (LHC I) and a photosystem I-core complex from the chlorophyll c-containing alga Pleurochloris meiringensis (Xanthophyceae). J Photochem Photobiol B, Biol 1993, 20:87-93.
34. Büchel C., Wilhelm C., Hauswirth N., Wild A. Evidence for a lateral heterogeneity by patch-work like areas enriched in photosystem I complexes in the three thylakoid lamellae of Pleurochloris meiringensis (Xanthophyceae). Cryptogamic Bot 1992, 2:375-386.
35. Burki F., Shalchian-Tabrizi K., Minge M., Skjæveland Å., Nikolaev S.I., Jakobsen K.S., et al. Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2007, 2:790.
36. Busch A., Petersen J., Webber-Birungi M.T., Powikrowska M., Lassen L.M.M., Naumann-Busch B., et al. Composition and structure of photosystem I in the moss Physcomitrella patens. J Exp Bot 2013, 64:2689-2699.
37. Caffarri S., Kouřil R., Kereïche S., Boekema E.J., Croce R. Functional architecture of higher plant photosystem II supercomplexes. EMBO J 2009, 28:3052-3063.
38. Caron L., Brown J.S. Chlorophyll-carotenoid protein complexes from the diatom, Phaeodactylum tricornutum: spectrophotometric, pigment and polypeptide analyses. Plant Cell Physiol 1987, 28:775-785.
39. Cavalier-Smith T. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 1999, 46:347-366.
40. Cavalier-Smith T. Symbiogenesis: mechanisms, evolutionary consequences, and systematic implications. Annu Rev Ecol Evol Syst 2013, 44:145-172.
41. Cock J.M., Sterck L., Rouzé P., Scornet D., Allen A.E., Amoutzias G., et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 2010, 465:617-621.
42. Croce R., Morosinotto T., Castelletti S., Breton J., Bassi R. The Lhca antenna complexes of higher plants photosystem I. Biochim Biophys Acta 2002, 1556:29-40.
43. Croce R., van Amerongen H. Light-harvesting and structural organization of Photosystem II: from individual complexes to thylakoid membrane. J Photochem Photobiol B, Biol 2011, 104:142-153.
44. Curtis B.A., Tanifuji G., Burki F., Gruber A., Irimia M., Maruyama S., et al. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 2012, 492:59-65.
45. de Bianchi S., Dall'Osto L., Tognon G., Morosinotto T., Bassi R. Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 2008, 20:1012-1028.
46. de Martino A., Douady D., Quinet-Szely M., Rousseau B., Crepineau F., Apt K., et al. The light-harvesting antenna of brown algae. Highly homologous proteins encoded by a multigene family. Eur J Biochem 2000, 267:5540-5549.
47. Demming-Adams B, Garab G, Adams WW, Govindjee, editors. Non-photochemical fluorescence quenching and energy dissipation in plants, algae, and cyanobacteria, Vol 40, Dordrecht: Springer Verlag, in press.
48. Dekker J.P., Boekema E.J. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 2005, 1706:12-39.
49. Deschamps P., Moreira D. Reevaluating the green contribution to diatom genomes. Genome Biol Evol 2012, 4:795-800.
50. Dietzel L., Bräutigam K., Steiner S., Schüffler K., Lepetit B., Grimm B., et al. Photosystem II supercomplex remodeling serves as an entry mechanism for state transitions in Arabidopsis. Plant Cell 2011, 23:2964-2977.
51. Dittami S.M., Michel G., Collén J., Boyen C., Tonon T. Chlorophyll-binding proteins revisited-a multigenic family of light-harvesting and stress proteins from a brown algal perspective. BMC Evol Biol 2010, 10:365.
52. Dominici P.J., Caffarri S., Armeenante F., Ceoldo S., Crimi M., Bassi R. Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem 2002, 277:22750-22758.
53. Dong J., Tu W., Liu K., Sun R., Liu C., Wang K., et al. The PsbS protein plays important roles in photosystem II supercomplex remodeling under elevated light conditions. J Plant Physiol 2015, 172:pp-pp.
