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How Protein Disorder Controls Non-Photochemical Fluorescence Quenching

  • Tjaart P. J. KrügerEmail author
  • Cristian Ilioaia
  • Peter Horton
  • Maxime T. A. Alexandre
  • Rienk van Grondelle
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 40)

Summary

We discuss the de-excitation of electronically excited states of chlorophyll a, monitored via non-photochemical quenching (NPQ) of chlorophyll fluorescence, with respect to (i) involvement of the main light-harvesting complex of photosystem II (LHCII trimers) and (ii) a change in pigment properties following a change in the conformation of this protein complex. We suggest that LHCII exhibits dynamic behavior arising from a fundamental property of proteins, i.e., their intrinsic disorder. Photosynthetic pigment-protein complexes, such as LHCII, constitute complex environments. The pigments responsible for absorption and subsequent transfer of light energy are subject to multiple interactions in a highly heterogeneous protein environment. This feature gives rise to an intrinsic structural and energetic disorder of the pigment-protein complexes as well as complicated dynamics of excitation-energy transfer within the complexes. In particular, individual complexes show rapid and reversible quenching on timescales of milliseconds to minutes. We propose that plants employ this intrinsic capacity to reversibly switch between unquenched and quenched states to control the de-excitation (i.e., thermal dissipation) of potentially harmful excess excitation energy. Modulation of de-excitation by the local environment of pigment complexes will be demonstrated, with a particular focus on how this modulation manifests itself as chlorophyll fluorescence quenching of individually measured LHCII trimers. It will be shown how the results point to the concept of environmentally controlled disorder as a basis for the energy-dependent component of NPQ, i.e., that the intrinsic capacity of a pigment-protein complex to rapidly switch between light-harvesting and dissipating states can be controlled by the local environment of the complex. This can be explained by assuming that pigment-protein complexes are in an unstable equilibrium between different structural and corresponding emissive states, where subtle perturbations in the physico-chemical environment can shift the equilibrium to favor one or more of these states. As such, regulation of a disordered conformational nanoswitch provides a satisfying explanation for NPQ.

Keywords

Dissipative State Thermal Energy Dissipation LHCII Trimer Conformational Selection LHCII Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

Chl

Chlorophyll

CT

Charge transfer

FL

Fluorescence

KD

Degree of thermal energy dissipation of a single complex

KD = IU/IQ − 1

Where IU and IQ refer to the fluorescence intensity in the unquenched and quenched environments, respectively

L

Lutein

LH

Light harvesting

Lhca

Light-harvesting complex of photosystem I

Lhcb

Light-harvesting complex of photosystem II

LHCII

Major light-harvesting complex II of plants

NPQ

Non-photochemical quenching of chlorophyll a fluorescence

PS I

Photosystem I

PS II

Photosystem II

qE

Energy-dependent component of NPQ

RC

Reaction center

S1

First excited state

SMS

Single-molecule spectroscopy

ß-DM

n-dodecyl-β, D-maltoside

V

Violaxanthin

VAZ

Violaxanthin-antheraxanthin-zeaxanthin

Z

Zeaxanthin

Notes

Acknowledgments

This work was supported by the EU FP6 Marie Curie Early Stage Training Network via the Advanced Training in Laser Sciences project (T.P.J.K.); EU FP7 Marie Curie Reintegration Grant (ERG 224796) (C.I.); CEA-Eurotalents program (European contract PCOFUND-GA-2008-228664) (C.I.); Project Sunshine, University of Sheffield (P.H.); TOP grant (700.58.305) from the Foundation of Chemical Sciences, part of the Netherlands Organization for Scientific Research (C.I. and R.v.G.); Netherlands Organization for Scientific Research program in Fundamental Research of Matter (The Thylakoid Membrane: A Dynamic Switch; FP126; 12.0344) (M.T.A.A. and R.v.G); Advanced Investigator Grant (267333, PHOTPROT) from the European Research Council (ERC) (C.I., T.P.J.K., and R.v.G.).

