Photosynthetica 2004, 42(3):323-337 | DOI: 10.1023/B:PHOT.0000046149.97220.18

Non-Radiative Dissipation of Absorbed Excitation Energy Within Photosynthetic Apparatus of Higher Plants

M. ©troch1, V. ©punda1,2, I. Kurasová1
1 Department of Physics, Faculty of Science, Ostrava University, Czech Republic
2 Institute of Physical Biology, University of South Bohemia, Czech Republic

The review deals with thermal dissipation of absorbed excitation energy within pigment-protein complexes of thylakoid membranes in higher plants. We focus on the de-excitation regulatory processes within photosystem 2 (PS2) that can be monitored as non-photochemical quenching of chlorophyll (Chl) a fluorescence consisting of three components known as energy-dependent quenching (qE), state-transition quenching (qT), and photoinhibitory quenching (qI). We summarize the role of thylakoid lumen pH, xanthophylls, and PS2 proteins in qE mechanism. Further, both the similarity between qE and qI and specific features of qI are described. The other routes of thermal energy dissipation are also mentioned, that is dissipation within photosystem 1 and dissipation through the triplet Chl pathway. The significance of the individual de-excitation processes in protection against photo-oxidative damage to the photosynthetic apparatus under excess photon supply is stretched.

Additional key words: carotenoids; non-photochemical fluorescence quenching; non-radiative dissipation; photoinhibition; photo-protection; photosynthesis; xanthophyll cycle

Published: September 1, 2004  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
©troch, M., ©punda, V., & Kurasová, I. (2004). Non-Radiative Dissipation of Absorbed Excitation Energy Within Photosynthetic Apparatus of Higher Plants. Photosynthetica42(3), 323-337. doi: 10.1023/B:PHOT.0000046149.97220.18
Download citation

References

  1. Adams, W.W., III, Demmig-Adams, B., Logan, B.A., Barker, D.H., Osmond, C.B.: Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understory of an open Eucalyptus forest.-Plant Cell Environ. 22: 125-136, 1999. Go to original source...
  2. Adams, W.W., III, Demmig-Adams, B., Rosenstiel, T.N., Ebbert, V.: Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter.-Photosynth. Res. 67: 51-62, 2001. Go to original source...
  3. Allen, J.F., Forsberg, J.: Molecular recognition in thylakoid structure and function.-Trends Plant Sci. 6: 317-326, 2001. Go to original source...
  4. Andersson, B., Aro, E.-M.: Photodamage and D1 protein turn-over in photosystem II.-In: Aro, E.-M., Andersson, B. (ed.): Regulation of Photosynthesis. Pp. 377-393. Kluwer Academic Publ., Dordrecht-Boston-London 2001. Go to original source...
  5. Andersson, J., Walters, R.G., Horton, P., Jansson, S.: Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: Implications for the mechanism of protective energy dissipation.-Plant Cell 13: 1193-1204, 2001. Go to original source...
  6. Andersson, J., Wentworth, M., Walters, R.G., Howard, C.A., Ruban, A.V., Horton, P., Jansson, S.: Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photo-system II-effects on photosynthesis, grana stacking and fitness.-Plant J. 35: 350-361, 2003. Go to original source...
  7. Aro, E.-M., Virgin, I., Andersson, B.: Photoinhibition of Photo-system II. Inactivation, protein damage and turnover.-Biochim. biophys. Acta 1143: 113-134, 1993. Go to original source...
  8. Asada, K.: 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, 1999. Go to original source...
  9. Asada, K.: The water-water cycle as alternative photon and electron sinks.-Phil. Trans. roy. Soc. London B 355: 1419-1431, 2000. Go to original source...
  10. Aspinall-O'Dea, M., Wentworth, M., Pascal, A., Robert, B., Ruban, A., Horton, P.: In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants.-Proc. nat. Acad. Sci. USA 99: 16331-16335, 2002. Go to original source...
  11. Baier, M., Dietz, K.-J.: Alkyl hydroperoxide reductases: the way out of the oxidative breakdown of lipids in chloroplasts.-Trends Plant Sci. 4: 166-168, 1999. Go to original source...
  12. Bailey, S., Walters, R.G., Jansson, S., Horton, P.: Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses.-Planta 213: 794-801, 2001. Go to original source...
  13. Barnes, J.D., Cardoso-Vilhena, J.: Interactions between electro-magnetic radiation and the plant cuticle.-In: Kerstiens, G. (ed.): Plant Cuticles and Integrated Functional Approach. Pp. 157-174. BIOS Scientific Publishers, Oxford 1996.