54. Drop B., Webber-Birungi M., Fusetti F., Kouril R., Redding K.E., Boekema E.J., et al. Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 2011, 286:44878-44887.
55. Durchan M., Tichý J., Litvín R., Šlouf V., Gardian Z., Hříbek P., et al. Role of carotenoids in light-harvesting processes in an antenna protein from the chromophyte Xanthonema debile. J Phys Chem B 2012, 116:8880-8889.
56. Elrad D., Grossman A.R. A genome's-eye view of the light-harvesting polypeptides of Chlamydomonas reinhardtii. Curr Gen 2004, 45:61-75.
57. Engelken J., Brinkmann H., Adamska I. Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol Biol 2010, 10:233.
58. Eppard M., Krumbein W.E., von Haesler A., Rhiel E. Characterization of fcp4 and fcp12, two additional genes encoding light harvesting proteins of Cyclotella cryptica (Bacillariophyceae) and phylogenetic analysis of this complex gene family. Plant Biol 2000, 2:283-289.
59. Eppard M., Rhiel E. The genes encoding light-harvesting subunits of Cyclotella cryptica (Bacillariophyceae) constitute a complex and heterogeneous family. Mol Gen Genet 1998, 260:335-345.
60. Eppard M., Rhiel E. Investigation on gene copy number, introns and chromosomal arrangements of genes encoding the fucoxanthin chlorophyll a/c-binding proteins of the centric diatom Cyclotella cryptica. Protist 2000, 151:27-39.
61. Fawley M.W., Grossman A.R. Polypeptides of a light-harvesting complex of the diatom Phaeodactylum tricornutum are synthesized in the cytoplasm of the cell as precursors. Plant Physiol 1986, 81:149-155.
62. Fork D.C., Herbert S.K., Malkin S. Light energy distribution in the brown alga Macrocystis pyrifera (giant kelp). Plant Physiol 1991, 95:731-739.
63. Friedman A.L., Alberte R.S. A diatom light-harvesting pigment-protein complex. Plant Physiol 1984, 76:483-489.
64. Friedman A.L., Alberte R.S. Biogenesis and light regulation of the major light harvesting chlorophyll-protein of diatoms. Plant Physiol 1986, 80:43-51.
65. Frommolt R., Werner S., Paulsen H., Goss R., Wilhelm C., Zauner S., et al. Ancient recruitment by chromists of green algal genes encoding enzymes for carotenoid biosynthesis. Mol Biol Evol 2008, 25:2653-2667.
66. Funk C., Adamska I., Green B.R., Andersson B., Renger G. The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments. J Biol Chem 1995, 270:30141-30147.
67. Galka P., Santabarbara S., Khuong T.T.H., Degand H., Morsomme P., Jennings R.C., 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 2012, 24:2963-2978.
68. Gardian Z., Tichý J., Vácha F. Structure of PSI, PSII and antennae complexes from yellow-green alga Xanthonema debile. Photosynth Res 2011, 108:25-32.
69. Garrido J.L., Zapata M. Detection of new pigments from Emiliania huxleyi (Prymnesiophyceae) by high-performance liquid chromatiography, liquid chromatography-mass spectrometry, visible spectroscopy, and fast atom bombardment mass spectrometry. J Phycol 1998, 34:70-78.
70. Georgakopoulou S., van der Zwan G., Bassi R., van Grondelle R., van Amerongen H., Croce R. Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry 2007, 46:4745-4754.
71. Gildenhoff N., Amarie S., Gundermann K., Beer A., Büchel C., Wachtveitl J. Oligomerization and pigmentation dependent excitation energy transfer in fucoxanthin-chlorophyll proteins. Biochim Biophys Acta 2010, 1797:543-549.
72. Goss R., Pinto E.A., Wilhelm C., Richter M. The importance of a highly active and δ-pH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 2006, 163:1008-1021.