References

  1. Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH (1995) ‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–276Google Scholar
  2. Adams WW III, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2006) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams WW III, Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, Volume 21. Springer, Dordrecht, pp 49–64Google Scholar
  3. Barkai E, Jung YJ, Silbey R (2004) Theory of single-molecule spectroscopy: beyond the ensemble average. Annu Rev Phys Chem 55:457–507PubMedGoogle Scholar
  4. Barros T, Royant A, Standfuss J, Dreuw A, Kühlbrandt W (2009) Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state. EMBO J 28:298–306PubMedCentralPubMedGoogle Scholar
  5. Barzda V, Jennings RC, Zucchelli G, Garab G (1999) Kinetic analysis of the light-induced fluorescence quenching in light-harvesting chlorophyll a/b pigment-protein complex of photosystem II. Photochem Photobiol 70:751–759Google Scholar
  6. Beddard GS, Porter G (1976) Concentration quenching in chlorophyll. Nature 260:366–367Google Scholar
  7. 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 284:15255–15266PubMedCentralPubMedGoogle Scholar
  8. Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA 106:12311–12316PubMedCentralPubMedGoogle Scholar
  9. Boehr DD, Nussinov R, Wright PE (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5:789–796PubMedCentralPubMedGoogle Scholar
  10. Boekema EJ, Van Breemen JFL, Van Roon H, Dekker JP (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301:1123–1133PubMedGoogle Scholar
  11. Brecht M, Radics V, Nieder JB, Bittl R (2009) Protein dynamics-induced variation of excitation energy transfer pathways. Proc Natl Acad Sci USA 106:11857–11861PubMedCentralPubMedGoogle Scholar
  12. Brixner T, Stenger J, Vaswani HM, Cho M, Blankenship RE, Fleming GR (2005) Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434:625–628PubMedGoogle Scholar
  13. Bryngelson JD, Wolynes PG (1987) Spin glasses and the statistical mechanics of protein folding. Proc Natl Acad Sci USA 84:7524–7528PubMedCentralPubMedGoogle Scholar
  14. Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: differential analysis of the Lhcbl-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43:9467–9476PubMedGoogle Scholar
  15. Castelletti S, Morosinotto T, Robert B, Caffarri S, Bassi R, Croce R (2003) Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry 42:4226–4234PubMedGoogle Scholar
  16. Chin AW, Prior J, Rosenbach R, Caycedo-Soler F, Huelga SF, Plenio MB (2013) The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment-protein complexes. Nat Phys 9:113–118Google Scholar
  17. Chmeliov J, Valkunas L, Krüger TPJ, Ilioaia C, van Grondelle R (2013) Fluorescence blinking of single major light-harvesting complexes. New J Phys 15:085007Google Scholar
  18. Collini E, Wong CY, Wilk KE, Curmi PMG, Brumer P, Scholes GD (2010) Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463:644–647PubMedGoogle Scholar
  19. Croce R, Chojnicka A, Morosinotto T, Ihalainen JA, van Mourik F, Dekker JP, Bassi R, van Grondelle R (2007) The low-energy forms of photosystem I light-harvesting complexes: spectroscopic properties and pigment-pigment interaction characteristics. Biophys J 93:2418–2428PubMedCentralPubMedGoogle Scholar
  20. Cseh Z, Vianelli A, Rajagopal S, Krumova S, Kovacs L, Papp E, Barzda V, Jennings R, Garab G (2005) Thermo-optically induced reorganizations in the main light harvesting antenna of plants. I. Non-arrhenius type of temperature dependence and linear light-intensity dependencies. Photosynth Res 86:263–273PubMedGoogle Scholar
