A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26

Plant Cell

Volumn 17, Issue 4, 2005, Pages 1217-1232

  Dall'Osto, Luca ^a,b   Caffarri, Stefano ^a,b   Bassi, Roberto ^a,b  

^a UNIVERSITY OF VERONA   (Italy)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; PHOTOSYNTHESIS; PLANTS (BOTANY); PROTEINS;

ANTENNA PROTEINS; PROTEIN COMPLEXES; THALAKOID PROTEINS;

ENERGY DISSIPATION;

ENERGY; MOLECULAR STRUCTURE; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; ESCHERICHIA COLI; MOYA;

EID: 23744439566     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.030601     Document Type: Article

References (82)

1. Andersson, J., Walters, R.G., Horton, P., and Jansson, S. (2001). Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: Implications for the mechanism of protective energy dissipation. Plant Cell 13, 1193-1204.
2. Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
3. Aro, E.-M., McCaffery, S., and Anderson, J.M. (1993a). Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol. 103, 835-843.
4. Aro, E.-M., Virgin, I., and Andersson, B. (1993b). Photoinhibition of photosystem-2. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113-134.
5. Asada, K., and Takahashi, M. (1987). Production and scavenging of active oxygen in photosynthesis. In Photoinhibition, D.J. Kyle, C.B. Osmond, and C.J. Arntzen, eds (Amsterdam: Elsevier), pp. 227-287.
6. Aspinall-O'Dea, M., Wentworth, M., Pascal, A., Robert, B., Ruban, A., and Horton, P. (2002). In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc. Natl. Acad. Sci. USA 99, 16331-16335.
7. Baroli, I., Do, A.D., Yamane, T., and Niyogi, K.K. (2003). Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlorophyllamydomonas reinhardtii from photooxidative stress. Plant Cell 15, 992-1008.
8. Bassi, R., Pineau, B., Dainese, P., and Marquardt, J. (1993). Carotenoid-binding proteins of photosystem-II. Eur. J. Biochem. 212, 297-303.
9. Bassi, R., Rigoni, F., Barbato, R., and Giacometti, G.M. (1988). Light-harvesting chlorophyll a/b proteins (LHCII) populations in phosphorylated membranes. Biochim. Biophys. Acta 936, 29-38.
10. Ben Or, S., and Chrambach, A. (1983). Heterogeneity of the glucocorticoid receptors: Molecular transformations during activation, detected by electrofocusing. Arch. Biochem. Biophys. 221, 343-353.
11. Bergantino, E., Dainese, P., Cerovic, Z., Sechi, S., and Bassi, R. (1995). A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress. J. Biol. Chem. 270, 8474-8481.
12. Caffarri, S., Croce, R., Breton, J., and 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.
13. Crimi, M., Dorra, D., Bosinger, C.S., Giuffra, E., Holzwarth, A.R., and Bassi, R. (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.
14. Croce, R., Canino, G., Ros, F., and Bassi, R. (2002). Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 41, 7334-7343.
15. Dainese, P., and 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.
16. Dainese, P., Hoyer-hansen, G., and Bassi, R. (1990). The resolution of chlorophyll a/b binding proteins by a preparative method based on flat bed isoelectric focusing. Photochem. Photobiol. 51, 693-703.
17. Demmig-Adams, B., and Adams III, W.W. (1996). The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1, 21-26.
18. Demmig-Adams, B., and Adams, W.W. (2000). Harvesting sunlight safely. Nature 403, 371-374.
19. Demmig-Adams, B., Adams, W.W., Heber, U., Neimanis, S., Winter, K., Krüger, A., Czygan, F.-C., Bilger, W., and Björkman, O. (1990). Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol. 92, 293-301.
20. Demmig-Adams, B., Winter, K., Kruger, A., and Czygan, F.-C. (1989). Light stress and photoprotection related to the carotenoid zeaxanthin in higher plants. In Photosynthesis. Plant Biology, Vol. 8, W.R. Briggs, ed (New York: Alan R. Liss), pp. 375-391.
