Ethylene Regulates Energy-Dependent Non-Photochemical Quenching in Arabidopsis through Repression of the Xanthophyll Cycle

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Chen, Zhong ^a   Gallie, Daniel R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; CARBON DIOXIDE; CHLOROPHYLL A; CHLOROPHYLL B; ENZYME; ETHYLENE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; UNCLASSIFIED DRUG; VIOLAXANTHIN; VIOLAXANTHIN DEEPOXIDASE; XANTHOPHYLL; ETHYLENE DERIVATIVE; OXIDOREDUCTASE; PHOTOSYSTEM II; VIOLAXANTHIN DE-EPOXIDASE;

ALCOHOL PRODUCTION; ARABIDOPSIS; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CTR1 GENE; ENERGY; ENZYME ACTIVATION; ENZYME SYNTHESIS; EPOXIDATION; ETO1 GENE; GENETIC VARIABILITY; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; PH; PHENOTYPE; PHOTOINHIBITION; PHOTOSYNTHESIS; PLANT GENE; PLANT GROWTH; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SOLUBILITY; VITAMIN METABOLISM; WILD TYPE; DRUG EFFECTS; ENERGY METABOLISM; LIGHT; METABOLISM; PHOTOCHEMISTRY; PHOTOSYSTEM II; PROCEDURES; THYLAKOID;

ARABIDOPSIS; CARBON DIOXIDE; ENERGY METABOLISM; ETHYLENES; LIGHT; OXIDOREDUCTASES; PHOTOCHEMISTRY; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; SUPEROXIDES; THYLAKOIDS; XANTHOPHYLLS;

EID: 84955571554     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0144209     Document Type: Article

References (150)

1. Feldman LJ. Regulation of root development. Ann. Rev. Plant Physiol. 1984; 35: 223-242.
2. Mattoo AK, Suttle JC. The Plant Hormone Ethylene. Boca Raton: CRC Press; 1991.
3. Abeles FB, Morgan PW, Saltveit ME Jr. In: Ethylene in Plant Biology. 2nd ed San Diego: Academic Press, Inc; 1992.
4. Morgan PG, Drew MC. Ethylene and plant responses to stress. Physiol. Plant. 1997; 100: 620-630.
5. Bleecker AB, Kende H. Ethylene: a gaseous signal molecule in plants. Ann. Rev. Cell Dev. Biol. 2000; 16: 1-18.
6. Klee HJ. Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol. 2004; 135: 660-667. PMID: 15208412
7. Lin Z, Zhong S, Grierson D. Recent advances in ethylene research. J. Exp. Bot. 2009; 60: 3311-3336. doi: 10.1093/jxb/erp204 PMID: 19567479
8. Yang SF, Hoffman NE. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 1984; 35: 155-189.
9. Chen YF, Randlett MD, Findell JL, Schaller GE. Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J. Biol. Chem. 2002; 277: 19861-19866. PMID: 11916973
10. Chang C, Shockey JA. The ethylene-response pathway: signal perception to gene regulation. Curr. Opin. Plant Biol. 1999; 2: 352-358. PMID: 10508761
11. Chang C, Stadler R. Ethylene hormone receptor action in Arabidopsis. Bioessays 2001; 23: 619-627. PMID: 11462215
12. Wang KL, Li H, Ecker JR. Ethylene biosynthesis and signaling networks. Plant Cell 2002; 14: S131-S151. PMID: 12045274
13. Stepanova AN, Alonso JM. Arabidopsis ethylene signaling pathway. Sci STKE 2005; 276: cm4.
14. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 1993; 72: 427-441. PMID: 8431946
15. Hua J, Meyerowitz EM. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 1998; 94: 261-271. PMID: 9695954
16. Clark KL, Larsen PB, Wang X, Chang C. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc. Natl. Acad. Sci. USA 1998; 95: 5401-5406. PMID: 9560288
17. Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 1997; 89: 1133-1144. PMID: 9215635
18. Solano R, Stepanova A, Chao Q, Ecker JR. Genes Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Develop 1998; 12: 3703-3714.
19. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 1999; 284: 2148-2152. PMID: 10381874
20. Zhao Q, Guo HW. Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol. Plant 2011; 4: 626-634. doi: 10.1093/mp/ssr042 PMID: 21690206
21. Flexas J, Medrano H. Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Annals Bot. 2002; 89: 183-189.
22. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osorio ML, et al. How plants cope with water stress in the field. Photosynthesis and growth. Annals Bot. 2002; 89: 907-916.
23. Ramachandra Reddy A, Chaitanya KV, Vivekanandan M. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J. Plant Physiol. 2004; 161: 1189-1202. PMID: 15602811
24. Kays SJ. Pallas JE. Inhibition of photosynthesis by ethylene. Nature 1980; 285: 51-52.
25. Pallas JE, Kays SJ. Inhibition of photosynthesis by ethylene - a stomatal effect. Plant Physiol. 1982; 70: 598-601. PMID: 16662540
26. Madhavan S, Chrmoinski A, Smith BN. Effect of ethylene on stomatal opening in tomato and carnation leaves. Plant Cell Physiol. 1983; 24: 569-572.
27. Taylor GE Jr, Gunderson CA. The response of foliar gas exchange to exogenously applied ethylene. Plant Physiol. 1986; 82: 653-657. PMID: 16665086
28. Gunderson CA, Taylor GE. Ethylene directly inhibits foliar gas exchange in glycine max. Plant Physiol. 1991; 95: 337-339. PMID: 16667976
29. Levitt LK, Stein DB, Rubinstein B. Promotion of stomatal opening by indoleacetic acid and ethrel in epidermal strips of Vicia faba L. Plant Physiol. 1987; 85: 318-321. PMID: 16665694
30. Merritt F, Kemper A, Tallman G. Inhibitors of ethylene biosynthesis inhibit auxin-induced stomatal opening in epidermis detached from leaves of Vicia faba L. Plant Cell Physiol. 2001; 42: 223-230. PMID: 11230577
31. Pallaghy CK, Raschke K. No stomatal response to ethylene. Plant Physiol. 1972; 49: 275-276. PMID: 16657942
32. Woodrow L, Thompson RG, Grodzinski B. Effects of ethylene on photosynthesis and partitioning in tomato, Lycopersicon esculentum Mill. J. Exp. Bot. 1988; 39: 667-684.
33. Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S. Ethylene inhibits abscisic acidinduced stomatal closure in Arabidopsis. Plant Physiol. 2005; 138: 2337-2343. PMID: 16024687
34. Desikan R, Hancock JT, Bright J, Harrison J, Weir I, Hooley R, et al. A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol. 2005; 137: 831-834. PMID: 15761208
35. Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, et al. Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J. 2006; 47: 907-916. PMID: 16961732
36. Tholen D, Voesenek LA, Poorter H. Ethylene insensitivity does not increase leaf area or relative growth rate in Arabidopsis, Nicotiana tabacum, and Petunia x antho. Plant Physiol. 2004; 134: 1803-1812. PMID: 15064382
37. Tholen D, Pons TL, Voesenek LA, Poorter H. The role of ethylene perception in the control of photosynthesis. Plant Signal Behav. 2008; 3: 108-109. PMID: 19704724
38. Zhong S, Zhao M, Shi T, Shi H, An F, Zhao Q, et al. EIN3/EIL1 cooperate with PIF1 to prevent photooxidation and to promote greening of Arabidopsis seedlings. Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 21431-21436. doi: 10.1073/pnas.0907670106 PMID: 19948955
39. Zhong S, Shi H, Xi Y, Guo H. Ethylene is crucial for cotyledon greening and seedling survival during de-etiolation. Plant Signal Behav. 2010; 5: 739-742. PMID: 20404499
40. Li Z, Peng J, Wen X, Guo H. Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 2013; 25: 3311-3328. doi: 10.1105/tpc.113.113340 PMID: 24064769
41. Young TE, Meeley RB, Gallie DR. ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J. 2004; 40: 813-825. PMID: 15546363
42. Asada K, Takahashi M. Photoinhibition. In: Kyle DJ, Osmond CB, Arntzen CJ, editors. Amsterdam: Elsevier; 1987. pp 227-287.