  14. Baroli, I., Do, A.D., Yamane, T., Niyogi, K.K.: Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress.-Plant Cell 15: 992-1008, 2003. Go to original source...
  15. Baroli, I., Niyogi, K.K.: Molecular genetics of xanthophyll-de-pendent photoprotection in green algae and plants.-Phil. Trans. roy. Soc. London B 355: 1385-1394, 2000. Go to original source...
  16. Barth, C., Krause, G.H., Winter, K.: Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves.-Plant Cell Environ. 24: 163-176, 2001. Go to original source...
  17. Bassi, R., Caffarri, S.: Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls.-Photosynth. Res. 64: 243-256, 2000. Go to original source...
  18. Bassi, R., Pineau, B., Dainese, P., Marquardt, J.: Carotenoid-binding proteins of photosystem II.-Eur. J. Biochem. 212: 297-303, 1993. Go to original source...
  19. Bilger, W., Björkman, O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced ab-sorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis.-Photosynth. Res. 25: 173-185, 1990. Go to original source...
  20. Bilger, W., Björkman, O.: Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and non-photochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.).-Planta 193: 238-246, 1994. Go to original source...
  21. Björkman, O., Demmig-Adams, B.: Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants.-In: Schulze, E.-D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 17-47. Springer-Verlag, Berlin 1994. Go to original source...
  22. Brugnoli, E., Scartazza, A., De Tullio, M.C., Monteverdi, M.C., Lauteri, M., Augusti, A.: Zeaxanthin and non-photochemical quenching in sun and shade leaves of C3 and C4 plants.-Physiol. Plant. 104: 727-734, 1998. Go to original source...
  23. Bukhov, N.G., Carpentier, R.: Measurement of photochemical quenching of absorbed quanta in photosystem I of intact leaves using simultaneous measurements of absorbance changes at 830 nm and thermal dissipation.-Planta 216: 630-638, 2003. Go to original source...
  24. Bukhov, N.G., Heber, U., Wiese, C., Shuvalov, V.A.: Energy dissipation in photosynthesis: Does the quenching of chlorophyll fluorescence originate from antenna complexes of photosystem II or from the reaction center?-Planta 212: 749-758, 2001. Go to original source...
  25. Chang, S.-H., Bugos, R.C., Sun, W.-H., Yamamoto, H.Y.: Anti-sense suppression of violaxanthin de-epoxidase in tobacco does not affect plant performance in controlled growth conditions.-Photosynth. Res. 64: 95-103, 2000. Go to original source...
  26. Choudhury, N.K., Behera, R.K.: Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents.-Photosynthetica 39: 481-488, 2001. Go to original source...
  27. Chow, W.S., Funk, C., Hope, A.B., Govindjee: Greening of intermittent-light-grown bean plants in continuous light: Thylakoid components in relation to photosynthetic performance and capacity for photoprotection.-Indian J. Biochem. Biophys. 37: 395-404, 2000.
  28. Chow, W.S., Lee, H.-Y., Park, Y.-I., Park, Y.-M., Hong, Y.-N., Anderson, J.M.: The role of inactive photosystem-II-mediated quenching in a last-ditch community defence against high light stress in vivo.-Phil. Trans. roy. Soc. London B 357: 1441-1450, 2002. Go to original source...
  29. Croce, R., Weiss, S., Bassi, R.: Carotenoid-binding sites of the major light-harvesting complex II of higher plants.-J. biol. Chem. 274: 29613-29623, 1999. Go to original source...
  30. Croce, R., Zucchelli, G., Garlaschi, F.M., Bassi, R., Jennings, R.C.: Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna.-Biochemistry 35: 8572-8579, 1996. Go to original source...
  31. Crofts, A.R., Yerkes, C.T.: A molecular mechanism for qE-quenching.-FEBS Lett. 352: 265-270, 1994. Go to original source...
  32. Davison, P.A., Hunter, C.N., Horton, P.: Over-expression of â-carotene hydroxylase enhances stress tolerance in Arabidopsis.-Nature 418: 203-206, 2002. Go to original source...
  33. Demmig, B., Winter, K.: Characterisation of three components of non-photochemical fluorescence quenching and their response to photoinhibition.-Aust. J. Plant Physiol. 15: 163-177, 1988. Go to original source...
  34. Demmig, B., Cleland, R.E., Björkman, O.: Photoinhibition, 77 K chlorophyll fluorescence quenching and phosphorylation of the light-harvesting chlorophyll-protein complex of photo-system II in soybean leaves.-Planta 172: 378-385, 1987. Go to original source...
  35. Demmig-Adams, B.: Survey of thermal energy dissipation and pigment composition in sun and shade leaves.-Plant Cell Physiol. 39: 474-482, 1998. Go to original source...
