On the origin of a slowly reversible fluorescence decay component in the Arabidopsis npq4 mutant

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1640, 2014, Pages

  Dall'Osto, Luca ^a   Cazzaniga, Stefano ^a   Wada, Masamitsu ^b   Bassi, Roberto ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Chloroplast avoidance; Energy dissipation; Lhcb; Non photochemical quenching; Photosynthesis; Xanthophyll

Indexed keywords

CAROTENOID; CHLOROPLAST; DICOTYLEDON; ENERGY DISSIPATION; FLUORESCENCE; GENETIC ANALYSIS; INHIBITOR; MUTATION; PHOTOCHEMISTRY; PHOTOINHIBITION; PHOTOSYNTHESIS; PROTEIN; REACTION KINETICS;

ARABIDOPSIS PROTEIN; CAROTENOID; NPQ4 PROTEIN, ARABIDOPSIS; XANTHOPHYLL;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CHLOROPLAST AVOIDANCE; ENERGY DISSIPATION; FLUORESCENCE; GENETICS; KINETICS; LHCB; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; MUTATION; NONPHOTOCHEMICAL QUENCHING; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY;

CHLOROPLAST AVOIDANCE; ENERGY DISSIPATION; LHCB; NON-PHOTOCHEMICAL QUENCHING; PHOTOSYNTHESIS; XANTHOPHYLL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CAROTENOIDS; FLUORESCENCE; KINETICS; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; MUTATION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX;

EID: 84908323777     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0221     Document Type: Article

References (54)