43. Niyogi KK. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999; 50: 333-359. PMID: 15012213
44. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann. Rev. Plant Physiol. Plant Mol. Biol. 1999; 50: 601-639.
45. Wraight CA, Crofts AR. Energy-dependent quenching of chlorophyll alpha fluorescence in isolated chloroplasts. Eur. J. Biochem. 1970; 17: 319-327. PMID: 5500400
46. Briantais JM, Vernotte C, Picaud M, Krause GH. A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim. Biophys. Acta 1979; 548: 128-138. PMID: 486438
47. Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth AR, et al. Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim. Biophys. Acta 2010; 1797: 466-475. doi: 10.1016/j.bbabio.2010.01.001 PMID: 20067757
48. Horton P, Ruban AV, Walters RG. Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996; 47: 655-684. PMID: 15012304
49. Niyogi KK, Grossman AR, Bjorkman O. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 1998; 10: 1121-1134. PMID: 9668132
50. Li X-P, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, et al. (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395. PMID: 10667783
51. Jahns P, Graf M, Munekage Y, Shikanai T. Single point mutation in the Rieske iron-sulfur subunit of cytochrome b(6)/f leads to an altered pH dependence of plastoquinol oxidation in Arabidopsis. FEBS Lett. 2002; 519: 990-102.
52. Munekage Y, Takeda S, Endo T, Jahns P, Hashimoto T, Shikanai T. Cytochrome b(6)f mutation specifically affects thermal dissipation of absorbed light energy in Arabidopsis. Plant J. 2001; 28: 351-359. PMID: 11722777
53. Osmond CB. In: Baker NR, Bowyer JR, editors. Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. Oxford: BIOS Scientific Publishers; 1994. pp 1-24.
54. Müller-Moulé P, Golan T, Niyogi KK. Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiol. 2004; 134: 1163-1172. PMID: 14963245
55. Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 2008; 13: 178-182. doi: 10.1016/j.tplants.2008.01.005 PMID: 18328775
56. Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 2005; 307: 433-436. PMID: 15662017
57. Dall'Osto L, Caffarri S, Bassi R. A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 2005; 17: 1217-1232. PMID: 15749754
58. Havaux M, Dall'osto L, Bassi R. Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol. 2007; 145: 1506-1520. PMID: 17932304
59. Dall'Osto L, Cazzaniga S, Havaux M, Bassi R. Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Mol Plant 2010; 3: 576-593. doi: 10.1093/mp/ssp117 PMID: 20100799
60. Niyogi KK, Bjorkman O, Grossman AR. The roles of specific xanthophylls in photoprotection. Proc. Natl. Acad. Sci. USA 1997; 94: 14162-14167. PMID: 9391170
61. Pogson BJ, Niyogi KK, Bjorkman O, DellaPenna D. Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc. Natl. Acad. Sci. U.S.A. 1998; 95: 13324-13329. PMID: 9789087
62. Pogson BJ, Rissler HM. Genetic manipulation of carotenoid biosynthesis and photoprotection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2000; 355: 1395-1403. PMID: 11127994
63. Niyogi KK, Shih C, Soon Chow W, Pogson BJ, Dellapenna D, Bjorkman O. Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res 2001; 67: 139-145. PMID: 16228323
64. Lokstein H, Tian L, Polle JEW, 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 2002; 1553: 309-319. PMID: 11997140
65. Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, et al. Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 2009; 21: 1798-1812. doi: 10.1105/tpc.109.066571 PMID: 19549928
66. Johnson MP, Pérez-Bueno ML, Zia A, Horton P, Ruban AV. The zeaxanthin-independent and zeaxanthin- dependent qE components of nonphotochemical quenching involve common conformational changes within the photosystem II antenna in Arabidopsis. Plant Physiol. 2009; 149: 1061-1075. doi: 10.1104/pp.108.129957 PMID: 19011000
67. Ruban AV, Berera R, Ilioaia C, van Stokkum IH, Kennis JT, Pascal AA, et al. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 2007; 450: 575-578. PMID: 18033302
68. Dall'Osto L, Cazzaniga S, North H, Marion-Poll A, Bassi R. The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell 2007; 19: 1048-1064. PMID: 17351115
69. Hager A, Holocher K. Localization of the xanthophyll -cycle enzyme violaxanthin de-epoxidase within the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease. Planta 1994; 192: 581-589.