  36. Demmig-Adams, B., Adams, W.W., III: The role of xanthophyll cycle carotenoids in the protection of photosynthesis.-Trends Plant Sci. 1: 21-26, 1996a. Go to original source...
  37. Demmig-Adams, B., Adams, W.W., III: Xanthophyll cycle and light stress in nature: uniform response to excess direct sun-light among higher plant species.-Planta 198: 460-470, 1996b. Go to original source...
  38. Demmig-Adams, B., Adams, W.W., III: Harvesting sunlight safely.-Nature 403: 371-374, 2000. Go to original source...
  39. Demmig-Adams, B., Adams, W.W., III, Barker, D.H., Logan, B.A., Bowling, D.R., Verhoeven, A.S.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.-Physiol. Plant. 98: 253-264, 1996a. Go to original source...
  40. Demmig-Adams, B., Adams, W.W., III, Heber, U., Neimanis, S., Winter, K., Krüger, A., Czygan, F.-C., Bilger, W., Björkman, O.: Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts.-Plant Physiol. 92: 293-301, 1990. Go to original source...
  41. Demmig-Adams, B., Gilmore, A.M., Adams, W.W., III: In vivo functions of carotenoids in higher plants.-FASEB J. 10: 403-412, 1996b. Go to original source...
  42. Demmig-Adams, B., Moeller, D.L., Logan, B.A., Adams, W.W., III: Positive correlation between levels of retained zeaxanthin+ antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill.-Planta 205: 367-374, 1998. Go to original source...
  43. Dominici, P., Caffarri, S., Armenante, F., Ceoldo, S., Crimi, M., Bassi, R.: Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant.-J. biol. Chem. 277: 22750-22758, 2002. Go to original source...
  44. Ebbert, V., Demmig-Adams, B., Adams, W.W., III, Mueh, K.E., Staehelin, L.A.: Correlation between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation.-Photosynth. Res. 67: 63-78, 2001. Go to original source...
  45. Ebbert, V., Godde, D.: Regulation of thylakoid protein phosphorylation in intact chloroplasts by the activity of kinases and phosphatases.-Biochim. biophys. Acta 1187: 335-346, 1994. Go to original source...
  46. Elrad, D., Niyogi, K.K., Grossman, A.R.: A major light-harvesting polypeptide of photosystem II functions in thermal dissipation.-Plant Cell 14: 1801-1816, 2002. Go to original source...
  47. Eskling, M., Arvidsson, P.-O., Åkerlund, H.-E.: The xanthophyll cycle, its regulation and components.-Physiol. Plant. 100: 806-816, 1997. Go to original source...
  48. Färber, A., Young, A.J., Ruban, A.V., Horton, P., Jahns, P.: Dynamics of xanthophyll-cycle activity in different antenna sub-complexes in the photosynthetic membranes of higher plants. The relationship between zeaxanthin conversion and non-photochemical fluorescence quenching.-Plant Physiol. 115: 1609-1618, 1997. Go to original source...
  49. Foyer, C.H., Harbinson, J.: Relationships between antioxidant metabolism and carotenoids in the regulation of photosynthesis.-In: Frank, H.A., Young, A.J., Britton, G., Cogdell, R.J. (ed.): The Photochemistry of Carotenoids. Pp. 305-325. Kluwer Academic Publ., Dordrecht 1999. Go to original source...
  50. Frank, H.A., Bautista, J.A., Josue, J.S., Young, A.J.: Mechanism of non-photochemical quenching in green plants: energies of the lowest excited singlet states of violaxanthin and zeaxanthin.-Biochemistry 39: 2831-2837, 2000. Go to original source...
  51. Frank, H.A., Cua, A., Chynwat, V., Young, A., Gosztola, D., Wasielewski, M.R.: Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis.-Photo-synth. Res. 41: 389-395, 1994. Go to original source...
  52. García-Plazaola, J.I., Becerril, J.M.: Photoprotection mechanisms in European beech (Fagus sylvatica L.) seedlings from diverse climatic origins.-Trees 14: 339-343, 2000. Go to original source...
  53. Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves.-Physiol. Plant. 99: 197-209, 1997. Go to original source...
  54. Gilmore, A.M., Ball, M.C.: Protection and storage of chlorophyll in overwintering evergreens.-Proc. nat. Acad. Sci. USA 97: 11098-11101, 2000. Go to original source...
  55. Gilmore, A.M., Yamamoto, H.Y.: Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP.-Proc. nat. Acad. Sci. USA 89: 1899-1903, 1992. Go to original source...