  21. Dainese P, Bassi R (1991) Subunit stoichiometry of the chloroplast photosystem-II antenna system and aggregation state of the component chlorophyll a/b binding-proteins. J Biol Chem 266:8136–8142PubMedGoogle Scholar
  22. Damjanović A, Ritz T, Schulten K (2000) Excitation energy trapping by the reaction center of Rhodobacter sphaeroides. Int J Quantum Chem 77:139–151Google Scholar
  23. Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482Google Scholar
  24. Demmig-Adams B, Adams WW III (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470Google Scholar
  25. Demmig-Adams B, Adams WW III, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy-dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22:249–260Google Scholar
  26. Demmig-Adams B, Moeller DL, Logan BA, Adams WW III (1998) Positive correlation between levels of retained zeaxanthin plus antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill. Planta 205:367–374Google Scholar
  27. Elber R, Karplus M (1987) Multiple conformational states of proteins – a molecular-dynamics analysis of myoglobin. Science 235:318–321PubMedGoogle Scholar
  28. Engel GS, Calhoun TR, Read EL, Ahn TK, Mančal T, Cheng YC, Blankenship RE, Fleming GR (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782–786PubMedGoogle Scholar
  29. Förster T (1965) Delocalized excitation and excitation transfer. In: Sinanoglu O (ed) Modern Quantum Chemistry. Academic, New York, pp 93–137Google Scholar
  30. Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR (1994) Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth Res 41:389–395PubMedGoogle Scholar
  31. Frauenfelder H, Petsko GA, Tsernoglou D (1979) Temperature-dependent X-ray-diffraction as a probe of protein structural dynamics. Nature 280:558–563PubMedGoogle Scholar
  32. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254:1598–1603PubMedGoogle Scholar
  33. Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proc Natl Acad Sci USA 97:11098–11101PubMedCentralPubMedGoogle Scholar
  34. Gilmore AM, Matsubara S, Ball MC, Barker DH, Itoh S (2003) Excitation energy flow at 77 K in the photosynthetic apparatus of overwintering evergreens. Plant Cell Environ 26:1021–1034Google Scholar
  35. Green BR, Pichersky E, Kloppstech K (1991) Chlorophyll-a/b-binding proteins – an extended family. Trends Biochem Sci 16:181–186PubMedGoogle Scholar
  36. Gulbinas V, Karpicz R, Garab G, Valkunas L (2006) Nonequilibrium heating in LHCII complexes monitored by ultrafast absorbance transients. Biochemistry 45:9559–9565PubMedGoogle Scholar
  37. 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 483:262–267Google Scholar
  38. Horton P (2012) Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences. Phil Trans R Soc B 367:3455–3465PubMedCentralPubMedGoogle Scholar
  39. 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 Lett 292:1–4PubMedGoogle Scholar
  40. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684PubMedGoogle Scholar
  41. Horton P, Ruban AV, Wentworth M (2000) Allosteric regulation of the light-harvesting system of photosystem II. Phil Trans R Soc B 355:1361–1370PubMedCentralPubMedGoogle Scholar
  42. Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069–1079PubMedGoogle Scholar
  43. Ihalainen JA, Rätsep M, Jensen PE, Scheller HV, Croce R, Bassi R, Korppi-Tommola JEI, Freiberg A (2003) Red spectral forms of chlorophylls in green plant PSI – a site-selective and high-pressure spectroscopy study. J Phys Chem B 107:9086–9093Google Scholar
  44. Ilioaia C, Johnson MP, 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. J Biol Chem 283:29505–29512PubMedCentralPubMedGoogle Scholar