1. Croce R, Van Amerongen H. 2011 Light-harvesting and structural organization of photosystem II: from individual complexes to thylakoid membrane. J. Photochem. Photobiol. B 104, 142-153. (doi:10. 1016/j.jphotobiol.2011.02.015)
2. Krieger-Liszkay A. 2005 Singlet oxygen production in photosynthesis. J. Exp. Bot. 56, 337-346. (doi:10.1093/jxb/erh237)
3. Alboresi A, Dall'Osto L, Aprile A, Carillo P, Roncaglia E, Cattivelli L, Bassi R. 2011 Reactive oxygen species and transcript analysis upon excess light treatment in wildtype Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein. BMC. Plant Biol. 11, 62. (doi:10.1186/1471-2229-11-62)
4. Wada M, Kagawa T, Sato Y. 2003 Chloroplast movement. Ann. Rev. Plant Biol. 54, 455-468. (doi:10.1146/annurev.arplant.54.031902.135023)
5. Niyogi KK. 2000 Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3, 455-460. (doi:10.1016/ S1369-5266(00)00113-8)
6. Dall'Osto L, Holt NE, Kaligotla S, Fuciman M, Cazzaniga S, Carbonera D, Frank HA, Alric J, Bassi R. 2012 Zeaxanthin protects plant photosynthesis by modulating chlorophyll triplet yield in specific lightharvesting antenna subunits. J. Biol. Chem. 287, 41 820-41 834. (doi:10.1074/jbc.M112.405498)
7. Kulheim C, Agren J, Jansson S. 2002 Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91-93. (doi:10.1126/science. 1072359)
8. Walters RG, Horton P. 1991 Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth. Res. 27, 121-133. (doi:10.1007/BF00033251)
9. Briantais J-M, Vernotte C, Picaud M, Krause GH. 1980 Chlorophyll fluorescence as a probe for the determination of the photoinduced proton gradient in isolated chloroplasts. Biochim. Biophys. Acta 591, 198-202. (doi:10.1016/0005-2728(80)90233-9)
10. Dominici P, Caffarri S, Armenante F, Ceoldo S, Crimi M, Bassi R. 2002 Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J. Biol. Chem. 277, 22 750-22 758. (doi:10.1074/jbc.M200604200)
11. Wilk L, Grunwald M, Liao PN, Walla PJ, Kuhlbrandt W. 2013 Direct interaction of the major lightharvesting complex II and PsbS in nonphotochemical quenching. Proc. Natl Acad. Sci. USA 110, 5452-5456. (doi:10.1073/pnas. 1205561110)
12. Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Björkman O. 2001 Photoprotection in a zeaxanthin-and lutein-deficient double mutant of Arabidopsis. Photosynth. Res. 67, 139-145. (doi:10. 1023/A:1010661102365)
13. Anderson JM, Park YI, Chow WS. 1997 Photoinactivation and photoprotection of photosystem II in nature. Physiol. Plant. 100, 214-223. (doi:10. 1111/j.1399-3054.1997.tb04777.x)
14. Dall'Osto L, Caffarri S, Bassi R. 2005 A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17, 1217-1232. (doi:10.1105/tpc.104.030601)
15. Nilkens M, Kress E, Lambrev P, Miloslavina Y, Muller M, Holzwarth AR, Jahns P. 2010 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 1797, 466-475. (doi:10.1016/j.bbabio. 2010.01.001)
16. Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR. 2008 Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320, 794-797. (doi:10.1126/science.1154800)
17. Ruban AV et al. 2007 Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575-578. (doi:10.1038/ nature06262)
18. Kruger TPJ, Novoderezhkin VI, Ilioaia C, van Grondelle R. 2010 Fluorescence spectral dynamics of single LHCII trimers. Biophys. J. 98, 3093-3101. (doi:10.1016/j.bpj.2010.03.028)
19. Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall'Osto L, Morosinotto T, Bassi R. 2009 Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J. Biol. Chem. 284, 15 255-15 266. (doi:10.1074/jbc.M808625200)
20. Johnson MP, Goral TK, Duffy CD, Brain AP, Mullineaux CW, Ruban AV. 2011 Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23, 1468-1479. (doi:10.1105/tpc.110.081646)
21. Johnson MP, Ruban AV. 2010 Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J. 61, 283-289. (doi:10.1111/j. 1365-313X.2009.04051.x)
22. de Bianchi S, Dall'Osto L, Tognon G, Morosinotto T, Bassi R. 2008 Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 20, 1012-1028. (doi:10.1105/tpc.107.055749)
23. de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall'Osto L. 2011 Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23, 2659-2679. (doi:10.1105/tpc. 111.087320)
24. Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M. 2001 Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291, 2138-2141. (doi:10.1126/ science.291.5511.2138)
25. Van Kooten O, Snel JFH. 1990 The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynt. Res. 25, 147-150. (doi:10.1007/BF00033156)
26. Gilmore AM, Shinkarev VP, Hazlett TL, Govindjee G. 1998 Quantitative analysis of the effects of intrathylakoid pH and xanathophyll cycle pigments on chlorophyll a fluorescence lifetime distributions and intensity in thylakoids. Biochemistry 37, 13 582-13 593. (doi:10.1021/bi981384x)
27. Aro E-M, Virgin I, Andersson B. 1993 Photoinhibition of photosystem II-inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113-134. (doi:10.1016/0005-2728(93)90134-2)
