Photoprotection revisited: Genetic and molecular approaches

Annual Review of Plant Biology

Volumn 50, Issue , 1999, Pages 333-359

  Niyogi, Krishna K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antioxidant; Oxidative stress; Photoinhibition; Photosynthesis; Thermal dissipation

Indexed keywords

ALGAE; CHLOROPHYTA;

EID: 0033506468     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.50.1.333     Document Type: Article

References (161)

1. Alizadeh S, Nechushtai R, Barber J, Nixon P. 1994. Nucleotide sequence of the psbE, psbF and trnM genes from the chloroplast genome of Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1188:439-42
2. Allen JF. 1995. Thylakoid protein phosphorylation, state 1-state 2 transitions, and photosystem stoichiometry adjustment: redox control at multiple levels of gene expression. Physiol. Plant. 93: 196-205
3. Allen RD. 1995. Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol. 107:1049-54
4. Allen RD, Webb RP, Schake SA. 1997. Use of transgenic plants to study antioxidant defenses. Free Rad. Biol. Med. 23:473-79
5. Alscher RG, Donahue JL, Cramer CL. 1997. Reactive oxygen species and antioxidants: relationships in green cells. Physiol. Plant. 100:224-33
6. Anderson IC, Robertson DS. 1960. Role of carotenoids in protecting chlorophyll from photodestruction. Plant Physiol. 35:531-34
7. Anderson JM. 1986. Photoregulation of the composition, function and structure of thylakoid membranes. Annu. Rev. Plant Physiol. 37:93-136
8. Anderson JM, Andersson B. 1988. The dynamic photosynthetic membrane and regulation of solar energy conversion. Trends Biochem. Sci. 13:351-55
9. Anderson JM, Park Y-I, Chow WS. 1997. Photoinactivation and photoprotection of photosystem II in nature. Physiol. Plant. 100:214-23
10. Anderson JM, Park Y-I, Chow WS. 1998. Unifying model for the photoinactivation of Photosystem II in vivo under steady-state photosynthesis. Photosynth. Res. 56:1-13
11. Andersson B, Barber J. 1996. Mechanisms of photodamage and protein degradation during photoinhibition of photosystem II. See Ref. 17a, pp. 101-21
12. Andrews JR, Fryer MJ, Baker NR. 1995. Consequences of LHC II deficiency for photosynthetic regulation in chlorina mutants of barley. Photosynth. Res. 44:81-91
13. Aro E-M, Virgin I, Andersson B. 1993. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143:113-34
14. Artus NN, Somerville SC, Somerville CR. 1986. The biochemistry and cell biology of photorespiration. CRC Crit. Rev. Plant Sci. 4:121-47
15. Asada K. 1994. Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. See Ref. 17b, pp. 129-42
16. Asada K. 1994. Production and action of active oxygen species in photosynthetic tissues. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, ed. CH Foyer, PM Mullineaux, pp. 77-104. Boca Raton: CRC Press