  45. Ilioaia C, Johnson MP, Liao P-N, Pascal AA, van Grondelle R, Walla PJ, Ruban AV, Robert B (2011) Photoprotection in plants involves a change in lutein 1 binding domain in the major light-harvesting complex of photosystem II. J Biol Chem 286:27247–27254PubMedCentralPubMedGoogle Scholar
  46. Ishizaki A, Calhoun TR, Schlau-Cohen GS, Fleming GR (2010) Quantum coherence and its interplay with protein environments in photosynthetic electronic energy transfer. Phys Chem Chem Phys 12:7319–7337PubMedGoogle Scholar
  47. Jang S, Newton MD, Silbey RJ (2004) Multichromophoric Förster resonance energy transfer. Phys Rev Lett 92:218301–218304PubMedGoogle Scholar
  48. Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240PubMedGoogle Scholar
  49. Jennings RC, Garlaschi FM, Zucchelli G (1991) Light-induced fluorescence quenching in the light-harvesting chlorophyll a/b protein complex. Photosynth Res 27:57–64PubMedGoogle Scholar
  50. Johnson MP, Ruban AV (2009) Photoprotective energy dissipation in higher plants involves alteration of the excited state energy of the emitting chlorophyll(s) in the light harvesting antenna II (LHCII). J Biol Chem 284:23592–23601PubMedCentralPubMedGoogle Scholar
  51. 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 23:1468–1479PubMedCentralPubMedGoogle Scholar
  52. Koshland DE (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 44:98–104PubMedCentralPubMedGoogle Scholar
  53. Krüger TPJ, Novoderezhkin VI, Ilioaia C, van Grondelle R (2010) Fluorescence spectral dynamics of single LHCII trimers. Biophys J 98:3093–3101PubMedCentralPubMedGoogle Scholar
  54. Krüger TPJ, Ilioaia C, Valkunas L, van Grondelle R (2011a) Fluorescence intermittency from the main plant light-harvesting complex: sensitivity to the local environment. J Phys Chem B 115:5083–5095PubMedGoogle Scholar
  55. Krüger TPJ, Ilioaia C, van Grondelle R (2011b) Fluorescence intermittency from the main plant light-harvesting complex: resolving shifts between intensity levels. J Phys Chem B 115:5071–5082PubMedGoogle Scholar
  56. Krüger TPJ, Wientjes E, Croce R, van Grondelle R (2011c) Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc Natl Acad Sci USA 108:13516–13521PubMedCentralPubMedGoogle Scholar
  57. Krüger TPJ, Ilioaia C, Johnson MP, Ruban AV, Papagiannakis E, Horton P, van Grondelle R (2012) Controlled disorder in plant light-harvesting complex II explains its photoprotective role. Biophys J 102:2669–2676PubMedCentralPubMedGoogle Scholar
  58. Krüger TPJ, Ilioaia C, Johnson MP, Belgio E, Horton P, Ruban AV, van Grondelle R (2013) The specificity of controlled protein disorder in the photoprotection of plants. Biophys J 105:1018–1026PubMedCentralPubMedGoogle Scholar
  59. Krüger TPJ, Ilioaia C, Johnson MP, Ruban AV, van Grondelle R (2014) Disentangling the low energy states of the major light-harvesting complex of plants and their role in photoprotection. Biochim Biophys Acta 1837:1027–1038PubMedGoogle Scholar
  60. Kulzer F, Orrit M (2004) Single-molecule optics. Annu Rev Phys Chem 55:585–611PubMedGoogle Scholar
  61. Lambrev PH, Nilkens M, Miloslavina Y, Jahns P, Holzwarth AR (2010) Kinetic and spectral resolution of multiple nonphotochemical quenching components in Arabidopsis leaves. Plant Physiol 152:1611–1624PubMedCentralPubMedGoogle Scholar
  62. Liao P-N, Holleboom CP, Wilk L, Kuhlbrandt W, Walla PJ (2010) Correlation of Car S1 -> Chl with Chl -> Car S1 energy transfer supports the excitonic model in quenched light harvesting complex II. J Phys Chem B 114:15650–15655PubMedGoogle Scholar
  63. Liao P-N, Pillai S, Kloz M, Gust D, Moore AL, Moore TA, Kennis JTM, van Grondelle R, Walla PJ (2012) On the role of excitonic interactions in carotenoid-phthalocyanine dyads and implications for photosynthetic regulation. Photosynth Res 111:237–243PubMedGoogle Scholar
