Analysis of LHcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii

PLoS Biology

Volumn 9, Issue 1, 2011, Pages

  Bonente, Giulia ^a   Ballottari, Matteo ^a   Truong, Thuy B ^b,c   Morosinotto, Tomas ^d   Ahn, Tae K ^c,e,f   Fleming, Graham R ^c,e   Niyogi, Krishna K ^b,c   Bassi, Roberto ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Sungkyunkwan University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DICYCLOHEXYLCARBODIIMIDE; GENE PRODUCT; PROTEIN LHCSR3; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; XANTHOPHYLL; XANTHOPHYLL BINDING PROTEIN; ZEAXANTHIN; ALGAL PROTEIN; CHLOROPHYLL; ISOPROTEIN; LI818R 1 PROTEIN, CHLAMYDOMONAS REINHARDTII; LI818R-1 PROTEIN, CHLAMYDOMONAS REINHARDTII; NEOXANTHIN; VIOLAXANTHIN;

ARTICLE; CELL GROWTH; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; FLUORESCENCE; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; PH; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; ABSORPTION; AMINO ACID SEQUENCE; FEEDBACK SYSTEM; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; MOLECULAR GENETICS; PROTEIN REFOLDING; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; THERMODYNAMICS; THYLAKOID;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; EMBRYOPHYTA;

ABSORPTION; ALGAL PROTEINS; AMINO ACID SEQUENCE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL; FEEDBACK, PHYSIOLOGICAL; FLUORESCENCE; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; LUTEIN; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN REFOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; THERMODYNAMICS; THYLAKOIDS; XANTHOPHYLLS;

EID: 79851485918     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000577     Document Type: Article

References (102)

