Biochemical and structural analyses of a higher plant photosystem II supercomplex of a photosystem I-less mutant of barley: Consequences of a chronic over-reduction of the plastoquinone pool

FEBS Journal

Volumn 273, Issue 20, 2006, Pages 4616-4630

  Morosinotto, Tomas ^a,b   Bassi, Roberto ^a,b   Frigerio, Sara ^a,b   Finazzi, Giovanni ^c   Morris, Edward ^d   Barber, James ^e  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF VERONA   (Italy)

^c National de la Recherche Scientifique Université Pierre et Marie Curie   (France)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Acclimation; Lhc; Photosystem; Plastoquinone; Supercomplexes

Indexed keywords

CAROTENOID; CHLOROPHYLL;

ANTENNA; ARTICLE; BARLEY; BIOSYNTHESIS; CHEMICAL ANALYSIS; ELECTRON MICROSCOPY; ELECTRON TRANSPORT; IN VIVO STUDY; MUTANT; MUTATION; NONHUMAN; PHOTOSYSTEM I; PHOTOSYSTEM II; PRIORITY JOURNAL;

CRYOELECTRON MICROSCOPY; CRYSTALLIZATION; HORDEUM; LIGHT; MUTATION; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PLASTOQUINONE; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; THYLAKOIDS;

EMBRYOPHYTA; HORDEUM VULGARE; HORDEUM VULGARE SUBSP. VULGARE;

EID: 33749373006     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05465.x     Document Type: Article

References (67)