73. Goss R., Lepetit B. Biodiversity of NPQ. J Plant Physiolol 2015, 172:pp-pp.
74. Grabowski B., Cunningham F.X., Gantt E. Chlorophyll and carotenoid binding in a simple red algal light-harvesting complex crosses phylogenetic lines. Proc Natl Acad Sci USA 2001, 98:2911-2916.
75. Green B.R. After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynth Res 2011, 107:103-115.
76. Green B.R., Pichersky E. Hypothesis for the evolution of three-helix Chl a/b and Chl a/c light-harvesting antenna proteins from two-helix and four-helix ancestors. Photosynth Res 1994, 39:149-162.
77. Grouneva I., Jakob T., Wilhelm C., Goss R. A new multicomponent NPQ mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol 2008, 49:1217-1225.
78. Grouneva I., Rokka A., Aro E. The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J Proteome Res 2011, 10:5338-5353.
79. Guglielmi G., Lavaud J., Rousseau B., Etienne A., Houmard J., Ruban A.V. The light-harvesting antenna of the diatom Phaeodactylum tricornutum. Evidence for a diadinoxanthin-binding subcomplex. FEBS J 2005, 272:4339-4348.
80. Gugliemelli A. Isolation and characterization of pigment-protein particles from the light-harvesting complex of Phaeodactylum tricornutum. Biochim Biophys Acta 1984, 766:45-50.
81. Gundermann K., Büchel C. The fluorescence yield of the trimeric fucoxanthin-chlorophyll-protein FCPa in the diatom Cyclotella meneghiniana is dependent on the amount of bound diatoxanthin. Photosynth Res 2008, 95:229-235.
82. Gundermann K., Büchel C. Factors determining the fluorescence yield of fucoxanthin-chlorophyll complexes (FCP) involved in non-photochemical quenching in diatoms. Biochim Biophys Acta 2012, 1817:1044-1052.
83. Gundermann K., Schmidt M., Weisheit W., Mittag M., Büchel C. Identification of several sub-populations in the pool of light harvesting proteins in the pennate diatom Phaeodactylum tricornutum. Biochim Biophys Acta 2013, 1827:303-310.
84. Hegazi M.M., Pérez-Ruzafa A., Almela L., Candela M. Separation and identification of chlorophylls and carotenoids from Caulerpa prolifera, Jania rubens and Padina pavonica by reversed-phase high-performance liquid chromatography. J Chromatogr A 1998, 829:153-159.
85. Hiller R.G., Scaramuzzi C.D., Breton J. The organisation of photosynthetic pigments in a cryptophyte alga: a linear dichroism study. Biochim Biophys Acta 1992, 1102:360-364.
86. Hiller R.G., Wrench P.M., Gooley A.P., Shoebridge G., Breton J. The major intrinsic light-harvesting protein of Amphidinium: characterization and relation to other light-harvesting proteins. Photochem Photobiol 1993, 57:125-131.
87. Hobe S., Fey H., Rogl H., Paulsen H. Determination of relative chlorophyll binding affinities in the major light-harvesting chlorophyll a/b complex. J Biol Chem 2003, 278:5912-5919.
88. Hoffman G.E., Sanchez Puerta M.V., Delwiche C.F. Evolution of light-harvesting complex proteins from Chl c-containing algae. BMC Evol Biol 2011, 11:101.
89. Holt N.E., Zigmantas D., Valkunas L., Li X., Niyogi K.K., Fleming G.R. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 2005, 307:433-436.
90. Holzwarth A.R., Miloslavina Y., Nilkens M., Jahns P. Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 2009, 483:262-267.
91. Ikeda Y., Yamagishi A., Komura M., Suzuki T., Dohmae N., Shibata Y., et al. Two types of fucoxanthin-chlorophyll-binding proteins I tightly bound to the photosystem I core complex in marine centric diatoms. Biochim Biophys Acta 2013, 1827:529-539.
