Evolution under the sun: Optimizing light harvesting in photosynthesis

Journal of Experimental Botany

Volumn 66, Issue 1, 2015, Pages 7-23

  Ruban, Alexander V ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Evolution of light harvesting antennae; Light adaptation; Photoinhibition; Photoprotection; Photosynthetic light harvesting; Reaction centre turnover

Indexed keywords

EMBRYOPHYTA;

ADAPTATION; EVOLUTION; METABOLISM; PHOTOSYNTHESIS; PLANT; SUNLIGHT;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; PHOTOSYNTHESIS; PLANTS; SUNLIGHT;

EID: 84922544674     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru400     Document Type: Article

References (114)

1. Allen JF, Nilsson A. 1997. Redox signalling and the structural basis of regulation of photosynthesis by protein phosphorylation. Physiologia Plantarum 100, 863-868.
2. Anderson J, Chow WS, De Las Rivas J. 2008. Dynamic flexibility in the structure and function of photosystem II in higher plant thylakoid membranes: the grana enigma. Photosynthesis Research 98, 575-587.
3. Anderson JM, Chow WS, Goodchild DJ. 1988. Thylakoid membrane organisation in sun/shade acclimation. Australian Journal of Plant Physiology 15, 11-26.
4. Anderson JM, Osmond B. 2001. Sun-shade responses: Compromises between acclimation and photoinhibition. In: Kyle, DJ, Osmond B, Arntzen CJ, eds. Photoinhibition. Amsterdam: Elsevier, 1-38.
5. Andersson B, Aro EM. 1997. Proteolytic activities and proteases of plant chloroplasts. Physiologia Plantarum 100, 780-793.
6. Baker NR, Horton P. 1987. Physiological factors associated with fluorescence quenching during photoinhibition. In: Arntzen CJ, Kyle DJ, Osmond CB, eds. Topics in photosynthesis, photoinhibition , vol. 9. Amsterdam: Elsevier, 145-168.
7. Barber J. 1995. Molecular-basis of the vulnerability of photosystem-II to damage by light. Australian Journal of Plant Physiology 22, 201-208.
8. Bassi R, Caffarri S. 2000. Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls. Photosynthesis Research 64, 243-256.
9. Beddard GS, Porter G. 1976. Concentration quenching in chlorophyll. Nature 260, 366-367.
10. Belgio E, Johnson MP, Juri 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. Biophysical Journal 102, 2761-2771.
11. 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. Nature Communications , doi: 10.1038/ncomms5433.
12. Bennett J. 1977. Phosphorylation of chloroplast membrane proteins. Nature 269, 344-346.
13. Bennett J. 1983. Regulation of photosynthesis by reversible phosphorylation of the light-harvesting chlorophyll a/b protein. Biochemical Journal 212, 1-13.
14. Bergantino E, Segalia A, Brunetta A, Teardo E, Rogoni F, Giacometti GM, Szabo I. 2003. Light-and pH-dependent structural changes in the PsbS protein of photosystem II. Proceedings of the National Academy of Sciences, USA 100, 15265-15270.
15. Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, DallOsto L, Morosinotto T, Bassi R. 2009. Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. Journal of Biological Chemistry 284, 15255-15266.
16. Blankenship R. 2002. Molecular mechanisms of photosynthesis. London: Blackwell Science.
17. Bonaventura C, Mayers J. 1969. Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochimica et Biophysica Acta 189, 366-383.
18. Briantais, J-M, Vemotte C, Picaud M, Krause GH. 1979. A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochimica et Biophysica Acta 548, 128-138.
19. Brugnoli E, Scartazza A, De Tullio MC, Monteverdi MC, Lauteri M, Augusti A. 1998. Zeaxanthin and non-photochemical quenching in sun shade leaves of C3 and C4 plants. Physiologia Plantarum 104, 727-734.
20. Camm EL, Green BR. 2004. How the chlorophyll-proteins got their names. Photosynthesis Research , 80, 189-196.
21. Clayton RK. 1970. Light and living matter, vol. 2. The biological. New York: McGraw-Hill.
22. Clayton RK. 1980. Photosynthesis. Physical mechanisms and chemical patterns. Cambridge: Cambridge University Press.
