Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the arabidopsis thaliana npq1 mutant

Plant Cell

Volumn 21, Issue 6, 2009, Pages 1798-1812

  Li, Zhirong ^a,b   Ahn, Tae Kyui ^b,c   Avenson, Thomas J ^a,b,c   Ballottari, Matteo ^d   Cruz, Jeffrey A ^e   Kramer, David M ^e   Bassi, Roberto ^d   Fleming, Graham R ^b   Keasling, Jay D ^b,f   Niyogi, Krishna K ^a,b,g  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF VERONA   (Italy)

^e WASHINGTON STATE UNIVERSITY   (United States)

^f University of California   (United States)

^g MONSANTO COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 70349260207     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.066571     Document Type: Article

References (70)

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 charge-transfer state regulating light harvesting in a plant antenna protein. Science 320: 794-797.
2. Al-Babili, S-, Hugueney, P., Schledz, M., Welsch, R., Frohnmeyer, H., Laule, O., and Beyer, P. (2000). Identification of a novel gene coding for neoxanthin synthase from Solanum tuberosum. FEBS Lett. 485: 168-172.
3. Amarie, S., Standfuss, J., Barros, T., Kuhlbrandt, W., Dreuw, A., and Wachtveitl, J. (2007). Carotenoid radical cations as a probe for the molecular mechanism of nonphotochemical quenching in oxygenic photosynthesis. J. Phys. Chem. 111: 3481-3487.
4. Andersson, J., Walters, R.G., Horton, P., and Jansson, S. (2001). Antlsense inhibition of the photosynthetic antenna proteins CP29 and CP26: Implications for the mechanism of protective energy dissipation. Plant Cell 13: 1193-1204.
5. Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141: 391-396.
6. Avenson, T.J., Ahn, T.K., Niyogi, K.K., Ballottari, M., Bassi, R., and Fleming, G.R. (2009). Lutein can act as a switchable charge-transfer quencher in the CP26 light-harvesting complex. J. Biol. Chem. 284: 2830-2835.
7. Avenson, T.J., Ahn, T.K., Zigmantas, D., Niyogi, K.K., Li, Z., Ballottari, M., Bassi, R., and Fleming, G.R. (2008). Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283: 3550-3558.
8. Ballottari, M., Mozzo, M., Croce, R., Morosinotto, T., and Bassi, R. (2009). Occupancy and functional architecture of the pigment binding sites of photosystem Il antenna complex Lhcb5. J. Biol. Chem. 284: 8103-8113.
9. Bassi, R., and Dainese, P. (1992). A supramolecular light-harvesting complex from chloroplast photosystem-II membranes. Eur. J. Biochem. 204: 317-326.
10. Betterle, N., Ballottari, M., Zorzan, S., de Bianchi, S., Cazzaniga, S., Dall'Osto, L., Morosinotto, T., and Bassi, R. (2009). Light induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J. Biol. Chem. 284: 15255-15266.
11. Bilger, W., and Björkman, O. (1994). Relationships among violaxanthin deepoxidatlon, thylakoid membrane conformation, and nonphotochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L). Planta 193: 238-246.
12. Bouvier, F., D'Harlingue, A., Backhaus, R.A., Kumagai, M.H., and Cámara, B. (2000). Identification of neoxanthin synthase as a carotenoid cyclase paralog. Eur. J. Biochem. 267: 6346-6352.
13. Caffarri, S., Croce, R., Breton, J., and Bassi, R. (2001). The major antenna complex of photosystem Il has a xanthophyll binding site not involved in light harvesting. J. Biol. Chem. 276: 35924-35933.
14. Crouchman, S., Ruban, A., and Horton, P. (2006). PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin. FEBS Lett. 580: 2053-2058.
15. Cunningham, F.X, Sun, Z.R., Chamovitz, D., Hirschberg, J., and Gantt, E. (1994). Molecular-structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp strain PCC7942. Plant Cell 6: 1107-1121.
16. Cunningham, F.X., Jr., Pogson, B., Sun, Z., McDonald, K.A., DellaPenna, D., and Gantt, E. (1996). Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8: 16131626.
17. Dall'Osto, L., Fiore, A., Cazzaniga, S., Giuliano, G., and Bassi, R. (2007). Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection. J. Biol. Chem. 282: 35056-35068.
18. Demmig-Adams, B., and Adams, W.W. (1992). Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 599-626.
19. Diretto, G., Tavazza, R., Welsch, R., Pizzichini, D., Mourgues, F., Papacchioli, V., Beyer, P., and Giuliano, G. (2006). Metabolic engineering of potato tuber carotenolds through tuber-specific silencing of lycopene epsilon cyclase. BMC Plant Biol. 6: 13.