1. Neilson J. A. D, Durnford D. G (2010) Evolutionary distribution of light-harvesting complex-like proteins in photosynthetic eukaryotes. Genome 53: 68-78.
2. Schmid V. H. R, Cammarata K. V, Bruns B. U, Schmidt G. W (1997) In vitro reconstitution of the photosystem I light-harvesting complex LHCI-730: heterodimerization is required for antenna pigment organization. Proc Natl Acad Sci U S A 94: 7667-7672.
3. Dall'Osto L, Cazzaniga S, North H, Marion-Poll A, Bassi R (2007) The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell 19: 1048-1064.
4. Dall'Osto L, Lico C, Alric J, Giuliano G, Havaux M, et al. (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6: 32-75.
5. Mozzo M, Dall'Osto L, Hienerwadel R, Bassi R, Croce R (2008) Photoprotection in the antenna complexes of photosystem II: role of individual xanthophylls in chlorophyll triplet quenching. J Biol Chem 283: 6184-6192.
6. Ahn T. K, Avenson T. J, Ballottari M, Cheng Y. C, Niyogi K. K, et al. (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320: 794-797.
7. Koyama Y (1991) Structures and functions of carotenoids in photosynthetic systems. J Photochem Photobiol B 9: 265-280.
8. Schodel R, Irrgang K. D, Voigt J, Renger G (1999) Quenching of chlorophyll fluorescence by triplets in solubilized light-harvesting complex II (LHCII). Biophys J 76: 2238-2248.
9. Koyama Y, Kubo K, Komori M, Yasuda H, Mukai Y (1991) Effect of protonation on the isomerization properties of n-butylamine Schiff base of isomeric retinal as revealed by direct HPLC analyses: selection of isomerization pathways by retinal proteins. Photochem Photobiol 54: 433-443.
10. Niyogi K. K, Grossman A. R, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134.
11. Pogson B. J, Niyogi K. K, Bjorkman O, DellaPenna D (1998) Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc Natl Acad Sci U S A 95: 13324-13329.
12. Ballottari M, Dall'Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282: 8947-8958.
13. Klimmek F, Sjodin A, Noutsos C, Leister D, Jansson S (2006) Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol 140: 793-804.
14. Richard C, Ouellet H, Guertin M (2000) Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii. Plant Mol Biol 42: 303-316.
15. Adamska I (1997) ELIPs-light-induced stress proteins. Physiol Plant 100: 794-805.
16. Tzvetkova-Chevolleau T, Franck F, Alawady A. E, Dall'Osto L, Carriere F, et al. (2007) The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant J 50: 795-809.
17. Li X. P, Bjorkman O, Shih C, Grossman A. R, Rosenquist M, et al. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395.
18. Li X. P, Gilmore A. M, Caffarri S, Bassi R, Golan T, et al. (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279: 22866-22874.
19. Bonente G, Howes B. D, Caffarri S, Smulevich G, Bassi R (2008) Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J Biol Chem 283: 8434-8445.
20. Koziol A. G, Borza T, Ishida K, Keeling P, Lee R. W, et al. (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143: 1802-1816.
21. Alboresi A, Gerotto C, Giacometti G. M, Bassi R, Morosinotto T (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci U S A 107: 11128-11133.
22. Peers G, Truong T. B, Ostendorf E, Busch A, Elrad D, et al. (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462: 518-521.
23. Li X. P, Phippard A, Pasari J, Niyogi K. K (2002) Structure-function analysis of photosystem II subunit S (PsbS) in vivo. Funct Plant Biol 29: 1131-1139.
24. Crofts A. R, Yerkes C. T (1994) A molecular mechanism for Q(E)-quenching. FEBS Lett 352: 265-270.
25. Dominici P, Caffarri S, Armenante F, Ceoldo S, Crimi M, et al. (2002) Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem 277: 22750-22758.
26. Niyogi K. K, Shih C, Chow W. S, Pogson B. J, DellaPenna D, et al. (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res 67: 139-145.
27. Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, et al. (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284: 15255-15266.
28. de Bianchi S, Dall'Osto L, Tognon G, Morosinotto T, Bassi R (2008) 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 20: 1012-1028.
29. Johnson M. P, Perez-Bueno M. L, Zia A, Horton P, Ruban A. V (2009) The zeaxanthin-independent and zeaxanthin-dependent qE components of nonphotochemical quenching involve common conformational changes within the photosystem II antenna in Arabidopsis. Plant Physiol 149: 1061-1075.
30. Kovacs L, Damkjaer J, Kereiche S, Ilioaia C, Ruban A. V, et al. (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18: 3106-3120.
31. Avenson T. J, Ahn T. K, Zigmantas D, Niyogi K. K, Li Z, et al. (2008) Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 283: 3550-3558.
32. Li Z, Ahn T. K, Avenson T. J, Ballottari M, Cruz J. A, et al. (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21: 1798-1812.
33. Bassi R, Croce R, Cugini D, Sandona D (1999) Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc Natl Acad Sci U S A 96: 10056-10061.
34. Giuffra E, Cugini D, Croce R, Bassi R (1996) Reconstitution and pigment-binding properties of recombinant CP29. Eur J Biochem 238: 112-120.
35. Remelli R, Varotto C, Sandona D, Croce R, Bassi R (1999) Chlorophyll binding to monomeric light-harvesting complex-a mutation analysis of chromophore-binding residues. J Biol Chem 274: 33510-33521.
36. Merchant S. S, Prochnik S. E, Vallon O, Harris E. H, Karpowicz S. J, et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