17. Asada K. 1999. The water-water cycle. Annu. Rev. Plant Physiol. Plant Mol. Biol 50:601-39
18. Baker NR, ed. 1996. Photosynthesis and the Environment. Dordrecht: Kluwer
19. Baker NR, Bowyer JR, eds. 1994. Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. Oxford: BIOS Sci. Publ.
20. Barber J, Andersson B. 1992. Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem. Sci. 17:61-66
21. Baroli I, Melis A. 1996. Photoinhibition and repair in Dunaliella sauna acclimated to different growth irradiances. Planta 198:640-46
22. Baroli I, Melis A. 1998. Photoinhibitory damage is modulated by the rate of photosynthesis and by the photosystem II light-harvesting chlorophyll antenna size. Planta 205:288-96
23. Bendall DS, Manasse RS. 1995. Cyclic photophosphorylation and electron transport. Biochim. Biophys. Acta 1229: 23-38
24. Biehler K, Fock H. 1996. Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiol. 112:265-72
25. Bilger W, Björkman O. 1990. Role of the xanthophyll cycle in photoprotection elucidated by measurements of lightinduced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth. Res. 25:173-85
26. Bilger W, Björkman O. 1994. Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and nonphotochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.). Planta 193:238-46
27. Bilger W, Björkman O, Thayer SS. 1989. Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiol. 91:542-51
28. Bishop NI. 1996. The β,ε-carotenoid, lutein, is specifically required for the formation of the oligomeric forms of the light harvesting complex in the green alga, Scenedesmus obliquus. J. Photochem. Photobiol. B: Biol. 36:279-83
29. Bishop NI, Bugla B, Senger H. 1998. Photosynthetic capacity and quantum requirement of three secondary mutants of Scenedesmus obliquus with deletions in carotenoid biosynthesis. Bot. Acta 111 : 231-35
30. Bishop NI, Urbig T, Senger H. 1995. Complete separation of the β,ε-and β,δ-carotenoid biosynthetic pathways by a unique mutation of the lycopene cyclase in the green alga, Scenedesmus obliquus. FEBS Lett. 367:158-62
31. Bishop NI, Wong J. 1974. Photochemical characteristics of a vitamin E deficient mutant of Scenedesmus obliquus. Ber. Dtsch. Bot. Ges. 87:359-71
32. Björkman O. 1981. Responses to different quantumflux densities. In Physiological Plant Ecology I. Responses to the Physical Environment, ed. OL Lange, PS Nobel, CB Osmond, H Ziegler, pp. 57-107. Berlin: Springer-Verlag
33. Björkman O, Demmig-Adams B. 1994. Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In Eco-physiology of Photosynthesis, ed. E-D Schulze, MM Caldwell, pp. 17-47. Berlin: Springer
34. Bossmann B, Knoetzel J, Jansson S. 1997. Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynth. Res. 52: 127-36
35. Bowler C, Van Camp W, Van Montagu M, Inzé D. 1994. Superoxide dismutase in plants. Crut. Rev. Plant Sci. 13:199-218
36. Briantais J-M. 1994. Light-harvesting chlorophyll a-b complex requirement for regulation of Photosystem II photo-chemistry by non-photochemical quenching. Photosynth. Res. 40:287-94
37. Bugos RC, Hieber AD, Yamamoto HY. 1998. Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. J. Biol. Chem. 273:15321-24
38. Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ. 1998. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 17:868-76
39. Chow WS. 1994. Photoprotection and photoinhibitory damage. In Advances in Molecular and Cell Biology, ed. EE Bittar, J Barber, 10:151-96. London: JAI Press
40. Chunaev AS, Mirnaya ON, Maslov VG, Boschetti A. 1991. Chlorophyll b-and loroxanthin-deficient mutants of Chlamydomonas reinhardtii. Photosynthetica 25:291-301
41. Cobbett CS, May MJ, Howden R, Rolls B. 1998. The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant J. 16:73-78
42. Conklin PL, Pallanca JE, Last RL, Smirnoff N. 1997. L-ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtcl. Plant Physiol. 115:1277-85
43. Conklin PL, Williams EH, Last RL. 1996. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc. Natl. Acad. Sci. USA 93:9970-74
44. E-quenching. FEBS Lett. 352:265-70
45. Cunningham FX Jr, Gantt E. 1998. Genes and enzymes of carotenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:557-83
46. Dau H. 1994. Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochem. Photobiol 60:1-23