23. Cogdell RJ, Isaacs NW. 1995. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374, 517-521.
24. Crouchman S, Ruban AV, Horton P. 2006. PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin. FEBS Letters 580, 2053-2058.
25. Darwin CR. 1865. On the movements and habits of climbing plants. Journal of the Linnean Society of London (Botany) 9, 1-118.
26. Darwin CR. 1877. The genus agave. The Gardeners Chronicle , 29 December, 807.
27. Darwin CR. 1880. The power of movement in plants. London: John Murray.
28. Darwin CR. 1881. Movements of plants. Nature. A Weekly Illustrated Journal of Science 23, 409.
29. Demetrius L, Ziehe M. 2007. Darwinian fitness. Theoretical Population Biology 72, 323-345.
30. Demmig B, Winter K, Kruger A, Czygan F-C. 1987. Photoinhibition and zeaxanthin formation in intact leaves. Plant Physiology 84, 218-224.
31. Demmig-Adams B. 1990. Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. Biochimica et Biophysica Acta 1020, 1-24.
32. Demmig-Adams B. 1998. Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiology 39, 474-482.
33. Demmig-Adams B, Adams III WW. 1992. Photoprotection and other responses of plants to high light stress. Annual Reviews of Plant Physiology and Plant Molecular Biology 43, 599-626.
34. Deng XW, Melis A. 1986. Phosphorylation of the light-harvesting complex-ii in higher-plant chloroplasts-effect on photosystem-II and photosystem-II absorption cross-section. Photobiochemistry and Photobiophysics 13, 41-52.
35. Duffy CDP, Chmeliov J, Macernis M, Sulskus J, Valkunas L, Ruban AV. 2013b. Modeling of fluorescence quenching by lutein in the plant light-harvesting complex LHCII. Journal of Physical Chemistry B 117, 10975-10986.
36. Duffy CDP, Valkunas L, Ruban AV. 2013a. Light-harvesting processes in the dynamic photosynthetic antenna. Physical Chemistry and Chemical Physics 15, 18752-18770.
37. Emerson R, Arnold W. 1932. The photochemical reaction in photosynthesis. Journal of General Physiology 16, 191-205.
38. Fork DC, Herbert SK. 1993. Electron-transport and photophosphorylation by photosystem-I in-vivo in plants and cyanobacteria. Photosynthesis Research 36, 149-168.
39. Frster T. 1948. Zwischenmolekulare Energiewanderung und Fluoreszenz. Annalen der Physik 437, 55-75.
40. Genty B, Briantais J-M, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87-92.
41. Goral TK, Johnson MP, Duffy CDP, Brain APR, Ruban AV, Mullineaux CW. 2012. Light-harvesting antenna composition controls the macromolecular organization and dynamics of thylakoid membranes in Arabidopsis. Plant Journal 69, 289-301.
42. Green BR, Durnford DG. 1996. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annual Reviews of Plant Physiology Plant Molecular Biology 47, 685-714.
43. Grime JP. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist 111, 1169-1194.
44. Harrison MA, Allen JF. 1992. Protein-phosphorylation and Mg-2+ influence light harvesting and electron-transport in chloroplast thylakoid membrane material containing only the chlorophyll-a/b-binding lightharvesting complex of photosystem-II and photosystem-I. European Journal of Biochemistry 204, 1107-1114.
45. Harrison MA, Allen JF. 1993. Differential phosphorylation of individual LHC-II polypeptides during short-term and long-term acclimation to light regime in the green-alga Dunaliella salina. Biochimica et Biophysica Acta 1141, 37-44.
46. Haworth P, Melis A. 1983. Phosphorylation of chloroplast thylakoid membrane-proteins does not increase the absorption cross-section of photosystem-1. FEBS Letters 160, 277-280.
47. Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P. 2009. Identification of two quenching sites active in the regulation of photosynthetic lightharvesting studied by time-resolved fluorescence. Chemical Physics Letters 483, 262-267.
