Enhanced photoprotection by protein-bound vs free xanthophyll pools: A comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants

Molecular Plant

Volumn 3, Issue 3, 2010, Pages 576-593

  Dall'Osto, Luca ^a   Cazzaniga, Stefano ^a   Havaux, Michel ^b,c,d   Bassi, Roberto ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b IRFM   (France)

^c CNRS   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Chloroplast; Light harvesting complexes; Photoprotection; Singlet oxygen; Zeaxanthin

Indexed keywords

ZEA;

EID: 77953014996     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssp117     Document Type: Article

References (80)

1. Ahn, T.K., Avenson, T.J., Ballottari, M., Cheng, Y.C., Niyogi, K.K., Bassi, R., and Fleming, G.R. (2008). Architecture of a chargetransfer state regulating light harvesting in a plant antenna protein. Science. 320, 794-797.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301, 653-657.
3. Anderson, J.M., and Chow, W.S. (2002). Structural and functional dynamics of plant photosystem II. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357, 1421-1430.
4. Asada, K. (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639. (Pubitemid 129491975)
5. Baroli, I., Do, A.D., Yamane, T., and Niyogi, K.K. (2003). Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell. 15, 992-1008.
6. Baroli, I., Gutman, B.L., Ledford, H.K., Shin, J.W., Chin, B.L., Havaux, M., and Niyogi, K.K. (2004). Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. J. Biol. Chem. 279, 6337-6344.
7. Bassi, R., Hinz, U., and Barbato, R. (1985). The role of the light harvesting complex and photosystem II in thylakoid stacking in the chlorina F2 barley mutant. Carlsberg Res. Commun. 50, 347-367.
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). Lightharvesting chlorophyll a/b proteins (LHCII) populations in phosphorylated membranes. Biochim. Biophys. Acta. 936, 29-38.
10. Berthold, D.A., Babcock, G.T., and Yocum, C.F. (1981). A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties. FEBS Lett. 134, 231-234.
11. Briantais, J.-M., Vernotte, C., Krause, G.H., andWeis, E. (1986). Chlorophyll a fluorescence of higher plants: chloroplasts and leaves. In Light Emission by Plants and Bacteria, Govindjee, Amesz, J., and Fork, DC., eds (New York: Academic Press), pp. 539-586.
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. Caffarri, S., Kouril, R., Kereiche, S., Boekema, E.J., and Croce, R. (2009). Functional architecture of higher plant photosystem II supercomplexes. EMBO J. 28, 3052-3063.
14. Casazza, A.P., Tarantino, D., and Soave, C. (2001). Preparation and functional characterization of thylakoids from Arabidopsis thaliana. Photosynth. Res. 68, 175-180.
15. 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.
16. Croce, R., Weiss, S., and Bassi, R. (1999). Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J. Biol. Chem. 274, 29613-29623.
17. Dainese, P., Marquardt, J., Pineau, B., and Bassi, R. (1992). Identification of violaxanthin and zeaxanthin binding proteins in maize photosytem II. In Research in Photosynthesis, Vol.I, Murata, N., ed. (Dordrecht: Kluwer Academic Publishers), pp. 287-290.
18. Dall'Osto, L., Caffarri, S., and 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.
19. Dall'Osto, L., Cazzaniga, S., North, H., MArion-Poll, A., and Bassi, R. (2007). The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photoxidative stress. Plant Cell. 19, 1048-1064.
20. Dall'Osto, L., Lico, C., Alric, J., Giuliano, G., Havaux, M., and Bassi, R. (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 Biology. 6, 32.
21. Davies, M.J. (2004). Reactive species formed on proteins exposed to singlet oxygen. Photochem. Photobiol. Sci. 3, 17-25.
22. Demmig-Adams, B. (1990). Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta. 1020, 1-24.
23. Ducruet, J.M. (2003). Chlorophyll thermoluminescence of leaf discs: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators. J. Exp. Bot. 54, 2419-2430.
24. Ducruet, J.M., and Vavilin, D. (1999). Chlorophyll high-temperature thermoluminescence emission as an indicator of oxidative stress: perturbating effects of oxygen and leaf water content. Free Radic. Res. 31 Suppl, S187-S192.
