Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities

Photosynthesis Research

Volumn 126, Issue 2-3, 2015, Pages 261-274

  Ware, Maxwell A ^a   Belgio, Erica ^a   Ruban, Alexander V ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Arabidopsis; LHCII; Light acclimation; Photosystem II; Protective NPQ

Indexed keywords

CHLOROPHYLL; LIGHT HARVESTING SYSTEM; PHOTOSYSTEM II;

ACCLIMATIZATION; ARABIDOPSIS; CHLOROPLAST; FLUORESCENCE; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; RADIATION RESPONSE; THYLAKOID;

ACCLIMATIZATION; ARABIDOPSIS; CHLOROPHYLL; CHLOROPLASTS; FLUORESCENCE; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; THYLAKOIDS;

EID: 84942828707     PISSN: 01668595     EISSN: 15735079     Source Type: Journal    
DOI: 10.1007/s11120-015-0102-4     Document Type: Article

References (93)

1. 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
2. Amunts A, Toporik H, Borovikova A, Nelson N (2010) Model of plant photosystem I structure determination and improved and biogenesis: membrane transport, structure, function. J Biol Chem 285:3478-3486
3. Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organisation in sun/shade acclimation. Aust J Plant Physiol 15:11-26
4. Aro E-M, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 130:835-843
5. Bailey S, Horton P, Walters RG (2004) Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta 218:793-802
6. Bassi R, Dainese P (1992) A supramolecular light-harvesting complex from chloroplast photosystem-II membranes. Eur J Biochem 204:317-326
7. Bassi R, Høyer-Hansen G, Barbato R et al (1987) Chlorophyll-proteins of the photosystem II antenna system. J Biol Chem 27:13333-13341
8. Belgio E, Johnson MP, Jurić S, Ruban AV (2012) Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime-both the maximum and the nonphotochemically quenched. Biophys J 102:2761-2771
9. Belgio E, Kapitonova E, Chmeliov E, Duffy CDP, Ungerer P, Valkunas L, Ruban AV (2014) Economic photoprotection in Photosystem II that retains a complete light harvesting system with slow energy traps. Nat Commun 5:4433
10. 2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489-504
11. Björkman O, Demmig-Adams B (1994) Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer-Verlag, Berlin, pp 17-47
12. Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J, Rögner M (1995) Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci 92:175-179
13. Boekema EJ, van Roon H, Dekker JP (1998) Specific association of photosystem II and light-harvesting complex II in partially solubilized photosystem II membranes. FEBS Lett 424:95-99
14. Briantais J-M, Vemotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128-138
15. Butler WL (1980) Energy transfer between photosystem II units in a connected package model of the photochemical apparatus of photosynthesis (photochemical model). Proc Natl Acad Sci USA 77:4697-4701
16. Caffarri S, Broess K, Croce R, van Amerongen H (2009) Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys J 100:2094-2103
17. Caffarri S, Croce R, Breton J, Bassi R (2001) The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J Biol Chem 276:35924-35933
18. Chazdon RL, Pearcy RW (1991) The importance of sunflecks for forest understory plants. Bioscience 41:760-766
19. Chow WS, Melis A, Anderson JM (1990) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc Natl Acad Sci 87:7502-7506
20. Dall'Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6:32
21. 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
22. De Las Rivas J, Andersson B, Barber J (1992) Two sites of primary degradation of the D1-protein induced by acceptor or donor side photo-inhibition in photosystem II core complexes. FEBS Lett 301:246-252
23. De Las Rivas J, Shipton CA, Ponticos M, Barber J (1993) Acceptor side mechanism of photoinduced proteolysis of the D1 protein in photosystem II reaction centers. Biochemistry 32:6944-6950
24. Demmig-Adams B (1990) Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1-24
25. Duffy CDP, Chmeliov J, Macernis M, Sulskus J, Valkunas L, Ruban AV (2013) Light-harvesting processes in the dynamic photosynthetic antenna. J Phys Chem B 15:18752-18770
26. Engelmann ECM, Zucchelli G, Garlaschi FM, Casazza AP, Jennings RC (2005) The effect of outer antenna complexes on the photochemical trapping rate in barley thylakoid Photosystem II. BBA 1706:276-286
27. 2 assimilation and photochemical efficiency of photosystem II. Plant, Cell Environ 15:809-820
28. Farber A, Young AJ, Ruban AV, Horton P, Jahns P (1997) Dynamics of xanthophyll cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants. Plant Physiol 115:1609-1618
29. Frank HA, Chynwat V, Desamero RZB, Farhoosh R, Erickson J, Bautista J (1997) On the photophysics and photochemical properties of carotenoids and their role as light-harvesting pigments in photosynthesis. Pure Appl Chem 69:2117-2124
