Violaxanthin de-epoxidase is rate-limiting for non-photochemical quenching under subsaturating light or during chilling in Arabidopsis

Plant Physiology and Biochemistry

Volumn 58, Issue , 2012, Pages 66-82

  Chen, Zhong ^a   Gallie, Daniel R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Non photochemical quenching; Photoinhibition; VDE; Xanthophyll cycle; Zeaxanthin

Indexed keywords

ARABIDOPSIS PROTEIN; ENZYME; PIGMENT; REACTIVE OXYGEN METABOLITE; VIOLAXANTHIN; XANTHOPHYLL;

ADAPTATION; ARABIDOPSIS; ARTICLE; COLD; ENZYMOLOGY; LIGHT; METABOLISM; PHOTOSYSTEM II; PHYSIOLOGICAL STRESS;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; COLD TEMPERATURE; ENZYMES; LIGHT; PHOTOSYSTEM II PROTEIN COMPLEX; PIGMENTS, BIOLOGICAL; REACTIVE OXYGEN SPECIES; STRESS, PHYSIOLOGICAL; XANTHOPHYLLS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84863436960     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2012.06.010     Document Type: Article

References (53)

1. Asada K., Takahashi M. Photoinhibition 1987, 227-287. Elsevier, Amsterdam. D.J. Kyle, C.B. Osmond, C.J. Arntzen (Eds.).
2. Niyogi K.K. Photoprotection revisited: genetic and molecular approaches. Ann. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50:333-339.
3. 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.
4. Niyogi K.K., Grossman A.R., 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.
5. Li X.-P., Bjorkman 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 2000, 403:391-395.
6. 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, 519:99-102.
7. 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.
8. Hager A. Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin-Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta 1969, 89:224-243.
9. Bugos R.C., Hieber A.D., Yamamoto H.Y. Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. J. Biol. Chem. 1998, 273:15321-15324.
10. 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.
11. Pfündel E.E., Dilley R.A. The pH dependence of violaxanthin de-epoxidation in isolated pea chloroplasts. Plant Physiol. 1993, 101:65-71.
12. 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.
13. Briantais J.-M., Vernotte C., Picaud M., Krause G.H. A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim. Biophys. Acta 1979, 548:128-138.
14. Yamamoto H.Y., Higashi R.M. Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch. Biochem. Biophys. 1978, 190:514-522.
15. Bratt C.E., Arvidsson P.-O., Carlsson M., Akerlund H.-E. Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosyn. Res. 1995, 45:169-175.
16. Saga G., Giorgetti A., Fufezan C., Giacometti G.M., Bassi R., Morosinotto T. Mutation analysis of violaxanthin de-epoxidase identifies substrate-binding sites and residues involved in catalysis. J. Biol. Chem. 2010, 285:23763-23770.
17. Niyogi K.K., Bjorkman O., Grossman A.R. The roles of specific xanthophylls in photoprotection. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14162-14167.
18. Pogson B.J., Niyogi K.K., 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.
19. Pogson B.J., Rissler H.M. Genetic manipulation of carotenoid biosynthesis and photoprotection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2000, 355:1395-1403.
20. Niyogi K.K., Shih C., Soon Chow W., Pogson B.J., Dellapenna D., Bjorkman O. Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth. Res. 2001, 67:139-145.
21. 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 2002, 1553:309-319.
22. Li Z., Ahn T.K., Avenson T.J., Ballottari M., Cruz J.A., Kramer D.M., Bassi R., Fleming G.R., Keasling J.D., Niyogi K.K. Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 2009, 21:1798-1812.
23. Ruban A.V., Berera R., Ilioaia C., van Stokkum I.H., Kennis J.T., Pascal A.A., van Amerongen H., Robert B., Horton P., van Grondelle R. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 2007, 450:575-578.
24. 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.
25. Hieber A.D., Bugos R.C., Verhoeven A.S., Yamamoto H.Y. Overexpression of violaxanthin de-epoxidase: properties of C-terminal deletions on activity and pH-dependent lipid binding. Planta 2002, 214:476-483.