70. Eskling M, Arvidsson PO, Åkerlund HE. The xanthophyll cycle, its regulation and components. Physiol. Plant. 1997; 100: 806-816.
71. Yamamoto HY, Bugos RC, Hieber AD. Biochemistry and molecular biology of the xanthophyll cycle. In: Frank H.A., Young AJ, Britton G, Cogdell RJ editors. The Photochemistry of Carotenoids, Dordrecht: Kluwer Academic; 1999. pp. 293-303.
72. Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D. A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 2009; 21: 2036-2044. doi: 10.1105/tpc.109.068007 PMID: 19638474
73. Havaux M, Bonfils JP, Lütz C, Niyogi KK. 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. 2000; 124: 273-284. PMID: 10982442
74. Sharma PK, Singhal GS. The role of thylakoid lipids in the photodamage of photosynthetic activity. Physiol. Plant. 1992; 86: 623-629.
75. Hideg E, Spetea C, Vass I. Singlet oxygen and free radical production during acceptor- and donorsideinduced photoinhibition: studies with spin trapping EPR spectroscopy. Biochim Biophys Acta 1994; 1186: 143-152.
76. Lim BP, Nagao A, Terao J, Tanaka K, Suzuki T, Takama K. Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipid peroxidation. Biochim. Biophys. Acta 1992; 1120: 178-184.
77. Frank HA, Cogdell RJ. The photochemistry and function of carotenoids in photosynthesis. In: Young A, Britton G. editors. Carotenoids in Photosynthesis, London: Chapman and Hall; 1993. pp. 252-326.
78. Demmig-Adams B, Gilmore AM, AdamsWWIII. In vivo functions of carotenoids in higher plants. FASEB J. 1996; 10: 403-412. PMID: 8647339
79. Sielewiesiuk J, Matula M, Gruszecki WI. Photooxidation of chlorophyll a in digalactosyldiacylglycerol liposomes containing xanthophyll pigments: indication of a special photoprotective ability of zeaxanthin. Cell Mol. Biol. Lett. 1997; 2: 59-68.
80. Guzman P, Ecker JR. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 1990; 2: 513-523. PMID: 2152173
81. Vogel JP, Woeste KE, Theologis A, Kieber JJ. Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl. Acad. Sci. USA 1998; 95: 4766-4771. PMID: 9539813
82. Wang KL, Yoshida H, Lurin C, Ecker JR. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 2004; 428: 945-950. PMID: 15118728
83. Ji Y, Guo H. From endoplasmic reticulum (ER) to nucleus: EIN2 bridges the gap in ethylene signaling. Mol. Plant 2013; 6: 11-14. doi: 10.1093/mp/sss150 PMID: 23239828
84. Maxwell K, Johnson GN. Chlorophyll fluorescence - a practical guide. J. Exp. Bot. 2000; 51: 659-668. PMID: 10938857
85. Walters RG, Horton P. Resolution of non photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth. Res. 1991; 27: 121-133. doi: 10.1007/BF00033251 PMID: 24414575
86. Jeffrey SW, Humphrey GF. New spectrophotometric equations for determining chlorophylls a1, b1, c1 and c2 in higher plants, algae and natural phytoplankton. New Biochem. Physiol. Pflanz. 1975; 167: 191-194.
87. Gilmore AM, Yamamoto HY. Resolution of lutein and zeaxanthin using a non-endcapped, highly carbon- loaded C18 high-performance liquid chromatographic column. Annals Chromatography 1991; 543: 137-145.