47. de Jesus MD, Tabatabai F, Chapman DJ. 1989. Taxonomic distribution of copper-zinc Superoxide dismutase in green algae and its phylogenetic importance. J. Phycol. 25:767-72
48. Demmig B, Cleland RE, Björkman O. 1987. Photoinhibition, 77K chlorophyll fluorescence quenching and phosphorylation of the light-harvesting chlorophyll-protein complex of photosystem II in soybean leaves. Planta 172:378-85
49. Demmig-Adams B. 1990. Carotenoids and photoprotection in plants: a role for the xanthophy 11 zeaxanthin. Biochim. Biophys. Acta 1020:1-24
50. Demmig-Adams B, Adams WW III. 1992. Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:599-626
51. Demmig-Adams B, Adams WW III. 1996. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1:21-26
52. Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Bowling DR, Verhoeven AS. 1996. Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol. Plant. 98:253-64
53. Demmig-Adams B, Gilmore AM, Adams WW III. 1996. In vivo functions of carotenoids in higher plants. FASEB J. 10:403-12
54. Demmig-Adams B, Moeller DL, Logan BA, Adams WW III. 1998. Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill. Planta 205:367-74
55. Duckham SC, Linforth RST, Taylor IB. 1991. Abscisic-acid-deficient mutants at the aba gene locus of Arabidopsis thaliana are impaired in the epoxidation of zeaxanthin. Plant Cell Environ. 14:601-6
56. Escoubas J-M, 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 92:10237-41
57. Eskling M, Arvidsson P-O, Åkerlund H-E. 1997. The xanthophyll cycle, its regulation and components. Physiol. Plant. 100:806-16
58. Foote CS. 1976. Photosensitized oxidation and singlet oxygen: consequences in biological systems. In Free Radicals in Biology, ed. WA Pryor, 2:85-133. New York: Academic
59. Foyer CH, Descourvières P, Kunert KJ. 1994. Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ. 17:507-23
60. Foyer CH, Harbinson J. 1994. Oxygen metabolism and the regulation of photosynthetic electron transport. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, ed. CH Foyer, PM Mullineaux, pp. 1-42. Boca Raton: CRC Press
61. Foyer CH, Lelandais M, Kunert KJ. 1994. Photooxidative stress in plants. Physiol. Plant. 92:696-717
62. Frank HA, Cogdell RJ. 1993. The photochemistry and function of carotenoids in photosynthesis. In Carotenoids in Photosynthesis, ed. A Young, G Britton, pp. 252-326. London: Chapman & Hall
63. Frank HA, Cogdell RJ. 1996. Carotenoids in photosynthesis. Photochem. Photobiol. 63:257-64
64. Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR. 1994. Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth. Res. 41:389-95
65. Friedrich T, Steinmüller K, Weiss H. 1995. The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett. 367:107-11
66. Fryer MJ. 1992. The antioxidant effects of thylakoid Vitamin E (α-tocopherol). Plant Cell Environ. 15:381-92
67. Gilmore AM. 1997. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol. Plant. 99:197-209
68. Gilmore AM, Hazlett TL, Debrunner PG, Govindjee. 1996. Photosystem II chlorophyll a fluorescence lifetimes and intensity are independent of the antenna size differences between barley wild-type and chlorina mutants: photochemical quenching and xanthophyll cycle-dependent nonphotochemical quenching of fluorescence. Photosynth. Res. 48: 171-87
69. Grace SC, Logan BA. 1996. Acclimation of foliar antioxidant systems to growth irradiance in three broadleaved evergreen species. Plant Physiol. 112:1631-40
70. Härtel H, Lokstein H. 1995. Relationship between quenching of maximum and dark-level chlorophyll fluorescence in vivo: dependence on Photosystem II antenna size. Biochim. Biophys. Acta 1228:91-94
71. Härtel H, Lokstein H, Grimm B, Rank B. 1996. Kinetic studies on the xanthophyll cycle in barley leaves. Influence of antenna size and relations to non-photochemical chlorophyll fluorescence quenching. Plant Physiol. 110:471-82
72. Havaux M. 1998. Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci. 3:147-51
73. Heber U, Bligny R, Streb P, Douce R. 1996. Photorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinactivation under sunlight. Bot. Acta 109:307-15
74. Heber U, Walker D. 1992. Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol. 100:1621-26