26. Hieber A.D., Kawabata O., Yamamoto H.Y. Significance of the lipid phase in the dynamics and functions of the xanthophyll cycle as revealed by PsbS overexpression in tobacco and in-vitro de-epoxidation in monogalactosyldiacylglycerol micelles. Plant Cell Physiol. 2004, 45:92-102.
27. Deng Y., Lin R.C., Jing Y.X., Wang Q., Li L.B., Liu B.L., Kuang T.Y. Expression of vde gene integrated into tobacco genome in antisense and overexpressed ways. Photosynthetica 2003, 41:137-141.
28. Gao S., Han H., Feng H.L., Zhao S.J., Meng Q.W. Overexpression and suppression of violaxanthin de-epoxidase affects the sensitivity of photosystem II photoinhibition to high light and chilling stress in transgenic tobacco. J. Integr. Plant Biol. 2010, 52:332-339.
29. Han H., Gao S., Li B., Dong X.C., Feng H.L., Meng Q.W. Overexpression of violaxanthin de-epoxidase gene alleviates photoinhibition of PSII and PSI in tomato during high light and chilling stress. J. Plant Physiol. 2010, 167:176-183.
30. Macko S., Wehner A., Jahns P. Comparison of violaxanthin de-epoxidation from the stroma and lumen sides of isolated thylakoid membranes from Arabidopsis: implications for the mechanism of de-epoxidation. Planta 2002, 216:309-314.
31. Havaux M., Niyogi K.K. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:8762-8767.
32. 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. 2000, 124:273-284.
33. Kalituho L., Rech J., Jahns P. The roles of specific xanthophylls in light utilization. Planta 2007, 225:423-439.
34. Li X.P., Muller-Moule P., Gilmore A.M., Niyogi K.K. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:15222-15227.
35. Barrero J.M., Piqueras P., González-Guzmán M., Serrano R., Rodríguez P.L., Ponce M.R., Micol J.L. A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J. Exp. Bot. 2005, 56:2071-2083.
36. 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.
37. Pérez-Bueno M.L., Johnson M.P., Zia A., Ruban A.V., Horton P. The Lhcb protein and xanthophyll composition of the light harvesting antenna controls the ΔpH-dependency of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett. 2008, 582:1477-1482.
38. Nilkens M., Kress E., Lambrev P., Miloslavina Y., Müller M., Holzwarth A.R., Jahns P. 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.
39. Finazzi G., Johnson G.N., Dallosto L., Joliot P., Wollman F.A., Bassi R. A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:12375-12380.
40. D'Haese D., Vandermeiren K., Caubergs R.J., 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.
41. Kalituho L., Beran K.C., Jahns P. The transiently generated nonphotochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin. Plant Physiol. 2007, 143:1861-1870.
42. 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.
43. Demmig-Adams B., Adams W.W. Carotenoid composition in sun and shade leaves of plants with different life forms, Plant. Cell Environ. 1992, 15:411-419.
44. Eskling M., Arvidsson P.O., åkerlund H.E. The xanthophyll cycle, its regulation and components. Physiol. Plant 1997, 100:806-816.
45. Jahns P., Latowski D., Strzalka K. Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim. Biophys. Acta 2009, 1787:3-14.
46. Havir E.A., Tauska S.L., Peterson R.B. Purification and properties of violaxanthin de-epoxidase from spinach. Plant Sci. 1997, 123:57-66.
47. Chang S.H., Bugos R.C., Sun W.H., Yamamoto H.Y. Antisense suppression of violaxanthin de-epoxidase in tobacco does not affect plant performance in controlled growth conditions. Photosynth. Res. 2000, 64:95-103.
48. Külheim C., Agren J., Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science 2002, 297:91-93.
49. Bugos R.C., Chang S.-H., Yamamoto H.Y. Developmental expression of violaxanthin de-expoxidase in leaves of tobacco growing under high and low light. Plant Physiol. 1999, 121:207-214.
50. 18 high-performance liquid chromatographic column. Ann. Chromatogr. 1991, 543:137-145.
51. Sutherland M.W., Learmonth B.A. The tetrazolium dyes MTS and XTT provide new quantitative assay for superoxide and superoxide dismutase. Free Rad. Res. 1997, 27:283-289.
52. Frahry G., Schopfer P. NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 2001, 212:175-183.
53. Gay C.A., Gebicki J.M. Perchloric acid enhances sensitivity and reproducibility of the ferric-xylenol orange peroxide assay. Anal. Biochem. 2002, 304:42-46.