88. Savidge B, Weiss JD, Wong YH, Lassner MW, Mitsky TA, Shewmaker CK, et al. Isolation and characterization of homogentisate phytyltransfrase gene from Synechocystis sp. PCC6803 and Arabidopsis. Plant Physiol. 2002; 129: 321-332. PMID: 12011362
89. Bugos RC, Chang S-H, Yamamoto HY. Developmental expression of violaxanthin de-expoxidase in leaves of tobacco growing under high and low light. Plant Physiol. 1999; 121: 207-214. PMID: 10482676
90. Conklin PL, Saracco SA, Norris SR, Last RL. Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 2000; 154: 847-856. PMID: 10655235
91. Grouneva I, Jakob T, Wilhelm C, Goss R. Influence of ascorbate and pH on the activity of the diatom xanthophyll cycle-enzyme diadinoxanthin de-epoxidase. Physiol. Plant. 2006; 126: 205-211.
92. Siefermann D, Yamamoto HY. Properties of NADHP and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts. Arch. Biochem. Biophys. 1975; 171: 70-77.
93. Roberts CS, Spalding MH. Post-translational processing of the highly processed, secreted periplasmic carbonic anhydrase of Chlamydomonas is largely conserved in transgenic tobacco. Plant Mol. Biol. 1995; 29: 303-315. PMID: 7579181
94. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976; 72: 248-254. PMID: 942051
95. Frahry G, Schopfer P. NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 2001; 212: 175-183. PMID: 11216837
96. Sutherland MW, Learmonth BA. The tetrazolium dyes MTS and XTT provide new quantitative assay for superoxide and superoxide dismutase. Free Rad. Res. 1997; 27: 283-289.
97. Corbin DR, Grebenok RJ, Ohnmeiss TE, Greenplate JT, Purcell JP. Expression and chloroplast targeting of cholesterol oxidase in transgenic tobacco plants. Plant Physiol. 2001; 126: 1116-1128. PMID: 11457962
98. Schuldiner S, Rottenberg H, Avron M. Fluorescent amines as a probe for the determination of ΔpH in chloroplasts. Eur. J. Biochem, 1972; 25: 64-70.
99. Finazzi G, Johnson GN, Dallosto L, Joliot P, Wollman FA, Bassi R. A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc. Natl. Acad. Sci. USA 2004; 101: 12375-12380. PMID: 15304641
100. D'Haese D, Vandermeiren K, Caubergs RJ, Guisez Y, De Temmerman L, Horemans N. Non-photochemical quenching kinetics during the dark to light transition in relation to the formation of antheraxanthin and zeaxanthin. J. Theor. Biol. 2004; 227: 175-186. PMID: 14990382
101. Kalituho L, Rech J, Jahns P. The role of specific xanthophylls in light utilization. Planta 2007; 225: 423-439. PMID: 16896791
102. Horton P. Effects of changes in the capacity for photosynthetic electron transfer and photophosphorylation on the kinetics of fluorescence induction in isolated chloroplasts. Biochim. Biophys. Acta 1983; 724: 404-410.
103. Serek M, Tamari G, Sisler EC, Borochov A. Inhibition of ethylene-induced cellular senescence symptoms by 1-methylcyclopropene, a new inhibitor of ethylene action. Physiol. Plant 1995; 94: 229-232.
104. Holt NE, Fleming GR, Niyogi KK. Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochem. 2004; 43: 8281-8289.
105. Hager A. Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin-Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta 1969; 89: 224-243. doi: 10.1007/BF00385028
106. Bratt CE, Arvidsson P-O, Carlsson M, Akerlund H-E. Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynth Res. 1995; 45: 169-175. doi: 10.1007/BF00032588 PMID: 24301483
107. Li XP, Muller-Moule P, Gilmore AM, Niyogi KK. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl. Acad. Sci. USA 2002; 99: 15222-15227. PMID: 12417767
108. Oja V, Laisk A, Heber U. Light-induced alkalization of the chloroplast stroma in vivo as estimated from the CO2 capacity of intact sunflower leaves. Biochim. Biophys. Acta 1986; 849: 355-365
109. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004; 9: 490-498. PMID: 15465684
110. Haraux F, De Kouchkovsky Y. Measurement of chloroplast internal protons with 9-aminoacridine. Biochim. Biophys. Acta. 1980; 592: 153-168. PMID: 6249352
111. Hope AB, Matthews DB. Adsorption of amines to thylakoid surfaces and estimations of ΔpH. Aust. J. Plant Physiol. 1985; 12: 9-19.