75. Heifetz PB, Lers A, Turpin DH, Gillham NW, Boynton JE, Osmond CB. 1997. dr and spr/sr mutations of Chlamydomonas reinhardtii affecting D1 protein function and synthesis define two independent steps leading to chronic photoinhibition and confer differential fitness. Plant Cell Environ. 20:1145-57
76. Henry A, Powls R, Pennock JF. 1986. Scenedesmus obliquus PS28: a tocopherol-free mutant which cannot form phytol. Biochem. Soc. Trans. 14:958-59
77. Horton P, Ruban AV. 1994. The role of light-harvesting complex II in energy quenching. See Ref. 17b, pp. 111-28
78. Horton P, Ruban AV, Walters RG. 1994. Regulation of light harvesting in green plants. Indication by nonphotochemical quenching of chlorophyll fluorescence. Plant Physiol. 106:415-20
79. Horton P, Ruban AV, Walters RG. 1996. Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:655-84
80. Howden R, Andersen CR, Goldsbrough PB, Cobbett CS. 1995. A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis. Plant Physiol. 107:1067-73
81. Huner NPA, Öquist G, Sarhan F. 1998. Energy balance and acclimation to light and cold. Trends Plant Sci. 3:224-30
82. 6lf in transgenic tobacco increases the excitation pressure on photosystem II without increasing the sensitivity to photoinhibition in vivo. Photosynth. Res. 50:159-69
83. Hurry V, Anderson JM, Chow WS, Osmond CB. 1997. Accumulation of zeaxanthin in abscisic acid-deficient mutants of Arabidopsis does not affect chlorophyll fluorescence quenching or sensitivity to photoinhibition in vivo. Plant Physiol. 113:639-48
84. Jahns P, Miehe B. 1996. Kinetic correlation of recovery from photoinhibition and zeaxanthin epoxidation. Planta 198:202-10
85. Jespersen HM, Kjaersgard IVH, Ostergaard L, Welinder KG. 1997. From sequence analysis of three novel ascorbate peroxidases from Ambidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase. Biochem. J. 326:305-10
86. Kaiser WM. 1979. Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145:377-82
87. Kitayama K, Kitayama M, Togasaki RK. 1995. Characterization of paraquat-resistant mutants of Chlamydomonas reinhardtii. In Photosynthesis: From Light to Biosphere, ed. P Mathis, 3:595-98. Dordrecht: Kluwer
88. Kliebenstein DJ, Monde R-A, Last RL. 1998. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118:637-50
89. Knox JP, Dodge AD. 1985. Singlet oxygen and plants. Phytochemistry 24:889-96
90. Kofer W, Koop H-U, Wanner G, Steinmüller K. 1998. Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Mol. Gen. Genet. 258:166-73
91. Kok B. 1956. On the inhibition of photosynthesis by intense light. Biochim. Biophys. Acta 21:234-44
92. Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC, Karssen CM. 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. 61:385-93
93. Kozaki A, Takeba G. 1996. Photorespiration protects C3 plants from photooxidation. Nature 384:557-60
94. Krause GH. 1988. Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol. Plant. 74:566-74
95. Król M, Spangfort MD, Huner NPA, Öquist G, Gustafsson P, Jansson S. 1995. Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol. 107:873-83
96. Kühlbrandt W, Wang DN, Fujiyoshi Y. 1994. Atomic model of plant light-harvesting complex by electron crystal-lography. Nature 367:614-21
97. Levine RP. 1969. The analysis of photosynthesis using mutant strains of algae and higher plants. Anna. Rev. Plant Physiol. 20:523-40
98. Lindahl M, Yang D-H, 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. 231:503-9
99. Lokstein H, Härtel H, Hoffmann P, Renger G. 1993. Comparison of chlorophyll fluorescence quenching in leaves of wild-type with a chlorophyll-b-less mutant of barley (Hordeum vulgare L.). J. Photochem. Photobiol. B: Biol 19: 217-25
100. Long SP, Humphries S, Falkowski PG. 1994. Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:633-62
101. Lovelock CE, Winter K. 1996. Oxygen-dependent electron transport and protection from photoinhibition in leaves of tropical tree species. Planta 198:580-87
102. Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, et al. 1996. Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J. 15:2331-42
103. Maxwell DP, Laudenbach DE, Huner NPA. 1995. Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol. 109:787-95
104. Mehler AH. 1951. Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 33:65-77
105. Melis A. 1991. Dynamics of photosynthetic membrane composition and function. Biochim. Biophys. Acta 1058:87-106