92. 2 light-harvesting protein from a Chroomonas species (Cryptophyceae). Biochim Biophys Acta 1983, 722:310-319.
93. Iwai M., Xokono M., Inada N., Minagawa J. Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc Natl Acad Sci USA 2010, 107:2337-2342.
94. Jahns P., Holzwarth A.R. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 2012, 1817:182-193.
95. Janssen M., Bathke L., Marquardt J., Krumbein W.E., Rhiel E. Changes in the photosynthetic apparatus of diatoms in response to low and high light intensities. Int Microbiol 2001, 4:27-33.
96. Jansson S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Biochem Sci 1999, 4:236-249.
97. Joshi-Deo J., Schmidt M., Gruber A., Weisheit W., Mittag M., Kroth P.G., et al. Characterization of a trimeric light-harvesting complex in the diatom Phaeodactylum tricornutum built of FcpA and FcpE proteins. J Exp Bot 2010, 61:3079-3087.
98. Juhas M., Büchel C. Properties of photosystem I antenna protein complexes of the diatom Cyclotella meneghiniana. J Exp Bot 2012, 63:3673-3681.
99. Kaňa R., Kotabová E., Sobotka R., Prášil O. Non-photochemical quenching in cryptophyte alga Rhodomonas salina is located in chlorophyll a/c antennae. PLoS One 2012, 7:e29700.
100. Katoh H., Mimuro M., Takaichi S. Light-harvesting particles isolated from a brown alga, Dictyota dichotoma. A supramolecular assembly of fucoxanthin-chlorophyll-protein complexes. Biochim Biophys Acta 1989, 976:233-240.
101. Keeling P.J. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 2013, 64:583-607.
102. Kereïche S., Kiss A.Z., Kouřil R., Boekema E.J., Horton P. The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 2010, 584:759-764.
103. Kereïche S., Kouřil R., Oostergetel G.T., Fusetti F., Boekema E.J., Doust A.B., et al. Association of chlorophyll a/c2 complexes to photosystem I and photosystem II in the cryptophyte Rhodomonas CS24. Biochim Biophys Acta 2008, 1777:1122-1128.
104. Kirchhoff H., Borinski M., Lenhert S., Chi L., Büchel C. Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 2004, 43:14508-14516.
105. Kiss A.Z., Ruban A.V., Horton P. The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 2008, 283:3972-3978.
106. Kouřil R., Zygadlo A., Arteni A.A., de Wit C.D., Dekker J.P., Jensen P.E., et al. Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 2005, 44:10935-10940.
107. Koziol A.G., Borza T., Ishida K., Keeling P., Lee R.W., Durnford D.G. Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 2007, 143:1802-1816.
108. Krauss N., Hinrichs W., Witt I., Fromme P., Pritzkow W., Dauter Z., et al. Three-dimensional structure of system I of photosynthesis at 6Å resolution. Nature 1993, 361:326-331.
109. Krueger B., Lampoura S.S., van Stokkum I.H.M., Papagiannakis E., Salverda J.M., Gradinaru C.C., et al. Energy transfer in the peridinin chlorophyll a protein of Amphidinium carterae studied by polarized transient absorption and target analysis. Biophys J 2001, 80:2843-2855.
110. Krüger T.P.J., Ilioaia C., Valkunas L., van Grondelle R. Fluorescence intermittency from the main plant light-harvesting complex: sensitivity to the local environment. J Phys Chem B 2011, 115:5083-5095.
111. Krüger T.P.J., Ilioaia C., van Grondelle R. Fluorescence intermittency from the main plant light-harvesting complex: resolving shifts between intensity levels. J Phys Chem B 2011, 115:5071-5082.
112. Krüger T.P.J., Novoderezhkin V.I., Ilioaia C., van Grondelle R. Fluorescence spectral dynamics of single LHCII trimers. Biophys J 2010, 98:3093-3101.
113. Krüger T.P.J., Wientjes E., Croce R., van Grondelle R. Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc Natl Acad Sci USA 2011, 108:13516-13521.