37. Bergantino E, Dainese P, Cerovic Z, Sechi S, Bassi R (1995) A posttranslational modification of the photosystem-II subunit Cp29 protects maize from cold stress. J Biol Chem 270: 8474-8481.
38. Bellafiore S, Bameche F, Peltier G, Rochaix J. D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892-895.
39. Depege N, Bellafiore S, Rochaix J. D (2003) Rote of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299: 1572-1575.
40. Tanaka A, Ito H, Tanaka R, Tanaka N. K, Yoshida K, et al. (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci U S A 95: 12719-12723.
41. White A. L, Melis A (2006) Biochemistry of hydrogen metabolism in Chlamydomonas reinhardtii wild type and a Rubisco-less mutant. Int J Hydrogen Energy 31: 455-464.
42. Morosinotto T, Ballottari M, Klimmek F, Jansson S, Bassi R (2005) The association of the antenna system to photosystem I in higher plants. Cooperative interactions stabilize the supramolecular complex and enhance red-shifted spectral forms. J Biol Chem 280: 31050-31058.
43. Elrad D, Niyogi K. K, Grossman A. R (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14: 1801-1816.
44. Bassi R, Wollman F. A (1991) The chlorophyll-A/B proteins of photosystem II in Chlamydomonas reinhardtii-isolation, characterization and immunological cross-reactivity to higher-plant polypeptides. Planta 183: 423-433.
45. Kuhlbrandt W, Wang D. N, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614-621.
46. Liu Z, Yan H, Wang K, Kuang T, Zhang J, et al. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428: 287-292.
47. Caffarri S, Passarini F, Bassi R, Croce R (2007) A specific binding site for neoxanthin in the monomeric antenna proteins CP26 and CP29 of Photosystem II. FEBS Lett 581: 4704-4710.
48. Formaggio E, Cinque G, Bassi R (2001) Functional architecture of the major light-harvesting complex from higher plants. J Mol Biol 314: 1157-1166.
49. Morosinotto T, Castelletti S, Breton J, Bassi R, Croce R (2002) Mutation analysis of Lhca1 antenna complex-low energy absorption forms originate from pigment-pigment interactions. J Biol Chem 277: 36253-36261.
50. Mozzo M, Mantelli M, Passarini F, Caffarri S, Croce R, et al. (2010) Functional analysis of Photosystem I light-harvesting complexes (Lhca) gene products of Chlamydomonas reinhardtii. Biochim Biophys Acta 1797: 212-221.
51. Wehner A, Storf S, Jahns P, Schmid V. H. R (2004) De-epoxidation of violaxanthin in light-harvesting complex I proteins. J Biol Chem 279: 26823-26829.
52. Ballottari M, Govoni C, Caffarri S, Morosinotto T (2004) Stoichiometry of LHCI antenna polypeptides and characterization of gap and linker pigments in higher plants Photosystem I. Eur J Biochem 271: 4659-4665.
53. Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: differential analysis of the Lhcb1-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43: 9467-9476.
54. Dainese P, Bassi R (1991) Subunit stoichiometry of the chloroplast photosystem II antenna system and aggregation state of the component chlorophyll a/b binding-proteins. J Biol Chem 266: 8136-8142.
55. Caffarri S, Croce R, Breton J, Bassi R (2001) The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J Biol Chem 276: 35924-35933.
56. Croce R, Weiss S, Bassi R (1999) Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J Biol Chem 274: 29613-29623.
57. Croce R, Cinque G, Holzwarth A. R, Bassi R (2000) The Soret absorption properties of carotenoids and chlorophylls in antenna complexes of higher plants. Photosynth Res 64: 221-231.
58. Gastaldelli M, Canino G, Croce R, Bassi R (2003) Xanthophyll binding sites of the CP29 (Lhcb4) subunit of higher plant photosystem II investigated by domain swapping and mutation analysis. J Biol Chem 278: 19190-19198.
59. Ballottari M, Mozzo M, Croce R, Morosinotto T, Bassi R (2009) Occupancy and functional architecture of the pigment binding sites of photosystem II antenna complex Lhcb5. J Biol Chem 284: 8103-8113.
60. Morosinotto T, Baronio R, Bassi R (2002) Dynamics of chromophore binding to Lhc proteins in vivo and in vitro during operation of the xanthophyll cycle. J Biol Chem 277: 36913-36920.
61. Georgakopoulou S, van der Zwan G, Bassi R, van Grondelle R, van Amerongen H, et al. (2007) Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry 46: 4745-4754.
62. Croce R, Chojnicka A, Morosinotto T, Ihalainen J. A, van Mourik F, et al. (2007) The low-energy forms of photosystem I light-harvesting complexes: spectroscopic properties and pigment-pigment interaction characteristics. Biophys J 93: 2418-2428.
63. Muller M. G, Lambrev P, Reus M, Wientjes E, Croce R, et al. (2010) Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. Chemphyschem 11: 1289-1296.
64. Moya I, Silvestri M, Vallon O, Cinque G, Bassi R (2001) Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 40: 12552-12561.
65. Ide J. P, Klug D. R, Kuhlbrandt W, Giorgi L. B, Porte G (1987) The state of detergent solubilised light-harvesting chlorophyll-a/b protein complex as monitored by picosecond time-resolved fluorescence and circular dichroism. Biochim Biophys Acta 893: 349-364.
66. Crimi M, Dorra D, Bosinger C. S, Giuffra E, Holzwarth A. R, et al. (2001) Time-resolved fluorescence analysis of the recombinant photosystem II antenna complex CP29. Effects of zeaxanthin, pH and phosphorylation. Eur J Biochem 268: 260-267.
67. Holt N. E, Zigmantas D, Valkunas L, Li X. P, Niyogi K. K, et al. (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307: 433-436.