1. Barber J (2003) Photosystem II: the engine of life. Q Rev Biophys 36, 71-89.
2. Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4, 236-240.
3. Lichtenthaler HK, Kuhn G, Prenzel U & Meier D (1982) Chlorophyll-protein levels and degree of thylakoid stacking in radish chloroplasts from high-light, low-light and bentazon-treated plants. Physiol Plant 56, 183-188.
4. Spangfort M & Andersson B (1989) Subpopulations of the main chlorophyll a/b light-harvesting complex of photosystem II ) isolation and biochemical characterization. Biochim Biophys Acta 977, 163-170.
5. Kim JH, Glick RE & Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102, 181-190.
6. Lindahl M, Yang DH & Andersson B (1995) Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem II by a light-induced membrane-associated enzymic system. Eur J Biochem 231, 503-509.
7. Escoubas JM, Lomas M, LaRoche J & Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92, 10237-10241.
8. Chen YB, Durnford DG, Koblizek M & Falkowski PG (2004) Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiol 136, 3737-3750.
9. Havaux M, Dall'Osto L, Cuine S, Giuliano G & Bassi R (2004) The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. J Biol Chem 279, 13878-13888.
10. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W & Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature 409, 739-743.
11. Kamiya N & Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc Natl Acad Sci USA 100, 98-103.
12. Ferreira KN, Iverson TM, Maghlaoui K, Barber J & Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838.
13. Loll B, Kern J, Saenger W, Zouni A & Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438, 1040-1044.
14. Morris EP, Hankamer B, Zheleva D, Friso G & Barber J (1997) The three-dimensional structure of a photosystem II core complex determined by electron crystallography. Structure 5, 837-849.
15. Hankamer B, Morris E, Nield J, Gerle C & Barber J (2001) Three-dimensional structure of the photosystem II core dimer of higher plants determined by electron microscopy. J Struct Biol 135, 262-269.
16. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X & Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428, 287-292.
17. Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M & Kuhlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24, 919-928.
18. Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J & Rögner M (1995) Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92, 175-179.
19. Boekema EJ, van Breemen JF, van Roon H & Dekker JP (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301, 1123-1133.
20. Nield J, Orlova EV, Morris EP, Gowen B, van Heel M & Barber J (2000) 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat Struct Biol 7, 44-47.
21. Nield J, Funk C & Barber J (2000) Supermolecular structure of photosystem II and location of the PsbS protein. Philos Trans R Soc Lond B Biol Sci 355, 1337-1344.
22. Harrer R, Bassi R, Testi MG & Schäfer C (1998) Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction center and antenna proteins. Eur J Biochem 255, 196-205.
23. Dekker JP & Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706, 12-39.
24. Boekema EJ, van Roon H, Calkoen F, Bassi R & Dekker JP (1999) Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38, 2233-2239.
25. Simpson DJ (1983) Freeze-fracture studies on barley plastid membranes. VI. Location of the P700-chlorophyll a-protein 1. Eur J Cell Biol 31, 305-314.
26. Krause GH & Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol 42, 313-349.
27. Hiller RG, Moller BL & Hoyerhansen C (1980) Characterization of 6 putative photosystem-I mutants in barley. Carlsberg Res Commun 45, 315-328.
28. Simpson DJ & von Wettstein D (1980) Macromolecular physiology of plastids. 14. Viridis mutants in barley - genetic, fluoroscopic and ultrastructural characterization. Carlsberg Res Commun 45, 283-314.
29. Bergantino E, Sandona D, Cugini D & Bassi R (1998) The photosystem II subunit CP29 can be phosphorylated in both C3 and C4 plants as suggested by sequence analysis. Plant Mol Biol 36, 11-22.
30. Cournac L, Redding K, Ravenel J, Rumeau D, Josse EM, Kuntz M & Peltier G (2000) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275, 17256-17262.
31. Genty B, Briantais J-M & Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990, 87-92.
32. Yamamoto HY, Chang JL & Aihara MS (1967) Light-induced interconversion of violaxanthin and zeaxanthin in New Zealand spinach-leaf segments. Biochim Biophys Acta 141, 342-347.
33. Demmig-Adams B & Adams WW (1994) Capacity for energy dissipation in the pigment bed in leaves with different xanthophyll cycle pools. Aust J Plant Physiol 21, 575-588.
34. Davison PA, Hunter CN & Horton P (2002) Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418, 203-206.
35. 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.
36. Miller KR & Jacob JS (1991) Surface structure of the photosystem II complex. In Proceedings of the 49th EMSA Meeting (Bailey GW & Hall EL, eds), pp. 196-197. San Francisco Press, San Francisco, CA.
37. Marr KM, McFeeters RL & Lyon MK (1996) Isolation and structural analysis of two-dimensional crystals of photosystem II from Hordeum vulgare viridis zb63. J Struct Biol 117, 86-98.
38. Berthold DA, Babcock GT & Yocum CF (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron-transport properties. FEBS Lett 134, 231-234.
39. Bassi R, Ghiretti MA, Tognon G, Giacometti GM & Miller KR (1989) Two-dimensional crystals of the photosystem II reaction center complex from higher plants. Eur J Cell Biol 50, 84-93.
40. Santini C, Tidu V, Tognon G, Ghiretti MA & Bassi R (1994) Three-dimensional structure of the higher-plant photosystem II reaction centre and evidence for its dimeric organization in vivo. Eur J Biochem 221, 307-315.
41. Hankamer B, Morris EP & Barber J (1999) Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography. Nat Struct Biol 6, 560-564.
42. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020, 1-24.
43. Ford RC, Stoylova SS & Holzenburg A (2002) An alternative model for photosystem II/light harvesting complex II in grana membranes based on cryo-electron microscopy studies. Eur J Biochem 269, 326-336.
44. Hankamer B, Nield J, Zheleva D, Boekema E, Jansson S & Barber J (1997) Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. Eur J Biochem 243, 422-429.
45. Barber J, Nield J, Morris EP, Zheleva D & Hankamer B (1997) The structure, function and dynamics of photosystem two. Physiol Plant 100, 817-827.
46. Rhee K-H, Morris EP, Barber J & Kühlbrandt W (1998) Three-dimensional structure of the plant photosystem II reaction centre at 8 A resolution. Nature 396, 283-284.
47. Barber J, Nield J, Morris EP & Hankamer B (1999) Subunit positioning in photosystem II revisited. Trends Biochem Sci 24, 43-45.
48. Bailey S, Walters RG, Jansson S & Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213, 794-801.
49. Elrad D, Niyogi KK & Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14, 1801-1816.
50. 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.
51. Caffarri S, Frigerio S, Olivieri E, Righetti PG & Bassi R (2005) Differential accumulation of Lhcb gene products in thylakoid membranes of Zea mays plants grown under contrasting light and temperature conditions. Proteomics 5, 758-768.
52. Horton P & Ruban A (2005) Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56, 365-373.
53. Yakushevska AE, Keegstra W, Boekema EJ, Dekker JP, Andersson J, Jansson S, Ruban AV & Horton P (2003) The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. Biochemistry 42, 608-613.
54. Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S & Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395.
55. Ma YZ, Holt NE, Li XP, Niyogi KK & Fleming GR (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci USA 100, 4377-4382.
56. Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK & Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433-436.
57. Ruban AV & Horton P (1999) The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiol 119, 531-542.
58. Joliot P & Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99, 10209-10214.
59. Bassi R, Rigoni F, Barbato R & Giacometti GM (1988) Light-harvesting chlorophyll a/b proteins (LHCII) populations in phosphorylated membranes. Biochim Biophys Acta 936, 29-38.
60. 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.
61. Schägger 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.
62. Peter GF & Thornber JP (1991) Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Biol Chem 266, 16745-16754.
63. Gilmore AM & Yamamoto HY (1991) Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol 96, 635-643.
64. Crowther RA, Henderson R & Smith JM (1996) MRC image processing programs. J Struct Biol 116, 9-16.
65. van Heel M, Harauz G, Orlova EV, Schmidt R & Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116, 17-24.
66. Kühlbrandt W, Wang DN & Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367, 614-621.
67. Jones TA, Zou J-Y & Cowan SW (1991) Improved methods for building protein models in electron denity maps and the location of errors in the models. Acta Crystallogr A47, 110-119.