  64. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 a resolution. Nature 428:287–292PubMedGoogle Scholar
  65. Liu L-N, Elmalk AT, Aartsma TJ, Thomas J-C, Lamers GEM, Zhou B-C, Zhang Y-Z (2008) Light-induced energetic decoupling as a mechanism for phycobilisome-related energy dissipation in red algae: a single molecule study. PLoS One 3:e3134PubMedCentralPubMedGoogle Scholar
  66. Loos D, Cotlet M, De Schryver F, Habuchi S, Hofkens J (2004) Single-molecule spectroscopy selectively probes donor and acceptor chromophores in the phycobiliprotein allophycocyanin. Biophys J 87:2598–2608PubMedCentralPubMedGoogle Scholar
  67. Ma B, Kumar S, Tsai CJ, Nussinov R (1999) Folding funnels and binding mechanisms. Protein Eng 12:713–720PubMedGoogle Scholar
  68. Meier T, Chernyak V, Mukamel S (1997) Femtosecond photon echoes in molecular aggregates. J Chem Phys 107:8759–8780Google Scholar
  69. 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 582:3625–3631PubMedGoogle Scholar
  70. Moerner WE (2002) A dozen years of single-molecule spectroscopy in physics, chemistry, and biophysics. J Phys Chem B 106:910–927Google Scholar
  71. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88–118PubMedGoogle Scholar
  72. Morosinotto T, Breton J, Bassi R, Croce R (2003) The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J Biol Chem 278:49223–49229PubMedGoogle Scholar
  73. Morton J, Hall J, Smith P, Fusamichi A, Faisal K, Shen JR, Krausz E (2014) Determination of the PS I content of PS II core preparations using selective emission: a new emission of PS II at 780 nm. Biochim Biophys Acta 1837:167–177PubMedGoogle Scholar
  74. Mukamel S (1995) Principles of Nonlinear Optical Spectroscopy. Oxford University Press, OxfordGoogle Scholar
  75. Mullineaux CW, Pascal AA, Horton P, Holzwarth AR (1993) Excitation-energy quenching in aggregates of the LHC-II chlorophyll-protein complex – a time-resolved fluorescence study. Biochim Biophys Acta 1141:23–28Google Scholar
  76. Nieder JB, Brecht M, Bittl R (2009) Dynamic intracomplex heterogeneity of phytochrome. J Am Chem Soc 131:69–71PubMedGoogle Scholar
  77. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359PubMedGoogle Scholar
  78. Novoderezhkin VI, Razjivin AP (1994) Exciton states of the antenna and energy trapping by the reaction center. Photosynth Res 42:9–15PubMedGoogle Scholar
  79. Novoderezhkin VI, Razjivin AP (1996) The theory of Förster-type migration between clusters of strongly interacting molecules: application to light-harvesting complexes of purple bacteria. Chem Phys 211:203–214Google Scholar
  80. Novoderezhkin VI, van Grondelle R (2010) Physical origins and models of energy transfer in photosynthetic light-harvesting. Phys Chem Chem Phys 12:7352–7365PubMedGoogle Scholar
  81. Novoderezhkin VI, Palacios MA, van Amerongen H, van Grondelle R (2005) Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Å crystal structure. J Phys Chem B 109:10493–10504PubMedGoogle Scholar
  82. Novoderezhkin VI, Rutkauskas D, van Grondelle R (2006) Dynamics of the emission spectrum of a single LH2 complex: interplay of slow and fast nuclear motions. Biophys J 90:2890–2902PubMedCentralPubMedGoogle Scholar
  83. Novoderezhkin VI, Dekker JP, van Grondelle R (2007) Mixing of exciton and charge-transfer states in photosystem II reaction centers: modeling of Stark spectra with modified Redfield theory. Biophys J 93:1293–1311PubMedCentralPubMedGoogle Scholar
  84. Novoderezhkin VI, Marin A, van Grondelle R (2011) Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield-Förster picture. Phys Chem Chem Phys 13:17093–17103PubMedGoogle Scholar