48. Horton P, Black MT. 1983. A comparison between cation and proteinphosphorylation effects on the fluorescence induction curve in chloroplasts treated with 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Biochimica et Biophysica Acta 722, 214-218.
49. Horton P, Ruban AV. 1992. Regulation of photosystem II. Photosynthesis Research 34, 375-385.
50. Horton P, Allen JF, Black MT, Bennett J. 1981. Regulation of phosphorylation of chloroplast membrane proteins by the redox state of plastoquinone. FEBS Letters 125, 193-196.
51. Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ. 1991. Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Letters 292, 1-4.
52. Horton P, Ruban AV, Walters RG. 1996. Regulation of light harvesting in green plants. Annual Reviews in Plant Physiology and Plant Molecular Biology 47, 655-684.
53. Horton P, Ruban AV, Wentworth M. 2000. Allosteric regulation of the light harvesting system of photosystem II. Philosophical Transactions of the Royal Society B 355, 1361-1370.
54. Ilioaia C, Johnson M, Horton P, Ruban AV. (2008) Induction of efficient energy dissipation in the isolated light harvesting complex of photosystem II in the absence of protein aggregation, Journal of Biological Chemistry 283, 29505-29512.
55. Jahns P, Holzwarth AR. 2012. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta 1817, 182-193.
56. Jia H, Liggins JR, Chow WS. 2012. Acclimation of leaves to low light produces large grana: the origin of the predominant attractive force at work. Philosophical Transactions of the Royal Society B 367, 3494-3502.
57. Johnson MP, Ruban AV. 2010. Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. The Plant Journal 61, 283-289.
58. Johnson MP, Ruban AV. 2011. Restoration of rapidly-reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced ΔpH. Journal of Biological Chemistry 286, 19973-19981.
59. 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. The Plant Cell 23, 1468-1479.
60. Johnson MP, Zia A, Horton P, Ruban AV. 2010. Effect of xanthophyll composition on the chlorophyll excited state lifetime in plant leaves and isolated LHCII. Chemical Physics 373, 23-32.
61. Kiss AZ, Ruban AV, Horton P. 2008. The PsbS protein controls the organisation of the photosystem II antenna in higher plant thylakoid membranes. Journal of Biological Chemistry 283, 3972-3978.
62. Kouril R, Wientjes E, Bultema JB, Croce R, Boekema EJ. 2013. Highlight vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochimica Biophysica Acta 1827, 411-419.
63. Kouril R, Zygadlo A, Arteni AA, de Wit CD, Dekker JP, Jensen P-E, Scheller HV, Boekema EJ. 2005. Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44, 10935-10940.
64. Krause GH. 1974. Changes in chlorophyll fluorescence in relation to lightdependent cation transfer across thylakoid membranes. Biochimica et Biophysica Acta 333, 301-313.
65. Krause GH, Weis E. 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annual Reviews in Plant Physiology and Plant Molecular Biology 42, 313-349.
66. Klheim C, gren J, Jansoon S. 2002. Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91-93.
67. Kyle DJ, Arntzen CJ. 1983. Thylakoid membrane protein phosphorylation selectively alters the local membrane surface charges near the primary acceptor of photosystem II. Photobiochemistry and Photobiophysics 5, 11-25.
68. Kyle DJ, Baker NR, Arntzen CJ. 1983. Spectral characterization of photosystem-I fluorescence at room-temperature using thylakoid proteinphosphorylation. Photobiochemistry and Photobiophysics 5, 79-85.
69. Lee AG. 1975. Segregation of chlorophyll a incorporated into lipid bilayers. Biochemistry 14, 4397-4402.
70. Li XP, Bjrkman, 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.
71. Lindahl M, Andersson B. 1992. A proteolytic activity associated with loss of LHCII during acclimation of spinach leaves from low to high light. Photosynthesis Research 34, 121-121.