112. Strotmann H, Thelen R, Muller W, Baum W. A ΔpH clamp method for analysis of steady-state kinetics of photophosphorylation. Eur. J. Biochem. 1990; 193: 879-886. PMID: 2174369
113. Rottenberg H, Moreno-Sanchez R. The proton pumping activity of H+-ATPases: an improved fluorescence assay. Biochim. Biophys. Acta 1993; 1183: 161-170. PMID: 8399374
114. Achninea L, Pereda-Miranda R, Iglesias-Prieto R, Moreno-Sanchez R, Lotina-Hennsen B. Tricolorin A, a potent natural uncoupler and inhibitor of photosystem II acceptor side of spinach chloroplasts. Physiologia Plant. 1999; 106: 246-252.
115. Chen Z, Gallie DR. Violaxanthin de-epoxidase is rate-limiting for non-photochemical quenching under subsaturating light or during chilling in Arabidopsis. Plant Physiol. Biochem. 2012; 58: 66-82. doi: 10. 1016/j.plaphy.2012.06.010 PMID: 22771437
116. Krieger-Liszkay A. Singlet oxygen production in photosynthesis. J. Exp. Bot. 2005; 56: 337-346.
117. Genty B, Harbinson J, Baker NR. Relative quantum efficiencies of the two photosystems of leaves in photo respiratory and non-photo respiratory conditions. Plant Physiol. Biochem. 1990; 28: 1-10.
118. Kyle DJ, Ohad I, Arntzen CJ. Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc. Natl. Acad Sci. U.S.A. 1984; 81: 4070-4074. PMID: 16593483
119. Prasil O, Adir N, Ohad I. Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In Barber J editor. In: Topics in Photosynthesis. Vol. 11. Amsterdam: Elsevier; 1992. pp. 295-348.
120. Aro E-M, Virgin I, Andersson B. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1993; 1143: 113-134. PMID: 8318516
121. Van Wijk KJ, Andersson B, Aro E-M. Kinetic resolution of the incorporation of the D1 protein into photosystem II and localization of assembly intermediates in thylakoid membranes of spinach chloroplasts. J. Biol. Chem. 1996; 271: 9627-9636. PMID: 8621638
122. Melis A. Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage? Trends Plant Sci. 1999; 4: 130-135. PMID: 10322546
123. Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR. How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol. 2009; 149: 1560-1567. doi: 10.1104/pp.108.134122 PMID: 19118124
124. Golan T, Müller-Moulé P, Niyogi KK. Photoprotection mutants of Arabidopsis thaliana acclimate to high light by increasing photosynthesis and specific antioxidants. Plant Cell Environ. 2006; 29: 879-887. PMID: 17087471
125. Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, et al. The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 2004; 306: 1183-1185. PMID: 15539603
126. Neljubow DN. Uber die horizontale Nutation der Stengel von Pisum sativum und einiger Anderen Pflanzen. Beih. Bot. Zentralbl. 1901; 10: 128-139.
127. Chen JF, Gallie DR. Analysis of the functional conservation of ethylene receptors between maize and Arabidopsis. Plant Mol. Biol. 2010; 74: 405-421. doi: 10.1007/s11103-010-9686-4 PMID: 20835883
128. Demmig-Adams B. Carotenoids and photoprotection: A role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1990; 1020: 1-24.
129. Krause GH. The high-energy state of the thylakoid system as indicated by chlorophyll fluorescence and chloroplast shrinkage. Biochim. Biophys. Acta 1973; 292: 715-728. PMID: 4705450
130. Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, et al. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 2004; 279: 22866-22874. PMID: 15033974
131. Kiss AZ, Ruban AV, Horton P. The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J. Biol. Chem. 2008; 283: 3972-3978. PMID: 18055452
132. Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall'osto L, et al. Light-induced dissociation of an antenna hetero-oligomer is needed for nonphotochemical quenching induction. J. Biol. Chem. 2009; 284: 15255-15266. doi: 10.1074/jbc.M808625200 PMID: 19307183
133. Kereiche S, Kiss AZ, Kouril R, Boekema E, Horton P. The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membarnes of higher plant chloroplasts. FEBS Lett. 2010; 584: 754-764.