  85. Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355PubMedGoogle Scholar
  86. Owens TG (1994) Excitation energy transfer between chlorophylls and carotenoids. A proposed molecular mechanism for non-photochemical quenching. In: Baker NR, Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. Bios Scientific Publishers, Oxford, pp 95–107Google Scholar
  87. Panitchayangkoon G, Hayes D, Fransted KA, Caram JR, Harel E, Wen J, Blankenship RE, Engel GS (2010) Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc Natl Acad Sci USA 107:12766–12770PubMedCentralPubMedGoogle Scholar
  88. Pascal AA, Liu ZF, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang W, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137PubMedGoogle Scholar
  89. Read EL, Engel GS, Calhoun TR, Mančal T, Ahn TK, Blankenship RE, Fleming GR (2007) Cross-peak-specific two-dimensional electronic spectroscopy. Proc Natl Acad Sci USA 104:14203–14208PubMedCentralPubMedGoogle Scholar
  90. Redfield AG (1957) On the theory of relaxation processes. IBM J Res Develop 1:19–31Google Scholar
  91. Redfield AG (1965) The theory of relaxation processes. Adv Magn Res 1:1–32Google Scholar
  92. Renger T (2004) Theory of optical spectra involving charge transfer states: dynamic localization predicts a temperature dependent optical band shift. Phys Rev Lett 93:188101PubMedGoogle Scholar
  93. Romero E, Mozzo M, van Stokkum IHM, Dekker JP, van Grondelle R, Croce R (2009) The origin of the low-energy form of photosystem I light-harvesting complex lhca4: mixing of the lowest exciton with a charge-transfer state. Biophys J 96:L35–L37PubMedCentralPubMedGoogle Scholar
  94. 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 1102:30–38Google Scholar
  95. Ruban AV, Rees D, Noctor GD, Young A, Horton P (1991) Long-wavelength chlorophyll species are associated with amplification of high-energy-state excitation quenching in higher-plants. Biochim Biophys Acta 1059:355–360Google Scholar
  96. Ruban AV, Young A, Horton P (1994) Modulation of chlorophyll fluorescence quenching in isolated light-harvesting complex of photosystem II. Biochim Biophys Acta 1186:123–127Google Scholar
  97. Ruban AV, Dekker JP, Horton P, van Grondelle R (1995) Temperature-dependence of chlorophyll fluorescence from the light-harvesting complex II of higher-plants. Photochem Photobiol 61:216–221Google Scholar
  98. Ruban AV, Young AJ, Horton P (1996) Dynamic properties of the minor chlorophyll a/b binding proteins of photosystem II, an in vitro model for photoprotective energy dissipation in the photosynthetic membrane of green plants. Biochemistry 35:674–678PubMedGoogle Scholar
  99. Ruban A, Calkoen F, Kwa SLS, Van Grondelle R, Horton P, Dekker JP (1997) Characterisation of the aggregated state of the light harvesting complex of photosystem II by linear and circular dichroism. Biochim Biophys Acta 1321:61–70Google Scholar
  100. Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578PubMedGoogle Scholar
  101. Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181PubMedGoogle Scholar
  102. Rutkauskas D, Novoderezkhin V, Cogdell RJ, van Grondelle R (2004) Fluorescence spectral fluctuations of single LH2 complexes from Rhodopseudomonas acidophila strain 10050. Biochemistry 43:4431–4438PubMedGoogle Scholar
  103. Rutkauskas D, Cogdell RJ, van Grondelle R (2006) Conformational relaxation of single bacterial light-harvesting complexes. Biochemistry 45:1082–1086PubMedGoogle Scholar
  104. Santabarbara S, Horton P, Ruban AV (2009) Comparison of the thermodynamic landscapes of unfolding and formation of the energy dissipative state in the isolated light harvesting complex II. Biophys J 97:1188–1197PubMedCentralPubMedGoogle Scholar