21. Dexter, D.L. (1953). A theory of sensitized luminescence in solids. J. Chem. Phys. 21, 836-850.
22. Dixon, R.A., and Paiva, N.L. (1995). Stress-induced phenylpropanoid metabolism. Plant Cell 7, 1085-1097.
23. Dominici, P., Caffarri, S., Armenante, F., Ceoldo, S., Crimi, M., and Bassi, R. (2002). Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J. Biol. Chem. 277, 22750-22758.
24. Ebbert, V., Adams III, W.W., Mattoo, A.K., Sokolenko, A., and Demmig-Adams, B. (2005). Up-regulation of a photosystem II core protein phosphatase inhibitor and sustained D1 phosphorylation in zeaxanthin-retaining, photoinhibited needles of overwintering Douglas fir. Plant Cell Environ. 28, 232-240.
25. Ebbert, V., Demmig-Adams, B., Adams III, W.W., Mueh, K.E., and Staehelin, L.A. (2001). Correlation between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. Photosynth. Res. 67, 63-78.
26. Ek, K., Gianazza, E., and Righetti, P.G. (1980). Affinity titration curves: Determination of dissociation constants of lectin-sugar complexes and of their pH-dependence by isoelectric focusing electrophoresis. Biochim. Biophys. Acta 626, 356-365.
27. Elrad, D., Niyogi, K.K., and Grossman, A.R. (2002). A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14, 1801-1816.
28. Färber, A., Young, A.J., Ruban, A.V., Horton, P., and Jahns, P. (1997). Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants. Plant Physiol. 115, 1609-1618.
29. Formaggio, E., Cinque, G., and Bassi, R. (2001). Functional architecture of the major light-harvesting complex from higher plants. J. Mol. Biol. 314, 1157-1166.
30. Forster, T. (1965). Delocalized excitation and excitation transfer. In Modern Quantum Chemistry, Part III: Action of Light and Organic Crystals, O. Sinanoglu, ed (New York: Academic Press), pp. 93-137.
31. Foyer, C.H., Lescure, J.C., Lefebvre, C., Morot-Gaudry, J.F., Vincentz, M., and Vaucheret, H. (1994). Adaptations of photosynthetic electron transport, carbon assimilation, and carbon partitioning in transgenic Nicotiana plumbaginifolia plants to changes in nitrate reductase activity. Plant Physiol. 104, 171-178.
32. Funk, C., Schröder, W.P., Napiwotzki, A., Tjus, S.E., Renger, G., and Andersson, B. (1995). The PSII-S protein of higher plants: A new type of pigment-binding protein. Biochemistry 34, 11133-11141.
33. Ganeteg, U., Kulheim, C., Andersson, J., and Jansson, S. (2004). Is each light-harvesting complex protein important for plant fitness? Plant Physiol. 134, 502-509.
34. Gilmore, A.M., and Ball, M.C. (2000). Protection and storage of chlorophyll in overwintering evergreens. Proc. Natl. Acad. Sci. USA 97, 11098-11101.
35. Gilmore, A.M., Hazlett, T.L., and Govindjee, G. (1995). Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: Formation of a quenching complex with a short fluorescence lifetime. Proc. Natl. Acad. Sci. USA 92, 2273-2277.
36. Gilmore, A.M., Matsubara, S., Ball, M.C., Barker, D.H., and Itoh, S. (2003). Excitation energy flow at 77 K in the photosynthetic apparatus of overwintering evergreens. Plant Cell Environ. 26, 1021-1034.
37. Gilmore, A.M., Shinkarev, V.P., Hazlett, T.L., and Govindjee, G. (1998). Quantitative analysis of the effects of intrathylakoid pH and xanathophyll cycle pigments on chlorophyll a fluorescence lifetime distributions and intensity in thylakoids. Biochemistry 37, 13582-13593.
38. Gilmore, A.M., and Yamamoto, H.Y. (1991). Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol. 96, 635-643.
39. Giuffra, E., Cugini, D., Croce, R., and Bassi, R. (1996). Reconstitution and pigment-binding properties of recombinant CP29. Eur. J. Biochem. 238, 112-120.