134. Horton P, Ruban AV, Walters RG. Regulation of light harvesting in green plants - indication by nonphotochemical quenching of chlorophyll fluorescence. Plant Physiol. 1994; 106: 415-420. PMID: 12232338
135. Walters RG, Ruban AV, Horton P. Higher plant lightharvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur. J. Biochem. 1994; 226: 1063-1069. PMID: 7813461
136. Johnson MP, Goral TK, Duffy CD, Brain AP, Mullineaux CW, Ruban AV. Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 2011; 23: 1468-1479. doi: 10.1105/tpc.110.081646 PMID: 21498680
137. Horton P, Wentworth M, Ruban A. Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett. 2005; 579: 4201-4206. PMID: 16051219
138. Barenyi B, Krause GH. Inhibition of photosynthetic reaction by light. A study with isolated spinach chloroplasts. Planta 1985; 163: 218-226. doi: 10.1007/BF00393510 PMID: 24249342
139. Kyle DJ. The biochemical basis of photoinhibition of Photosystem II. In: Kyle DJ, Osmond CB, Arntzen CJ editors. Topics in photosynthesis, photoinhibition, vol 9. Amsterdam: Elsevier Science Publishers BV; 1987. pp 197-226.
140. Mishra NP, Mishra RK, Singhal GS. Involvement of active oxygen species in photoinhibition of photosystem II: protection of photosynthetic efficiency and inhibition of lipid peroxidation by superoxide dismutase and catalase. J. Photochem. Photobiol. B Biol. 1993; 19: 19-24.
141. Foyer CH, Trebst A, Noctor G. Protective and signaling functions of ascorbate, glutathione and tocopherol in chloroplasts. In: Demmig-Adams B, Adams WW, editors. Advances in photosynthesis and respiration, Vol. 19. Photoprotection, photoinhibition, gene regulation, and environment. Dordrecht: Springer Science Publishers; 2005. pp. 241-268.
142. Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ, Mewett OP, et al. Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 2007; 19: 4091-4110. PMID: 18156220
143. Wang P, Du Y, Zhao X, Miao Y, Song CP. The MPK6-ERF6-ROS-responsive cis-acting Element7/ GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiol. 2013; 161: 1392-1408. doi: 10.1104/pp.112.210724 PMID: 23300166
144. Sewelam N, Kazan K, Thomas-Hall SR, Kidd BN, Manners JM, Schenk PM. Ethylene response factor 6 is a regulator of reactive oxygen species signaling in Arabidopsis. PLoS One 2013; 8: e70289. doi: 10.1371/journal.pone.0070289 PMID: 23940555
145. Havaux M, Niyogi KK. The violaxanthin cycle protects plants from photo-oxidative damage by more than one mechanism. Proc. Natl. Acad. Sci. U.S.A. 1999; 96: 8762-8767. PMID: 10411949
146. Külheim C, Ågren J, Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science 2002; 297: 91-93. PMID: 12098696
147. Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P. Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 2005; 17: 3451-3469. PMID: 16258032
148. Palozza P, Krinsky NI. β-Carotene and α-tocopherol are synergistic antioxidants. Arch. Biochem. Biophys. 1992; 297: 184-187. PMID: 1637180
149. Bohm F, Edge R, Land EJ, McGarvey DJ, Truscott TG. Carotenoids enhance vitamin E antioxidant efficiency. J. Am. Chem. Soc. 1997; 119: 621-622.
150. Wrona M, Rozanowska M, Sarna T. Zeaxanthin in combination with ascorbic acid or α-tocopherol protects ARPE-19 cells against photosensitized peroxidation of lipids. Free Radic. Biol. Med. 2004; 36: 1094-1101. PMID: 15082063