  105. Schlau-Cohen GS, Calhoun TR, Ginsberg NS, Read EL, Ballottari M, Bassi R, van Grondelle R, Fleming GR (2009) Pathways of energy flow in LHCII from two-dimensional electronic spectroscopy. J Phys Chem B 113:15352–15363PubMedGoogle Scholar
  106. Schmid VHR, Cammarata KV, Bruns BU, Schmidt GW (1997) In vitro reconstitution of the photosystem I light-harvesting complex LHCI-730: heterodimerization is required for antenna pigment organization. Proc Natl Acad Sci USA 94:7667–7672PubMedCentralPubMedGoogle Scholar
  107. Scholes GD, Fleming GR (2000) On the mechanism of light harvesting in photosynthetic purple bacteria: B800 to B850 energy transfer. J Phys Chem B 104:1854–1868Google Scholar
  108. Scholes GD, Fleming GR, Olaya-Castro A, van Grondelle R (2011) Lessons from nature about solar light harvesting. Nature Chem 3:763–774Google Scholar
  109. Siffel P, Vacha F (1998) Aggregation of the light-harvesting complex in intact leaves of tobacco plants stressed by CO2 deficit. Photochem Photobiol 67:304–311Google Scholar
  110. Sumi H (1999) Theory on rates of excitation-energy transfer between molecular aggregates through distributed transition dipoles with application to the antenna system in bacterial photosynthesis. J Phys Chem B 103:252–260Google Scholar
  111. Tang YL, Wen XG, Lu QT, Yang ZP, Cheng ZK, Lu CM (2007) Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. Plant Physiol 143:629–638PubMedCentralPubMedGoogle Scholar
  112. Tietz C, Jelezko F, Gerken U, Schuler S, Schubert A, Rogl H, Wrachtrup J (2001) Single molecule spectroscopy on the light-harvesting complex II of higher plants. Biophys J 81:556–562PubMedCentralPubMedGoogle Scholar
  113. Tsai CJ, Kumar S, Ma BY, Nussinov R (1999) Folding funnels, binding funnels, and protein function. Protein Sci 8:1181–1190PubMedCentralPubMedGoogle Scholar
  114. Vaitekonis S, Trinkunas G, Valkunas L (2005) Red chlorophylls in the exciton model of photosystem I. Photosynth Res 86:185–201PubMedGoogle Scholar
  115. Valkunas L, Chmeliov J, Krüger TPJ, Ilioaia C, van Grondelle R (2012) How photosynthetic proteins switch. J Phys Chem Lett 3:2779–2784Google Scholar
  116. Valkunas L, Abramavicius D, Mančal T (2013) Molecular excitation dynamics and relaxation: quantum theory and spectroscopy. Wiley-VCH, BerlinGoogle Scholar
  117. van Amerongen H, Valkunas L, van Grondelle R (2000) Photosynthetic Excitons. World Scientific Publishing, SingaporeGoogle Scholar
  118. van Grondelle R, Novoderezhkin VI (2006a) Energy transfer in photosynthesis: experimental insights and quantitative models. Phys Chem Chem Phys 8:793–807PubMedGoogle Scholar
  119. van Grondelle R, Novoderezhkin VI (2006b) Spectroscopy and dynamics of excitation transfer and trapping in purple bacteria. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The Purple Phototrophic Bacteria. Advances in Photosynthesis and Respiration, Volume 28. Springer, Dordrecht, pp 213–252Google Scholar
  120. van Gunsteren WF, Bakowies D, Baron R, Chandrasekhar I, Christen M, Daura X, Gee P, Geerke DP, Glättli A, Hünenberger PH, Kastenholz MA, Oostenbrink C, Schenk M, Trzesniak D, van der Vegt NF, Yu HB (2006) Biomolecular modeling: goals, problems, perspectives. Angew Chem Int Ed 45:4064–4092Google Scholar
  121. van Oijen AM, Ketelaars M, Kohler J, Aartsma TJ, Schmidt J (1999) Unraveling the electronic structure of individual photosynthetic pigment-protein complexes. Science 285:400–402PubMedGoogle Scholar