28. Garmier M, Carroll AJ, Delannoy E, Vallet C, Day DA, Small ID, Millar AH. 2008 Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol. 148, 1324-1341. (doi:10.1104/pp.108.125880)
29. Gilmore AM, Yamamoto HY. 1991 Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol. 96, 635-643. (doi:10.1104/pp.96. 2.635)
30. Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK. 2000 A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395. (doi:10. 1038/35000131)
31. 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, 1121-1134.
32. Johnson MP, Davison PA, Ruban AV, Horton P. 2008 The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett. 582, 262-266. (doi:10.1016/j. febslet.2007.12.016)
33. Krause GH. 1988 Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol. Plant. 74, 566-574. (doi:10. 1111/j.1399-3054.1988.tb02020.x)
34. Joliot PA, Finazzi G. 2010 Proton equilibration in the chloroplast modulates multiphasic kinetics of nonphotochemical quenching of fluorescence in plants. Proc. Natl Acad. Sci. USA 107, 12 728-12 733. (doi:10.1073/pnas.1006399107)
35. Li Z et al. 2009 Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21, 1798-1812. (doi:10.1105/tpc.109.066571)
36. Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR. 2008 Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283, 3550-3558. (doi:10.1074/jbc.M705645200)
37. Havaux M, Dall'Osto L, Bassi R. 2007 Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol. 145, 1506-1520. (doi:10.1104/pp. 107.108480)
38. Dall'Osto L, Cazzaniga S, Havaux M, Bassi R. 2010 Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Mol. Plant 3, 576-593. (doi:10.1093/mp/ssp117)
39. Galka P, Santabarbara S, Khuong TTH, Degand H, Morsomme P, Jennings RC, Boekema EJ, Caffarri S. 2012 Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24, 2963-2978. (doi:10.1105/tpc.112.100339)
40. Bellafiore S, Barneche F, Peltier G, Rochaix JD. 2005 State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892-895. (doi:10.1038/nature03286)
41. Brugnoli E, Bjorkman O. 1992 Chloroplast movements in leaves-influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to DeltapH and zeaxanthin formation. Photosynth. Res. 32, 23-35. (doi:10.1007/BF00028795)
42. Davis PA, Hangarter RP. 2012 Chloroplast movement provides photoprotection to plants by redistributing PSII damage within leaves. Photosynt. Res. 112, 153-161. (doi:10.1007/s11120-012-9755-4)
43. Quick WP, Stitt M. 1989 An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves. Biochim. Biophys. Acta 977, 287-296. (doi:10.1016/S0005-2728(89)80082-9)
44. Li XP, Muller-Moule P, Gilmore AM, Niyogi KK. 2002 PsbS-dependent enhancement of feedback deexcitation protects photosystem II from photoinhibition. Proc. Natl Acad. Sci. USA 99, 15 222-15 227. (doi:10.1073/pnas.232447699)
45. Miloslavina Y, de Bianchi S, Dall'Osto L, Bassi R, Holzwarth AR. 2011 Quenching in Arabidopsis thaliana mutants lacking monomeric antenna proteins of photosystem II. J. Biol. Chem. 286, 36 830-36 840. (doi:10.1074/jbc.M111.273227)
46. Cazzaniga S, Dall'Osto L, Kong SG, Wada M, Bassi R. 2013 Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photoxidative stress in Arabidopsis. Plant J. 76, 568-579. (doi:10.1111/ tpj.12314)
47. Davis PA, Caylor S, Whippo CW, Hangarter RP. 2011 Changes in leaf optical properties associated with light-dependent chloroplast movements. Plant Cell Environ. 34, 2047-2059. (doi:10.1111/j.1365-3040. 2011.02402.x)
48. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M. 2002 Chloroplast avoidance movement reduces photodamage in plants. Nature 420, 829-832. (doi:10.1038/nature01213)
49. Suetsugu N, Wada M. 2007 Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol. Chem. 388, 927-935. (doi:10.1515/BC.2007.118)
50. Ettinger WF, Clear AM, Fanning KJ, Peck ML. 1999 Identification of a Ca2{thorn}/Hflantiport in the plant chloroplast thylakoid membrane. Plant Physiol. 119, 1379-1386. (doi:10.1104/pp.119.4.1379)
51. Ruban AV, Horton P. 1995 An investigation of the sustained component of nonphotochemical quenching of chlorophyll fluorescence in isolated chloroplasts and leaves of spinach. Plant Physiol. 108, 721-726.
52. Horton P. 1996 Nonphotochemical quenching of chlorophyll fluorescence. In Light as an energy source and information carrier in plant physiology (ed. RC Jennings), pp. 99-111. New York, NY: Plenum Press.
53. Finazzi G, Johnson GN, Dall'Osto L, Joliot P, Wollman FA, Bassi R. 2004 A zeaxanthinindependent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc. Natl Acad. Sci. USA 101, 12 375-12 380. (doi:10.1073/pnas.0404798101)
54. Johnson MP, Ruban AV. 2011 Restoration of rapidlyreversible photoprotective energy dissipation in the absence of PsbS protein by enhanced DpH. J. Biol. Chem. 286, 19 973-19 981. (doi:10.1074/ jbc.M111.237255)