40. Giuffra, E., Zucchelli, G., Sandona, D., Croce, R., Cugini, D., Garlaschi, F.M., Bassi, R., and Jennings, R.C. (1997). Analysis of some optical properties of a native and reconstituted photosystem II antenna complex, CP29: Pigment binding sites can be occupied by chlorophyll a or chlorophyll b and determine spectral forms. Biochemistry 36, 12984-12993.
41. Gradinaru, C.C., Özdemir, S., Gülen, D., van Stokkum, I.H.M., van Grondelle, R., and Van Amerongen, H. (1998). The flow of excitation energy in LHCII monomers: Implications for the structural model of the major plant antenna. Biophys. J. 75, 3064-3077.
42. Grasses, T., Pesaresi, P., Schiavon, F., Varotto, C., Salamini, F., Jahns, P., and Leister, D. (2002). The role of delta pH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana. Plant Physiol. Biochem. 40, 41-49.
43. Havaux, M., and Kloppstech, K. (2001). The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213, 953-966.
44. Havaux, M., and Niyogi, K.K. (1999). The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl. Acad. Sci. USA 96, 8762-8767.
45. Henkes, K., Sonnewald, U., Badur, R., Flachmann, R., and Stitt, M. (2001). A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell 13, 535-551.
46. Holt, N.E., Fleming, G.R., and Niyogi, K.K. (2004). Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43, 8281-8289.
47. Holt, N.E., Zigmantas, D., Valkunas, L., Li, X.-P., Niyogi, K.K., and Fleming, G.R. (2005). Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433-436.
48. Holub, O., Seufferheld, M.J., Gohlke, C., Govindjee, G., and Clegg, R.M. (2000). Fluorescence lifetime imaging (FLI) in real-time: A new technique in photosynthesis research. Photosynthetica 38, 581-599.
49. Horton, P. (1996). Nonphotochemical quenching of chlorophyll fluorescence. In Light as an Energy Source and Information Carrier in Plant Physiology, R.C. Jennings, ed (New York: Plenum Press), pp. 99-111.
50. Horton, P., Ruban, A.V., and Wentworth, M. (2000). Allosteric regulation of the light-harvesting system of photosystem II. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1361-1370.
51. Jansson, S. (1999). A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4, 236-240.
52. Jennings, R.C., Bassi, R., Garlaschi, F.M., Dainese, P., and Zucchelli, G. (1993). Distribution of the chlorophyll spectral forms in the chlorophyll/protein complexes of photosystem-II antenna. Biochemistry 32, 3203-3210.
53. Koornneef, M., Jorna, M.L., Brinkhorst-Van der Swan, D.L.C., and Karssen, C.M. (1982). The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theor. Appl. Genet. 61, 385-393.
54. Kulheim, C., Agren, J., and Jansson, S. (2002). Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91-93.
55. Li, X.P., Bjorkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., and Niyogi, K.K. (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395.
56. Li, X.P., Gilmore, A.M., and Niyogi, K.K. (2002a). Molecular and global time-resolved analysis of a psbS gene dosage effect on pH- and xanthophyll cycle-dependent nonphotochemical quenching in photosystem II. J. Biol. Chem. 277, 33590-33597.
57. Li, X.P., Phippard, A., Pasari, J., and Niyogi, K.K. (2002b). Structure-function analysis of photosystem II subunit S (PsbS) in vivo. Funct. Plant Biol. 29, 1131-1139.
58. Matsubara, S., Gilmore, A.M., Ball, M.C., Anderson, J.M., and Osmond, B. (2002). Sustained downregulation of photosystem II in mistletoes during winter depression of photosynthesis. Funct. Plant Biol. 29, 1157-1169.
59. Morosinotto, T., Baronio, R., and 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.