  56. Gilmore, A.M., Yamamoto, H.Y.: Linear models relating xanthophylls and lumen acidity to non-photochemical fluo-rescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching.-Photosynth. Res. 35: 67-78, 1993. Go to original source...
  57. Gilmore, A.M., Yamamoto, H.Y.: Time-resolution of the antheraxanthin-and pH-dependent chlorophyll a fluorescence components associated with photosystem II energy dissipation in Mantoniella squamata.-Photochem. Photobiol. 74: 291-302, 2001. Go to original source...
  58. Goss, R., Böhme, K., Wilhelm, C.: The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxan-thin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical energy dissipation.-Planta 205: 613-621, 1998. Go to original source...
  59. Grace, S.C., Logan, B.A.: Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species.-Plant Physiol. 112: 1631-1640, 1996. Go to original source...
  60. Graßes, T., Pesaresi, P., Schiavon, F., Varotto, C., Salamini, F., Jahns, P., Leister, D.: The role of pH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana.-Plant Physiol. Biochem. 40: 41-49, 2002.
  61. Haldrup, A., Jensen, P.E., Lunde, C., Scheller, H.V.: Balance of power: a view of the mechanism of photosynthetic state transitions.-Trends Plant Sci. 6: 301-305, 2001. Go to original source...
  62. Hansen, U., Fiedler, B., Rank, B.: Variation of pigment composition and antioxidative systems along the canopy light gra-dient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance.-Trees 16: 354-364, 2002. Go to original source...
  63. Havaux, M., Bonfils, J.-P., Lütz, C., Niyogi, K.K.: 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 de-epoxidase.-Plant Physiol. 124: 273-284, 2000. Go to original source...
  64. Havaux, M., Niyogi, K.K.: The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism.-Proc. nat. Acad. Sci. USA 96: 8762-8767, 1999. Go to original source...
  65. Heber, U., Walker, D.: Concerning a dual function of coupled cyclic electron transport in leaves.-Plant Physiol. 100: 1621-1626, 1992. Go to original source...
  66. Horton, P., Hague, A.: Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching.-Biochim. biophys. Acta 932: 107-115, 1988. Go to original source...
  67. Horton, P., Lee, P.J.: Phosphorylation of chloroplast membrane proteins partially protects against photoinhibition.-Planta 165: 37-42, 1985. Go to original source...
  68. Horton, P., Ruban, A.V., Rees, D., Pascal, A.A., Noctor, G., Young, A.J.: Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex.-FEBS Lett. 292: 1-4, 1991. Go to original source...
  69. Horton, P., Ruban, A.V., Walters, R.G.: Regulation of light harvesting in green plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 655-684, 1996. Go to original source...
  70. Huner, N.P.A., Öquist, G., Hurry, V.M., Król, M., Falk, S., Griffith, M.: Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants.-Photosynth. Res. 37: 19-39, 1993. Go to original source...
  71. Ivanov, A.G., Sane, P.V., Hurry, V., Król, M., Sveshnikov, D., Huner, N.P.A., Öquist, G.: Low-temperature modulation of the redox properties of the acceptor side of photosystem II: photoprotection through reaction centre quenching of excess energy.-Physiol. Plant. 119: 376-383, 2003. Go to original source...
  72. Ivanov, A.G., Sane, P.V., Zeinalov, Y., Simidjiev, I., Huner, N.P.A., Öquist, G.: Seasonal responses of photosynthetic electron transport in Scots pine (Pinus sylvestris L.) studied by thermoluminescence.-Planta 215: 457-465, 2002. Go to original source...
  73. Jahns, P., Miehe, B.: Kinetic correlation of recovery from photoinhibition and zeaxanthin epoxidation.-Planta 198: 202-210, 1996. Go to original source...
  74. Jin, E.S., Polle, J.E.W., Melis, A.: Involvement of zeaxanthin and of the Cbr protein in the repair of photosystem II from photoinhibition in the green alga Dunaliella salina.-Biochim. biophys. Acta 1506: 244-259, 2001. Go to original source...
  75. Jin, E.S., Yokthongwattana, K., Polle, J.E.W., Melis, A.: Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina.-Plant Physiol. 132: 352-364, 2003. Go to original source...
  76. Josue, J.S., Frank, H.A.: Direct determination of the S1 excited-state energies of xanthophylls by low-temperature fluorescence spectroscopy.-J. phys. Chem. A 106: 4815-4824, 2002. Go to original source...
  77. Kalina, J., É ajánek, M., ©punda, V., Marek, M.V.: Changes of the primary photosynthetic reactions of Norway spruce under elevated CO2.-In: Mohren, G.M.J., Kramer, K., Sabaté, S. (ed.): Impacts of Global Change on Tree Physiology and Forest Ecosystems. Pp. 59-66. Kluwer Academic Publ., Dordrecht-Boston-London 1997. Go to original source...