106. Miyake C, Asada K. 1992. Thylakoidbound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product mondehydroascorbate radicals in thylakoids. Plant Cell Physiol. 33:541-53
107. Monod C, Takahashi Y, Goldschmidt-Clermont M, Rochaix J-D. 1994. The chloroplast ycf8 open reading frame encodes a photosystem II polypeptide which maintains photosynthetic activity under adverse growth conditions. EMBO J. 13:2747-54
108. Moon BY, Higashi S-I, Gombos Z, Murata N. 1995. Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA 92:6219-23
109. Mor TS, Ohad I, Hirschberg J, Pakrasi H. 1995. An unusual organization of the genes encoding cytochrome b-559 in Chlamydomonas reinhardtii: psbE and psbF separately transcribed from different regions of the plastid chromosome. Mol. Gen. Genet. 246:600-4
110. Murray DL, Kohorn BD. 1991. Chloroplasts of Arabidopsis thaliana homozygous for the ch-1 locus lack chlorophyll b, lack stable LHCPII and have stacked thylakoids. Plant Mol. Biol 16:71-79
111. Niyogi KK, Björkman O, Grossman AR. 1997. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9:1369-80
112. Niyogi KK, Björkman O, Grossman AR. 1997. The roles of specific xanthophylls in photoprotection. Proc. Natl. Acad. Sci. USA 94:14162-67
113. Niyogi KK, Grossman AR, Björkman O. 1998. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121-34
114. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol Biol. 49:249-79
115. Norris SR, Barrette TR, DellaPenna D. 1995. Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7:2139-49
116. Ogawa K, Kanematsu S, Takabe K, Asada K. 1995. Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of Superoxide generation (PSI) in spinach chloroplasts: detection by immuno-gold labeling after rapid freezing and substitution method. Plant Cell Physiol. 36:565-73
117. Ohad I, Keren N, Zer H, Gong H, Mor TS, et al. 1994. Light-induced degradation of the photosystem II reaction centre D1 protein in vivo: an integrative approach. See Ref. 17b, pp. 161-77
118. Öquist G, Chow WS, Anderson JM. 1992. Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186:450-60
119. Osmond CB. 1981. Photorespiration and photoinhibition: some implications for the energetics of photosynthesis. Biochim. Biophys. Acta 639:77-98
120. Osmond CB. 1994. What is photoinhibition? Some insights from comparisons of shade and sun plants. See Ref. 17b, pp. 1-24
121. Osmond CB, Grace SC. 1995. Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J. Exp. Bot. 46:1351-62
122. Owens TG. 1994. Excitation energy transfer between chlorophylls and carotenoids. A proposed molecular mechanism for non-photochemical quenching. See Ref. 17b, pp. 95-109
123. Owens TG. 1996. Processing of excitation energy by antenna pigments. See Ref. 17a, pp. 1-23
124. Park Y-I, Anderson JM, Chow WS. 1996. Photoinactivation of functional photosystem II and Dl-protein synthesis in vivo are independent of the modulation of the photosynthetic apparatus by growth irradiance. Planta 198:300-9
125. Park Y-I, Chow WS, Anderson JM. 1995. Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196:401-11
126. Park Y-I, Chow WS, Osmond CB, Anderson JM. 1996. Electron transport to oxygen mitigates against the photoinactivation of Photosystem II in vivo. Photosynth. Res. 50:23-32
127. Pfündel E, Bilger W. 1994. Regulation and possible function of the violaxanthin cycle. Photosynth. Res. 42:89-109
128. Pogson B, McDonald KA, Truong M, Britton G, DellaPenna D. 1996. Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell 8:1627-39
129. Pogson BJ, Niyogi KK, Björkman O, DellaPenna D. 1998. Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc. Natl. Acad. Sci. USA 95: 13324-29
130. Polle A. 1997. Defense against photooxidative damage in plants. In Oxidative Stress and the Molecular Biology of Antioxidant Defenses, ed. JG Scandalios, pp. 623-66. Plainview, NY: Cold Spring Harbor Lab. Press
131. Powles SB. 1984. Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35:14-44
132. Rintamäki E, Salonen M, Suoranta U-M, Carlberg I, Andersson B, Aro E-M. 1997. Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. J. Biol. Chem. 272:30476-82
133. Rock CD, Zeevaart JAD. 1991. The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc. Natl. Acad. Sci. USA 88:7496-99
134. Ruban AV, Young AJ, Horton P. 1993. Induction of nonphotochemical 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. 102:741-50