  122. van Oort B, van Hoek A, Ruban AV, van Amerongen H (2007) Equilibrium between quenched and nonquenched conformations of the major plant light-harvesting complex studied with high-pressure time-resolved fluorescence. J Phys Chem B 111:7631–7637PubMedGoogle Scholar
  123. Vasilev S, Irrgang KD, Schrotter T, Bergmann A, Eichler HJ, Renger G (1997) Quenching of chlorophyll alpha fluorescence in the aggregates of LHCII: steady state fluorescence and picosecond relaxation kinetics. Biochemistry 36:7503–7512Google Scholar
  124. 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 14:759–766PubMedGoogle Scholar
  125. Wentworth M, Ruban AV, Horton P (2000) Chlorophyll fluorescence quenching in isolated light harvesting complexes induced by zeaxanthin. FEBS Lett 471:71–74PubMedGoogle Scholar
  126. Wentworth M, Ruban AV, Horton P (2003) Thermodynamic investigation into the mechanism of the chlorophyll fluorescence quenching in isolated photosystem II light-harvesting complexes. J Biol Chem 278:21845–21850PubMedGoogle Scholar
  127. Wientjes E, Roest G, Croce R (2012) From red to blue to far-red in Lhca4: how does the protein modulate the spectral properties of the pigments? Biochim Biophys Acta Bioenerg 1817:711–717Google Scholar
  128. Yan H, Zhang P, Wang C, Liu Z, Chang W (2007) Two lutein molecules in LHCII have different conformations and functions: insights into the molecular mechanism of thermal dissipation in plants. Biochem Biophys Res Commun 355:457–463PubMedGoogle Scholar
  129. Yang M, Damjanović A, Vaswani HM, Fleming GR (2003) Energy transfer in photosystem I of cyanobacteria Synechococcus elongatus: model study with structure-based semi-empirical Hamiltonian and experimental spectral density. Biophys J 85:140–158PubMedCentralPubMedGoogle Scholar
  130. Zer H, Vink M, Keren N, Dilly-Hartwig HG, Paulsen H, Herrmann RG, Andersson B, Ohad I (1999) Regulation of thylakoid protein phosphorylation at the substrate level: reversible light-induced conformational changes expose the phosphorylation site of the light-harvesting complex II. Proc Natl Acad Sci USA 96:8277–8282PubMedCentralPubMedGoogle Scholar
  131. Zhang WM, Meier T, Chernyak V, Mukamel S (1998) Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J Chem Phys 108:7763–7774Google Scholar
  132. Zondervan R, Kulzer F, Orlinskii SB, Orrit M (2003) Photoblinking of Rhodamine 6G in poly(vinyl alcohol): radical dark state formed through the triplet. J Phys Chem A 107:6770–6776Google Scholar
  133. Zubik M, Luchowski R, Puzio M, Janik E, Bednarska J, Grudzinski W, Gruszecki WI (2013) The negative feedback molecular mechanism which regulates excitation level in the plant photosynthetic complex LHCII: towards identification of the energy dissipative state. Biochim Biophys Acta 1827:355–364PubMedGoogle Scholar
  134. Zucchelli G, Brogioli D, Casazza AP, Garlaschi FM, Jennings RC (2007) Chlorophyll ring deformation modulates Q(y) electronic energy in chlorophyll-protein complexes and generates spectral forms. Biophys J 93:2240–2254PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Tjaart P. J. Krüger
    • 1
    • 2
    Email author
  • Cristian Ilioaia
    • 1
    • 3
  • Peter Horton
    • 4
  • Maxime T. A. Alexandre
    • 1
  • Rienk van Grondelle
    • 1
  1. 1.Department of Physics and Astronomy, Faculty of SciencesVU University AmsterdamAmsterdamThe Netherlands
  2. 2.Department of Physics, Faculty of Natural and Agricultural SciencesUniversity of PretoriaHatfieldSouth Africa
  3. 3.Commisariat à l’Energie Atomique (CEA)Institut de Biologie et Technologies de Saclay and CNRS URA 2096Gif-sur-YvetteFrance
  4. 4.Department of Molecular Biology and BiotechnologyUniversity of SheffieldSheffieldUK

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