  78. Kautsky, H., Hirsch, A.: Neue Versuche zur Kohlensäure-assimilation.-Naturwissenschaften 19: 964, 1931. Go to original source...
  79. Krause, G.H.: Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms.-Physiol. Plant. 74: 566-574, 1988. Go to original source...
  80. Krieger, A., Moya, I., Weis, E.: Energy-dependent quenching of chlorophyll a fluorescence: effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid mem-branes and Photosystem II preparations.-Biochim. biophys. Acta 1102: 167-176, 1992. Go to original source...
  81. Külheim, C., Ågren, J., Jansson, S.: Rapid regulation of light harvesting and plant fitness in the field.-Science 297: 91-93, 2002. Go to original source...
  82. Kurasová, I., É ajánek, M., Kalina, J., Urban, O., ©punda, V.: Characterization of acclimation of Hordeum vulgare to high irradiation based on different responses of photosynthetic activity and pigment composition.-Photosynth. Res. 72: 71-83, 2002. Go to original source...
  83. Kurasová, I., Kalina, J., Urban, O., ©troch, M., ©punda, V.: Acclimation of two distinct plant species, spring barley and Norway spruce, to combined effect of various irradiance and CO2 concentration during cultivation in controlled environment.-Photosynthetica 41: 513-523, 2003. Go to original source...
  84. Lee, A.I., Thornber, J.P.: Analysis of the pigment stoichiometry of pigment-protein complexes from barley (Hordeum vulgare). The xanthophyll cycle intermediates occur mainly in the light-harvesting complexes of photosystem I and photosystem II.-Plant Physiol. 107: 565-574, 1995. Go to original source...
  85. Lee, H.-Y., Hong, Y.-N., Chow, W.S.: Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves.-Planta 212: 332-342, 2001. Go to original source...
  86. Li, X.-P., Björkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., Niyogi, K.K.: A pigment-binding protein essential for regulation of photosynthetic light harvesting.-Nature 403: 391-395, 2000. Go to original source...
  87. Li, X.-P., Gilmore, A.M., Niyogi, K.K.: Molecular and global time-resolved analysis of a psbS gene dosage effect on pH-and xanthophyll cycle-dependent non-photochemical quenching in photosystem II.-J. biol. Chem. 277: 33590-33597, 2002a. Go to original source...
  88. Li, X.-P., Müller-Moulé, P., Gilmore, A.M., Niyogi, K.K.: PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition.-Proc. nat. Acad. Sci. USA 99: 15222-15227, 2002b. Go to original source...
  89. Li, X.-P., Phippard, A., Pasari, J., Niyogi, K.K.: Structure-function analysis of photosystem II subunit S (PsbS) in vivo.-Funct. Plant Biol. 29: 1131-1139, 2002c. Go to original source...
  90. Logan, B.A., Barker, D.H., Demmig-Adams, B., Adams, W.W., III: Acclimation of leaf carotenoid composition and ascorbate levels to gradients in the light environment within an Australian rainforest.-Plant Cell Environ. 19: 1083-1090, 1996. Go to original source...
  91. Logan, B.A., Demmig-Adams, B., Adams, W.W., III, Grace, S.C.: Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field.-J. exp. Bot. 49: 1869-1879, 1998a. Go to original source...
  92. Logan, B.A., Grace, S.C., Adams, W.W., III, Demmig-Adams, B.: Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments.-Oecologia 116: 9-17, 1998b. Go to original source...
  93. Lokstein, H., Tian, L., Polle, J.E.W., DellaPenna, D.: Xanthophyll biosynthetic 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, 2002. Go to original source...
  94. Ma, Y.-Z., Holt, N.E., Li, X.-P., Niyogi, K.K., Fleming, G.R.: Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting.-Proc. nat. Acad. Sci. USA 100: 4377-4382, 2003. Go to original source...
  95. Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence-a practical guide.-J. exp. Bot. 51: 659-668, 2000. Go to original source...
  96. McCormac, D.J., Bruce, D., Greenberg, B.M.: State transitions, light-harvesting antenna phosphorylation and light-harvesting antenna migration in vivo in the higher plant Spriodela oli-gorrhiza.-Biochim. biophys. Acta 1187: 301-312, 1994. Go to original source...
  97. Melis, A.: Photostasis in plants. Mechanisms and regulation.-In: Williams, T.P., Thistle, A.B. (ed.): Photostasis and Related Phenomena. Pp. 207-221. Plenum Press, New York 1998. Go to original source...