114. Kühlbrandt W., Wang D.N., Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 1994, 367:614-621.
115. Lavaud J., Lepetit B. An explanation for the inter-species variability of the photoprotective non-photochemical chlorophyll fluorescence quenching in diatoms. Biochim Biophys Acta 2013, 1827:294-302.
116. Lavaud J., Rousseau B., Etienne A. Enrichment of the light-harvesting complex in diadinoxanthin and implications for the nonphotochemical fluorescence quenching in diatoms. Biochemistry 2003, 42:5802-5808.
117. Lavaud J., Rousseau B., van Gorkom H.J., Etienne A. Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 2002, 129:1398-1406.
118. Lepetit B., Goss R., Jakob T., Wilhelm C. Molecular dynamics of the diatom thylakoid membrane under different light conditions. Photosynth Res 2012, 111:245-257.
119. Lepetit B., Volke D., Gilbert M., Wilhelm C., Goss R. Evidence for the existence of one antenna-associated lipid-dissolved and two protein-bound pools of diadinoxanthin cycle pigments in diatoms. Plant Physiol 2010, 154:1905-1920.
120. Lepetit B., Volke D., Szabó M., Hoffmann R., Garab G., Wilhelm C., et al. Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum. Biochemistry 2007, 46:9813-9822.
121. Li X., Björkman O., Shih C., Grossman A.R., Rosenquist M., Jansson S., et al. A pigment-binding protein essential for regulation of photosynthetic light-harvesting. Nature 2000, 403:391-395.
122. Li X., Gilmore A.M., Caffarri S., Bassi R., Golan T., Kramer D., et al. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 2004, 279:22866-22874.
123. Lichtlé C., Duval J.C., Lemoine Y. Comparative biochemical, functional and ultrastructural studies of photosystem particles from a Cryptophycea: Cryptomonas rufescens; isolation of an active phycoerythrin particle. Biochim Biophys Acta 1987, 894:76-90.
124. Lichtlé C., Jupin H., Duval J.C. Energy transfers from photosystem II to photosystem I in Cryptomonas rufescens (Cryptophyceae). Biochim Biophys Acta 1980, 591:104-112.
125. Linden P.A., Zimmermann J., Brixner T., Holt N.E., Vaswani H.M., Hiller R.G., et al. Transient absorption study of peridinin and peridinin-chlorophyll a-protein after two-photon excitation. J Phys Chem B 2004, 108:10340-10345.
126. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., et al. Crystal structure of spinach major light-harvesting complex at 2.72Å resolution. Nature 2004, 428:287-292.
127. Manodori A., Melis A. Cyanobacterial acclimation to photosystem I or photosystem II light. Plant Physiol 1986, 82:185-189.
128. Matsubara S., Morosinotto T., Osmond C.B., Bassi R. Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes. Plant Physiol 2007, 144:926-941.
129. Miloslavina Y., Grouneva I., Lambrev P.H., Lepetit B., Goss R., Wilhelm C., et al. Ultrafast fluorescence study on the location and mechanism of non-photochemical quenching in diatoms. Biochim Biophys Acta 2009, 1787:1189-1197.
130. Mimuro M., Katoh T., Kawai H. Spatial arrangement of pigments and their interaction in the fucoxanthin/chlorophyll a/c protein assembly (FCPA) isolated from the brown alga Dictyota dichotoma. Analysis by means of polarized spectroscopy. Biochim Biophys Acta 1990, 1015:450-456.
131. Moustafa A., Beszteri B., Maier U.G., Bowler C., Valentin K., Bhattacharya D. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 2009, 324:1724-1726.
132. Mozzo M., Mantelli M., Passarini F., Caffarri S., Croce R., Bassi R. Functional analysis of photosystem I light-harvesting complexes (Lhca) gene products of Chlamydomonas reinhardtii. Biochim Biophys Acta 2010, 1797:212-221.
133. 6-f complex and regulation of PS I formation. Plant Cell Physiol 1993, 34:1175-1180.