135. Sager R, Zalokar M. 1958. Pigments and photosynthesis in a carotenoid-deficient mutant of Chlamydomonas. Nature 182:98-100
136. Schatz G, Brock H, Holzwarth AR. 1988. Kinetic and energetic model for the primary processes in photosystem II. Biophys. J. 54:397-405
137. 2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth. Res. 25: 279-93
138. Schuster G, Dewit M, Staehelin LA, Ohad I. 1986. Transient inactivation of the thylakoid photosystem II light-harvesting protein kinase system and concomitant changes in intramembrane particle size during photoinhibition of Chlamydomonas reinhardtii. J. Cell Biol. 103:71-80
139. Sen Gupta A, Heinen JL, Holaday AS, Burke JJ, Alien RD. 1993. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn Superoxide dismutase. Proc. Natl. Acad. Sci. USA 90:1629-33
140. Sen Gupta A, Webb RP, Holaday AS, Alien RD. 1993. Overexpression of superoxide dismutase protects plants from oxidative stress. Induction of ascorbate peroxidase in Superoxide dismutase-overexpressing plants. Plant Physiol. 103:1067-73
141. Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A. 1998. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl. Acad. Sci. USA 95:9705-9
142. Shikanai T, Shimizu K, Endo T, Hashimoto T. 1998. Screening of Arabidopsis mutants lacking down-regulation of photosystem II using an imaging system of chlorophyll fluorescence. In Photosynthesis: Mechanisms and Effects, ed. G Garah. Dordrecht: Kluwer. In press
143. Shintani D, DellaPenna D. 1998. Elevating the vitamin E content of plants through metabolic engineering. Science 282:2098-100
144. Smirnoff N. 1996. The function and metabolism of ascorbic acid in plants. Ann. Bot. 78:661-69
145. Somerville CR. 1986. Analysis of photosynthesis with mutants of higher plants and algae. Annu. Rev. Plant Physiol. 37: 467-507
146. Sonoike K. 1996. Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol. 37:239-47
147. Tardy F, Havaux M. 1996. Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. J. Photochem. Photobiol. B: Biol. 34:87-94
148. Telfer A, Dhami S, Bishop SM, Phillips D, Barber J. 1994. β-carotene quenches singlet oxygen formed by isolated photosystem II reaction centers. Biochemistry 33:14469-74
149. Tyystjärvi E, Aro E-M. 1996. The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc. Natl. Acad. Sci. USA 93:2213-18
150. Van Camp W, Capiau K, Van Montagu M, Inzé D, Slooten L. 1996. Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts. Plant Physiol. 112:1703-14
151. A species promote chlorophyll triplet formation. Proc. Natl. Acad. Sci. USA 89:1408-12
152. Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SWJ. 1987. Barley mutants lacking chloroplast glutamine synthetase - biochemical and genetic analysis. Plant Physiol. 83:155-58
153. Walters RG, Horton P. 1994. Acclimation of Arabidopsis thaliana to the light environment: changes in composition of the photosynthetic apparatus. Planta 195:248-56
154. Walters RG, Ruban AV, Horton P. 1994. Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur. J. Biochem. 226:1063-69
155. Walters RG, Ruban AV, Horton P. 1996. Identification of proton-active residues in a higher plant light-harvesting complex. Proc. Natl. Acad. Sci. USA 93: 14204-9
156. Wheeler GL, Jones MA, Smirnoff N. 1998. The biosynthetic pathway of vitamin C in higher plants. Nature 393: 365-69
157. Whitmarsh J, Samson G, Poulson M. 1994. Photoprotection in photosystem II - the role of cytochrome b559. See Ref. 17b, pp. 75-93
158. Wiese C, Shi L-B, Heber U. 1998. Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation. Physiol. Plant. 102:437-46
159. Winter K, Königer M. 1989. Dithiothreitol, an inhibitor of violaxanthin deepoxidation, increases the susceptibility of leaves of Nerium oleander L. to photoinhibition of photosynthesis. Planta 180:24-31
160. Yohn CB, Cohen A, Danon A, Mayfield SP. 1996. Altered mRNA binding activity and decreased translation initiation in a nuclear mutant lacking translation of the chloroplast psbA mRNA. Mol Cell Biol 16:3560-66
161. Zhang L, Niyogi KK, Baroli I, Nemson JA, Grossman AR, Melis A. 1997. DNA insertional mutagenesis for the elucidation of a Photosystem II repair process in the green alga Chlamydomonas reinhardtii. Photosynth. Res. 53:173-84