  98. Miyake, C., Okamura, M.: Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts.-Plant Cell Physiol. 44: 457-462, 2003. Go to original source...
  99. Morosinotto, T., Caffarri, S., Dall'Osto, L., Bassi, R.: Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids.-Physiol. Plant. 119: 347-354, 2003. Go to original source...
  100. Moya, I., Silvestri, M., Vallon, O., Cinque, G., Bassi, R.: Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes.-Biochemistry 40: 12552-12561, 2001. Go to original source...
  101. Müller, P., Li, X.-P., Niyogi, K.K.: Non-photochemical quenching. A response to excess light energy.-Plant Physiol. 125: 1558-1566, 2001. Go to original source...
  102. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., Shikanai, T.: PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis.-Cell 110: 361-371, 2002. Go to original source...
  103. Munné-Bosch, S., Alegre, L.: The function of tocopherols and tocotrienols in plants.-Crit. Rev. Plant Sci. 21: 31-57, 2002. Go to original source...
  104. Niyogi, K.K.: Photoprotection revisited: Genetic and molecular approaches.-Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 333-359, 1999. Go to original source...
  105. Niyogi, K.K.: Safety valves for photosynthesis.-Curr. Opin. Plant Biol. 3: 455-460, 2000. Go to original source...
  106. Niyogi, K.K., Björkman, O., Grossman, A.R.: Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching.-Plant Cell 9: 1369-1380, 1997a. Go to original source...
  107. Niyogi, K.K., Björkman, O., Grossman, A.R.: The roles of spe-cific xanthophylls in photoprotection.-Proc. nat. Acad. Sci. USA 94: 14162-14167, 1997b. Go to original source...
  108. Niyogi, K.K., Grossman, A.R., Björkman, O.: Arabidopsis mu-tants define a central role for the xanthophyll cycle in the re-gulation of photosynthetic energy conversion.-Plant Cell 10: 1121-1134, 1998. Go to original source...
  109. Niyogi, K.K., Shih, C., Chow, W.S., Pogson, B.J., DellaPenna, D., Björkman, O.: Photoprotection in a zeaxanthin-and lu-tein-deficient double mutant of Arabidopsis.-Photosynth. Res. 67: 139-145, 2001. Go to original source...
  110. Noctor, G., Foyer, C.H.: Ascorbate and glutathione: Keeping active oxygen under control.-Annu. Rev. Plant Physiol. Plant mol. Biol. 49: 249-279, 1998. Go to original source...
  111. Noguchi, T.: Dual role of triplet localization on the accessory chlorophyll in the photosystem II reaction center: photo-protection and photodamage of the D1 protein.-Plant Cell Physiol. 43: 1112-1116, 2002. Go to original source...
  112. Nuijs, A.M., Shuvalov, V.A., van Gorkom, H.J., Plijter, J.J., Duysens, L.N.M.: Picosecond absorbance difference spectroscopy on the primary reactions and the antenna-excited states in Photosystem I particles.-Biochim. biophys. Acta 850: 310-318, 1986. Go to original source...
  113. Öquist, G., Anderson, J.M., McCaffery, S., Chow, W.S.: Mechanistic differences in photoinhibition of sun and shade plants.-Planta 188: 422-431, 1992a. Go to original source...
  114. Öquist, G., Chow, W.S., Anderson, J.M.: Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II.-Planta 186: 450-460, 1992b. Go to original source...
  115. Ort, D.R., Baker, N.R.: A photoprotective role for O2 as an alternative electron sink in photosynthesis?-Curr. Opin. Plant Biol. 5: 193-198, 2002. Go to original source...
  116. Ottander, C., Campbell, D., Öquist, G.: Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris.-Planta 197: 176-183, 1995. Go to original source...
  117. Owens, T.G.: Processing of excitation energy by antenna pigments.-In: Baker, N.R. (ed.): Photosynthesis and the Environment. Pp. 1-23. Kluwer Academic Publ., Dordrecht-Boston-London 1996. Go to original source...
  118. Park, Y.-I., Chow, W.S., Anderson, J.M., Hurry, V.M.: Differential susceptibility of photosystem II to light stress in light-acclimated pea leaves depends on the capacity for photo-chemical and non-radiative dissipation of light.-Plant Sci. 115: 137-149, 1996. Go to original source...
  119. Peltier, G., Cournac, L.: Chlororespiration.-Annu. Rev. Plant Biol. 53: 523-550, 2002. Go to original source...
  120. Pesaresi, P., Sandona, D., Giuffra, E., Bassi, R.: A single point mutation (E166Q) prevents dicyclohexylcarbodiimide binding to the photosystem II subunit CP29.-FEBS Lett. 402: 151-156, 1997. Go to original source...