25. Espineda, C.E., Linford, A.S., Devine, D., and Brusslan, J.A. (1999). The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 96, 10507-10511.
26. Finazzi, G., Johnson, G.N., Dall'Osto, L., Joliot, P.,Wollman, F.A., and Bassi, R. (2004). A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc. Natl Acad. Sci. U S A. 101, 12375-12380.
27. Flors, C., Fryer, M.J., Waring, J., Reeder, B., Bechtold, U., Mullineaux, P.M., Nonell, S., Wilson, M.T., and Baker, N.R. (2006). Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J. Exp. Bot. 57, 1725-1734.
28. 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.
29. Gilmore, A.M., and Ball, M.C. (2000). Protection and storage of chlorophyll in overwintering evergreens. Proc. Natl Acad. Sci. U S A. 97, 11098-11101.
30. 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.
31. Girotti, A.W., and Kriska, T. (2004). Role of lipid hydroperoxides in photo-oxidative stress signaling. Antioxid. Redox. Signal. 6, 301-310.
32. Green, M.J., and Hill, H.A. (1984). Chemistry of dioxygen. Methods Enzymol. 105, 3-22.
33. Havaux, M. (2003). Spontaneous and thermoinduced photon emission: new methods to detect and quantify oxidative stress in plants. Trends in Plant Science. 8, 409-413.
34. Havaux, M., and Kloppstech, K. (2001). The protective functions of carotenoid and flavonoid pigments against excess visible radiations at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta. 213, 953-966.
35. Havaux, M., and Niyogi, K.K. (1999). The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl Acad. Sci. U S A. 96, 8762-8767.
36. Havaux, M., Bonfils, J.P., Lutz, C., and Niyogi, K.K. (2000). Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin deepoxidase. Plant Physiol. 124, 273-284.
37. Havaux, M., Dall'Osto, L., and Bassi, R. (2007). Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol. 145, 1506-1520.
38. Havaux, M., Dall'Osto, L., Cuine, S., Giuliano, G., and 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.
39. Havaux, M., Eymery, F., Porfirova, S., Rey, P., and Dormann, P. (2005). Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell. 17, 3451-3469.
40. 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.
41. 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.
42. Horton, P., Wentworth, M., and Ruban, A. (2005). Control of the light harvesting function of chloroplast membranes: the LHCIIaggregation model for non-photochemical quenching. FEBS Lett. 579, 4201-4206.
43. Jahns, P., Latowski, D., and Strzalka, K. (2009). Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim. Biophys. Acta. 1787, 3-14.
44. Johnson, M.P., Havaux, M., Triantaphylides, C., Ksas, B., Pascal, A.A., Robert, B., Davison, P.A., Ruban, A.V., and Horton, P. (2007). Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. J. Biol. Chem. 282, 22605-22618.
45. Keren, N., Berg, A., van Kan, P.J.M., Levanon, H., and Ohad, I. (1997). Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proc. Natl Acad. Sci. U S A. 94, 1579-1584.
46. Kim, E.H., Li, X.P., Razeghifard, R., Anderson, J.M., Niyogi, K.K., Pogson, B.J., and Chow, W.S. (2009). The multiple roles of light-harvesting chlorophyll a/b-protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants. Biochim. Biophys. Acta. 1787, 973-984.
47. Kim, J.H., Glick, R.E., and Melis, A. (1993). Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol. 102, 181-190.
48. Krieger, A., Rutherford, A.W., Vass, I., and Hideg, E. (1998). Relationship between activity, D1 loss, and Mn binding in photoinhibition of photosystem II. Biochemistry. 37, 16262-16269.
49. Krieger-Liszkay, A. (2005). Singlet oxygen production in photosynthesis. J. Exp. Bot. 56, 337-346.
50. Krieger-Liszkay, A., Fufezan, C., and Trebst, A. (2008). Singlet oxygen production in photosystem II and related protection mechanism. Photosynth. Res. 98, 551-564.
51. Kulheim, C., Agren, J., and Jansson, S. (2002). Rapid regulation of light harvesting and plant fitness in the field. Science. 297, 91-93.
52. Leverenz, J.W., Oquist, G., and Wingsle, G. (1992). Photosynthesis and photoinhibition in leaves of chlorophyll b-less barley in relation to absorbed light. Physiol. Plant. 85, 495-502.
53. 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.