72. Lindahl M, Yang DH, Andersson B. 1995. Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem-II by a light-induced membrane-associated enzymatic system. European Journal of Biochemistry 231, 503-509.
73. Liu ZF, Yan HC, Wang KB, Kuang TY, Zhang JP, Gui LL, An XM, Chang WR. 2004. Crystal structure of spinach major-light harvesting complex at 2.72 resolution. Nature 428, 287-292.
74. 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 Letters 582, 3625-3631.
75. Mullet JE. 1983. The amino-acid-sequence of the polypeptide segment which regulates membrane adhesion (grana stacking) in chloroplasts. Journal of Biological Chemistry 258, 9941-9948.
76. Murata N, Sugahara K. 1969. Control of excitation transfer in photosynthesis. III. Light-induced decrease of chlorophyll a fluorescence related to phosphorylation system in spinach chloroplasts. Biochimica et Biophysica Acta 189, 182-192.
77. Nilsson A, Stys D, Drakenberg T, Spangfort MD, Forsen S, Allen JF. 1997. Phosphorylation controls the three-dimensional structure of plant light harvesting complex II. Journal of Biological Chemistry 272, 18350-18357.
78. Niyogi KK, Truong TB. 2013. Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Current Opinions in Plant Biology 16, 307-314.
79. Noctor G, Rees D, Young A, Horton P. 1991. The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence and the transthylakoid pH-gradient in isolated chloroplasts, Biochimica et Biophysica Acta 1057, 320-330.
80. Noctor G, Ruban AV, Horton P. 1993. Interactions between the effects of potentiators and antagonists of ΔpH-dependent thermal dissipation of excitation energy in spinach thylakoids. Biochimica et Biophysica Acta 1183, 339-344.
81. Ohad I, Kyle DJ, Arntzen CJ. 1984. Membrane-protein damage and repair-removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. Journal of Cell Biology 99, 481-485.
82. Oxborough K, Baker NR. 1997. Resolving chlorophyll a fluorescence of photosynthetic efficiency into photochemical components-calculation of qP and Fv/Fm without measuring Fo. Photosynthesis Research 54, 135-142.
83. Pogson BJ, Niyogi KK, Bjrkman O, DellaPenna D. 1998. Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences, USA 95, 13324-13329.
84. Powles SB. 1984. Photoinhibition of photosynthesis induced by visiblelight. Annual Reviews in Plant Physiology Plant Molecular Biology 35, 15-44.
85. Raven JA. 1994. The cost of photoinhibition to plant communities. In: Baker NR, Bowyer JR, eds. Photoinhibition of photosynthesis. From molecular mechanisms to the field. Oxford: Bios Scientific Publishers, 449-464.
86. Rees D, Young A, Noctor G, Britton G, Horton P. 1989. Enhancement of the ΔpH-dependent dissipation of excitation energy in spinach chloroplasts by light-activation; correlation with the synthesis of zeaxanthin, FEBS Letters 256, 85-90.
87. Rees D, Noctor G, Ruban AV, Crofts J, Young A, Horton P. 1992. pH dependent chlorophyll fluorescence quenching in spinach thylakoids from light-treated or dark-adapted leaves, Photosynthesis Research 31, 11-19.
88. Rivas JD, 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.
89. Ruban AV. 1991. The use of excitation fluorescence spectroscopy in the study of short-term chloroplast membrane reorganization. Biochimica et Biophysica Acta 1058, 411-415.
90. Ruban A. 2012. The photosynthetic membrane: molecular mechanisms and biophysics of light harvesting. Wiley-Blackwell: Chichester.
91. Ruban AV, Belgio E. 2014. The relationship between maximum tolerated light intensity and non-photochemial chlorophyll fluorescence quenching: chloroplast gains and losses. Philosophical Transactions of the Royal Society B 369, 20130222.
92. Ruban AV, Horton P. 1999. The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiology 119, 531-542.
93. Ruban AV, Johnson MP. 2009. Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynthesis Research 99, 173-183.
94. Ruban AV, Murchie EH. 2012. Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: a new approach. Biochimica et Biophysica Acta 1817, 977-982.