134. Nagao R., Ishii A., Tada O., Suzuki T., Dohmae N., Okumura A., et al. Isolation and characterization of oxygen-evolving thylakoid membranes and photosystem II particles from a marine diatom Chaetoceros gracilis. Biochim Biophys Acta 2007, 1767:1353-1362.
135. Nagao R., Takahashi S., Suzuki T., Dohmae N., Nakazato K., Tomo T. Comparison of oligomeric states and polypeptide compositions of fucoxanthin chlorophyll a/c-binding protein complexes among various diatom species. Photosynth Res 2013, 117:281-288.
136. Nagao R., Tomo T., Noguchi E., Nakajima S., Suzuki T., Okumura A., et al. Purification and characterization of a stable oxygen-evolving photosystem II complex from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 2010, 1797:160-166.
137. Nagao R., Tomo T., Noguchi E., Suzuki T., Okumura A., Narikawa R., et al. Proteases are associated with a minor fucoxanthin chlorophyll a/c-binding protein from the diatom, Chaetoceros gracilis. Biochim Biophys Acta 2012, 1817:2110-2117.
138. Neilson J.A.D., Durnford D.G. Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 2010, 106:57-71.
139. Novoderezhkin V.I., Palacios M.A., van Amerongen H., van Grondelle R. Energy-transfer dynamics in the LHCII complex of higher plants: modified redfield approach. J Phys Chem B 2004, 108:10363-10375.
140. Nowack E.C., Melkonian M., Glockner G. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 2008, 18:410-418.
141. Nymark M., Valle K.C., Brembu T., Hancke K., Winge P.W., Andresen K., et al. An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PLoS One 2009, 4:e7743.
142. Nymark M., Valle K.C., Hancke K., Winge P., Andresen K., Johnsen G., et al. Molecular and photosynthetic responses to prolonged darkness and subsequent acclimation to re-illumination in the diatom Phaeodactylum tricornutum. PLoS One 2013, 8:e58722.
143. Oeltjen A., Krumbein W.E., Rhiel E. Investigations on transcript sizes, steady state mRNA concentrations and diurnal expression of genes encoding fucoxanthin chlorophyll a/c light harvesting polypeptides in the centric diatom Cyclotella cryptica. Plant Biol 2002, 4:250-257.
144. Oeltjen A., Marquardt J., Rhiel E. Differential circadian expression of genes fcp2 and fcp6 in Cyclotella cryptica. Int Microbiol 2004, 7:127-131.
145. Olive J., Ajlani G., Astier C., Reconvreur M., Vernotte C. Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis PCC 6803. Biochim Biophys Acta, Bioenerg 1997, 1319:275-282.
146. Owens T.G. Light-harvesting function in the diatom Phaeodactylum tricornutum-II. Distribution of excitation energy between the photosystems. Plant Physiol 1986, 80:739-746.
147. Owens T.G., Wold E.R. Light-harvesting function in the diatom Phaeodactylum tricornutum-I. Isolation and characterization of pigment-protein complexes. Plant Physiol 1986, 80:732-738.
148. Pan X., Li M., Wan T., Wang L., Jia C., Hou Z., et al. Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat Struct Mol Biol 2011, 18:309-315.
149. Papagiannakis E., Larsen D.S., van Stokkum I.H.M., Vengris M., Hiller R.G., van Grondelle R. Resolving the excited-state equilibrium of peridinin in solution. Biochemistry 2004, 43:15303-15309.
150. Papagiannakis E., van Stokkum I.H.M., Fey H., Büchel C. Spectroscopic characterization of the excitation energy transfer in the fucoxanthin-chlorophyll protein of diatoms. Photosynth Res 2005, 86:241-250.
151. Pascal A.A., Caron L., Rousseau B., Lapouge K., Duval J.C., Robert B. Resonance Raman spectroscopy of a light-harvesting protein from the brown alga Laminaria saccharina. Biochemistry 1998, 37:2450-2457.