54. Lin, Z.-F., Peng, C.-L., Lin, G.-Z., Ou, Z.Y., and Yang, C.-W. (2003). Photosynthetic characteristics of two new chlorophyll b-less rice mutants. Photosynthetica. 41, 61-67.
55. Martinez, G.R., et al. (2003). Oxidative and alkylating damage in DNA. Mutat. Res. 544, 115-127.
56. Mishra, N.P., and Ghanotakis, D.F. (1994). Exposure of a photosystem II complex to chemically generated singlet oxygen results in D1 fragments similar to the ones observed during aerobic photoinhibition. Biochim. Biophys. Acta. 1187, 296-300.
57. Moan, J., and Berg, K. (1991). The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem. Photobiol. 53, 549-553.
58. 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.
59. Morosinotto, T., Bassi, R., Frigerio, S., Finazzi, G., Morris, E., and Barber, J. (2006). 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 J. 273, 4616-4630.
60. Morosinotto, T., Breton, J., Bassi, R., and Croce, R. (2003a). The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystemI. J. Biol. Chem. 278, 49223-49229.
61. Morosinotto, T., Caffarri, S., Dall'Osto, L., and Bassi, R. (2003b). Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiologia Plantarum. 119, 347-354.
62. 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. (Pubitemid 32979708)
63. Mozzo, M., Dall'Osto, L., Hienerwadel, R., Bassi, R., and 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.
64. Muller-Moule, P., Havaux, M., and Niyogi, K.K. (2003). Zeaxanthin deficiency enhances the high light sensitivity of an ascorbatedeficient mutant of Arabidopsis. Plant Physiol. 133, 748-760.
65. Nayak, L., Raval, M.K., Biswal, B., and Biswal, U.C. (2002). Topology and photoprotective role of carotenoids in photosystem II of chloroplast: a hypothesis. Photochem. Photobiol. Sci. 1, 629-631.
66. Niyogi, K.K. (1999). Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333-359.
67. 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.
68. Niyogi, K.K., Shih, C., Chow,W.S., Pogson, B.J., DellaPenna, D., and Bjorkman, O. (2001). Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth. Res. 67, 139-145.
69. Plumley, F.G., and Schmidt, G.W. (1987). Reconstitution of chloroform a/b light-harvesting complexes: xanthophyll-dependent assembley and energy transfer. Proc. Natl Acad. Sci. U S A. 84, 146-150.
70. Pogson, B.J., Niyogi, K.K., Bjorkman, O., and 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.
71. Seigneurin-Berny, D., Salvi, D., Dorne, A.J., Joyard, J., and Rolland, N. (2008a). Percoll-purified and photosynthetically active chloroplasts from Arabidopsis thaliana leaves. Plant Physiol. Biochem. 46, 951-955.
72. Seigneurin-Berny, D., Salvi, D., Joyard, J., and Rolland, N. (2008b). Purification of intact chloroplasts from Arabidopsis and spinach leaves by isopycnic centrifugation. Curr. Protoc. Cell Biol. Chapter 3, Unit 3.30.
73. Tanaka, A., Ito, H., Tanaka, R., Tanaka, N.K., Yoshida, K., and Okada, K. (1998). Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc. Natl Acad. Sci. U S A. 95, 12719-12723.
74. Tardy, F., and Havaux, M. (1997). Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim. Biophys. Acta. 1330, 179-193.
75. Telfer, A. (2002). What is beta-carotene doing in the photosystem II reaction centre? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357, 1431-1439.
76. Triantaphylidè s, C., Krischke, M., Hoeberichts, F.A., Ksas, B., Gresser, G., Havaux, M., Van Breusegem, F., and Mueller, M.J. (2008). Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol. 148, 960-968.
77. Van Kooten, O., and Snel, J.F.H. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynt. Res. 25, 147-150.
78. Vavilin, D.V., and Ducruet, J.-M. (1998). The origin of 115-130 degrees C thermoluminescence bands in chlorophyll-containing material. Photochem. Photobiol. 68, 191-198.
79. Wentworth, M., Ruban, A.V., and Horton, P. (2004). The functional significance of the monomeric to trimeric states of the photosystem II light harvesting complexes. Biochemistry. 43, 501-509.
80. Xu, C.-C., Kuang, T., Li, L., and Lee, C.-H. (2000). D1 protein turnover and carotene synthesis in relation to zeaxanthin epoxidation in rice leaves during recovery from low temperature photoinhibition. Aust. J. Plant Physiol. 27, 239-244.