  121. Peterman, E.J.G., Dukker, F.M., van Grondelle, R., van Amerongen, H.: Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants.-Biophys. J. 69: 2670-2678, 1995. Go to original source...
  122. Peterman, E.J.G., Gradinaru, C.C., Calkoen, F., Borst, J.C., van Grondelle, R., van Amerongen, H.: Xanthophylls in light-harvesting complex II of higher plants: Light harvesting and triplet quenching.-Biochemistry 36: 12208-12215, 1997. Go to original source...
  123. Pfündel, E., Bilger, W.: Regulation and possible function of the violaxanthin cycle.-Photosynth. Res. 42: 89-109, 1994. Go to original source...
  124. Pogson, B.J., Niyogi, K.K., Björkman, O., DellaPenna, D.: Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants.-Proc. nat. Acad. Sci. USA 95: 13324-13329, 1998. Go to original source...
  125. Pogson, B.J., Rissler, H.M.: Genetic manipulation of carotenoid biosynthesis and photoprotection.-Phil. Trans. roy. Soc. London B 355: 1395-1403, 2000. Go to original source...
  126. Polívka, T., Herek, J.L., Zigmantas, D., ÅÅkerlund, H.-E., Sundström, V.: Direct observation of the (forbidden) S1 state in carotenoids.-Proc. nat. Acad. Sci. USA 96: 4914-4917, 1999. Go to original source...
  127. Polívka, T., Zigmantas, D., Sundström, V., Formaggio, E., Cinque, G., Bassi, R.: Carotenoid S1 state in a recombinant light-harvesting complex of photosystem II.-Biochemistry 41: 439-450, 2002. Go to original source...
  128. Pospí¹il, P.: Mechanisms of non-photochemical chlorophyll fluorescence quenching in higher plants.-Photosynthetica 34: 343-355, 1997. Go to original source...
  129. Pursiheimo, S., Mulo, P., Rintamäki, E., Aro, E.-M.: Coregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye.-Plant J. 26: 317-327, 2001. Go to original source...
  130. Quick, W.P., Stitt, M.: An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves.-Biochim. biophys. Acta 977: 287-296, 1989. Go to original source...
  131. Richter, M., Goss, R., Wagner, B., Holzwarth, A.R.: Characterization of the fast and slow reversible components of non-photochemical quenching in isolated pea thylakoids by pico-second time-resolved chlorophyll fluorescence analysis.-Biochemistry 38: 12718-12726, 1999. Go to original source...
  132. Rintamäki, E., Salonen, M., Suoranta, U.-M., Carlberg, I., Andersson, B., Aro, E.-M.: Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phos-phoproteins.-J. biol. Chem. 272: 30476-30482, 1997. Go to original source...
  133. Rohá É ek, K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships.-Photosynthetica 40: 13-29, 2002.
  134. Rohá É ek, K., Barták, M.: Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications.-Photosynthetica 37: 339-363, 1999.
  135. Ruban, A.V., Horton, P.: An investigation of the sustained component of nonphotochemical quenching of chlorophyll fluorescence in isolated chloroplasts and leaves of spinach.-Plant Physiol. 108: 721-726, 1995. Go to original source...
  136. Ruban, A.V., Pascal, A.A., Robert, B., Horton, P.: Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting.-J. biol. Chem. 277: 7785-7789, 2002. Go to original source...
  137. Ruban, A.V., Young, A.J., Horton, P.: Induction of non-photochemical energy dissipation and absorbance changes in leaves. Evidence for changes in the state of the light-harvesting system of photosystem II in vivo.-Plant Physiol. 102: 741-750, 1993. Go to original source...
  138. Sane, P.V., Ivanov, A.G., Hurry, V., Huner, N.P.A., Öquist, G.: Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis.-Plant Physiol. 132: 2144-2151, 2003. Go to original source...
  139. Savitch, L.V., Leonardos, E.D., Krol, M., Jansson, S., Grodzinski, B., Huner, N.P.A., Öquist, G.: Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation.-Plant Cell Environ. 25: 761-771, 2002. Go to original source...
  140. Schreiber, U., Schliwa, U., Bilger, W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. - Photosynth. Res. 10: 51-62, 1986. Go to original source...
  141. Siefermann-Harms, D.: The light-harvesting and protective functions of carotenoids in photosynthetic membranes.-Physiol. Plant. 69: 561-568, 1987. Go to original source...
  142. Sonoike, K.: Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants.-Plant Cell Physiol. 37: 239-247, 1996. Go to original source...
