The carotenoid pathway: what is important for excitation quenching in plant antenna complexes?

Plant light-harvesting is regulated by the Non-Photochemical Quenching (NPQ) mechanism involving the reversible formation of excitation quenching sites in the Photosystem II (PSII) antenna in response to high light. While the major antenna complex, LHCII, is known to be a site of NPQ, the precise mechanism of excitation quenching is not clearly understood. A preliminary model of the quenched crystal structure of LHCII implied that quenching arises from slow energy capture by Car pigments. It predicted a thoroughly quenched system but offered little insight into the defining aspects of this quenching. In this work, we present a thorough theoretical investigation of this quenching, addressing the factors defining the quenching pathway and possible mechanism for its (de)activation. We show that quenching in LHCII crystals is the result of slow energy transfer from chlorophyll to the centrally-bound lutein Cars, predominantly the Lut620 associated with the chlorophyll 'terminal emitter', one of the proposed in vivo pathways. We show that this quenching is rather independent of the particular species of Car and excitation 'site' energy. The defining parameter is the resonant coupling between the pigment co-factors. Lastly, we show that these interactions must be severely suppressed for a light-harvesting state to be recovered.

[1]  Benedetta Mennucci,et al.  Quantum Chemical Studies of Light Harvesting. , 2017, Chemical reviews.

[2]  Benedetta Mennucci,et al.  Combining classical molecular dynamics and quantum mechanical methods for the description of electronic excitations: The case of carotenoids , 2016, J. Comput. Chem..

[3]  R. Augulis,et al.  The nature of self-regulation in photosynthetic light-harvesting antenna , 2016, Nature Plants.

[4]  William P. Bricker,et al.  Distortions of the Xanthophylls Caused by Interactions with Neighboring Pigments and the LHCII Protein Are Crucial for Studying Energy Transfer Pathways within the Complex. , 2015, The journal of physical chemistry. B.

[5]  J. Hauer,et al.  Vibronic energy relaxation approach highlighting deactivation pathways in carotenoids. , 2015, Physical chemistry chemical physics : PCCP.

[6]  William P. Bricker,et al.  An 'all pigment' model of excitation quenching in LHCII. , 2015, Physical chemistry chemical physics : PCCP.

[7]  William P. Bricker,et al.  Efficient pathways of excitation energy transfer from delocalized S2 excitons in the peridinin-chlorophyll a-protein complex. , 2015, The journal of physical chemistry. B.

[8]  T. Mančal,et al.  Vibronic coupling explains the ultrafast carotenoid-to-bacteriochlorophyll energy transfer in natural and artificial light harvesters. , 2015, The Journal of chemical physics.

[9]  O. Andreussi,et al.  Carotenoids and light-harvesting: from DFT/MRCI to the Tamm-Dancoff approximation. , 2015, Journal of chemical theory and computation.

[10]  W. Thiel,et al.  Carotenoids as a shortcut for chlorophyll Soret-to-Q band energy flow. , 2014, Chemphyschem : a European journal of chemical physics and physical chemistry.

[11]  A. Ruban,et al.  Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps , 2014, Nature Communications.

[12]  Benedetta Mennucci,et al.  On the photophysics of carotenoids: a multireference DFT study of peridinin. , 2013, The journal of physical chemistry. B.

[13]  A. Ruban,et al.  Modeling of fluorescence quenching by lutein in the plant light-harvesting complex LHCII. , 2013, The journal of physical chemistry. B.

[14]  T. Mančal,et al.  Molecular Excitation Dynamics and Relaxation: Quantum Theory and Spectroscopy , 2013 .

[15]  Leonas Valkunas,et al.  Molecular Excitation Dynamics and Relaxation: VALKUNAS:MOLECULAR EXCITATION DYNAMICS AND RELAXATION O-BK , 2013 .

[16]  G. Fleming,et al.  A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes. , 2013, Journal of the American Chemical Society.

[17]  V. Balevičius,et al.  Excitation energy transfer and quenching in a heterodimer: applications to the carotenoid-phthalocyanine dyads. , 2013, The journal of physical chemistry. B.

[18]  A. Ruban,et al.  Electronic spectra of structurally deformed lutein. , 2012, The journal of physical chemistry. A.

[19]  T. Renger,et al.  Refined structure-based simulation of plant light-harvesting complex II: linear optical spectra of trimers and aggregates. , 2012, Biochimica et biophysica acta.

[20]  Matthew P. Johnson,et al.  Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime-both the maximum and the nonphotochemically quenched. , 2012, Biophysical journal.

[21]  J. Götze,et al.  Modeling of a violaxanthin-chlorophyll b chromophore pair in its LHCII environment using CAM-B3LYP. , 2012, Journal of photochemistry and photobiology. B, Biology.

[22]  Alessandro Marin,et al.  Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield-Förster picture. , 2011, Physical chemistry chemical physics : PCCP.

[23]  R. van Grondelle,et al.  Different crystal morphologies lead to slightly different conformations of light-harvesting complex II as monitored by variations of the intrinsic fluorescence lifetime. , 2011, Physical chemistry chemical physics : PCCP.