152. Pascal A.A., Liu Z., Broess K., van Oort B., van Amerongen H., Wang C., et al. Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 2005, 436:134-137.
153. Peers G., Truong T.B., Ostendorf E., Busch A., Elrad D., Grossman A.R., et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 2009, 462:518-521.
154. Pichersky E., Jansson S. The light-harvesting chlorophyll a/b-binding polypeptides and their genes in angiosperm and hymnosperm species. Oxygenic photosynthesis: the light reactions 1996, 507-521. Kluwer Academic Publishers, Dordrecht/Boston/London. D.R. Ort, C.F. Yocum (Eds.).
155. Polívka T., van Stokkum I.H.M., Zigmantas D., van Grondelle R., Sundström V., Hiller R.G. Energy transfer in the major intrinsic light-harvesting complex from Amphidinium carterae. Biochemistry 2006, 45:8516-8526.
156. 2 proteins from resonance Raman spectroscopy. J Phys Chem B 2009, 113:12565-12574.
157. Premvardhan L., Réfrégiers M., Büchel C. Pigment organization effects on energy transfer and Chl a emission imaged in the diatoms C. meneghiniana and P. tricornutum in vivo: a confocal laser scanning Fluorescence (CLSF) Microscopy and Spectroscopy Study. J Phys Chem B 2013, 117:11272-11281.
158. 2 proteins (FCP) based on resonance Raman spectroscopy and sequence analysis. Biochim Biophys Acta 2010, 1797:1647-1656.
159. 2 protein (FCP) based on Stark spectroscopy and molecular orbital theory. J Phys Chem B 2008, 112:11838-11853.
160. Price D.C., Chan C.X., Yoon H.S., Yang E.C., Qiu H., Weber A.P.M., et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 2012, 335:843-847.
161. Pyszniak A.M., Gibbs S.P. Immunocytochemical localization of photosystem I and the fucoxanthin-chlorophyll a/c light-harvesting complex in the diatom Phaeodactylum tricornutum. Protoplasma 1992, 166:208-217.
162. Rhiel E., Mörschel E., Wehrmeyer W. Characterization and structural analysis of a chlorophyll a/c light-harvesting complex and of photosystem I particles isolated from thylakoid membranes of Cryptomonas maculata (Cryptophyceae). Eur J Cell Biol 1987, 43:82-92.
163. Richard C., Ouellet H., Guertin M. Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii. Plant Mol Biol 2000, 42:303-316.
164. Romero E., Mozzo M., van Stokkum I.H.M., Dekker J.P., van Grondelle R., Croce R. The origin of the low-energy form of photosystem I light-harvesting complex Lhca4: mixing of the lowest exciton with a charge-transfer state. Biophys J 2009, 96:L35.
165. Ruban A.V., Berera R., Ilioaia C., van Stokkum I.H.M., Kennis J.T.M., Pascal A.A., et al. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 2007, 450:575-579.
166. Ruban A.V., Johnson M.P., Duffy C.D.P. The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 2012, 1817:167-181.
167. Ruban A.V., Lavaud J., Rousseau B., Guglielmi G., Horton P., Etienne A. The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 2004, 82:165-175.
168. Quaas T., Berteotti S., Ballottari M., Flieger K., Bassi R., Wilhelm C., et al. Non-photochemical quenching and xanthophyll cycle activities in six green algal species suggest mechanistic differences in the process of excess energy dissipation. J. Plant Physiol 2015, 172:pp-pp.
169. 2 to chlorophyll a in fucoxanthin-chlorophyll protein complex. J Phys Chem Lett 2013, 4:3590-3595.
170. Standfuss J., van Scheltinga A.C.T., Lamborghini M., Kühlbrandt W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5Å resolution. EMBO J 2005, 24:919-928.
171. Storf S., Jansson S., Schmid V.H.R. Pigment binding, fluorescence properties, and oligomerization behavior of Lhca5, a novel light-harvesting protein. J Biol Chem 2005, 280:5163-5168.