20. Edge, R., Land, E.J., McGarvey, D., Mulroy, L., and Truscott, T.G. (1998). Relative one-electron reduction potentials of carotenoid radical cations and the interactions of carotenoids with the vitamin E radical cation. J. Am. Chem. Soc. 120: 4087-4090.
21. Fiore, A., Dall'Osto, L., Fraser, P.D., Bassi, R., and Giuliano, G. (2006). Elucidation of the beta-carotene hydroxylation pathway in Arabidopsis thaliana. FEBS Lett. 580: 4718-4722.
22. Formaggio, E., Cinque, G., and Bassi, R. (2001). Functional architecture of the major light-harvesting complex from higher plants. J. Mol. BIoI. 314: 1157-1166.
23. Galinato, M.G.I., Niedzwiedzki, D., Deal, C., Birge, R.R., and Frank, H.A. (2007). Cation radicals of xanthophylls. Photosynth. Res. 94: 67-78.
24. Gastaldelli, M., Canino, G., Croce, R., and Bassi, R. (2003). Xanthophyll binding sites of the CP29 (Lhcb4) subunlt of higher plant photosystem Il investigated by domain swapping and mutation analysis. J. Biol. Chem. 278: 19190-19198.
25. 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 thylakolds. Biochemistry 37: 13582-13593.
26. Harjes, C.E., Rocheford, T.R., Bai, L., Brutneil, T.P., Kandianis, C.B., Sowinski, S.G., Stapleton, A.E., Vallabhaneni, R., Williams, M., Wurtzel, E.T., Yan, J.B., and Buckler, E.S. (2008). Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330-333.
27. Haughn, G.W., and Somerville, C. (1986). Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204: 430-434.
28. Hirschberg, J. (2001). Carotenoid biosynthesis in flowering plants. Curr. Opin. Plant Biol. 4:210-218.
29. 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.
30. Horton, P., Johnson, M.P., Pérez-Bueno, M.L., Kiss, A.Z., and Ruban, A.V. (2008). Photosynthetic acclimation: Does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J. 275: 1069-1079.
31. Horton, P., and Ruban, A.V. (1992). Regulation of photosystem II. Photosynth. Res. 34: 375-385.
32. Horton, P., Ruban, A.V., and Walters, R.G. (1996). Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 655-684.
33. Jahns, P., Latowski, D., and Strzalka, K. (2009). Mechanism and regulation of the violaxanthin cycle: The role of antenna proteins and membrane lipids. Biochim. Blophys. Acta 1787: 3-14.
34. Johnson, M.P., Pérez-Bueno, M.L., Zia, A., Horton, P., and Ruban, A.V. (2009). The zeaxanthin-independent and zeaxanthin-dependent qE components of non-photochemical quenching Involve a common conformational change within the photosystem II antenna in Arabidopsis thaliana. Plant Physiol. 149: 1061-1075.
35. Kramer, D.M., and Sacksteder, C.A. (1998). A diffused-optics flash kinetic spectrophotometer (DOFS) for measurements of absorbance changes in Intact plants in the steady-state. Photosynth. Res. 56: 103-112.
36. 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.
37. Li, X.P., Gilmore, A.M., Caffarri, S., Bassi, R., Golan, T., Kramer, D., and Niyogi, K.K. (2004). Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 279: 22866-22874.
38. Li, X.-P., Phippard, A., Pasari, J., and Niyogi, K.K. (2002). Structurefunction analysis of photosystem II subunit S (PsbS). Funct. Plant Biol. 29: 1131-1139.
39. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J.P., Gui, L., An, X., and Chang, W. (2004). Crystal structure of spinach major light-harvesting complex at 2.72 Â resolution. Nature 428: 287-292.
40. Lokstein, H., Tian, L., Polie, J.E.W., and DellaPenna, D. (2002). Xanthophyll blosynthetic mutants of Arabidopsis thaliana: Altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in photosystem II antenna size and stability. Biochim. Biophys. Acta 1553: 309-319.
41. Maresca, J.A., Graham, J.E., Wu, M., Eisen, J.A., and Bryant, D.A. (2007). Identification of a fourth family of lycopene cyclases in photosynthetic bacteria. Proc. Natl. Acad. Sci. USA 104: 11784-11789.
42. Mortensen, A., and Skibsted, L.H. (1997). Importance of carotenoid structure in radical-scavenging reactions. J. Agrlcult. Food Chem. 45: 2970-2977.
43. 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.
44. Müller, P., Li, X.P., and Niyogi, K.K. (2001). Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125: 1558-1566.
45. Müller-Moulé, P., Conklin, P.L., and Niyogi, K.K. (2002). Ascorbate deficiency can limit violaxanthin de-epoxldase activity in vivo. Plant Physiol. 128: 970-977.
46. Niyogi, K.K. (1999). Photoprotection revisited: Genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 333-359.