30. Gamon JA, Pearcy RW (1989) Leaf movement, stress avoidance and photosynthesis in Vitis californica. Oecologia 79:475-481
31. Gilmore AM, Mohanty N, Yamamoto HY (1994) Epoxidation of zeaxanthin and antheraxanthin reverses nonphotochemical quenching of photo-system-II chlorophyll-a fluorescence in the presence of trans-thylakoid delta-pH. FEBS Lett 350:271-274
32. Goral TK, Johnson MP, Duffy CD, Brain AP, Ruban AV, Mullineaux CW (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J 69:289-301
33. Groom QJ, Baker NR (1992) Analysis of light-induced depressions of photosynthesis in leaves of a wheat crop during the winter. Plant Physiol 100:1217-1223
34. Havaux M, Straser RJ, Greppin H (1991) A theoretical and experimental analysis of the qP and qN coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27:41-55
35. He J, Chee CW, Goh CJ (1996) 'Photoinhibition' of Heliconia under natural tropical conditions: the importance of leaf orientation for light interception and leaf temperature. Plant, Cell Environ 19:1238-1248
36. Hogewoning SW, Wientjes E, Douwstra P, Trouwborst G, van Ieperen W, Croce R, Harbinson J (2012) Photosynthetic quantum yield dynamics: from photosystems to leaves. Plant Cell 24:1921-1935
37. Holt NE, Zigmantas D, Valkunas L, Li X-P, Niyogi KK, Flemming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433-436
38. Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P (2009) Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 483:262-267
39. Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynth Res 34:375-385
40. Horton P, Ruban AV, Wentworth M (2000) Allosteric regulation of the light harvesting system of photosystem II. Philos Trans R Soc 355:1361-1370
41. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182-193
42. Johnson MP, Goral TK, Duffy CDP, Brain APR, 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
43. Johnson MP, Perez-Bueno ML, Zia A, Horton P, Ruban AV (2009) The zeaxanthin-independent and zeaxanthin-dependent qE components of nonphotochemical quenching involve common conformational changes within the photosystem II antenna in Arabidopsis. Plant Physiol 149:1061-1075
44. Johnson MP, Ruban AV (2010) Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J 61:283-289
45. 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
46. Kereïche S, Kiss AZ, Kouril R, Boekema E, Horton P (2010) The PsbS protein controls the macro-organization of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 584:754-764
47. Kouřil R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817:2-12
48. Krause GH, Behrend U (1986) ΔpH-dependent chlorophyll fluorescence quenching indicating a mechanism of protection against photoinhibition of chloroplasts. FEBS Lett 200:298-302
49. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313-349
50. Lee HY, Hong YN, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212:332-342
51. Leong TY, Anderson JM (1984a) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. 1. Study on the distribution of chlorophyll-protein complexes. Photosynth Res 5:105-115
52. Leong TY, Anderson JM (1984b) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. 2. Regulation of electron transport capacities, electron carriers, coupling factor (CF1) activity and rates of photosynthesis. Photosynth Res 5:117-128
53. Li X-P, Björkman 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
54. Lichtenthaler HK, Buschmann C, Döll M, Fietz HJ, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynth Res 2:115-141
55. Malkin S, Armond PA, Mooney HA, Fork DC (1981) Photosystem II photosynthetic unit sizes from fluorescence induction in leaves: correlation to photosynthetic capacity. Plant Physiol 67:570-579
56. Matsubara S, Chow W (2004) Populations of photoinhibited photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo. Proc Natl Acad Sci USA 101:18234-18239
57. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 345:659-668
58. Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M, Garab G, Croce R, Holzwarth AR (2008) Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett 582:3625-3631
59. Müller MG, Lambrev P, Reus M, Wientjes E, Croce R, Holzwarth AR (2010) Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. ChemPhysChem 11:1289-1296
60. Mullineaux CW, Ruban AV, Horton P (1994) Prompt heat release associated with ΔpH-dependent quenching in spinach thylakoid membranes. Biochim Biophys Acta 1185:119-123
61. Noctor G, Ruban AV, Horton P (1993) Modulation of ΔpH-dependent nonphotochemical quenching of chlorophyll fluorescence in spinach chloroplasts. Biochim Biophys Acta 1183:339-344
62. Ögren E, Sjöström M (1990) Estimation of the effect of photoinhibition on the carbon gain in leaves of a willow canopy. Planta 181:560-567
63. Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane-protein damage and repair - removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 99:481-485
64. Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence of photosynthetic efficiency into photochemical components - calculation of qP and Fv′/Fm′ without measuring Fo′. Photosynth Res 54:135-142
65. Pessarakli M (2005) Handbook of photosynthesis II, 2nd edn. Taylor and Francis Group, Boca Raton
66. Peter GF, Thornber PJ (1991) Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Biol Chem 266:16745-16754
67. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll a and chlorophyll b extracted with 4 different solvents - verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim Biophys Acta 975:384-394
68. Ruban AV (2009) Plants in light. Commun Integr Biol 2:50-55
69. Ruban AV (2012) The photosynthetic membrane: molecular mechanisms and biophysics of light harvesting. Wiley-Blackwell, Chichester. ISBN 978-1-1199-6053-9
70. Ruban AV, Belgio E (2014) The relationship between maximum tolerated light intensity and non-photochemical chlorophyll fluorescence quenching: chloroplast gains and losses. Philos Trans R Soc Lond B 369:20130222
71. Ruban AV, Horton P (1992) Mechanism of delta pH-dependent dissipation of absorbed excitation energy by photosynthetic membranes. I. Spectroscopic analysis of isolated light harvesting complexes. Biochim Biophys Acta 1102:30-38
72. Ruban AV, Horton P (1999) The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light harvesting complexes, intact chloroplasts and leaves. Plant Physiol 119:531-542
73. Ruban AV, Johnson MP, Duffy CDP (2012) Photoprotective molecular switch in photosystem II. Biochim Biophys Acta 1817:167-181
74. Ruban AV, Murchie MH (2012) Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: a new approach. Biochim Biophys Acta 1817:977-982
75. Ruban AV, Solovieva S, Horton P et al (2006) Plasticity in the composition of the light harvesting antenna of higher plants preserves structural integrity and biological function. J Biol Chem 281:14981-14990
76. Ruban AV, Young A, Pascal A, Horton P (1994) The effects of illumination on the xanthophyll composition of the photosystem II light harvesting complexes of spinach thylakoid membranes. Plant Physiology 104:227-234
77. Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci 98:6969-6974
78. Seeman JR, Sharkey TD, Wang J, Osmanod CB (1987) Environmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. Plant Physiol 84:796-802
79. Siefermann D, Yamamoto HY (1975) Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts: a transmembrane model for the violaxanthin cycle. Biochem Biophys Res Commun 62:456-461
80. Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM (2006) State transitions revisited - a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779-793
81. Trissl HW, Lavergne J (1994) Fluorescence induction from photosystem II: analytical equations for the yields of photochemistry and fluorescence derived from analysis of a model including exciton-radical pair equilibrium and restricted energy transfer between photosynthetic units. Aust J Plant Physiol 22:183-193
82. Tsuboi H, Wada M (2011) Chloroplasts can move in any direction to avoid strong light. J Plant Res 124:201-210
83. Valkunas L, Chmeliov J, Trinkunas G, Duffy CDP, van Grondelle R, Ruban AV (2011) Excitation migration, quenching, and regulation of photosynthetic light harvesting in photosystem II. J Phys Chem B 115:9252-9260
84. Valladares F, Pearcy RW (1997) Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia. Plant, Cell Environ 20:25-36
85. van Oort B, Alberts M, de Bianchi S, Dall'Osto L, Bassi R, Trinkunas G, Croce R, van Amerongen H (2010) Effect of antenna depletion in photosystem II on excitation energy transfer in Arabidopsis thaliana. Biophys J 98:922-931
86. Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci 89:1408-1412
87. Wahadoszamen M, Berera R, Ara AM, Romero E, van Grondelle R (2012) Identification of two emitting sites in the dissipative state of the major light harvesting antenna. Phys Chem Chem Phys 14:759-766
88. Walters RG, Horton P (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PS II fluorescence in barley leaves. Photosynth Res 36:119-139
89. Ware MA, Belgio E, Ruban AV (2014) Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin. J Exp Bot. doi: 10.1093/jxb/eru477
90. Wientjes E, van Amerongen H, Croce R (2013) Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation. J Phys Chem 117:11200-11208
91. Yakushevska AE, Keegstra W, Boekema EJ, Dekker JP, Andersson J, Jansson S, Ruban AV, Horton P (2003) The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. Biochemistry 42:608-613
92. Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51:639-648
93. Yamamoto HY, Kamite L (1972) The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochim Biophys Acta 267:538-543