172. Szabó M., Lepetit B., Goss R., Wilhelm C., Mustárdy L., Garab G. Structurally flexible macro-organization of the pigment-protein complexes of the diatom Phaeodactylum tricornutum. Photosynth Res 2008, 95:237-245.
173. Szabó M., Premvardhan L., Lepetit B., Goss R., Wilhelm C., Garab G. Functional heterogeneity of the fucoxanthins and fucoxanthin-chlorophyll proteins in diatom cells revealed by their electrochromic response and fluorescence and linear dichroism spectra. Chem Phys 2010, 373:110-114.
174. Szabò I., Bergantino E., Giacometti G.M. Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO Rep 2005, 6:629-634.
175. van der Weij-de Wit C.D., Doust A.B., van Stokkum I.H.M., Dekker J.P., Wilk K.E., Curmi P.M.G., et al. How energy funnels from the phycoerythrin antenna complex to photosystem I and photosystem II in cryptophyte Rhodomonas CS24 cells. J Phys Chem B 2006, 110:25066-25073.
176. Vaswani H.M., Hsu C., Head-Gordon M.P., Fleming G.R., Vaswani H.M., Hsu C., et al. Quantum chemical evidence for an intramolecular charge-transfer state in the carotenoid peridinin of peridinin-chlorophyll-protein. J Phys Chem B 2003, 107:7940-7946.
177. Veith T., Brauns J., Weisheit W., Mittag M., Büchel C. Identification of a specific fucoxanthin-chlorophyll protein in the light harvesting complex of photosystem I in the diatom Cyclotella meneghiniana. Biochim Biophys Acta 2009, 1787:905-912.
178. Veith T., Büchel C. The monomeric photosystem I-complex of the diatom Phaeodactylum tricornutum binds specific fucoxanthin chlorophyll proteins (FCPs) as light-harvesting complexes. Biochim Biophys Acta 2007, 1767:1428-1435.
179. Wahadoszamen M., Berera R., Ara A.M., Romero E., van Grondelle R. Identification of two emitting sites in the dissipative state of the major light harvesting antenna. Phys Chem Chem Phys 2012, 14:759-766.
180. Wahadoszamen M., Ghazaryan A., Cingil H.E., Ara A.M., Büchel C., van Grondelle R., et al. Stark fluorescence spectroscopy reveals two emitting sites in the dissipative state of FCP antennas. Biochim Biophys Acta 2013, 1837:193-200.
181. Wedel N., Klein R., Ljungberg U., Andersson B., Herrmann R.G. The single-copy gene psbS codes for a phylogenetically intriguing 22kDa polypeptide of photosystem II. FEBS Lett 1992, 314:61-66.
182. Wientjes E., Oostergetel G.T., Jansson S., Boekema E.J., Croce R. The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J Biol Chem 2009, 284:7803-7810.
183. Wilk L., Grunwald M., Liao P., Walla P.J., Kuhlbrandt W. Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching. Proc Natl Acad Sci USA 2013, 110:5452-5456.
184. Wilson A., Punginelli C., Gall A., Bonetti C., Alexandre M., Routaboul J., et al. A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci USA 2008, 105:12075-12080.
185. Wolfe G.R., Cunningham F.X., Durnford D., Green B.R., Gantt E. Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 1994, 367:566-568.
186. Zhu S., Green B.R. Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 2010, 1797:1449-1457.
187. Zigmantas D., Hiller R.G., Sundström V., Polívka T. Carotenoid to chlorophyll energy transfer in the peridininchlorophyll-a-protein complex involves an intramolecular charge transfer state. Proc Natl Acad Sci USA 2002, 99:16760-16765.
188. Zigmantas D., Hiller R.G., Yartsev A., Sundström V., Polívka T. Dynamics of excited states of the carotenoid peridinin in polar solvents: dependence on excitation wavelength, viscosity, and temperature. J Phys Chem B 2003, 107:5339-5348.