47. Niyogi, K.K. (2000). Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3: 455-460.
48. Niyogi, K.K., Bjorkman, O., and Grossman, A.R. (1997). The roles of specific xanthophylls in photoprotection. Proc. Natl. Acad. Sci. USA 94: 14162-14167.
49. Niyogi, K.K., Grossman, A.R., and 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.
50. Niyogi, K.K., Shih, C., Soon Chow, W., 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.
51. Noctor, G., Rees, D., Young, A., and Horton, P. (1991). The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence, and trans-thylakold pH gradient in isolated chloroplasts. Blochim. Biophys. Acta 1057: 320-330.
52. North, H.M., De Almeida, A., Boutin, J.P., Frey, A., To, A., Botran, L., Sotta, B., and Marion-Poll, A. (2007). The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. Plant J. 50: 810-824.
53. Pascal, A.A., Liu, Z., Broess, K., van Oort, B., van Amerongen, H., Wang, C, Horton, P., Robert, B., Chang, W., and Ruban, A. (2005). Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134-137.
54. Pagano, A., Cinque, G., and Bassi, R. (1998). In vitro reconstitution of the recombinant photosystem II light-harvesting complex CP24 and its spectroscopic characterization. J. Biol. Chem. 273: 17154-17165.
55. Pecker, I., Gabbay, R., Cunningham, F.X., and Hirschberg, J. (1996). Cloning and characterization of the cDNA for lycopene beta-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol. Biol. 30:807-819.
56. Peterson, R.B., and Havir, E.A. (2000). A nonphotochemical- quenchlngdeficient mutant of Arabidopsis thaliana possessing normal pigment composition and xanthophyll-cycle activity. Planta 210: 205-214.
57. Pogson, B., McDonald, K.A., Truong, M., Britton, G., and DellaPenna, D. (1996). Arabidopsis carotenoid mutants demonstrate that lutein Is not essential for photosynthesis in higher plants. Plant Cell 8: 1627-1639.
58. 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. USA 95: 13324-13329.
59. Pogson, B.J., and Rissler, H.M. (2000). Genetic manipulation of carotenoid biosynthesis and photoprotection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355: 1395-1403.
60. Polivka, T., Zigmantas, D., Sundstrom, V., Formaggio, E., Cinque, G., and Bassi, R. (2002). Carotenoid 3-1 state in a recombinant lightharvesting complex of photosystem II. Biochemistry 41: 439-450.
61. Ronen, G., Carmel-Goren, L., Zamir, D., and Hirschberg, J. (2000). An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. Proc. Natl. Acad. Sci. USA 97: 11102-11107.
62. Ruban, A.V., Berera, R., Ilioaia, C., van Stokkum, I.H.M., Kennis, J.T. M., Pascal, A.A., van Amerongen, H., Robert, B., Horton, P., and van Grondelle, R. (2007). Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450: 575-578.
63. Ruban, A.V., Lee, P.J., Wentworth, M., Young, A.J., and 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.
64. Ruban, A.V., Pascal, A.A., Robert, B., and Horton, P. (2002). Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting. J. Blol. Chem. 277: 7785-7789.
65. Ruban, A.V., Young, A.J., and Horton, P. (1993). Induction of nonphotochemical energy-dissipation and absórbanos changes in leaves: Evidence for changes in the state of the light-harvesting system of photosystem II In vivo. Plant Physiol. 102: 741-750.
66. Sacksteder, CA., Jacoby, M.E., and Kramer, D.M. (2001). A portable, non-focusing optics spectrophotometer (NoFOSpec) for measurements of steady-state absorbanos changes in intact plants. Photosynth. Res. 70: 231-240.
67. Stickforth, P., Steiger, S., Hess, W.R., and Sandmann, G. (2003). A novel type of lycopene epsilon-cyclase in the marine cyanobacterium Prochlorococcus marinus MED4. Arch. Microbiol. 179: 409-415.
68. Tracewell, CA., and Brudvig, G.W. (2003). Two redox-active betacarotene molecules in photosystem II. Biochemistry 42: 9127-9136.
69. Yamamoto, H.Y., Bugos, R.C., and Hieber, A.D. (1999). Biochemistry and molecular biology of the xanthophyll cycle. In The Photochemistry of Carotenoids, H.A. Frank, A.J. Young, G. Britton, and R.J. Cogdell, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 293-303.
70. Yu, B.Y., Lydiate, D.J., Schafer, U.A., and Hannoufa, A. (2007). Characterization of a beta-carotene hydroxylase of Adonis aestivalis and its expression in Arabidopsis thaliana. Planta 226: 181-192.