  143. ©punda, V., É ajánek, M., Kalina, J., Lachetová, I., ©prtová, M., Marek, M.V.: Mechanistic differences in utilization of ab-sorbed excitation energy within photosynthetic apparatus of Norway spruce induced by the vertical distribution of photosynthetically active radiation through the tree crown.-Plant Sci. 133: 155-165, 1998a. Go to original source...
  144. ©punda, V., Kalina, J., É ajánek, M., Pavlí É ková, H., Marek, M.V.: Long-term exposure of Norway spruce to elevated CO2 concentration induces changes in photosystem II mimicking an adaptation to increased irradiance.-J. Plant Physiol. 152: 413-419, 1998b. Go to original source...
  145. Sun, W.-H., Verhoeven, A.S., Bugos, R.C., Yamamoto, H.Y.: Suppression of zeaxanthin formation does not reduce photosynthesis and growth of transgenic tobacco under field conditions.-Photosynth. Res. 67: 41-50, 2001. Go to original source...
  146. Swiatek, M., Kuras, R., Sokolenko, A., Higgs, D., Olive, J., Cinque, G., Müller, B., Eichacker, L.A., Stern, D.B., Bassi, R., Herrmann, R.G., Wollman, F.-A.: The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture.-Plant Cell 13: 1347-1367, 2001. Go to original source...
  147. Tardy, F., Havaux, M.: Thylakoid membrane fluidity and ther-mostability during the operation of the xanthophyll cycle in higher-plant chloroplasts.-Biochim. biophys. Acta 1330: 179-193, 1997. Go to original source...
  148. Telfer, A.: What is â-carotene doing in the photosystem II reaction centre?-Phil. Trans. roy. Soc. London B 357: 1431-1440, 2002. Go to original source...
  149. Thayer, S.S., Björkman, O.: Carotenoid distribution and de-epoxidation in thylakoid pigment-protein complexes from cotton leaves and bundle-sheath cells of maize.-Photosynth. Res. 33: 213-225, 1992. Go to original source...
  150. Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B.: Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress.-Physiol. Plant. 96: 567-576, 1996. Go to original source...
  151. Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B.: Two forms of sustained xanthophyll cycle-dependent energy dissipation in over-wintering Euonymus kiautschovicus.-Plant Cell Environ. 21: 893-903, 1998. Go to original source...
  152. Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B.: The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress.-Oecologia 118: 277-287, 1999a. Go to original source...
  153. Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B., Croce, R., Bassi, R.: Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca major.-Plant Physiol. 120: 727-737, 1999b. Go to original source...
  154. Verhoeven, A.S., Bugos, R.C., Yamamoto, H.Y.: Transgenic tobacco with suppressed zeaxanthin formation is susceptible to stress-induced photoinhibition.-Photosynth. Res. 67: 27-39, 2001. Go to original source...
  155. Wada, M., Kagawa, T., Sato, Y.: Chloroplast movement.-Annu. Rev. Plant Biol. 54: 455-468, 2003. Go to original source...
  156. Walters, R.G., Horton, P.: Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves.-Photosynth. Res. 27: 121-133, 1991. Go to original source...
  157. Walters, R.G., Ruban, A.V., Horton, P.: Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by dicyclo-hexylcarbodiimide during inhibition of energy dissipation.-Eur. J. Biochem. 226: 1063-1069, 1994. Go to original source...
  158. Walters, R.G., Ruban, A.V., Horton, P.: Identification of proton-active residues in a higher plant light-harvesting complex.-Proc. nat. Acad. Sci. USA 93: 14204-14209, 1996. Go to original source...
  159. Weis, E., Berry, J.A.: Quantum efficiency of Photosystem II in relation to "energy"-dependent quenching of chlorophyll fluorescence.-Biochim. biophys. Acta 894: 198-208, 1987. Go to original source...
  160. Wingler, A., Lea, P.J., Quick, W.P., Leegood, R.C.: Photorespiration: metabolic pathways and their role in stress protection.-Phil. Trans. roy. Soc. London B 355: 1517-1529, 2000. Go to original source...
  161. Wollman, F.-A.: State transitions reveal the dynamics and flexibility of the photosynthetic apparatus.-EMBO J. 20: 3623-3630, 2001. Go to original source...
  162. Xu, C.C., Jeon, Y.A., Hwang, H.J., Lee, C.-H.: Suppression of zeaxanthin epoxidation by chloroplast phosphatase inhibitors in rice leaves.-Plant Sci. 146: 27-34, 1999. Go to original source...
  163. Yamamoto, H.Y., Kamite, L.: The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region.-Biochim. biophys. Acta 267: 538-543, 1972. Go to original source...