95. Ruban AV, Duffy CDP, Johnson MP. 2011. Natural light harvesting: principles and environmental trends. Energy and Environmental Science 4, 1643-1650.
96. Ruban AV, Johnson MP, Duffy CDP. 2012. Photoprotective molecular switch in photosystem II. Biochimica et Biophysica Acta 1817, 167-181.
97. Ruban AV, Lee PJ, Wentworth M, Young AJ, Horton P. 1999. Determination of the stoichiometry and strength of binding of different xanthophylls to the photosystem II light harvesting complexes. Journal of Biological Chemistry 274, 10458-10465.
98. Ruban AV, Pesaresi P, Wacker U, Irrgang K-DJ, Bassi R, Horton P. 1998. The relationship between the binding of dicyclohexylcarbodiimide and pH-dependent quenching of chlorophyll fluorescence in the light harvesting proteins of photosystem II. Biochemistry 37, 11586-11591.
99. Ruban AV, Walters RG, Horton P. 1992. The molecular mechanism of the control of excitation energy dissipation in the chloroplast membranes; inhibition of pH-dependent quenching of chlorophyll fluorescence by dicyclohexylcarbodiimide. FEBS Letters 309, 175-179.
100. Ruban AV, Young A, Horton P. 1994. Modulation of chlorophyll fluorescence quenching in isolated light-harvesting complex of photosystem-II. Biochimica et Biophysica Acta 1186, 123-127.
101. Santabarbara S, Barbato R, Zucchelli G, Garlaschi FM, Jennings RC. 2001. The quenching of photosystem II fluorescence does not protect the D1 protein against light induced degradation in thylakoids. FEBS Letters 505, 159-162.
102. Schreiber U. 1986. Detection of rapid induction kinetics with a new type of high frequency modulated chlorophyll fluorometer. Photosynthesis Research 9, 261-272.
103. Staehelin LA, Arntzen CJ. 1983. Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organisation of membrane components. Journal of Cell Biology 97, 1327-1337.
104. Sundby C, Andersson B. 1985. Temperature-induced reversible migration along the thylakoid membrane of photosystem-ii regulates its association with LHC-II. FEBS Letters 191, 24-28.
105. Sundby C, Melis A, Maenpaa P, Andersson B. 1986. Temperaturedependent changes in the antenna size of photosystem-II-reversible conversion of photosystem-II-alpha to photosystem-II-beta. Biochimica et Biophysica Acta 851, 475-483.
106. Teardo E, de Laureto PP, Bergantino E, Dalla Vecchia F, Rigoni F, Szabo D, Giacometti GM. 2007. Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids, Biochimica et Biophysica Acta 1767, 703-711.
107. Telfer A, He WZ, Barber J. 1990. Spectral resolution of more than one chlorophyll electron-donor in the isolated photosystem-II reaction center complex. Biochimica et Biophysica Acta 1017, 143-151.
108. Telfer A, Whitelegge JP, Bottin H, Barber J. 1986. Changes in the efficiency of P700 photooxidation in response to protein-phosphorylation detected by flash absorption-spectroscopy. Journal of The Chemical Society-Faraday Transactions II 82, 2207-2215.
109. Thornber, JP. 1975. Chlorophyll-proteins: light-harvesting and reaction center components of plants. Annual Review of Plant Physiology 26, 127-158.
110. Valkunas L, Chmeliov E, Trinkunas G, Duffy CDP, van Grondelle R, Ruban AV. 2011. Excitation migration, quenching and regulation of photosynthetic light harvesting in photosystem II. Journal of Physical Chemistry B 115, 9252-9260.
111. van Amerongen H, Croce R. 2013. Light harvesting in photosystem II. Photosynthesis Research 116, 251-263.
112. Wiesner J. 1875. Zum schutze des chlorophylls der lebenden pflanze. Die Naturlichen Einrichtungen der Zool.-Bot. Society 19-42.
113. Wraight CA, Crofts AR. 1970. Energy-dependent quenching of chlorophyll a fluorescence in isolated chloroplasts. European Journal Biochemistry 17, 319-327.
114. Zaks J, Amarnath K, Sylak-Glassman EJ, Fleming GR. 2013 Models and measurements of energy-dependent quenching. Photosynthesis Research 116, 389-409.