60. Morosinotto, T., Caffarri, S., Dall'Osto, L., and Bassi, R. (2003). Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol. Plant. 119, 347-354.
61. Moya, I., Silvestri, M., Vallon, O., Cinque, G., and Bassi, R. (2001). Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 40, 12552-12561.
62. Niyogi, K.K. (1999). Photoprotection revisited: Genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333-359.
63. Niyogi, K.K., Grossman, A.R., and Björkman, O. (1998). Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10, 1121-1134.
64. Paulsen, H., and Hobe, S. (1992). Pigment-binding properties of mutant light-harvesting chlorophyll-a/b-binding protein. Eur. J. Biochem. 205, 71-76.
65. Pesaresi, P., Sandona, D., Giuffra, E., and Bassi, R. (1997). A single point mutation (E166Q) prevents dicyclohexylcarbodiimide binding to the photosystem II subunit CP29. FEBS Lett. 402, 151-156.
66. Pogson, B.J., Niyogi, K.K., Björkman, O., and DellaPenna, D. (1998). Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc. Natl. Acad. Sci. USA 95, 13324-13329.
67. Polivka, T., Zigmantas, D., Sundstrom, V., Formaggio, E., Cinque, G., and Bassi, R. (2002). Carotenoid S(1) state in a recombinant light-harvesting complex of Photosystem II. Biochemistry 41, 439-450.
68. Porra, R.J., Thompson, W.A., and Kriedemann, P.E. (1989). Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384-394.
69. Rossel, J.B., Wilson, I.W., and Pogson, B.J. (2002). Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130, 1109-1120.
70. Ruban, A.V., and 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.
71. Ruban, A.V., Young, A.J., and Horton, P. (1993). Induction of non-photochemical energy dissipation and absorbance changes in leaves. Plant Physiol. 102, 741-750.
72. Ruban, A.V., Young, A.J., Pascal, A.A., and Horton, P. (1994). The effects of illumination on the xanthophyll composition of the photosystem II light-harvesting complexes of spinach thylakoid membranes. Plant Physiol. 104, 227-234.
73. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
74. Schagger, H., and 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.
75. Sorefan, K., Booker, J., Haurogne, K., Goussot, M., Bainbridge, K., Foo, E., Chatfield, S., Ward, S., Beveridge, C., Rameau, C., and Leyser, O. (2003). MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev. 17, 1469-1474.
76. Swiatek, M., Kuras, R., Sokolenko, A., Higgs, D., Olive, J., Cinque, G., Muller, B., Eichacker, L.A., Stern, D.B., Bassi, R., Herrmann, R.G., and Wollman, F.A. (2001). The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. Plant Cell 13, 1347-1367.
77. Van Kooten, O., and Snel, J.F.H. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25, 147-150.
78. Verhoeven, A.S., Adams, W.W., and Demmig-Adams, B. (1998). Two forms of sustained xanthophyll cycle-dependent energy dissipation in overwintering Euonymus kiautschovicus. Plant Cell Environ. 21, 893-903.
79. Verhoeven, A.S., Adams, W.W., Demmig-Adams, B., Croce, R., and Bassi, R. (1999). Xanthophyll cycle pigment localization and dynamics during exposure to low temperature and light stress in Vinca major. Plant Physiol. 120, 727-737.
80. Wagner, D., Przybyla, D., Op den Camp, R., Kim, C., Landgraf, F., Lee, K.P., Wursch, M., Laloi, C., Nater, M., Hideg, E., and Apel, K. (2004). The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183-1185.
81. Walters, R.G., Ruban, A.V., and Horton, P. (1996). Identification of proton-active residues in a higher plant light-harvesting complex. Proc. Natl. Acad. Sci. USA 93, 14204-14209.
82. Xiang, C., Werner, B., Christensen, E., and Oliver, D. (2001). The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol. 126, 564-574.