68. Galinato M. G, Niedzwiedzki D, Deal C, Birge R. R, Frank H. A (2007) Cation radicals of xanthophylls. Photosynth Res 94: 67-78.
69. Cheng Y. C, Ahn T. K, Avenson T. J, Zigmantas D, Niyogi K. K, et al. (2008) Kinetic modeling of charge-transfer quenching in the CP29 minor complex. J Phys Chem B 112: 13418-13423.
70. Niyogi K. K, Bjorkman O, Grossman A. R (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9: 1369-1380.
71. Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia M. C, et al. (2008) The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84: 1359-1370.
72. Pesaresi P, Sandona D, Giuffra E, Bassi R (1997) A single point mutation (E166Q) prevents dicyclohexylcarbodiimide binding to the photosystem II subunit CP29. FEBS Lett 402: 151-156.
73. Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, et al. (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7: 3964-3979.
74. Wollman F. A (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20: 3623-3630.
75. Castelletti S, Morosinotto T, Robert B, Caffarri S, Bassi R, et al. (2003) Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry 42: 4226-4234.
76. Zhu S. H, Green B. R (2010) Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 1797: 1449-1457.
77. Croce R, Remelli R, Varotto C, Breton J, Bassi R (1999) The neoxanthin binding site of the major light harvesting complex (LHCII) from higher plants. FEBS Lett 456: 1-6.
78. Pineau B, Gerard-Hirne C, Selve C (2001) Carotenoid binding to photosystems I and II of Chlamydomonas reinhardtii cells grown under weak light or exposed to intense light. Plant Physiol Biochem 39: 73-85.
79. Ballottari M, Mozzo M, Croce R, Morosinotto T, Bassi R (2009) Occupancy and functional architecture of the pigment binding sites of photosystem II antenna complex Lhcb5. J Biol Chem 284: 8103-8113.
80. Croce R, Canino G, Ros F, Bassi R (2002) Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 41: 7334-7343.
81. Ruban A. V, Lee P. J, Wentworth M, Young A. J, Horton P (1999) Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes. J Biol Chem 274: 10458-10465.
82. Croce R, Morosinotto T, Castelletti S, Breton J, Bassi R (2002) The Lhca antenna complexes of higher plants photosystem I. Biochim Biophys Acta 1556: 29-40.
83. Ben Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426: 630-635.
84. Savard F, Richard C, Guertin M (1996) The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cabI/II genes that is regulated during the cell cycle and in response to illumination. Plant Mol Biol 32: 461-473.
85. Holt N. E, Fleming G. R, Niyogi K. K (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43: 8281-8289.
86. Haferkamp S, Haase W, Pascal A. A, van Amerongen H, Kirchhoff H (2010) Efficient Light harvesting by photosystem II Requires an optimized protein packing density in Grana thylakoids. J Biol Chem 285: 17020-17028.
87. Cinque G, Croce R, Holzwarth A, Bassi R (2000) Energy transfer among CP29 chlorophylls: calculated Forster rates and experimental transient absorption at room temperature. Biophys J 79: 1706-1717.
88. Gradinaru C. C, Ozdemir S, Gulen D, van Stokkum I. H, van Grondelle R, et al. (1998) The flow of excitation energy in LHCII monomers: implications for the structural model of the major plant antenna. Biophys J 75: 3064-3077.
89. Gradinaru C. C, Pascal A. A, van Mourik F, Robert B, Horton P, et al. (1998) Ultrafast evolution of the excited states in the chlorophyll a/b complex CP29 from green plants studied by energy-selective pump-probe spectroscopy. Biochemistry 37: 1143-1149.
90. Morosinotto T, Mozzo M, Bassi R, Croce R (2005) Pigment-pigment interactions in Lhca4 antenna complex of higher plants photosystem I. J Biol Chem 280: 20612-20619.
91. Ruban A. V, Berera R, Ilioaia C, van Stokkum I. H. M, Kennis J. T. M, et al. (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450: 575-578.
92. Muller M. G, Lambrev P, Reus M, Wientjes E, Croce R, et al. (2010) Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. Chemphyschem 11: 1289-1296.
93. Finazzi G, Johnson G. N, Dall'Osto L, Zito F, Bonente G, et al. (2006) Nonphotochemical quenching of chlorophyll fluorescence in Chlamydomonas reinhardtii. Biochemistry 45: 1490-1498.
94. Jahns P, Wehner A, Paulsen H, Hobe S (2001) De-epoxidation of violaxanthin after reconstitution into different carotenoid binding sites of light-harvesting complex II. J Biol Chem 276: 22154-22159.
95. Niyogi K. K, Bjorkman O, Grossman A. R (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci U S A 94: 14162-14167.
96. Harris E. H (1989) The Chlamydomonas sourcebook. A comprehensive guide to biology and laboratory use San Diego Academic Press.
97. Fleischmann M. M, Ravanel S, Delosme R, Olive J, Zito F, et al. (1999) Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition. J Biol Chem 274: 30987-30994.
98. Chua N. H, Bennoun P (1975) Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc Natl Acad Sci U S A 72: 2175-2179.
99. Laemmli U. K (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
100. Lagarde D, Beuf L, Vermaas W (2000) Increased production of zeaxanthin and other pigments by application of genetic engineering techniques to Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 66: 64-72.
101. Schagger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379.
102. Dall'Osto L, Caffarri S, Bassi R (2005) A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17: 1217-1232.