[24]  R. Birge,et al.  Femtosecond transient absorption spectroscopic study of a carbonyl-containing carotenoid analogue, 2-(all-trans-retinylidene)-indan-1,3-dione. , 2011, The journal of physical chemistry. A.

[25]  T. Renger,et al.  Structure-based identification of energy sinks in plant light-harvesting complex II. , 2010, The journal of physical chemistry. B.

[26]  A. Holzwarth,et al.  Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. , 2010, Chemphyschem : a European journal of chemical physics and physical chemistry.

[27]  A. Dreuw,et al.  Quantum chemical excited state calculations on pigment–protein complexes require thorough geometry re-optimization of experimental crystal structures , 2010 .

[28]  J. Hauer,et al.  Two-dimensional electronic spectroscopy of beta-carotene. , 2009, The journal of physical chemistry. B.

[29]  Graham R Fleming,et al.  Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein , 2008, Science.

[30]  J. Kennis,et al.  Identification of a mechanism of photoprotective energy dissipation in higher plants , 2007, Nature.

[31]  J. Stewart.  Optimization of parameters for semiempirical methods V: Modification of NDDO approximations and application to 70 elements , 2007, Journal of molecular modeling.

[32]  A. van Hoek,et al.  Equilibrium between quenched and nonquenched conformations of the major plant light-harvesting complex studied with high-pressure time-resolved fluorescence. , 2007, The journal of physical chemistry. B.

[33]  Zhenfeng Liu,et al.  Two lutein molecules in LHCII have different conformations and functions: Insights into the molecular mechanism of thermal dissipation in plants. , 2007, Biochemical and biophysical research communications.

[34]  W. Maksymiec,et al.  Xanthophyll-induced aggregation of LHCII as a switch between light-harvesting and energy dissipation systems. , 2006, Biochimica et biophysica acta.

[35]  Bruno Robert,et al.  Molecular basis of photoprotection and control of photosynthetic light-harvesting , 2005, Nature.

[36]  R. van Grondelle,et al.  Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Angstrom crystal structure. , 2005, The journal of physical chemistry. B.

[37]  Leonas Valkunas,et al.  Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting , 2005, Science.

[38]  Zhenfeng Liu,et al.  Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution , 2004, Nature.

[39]  V. Sundström,et al.  Ultrafast dynamics of carotenoid excited States-from solution to natural and artificial systems. , 2004, Chemical reviews.

[40]  Bryan Q. Spring,et al.  Dipole Strengths in the Chlorophylls¶,† , 2003 .

[41]  K. Niyogi,et al.  Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Thomas Renger,et al.  On the relation of protein dynamics and exciton relaxation in pigment–protein complexes: An estimation of the spectral density and a theory for the calculation of optical spectra , 2002 .

[43]  H. Frank,et al.  Direct Determination of the S1 Excited-State Energies of Xanthophylls by Low-Temperature Fluorescence Spectroscopy† , 2002 .

[44]  K. Schulten,et al.  The quantum physics of photosynthesis. , 2002, Chemphyschem : a European journal of chemical physics and physical chemistry.

[45]  G. Fleming,et al.  Excited-State Kinetics of the Carotenoid S1 State in LHC II and Two-Photon Excitation Spectra of Lutein and β-Carotene in Solution: Efficient Car S1→Chl Electronic Energy Transfer via Hot S1 States?† , 2002 .

[46]  Gianfelice Cinque,et al.  Carotenoid S(1) state in a recombinant light-harvesting complex of Photosystem II. , 2002, Biochemistry.

[47]  P. Horton,et al.  Configuration and Dynamics of Xanthophylls in Light-harvesting Antennae of Higher Plants , 2001, The Journal of Biological Chemistry.

[48]  C. Gradinaru,et al.  Identifying the Pathways of Energy Transfer between Carotenoids and Chlorophylls in LHCII and CP29. A Multicolor, Femtosecond Pump-Probe Study , 2000 .

[49]  G. Fleming,et al.  Two-Photon Excitation Spectrum of Light-Harvesting Complex II and Fluorescence Upconversion after One- and Two-Photon Excitation of the Carotenoids , 2000 .

[50]  V. Sundström,et al.  Direct observation of the (forbidden) S1 state in carotenoids. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[51]  G. Fleming,et al.  Calculation of Couplings and Energy-Transfer Pathways between the Pigments of LH2 by the ab Initio Transition Density Cube Method , 1998 .

[52]  M. Wasielewski,et al.  Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis , 1994, Photosynthesis Research.

[53]  A. Becke.  Density-functional thermochemistry. III. The role of exact exchange , 1993 .

[54]  Eamonn F. Healy,et al.  Development and use of quantum mechanical molecular models. 76. AM1: a new general purpose quantum mechanical molecular model , 1985 .

[55]  Klaus Schulten,et al.  Correlation effects in the spectra of polyenes , 1976 .

[56]  P. C. Hariharan,et al.  The influence of polarization functions on molecular orbital hydrogenation energies , 1973 .

[57]  Matthew P. Johnson,et al.  The photoprotective molecular switch in the photosystem II antenna. , 2012, Biochimica et biophysica acta.

[58]  G. Renger.  The light reactions of photosynthesis. , 2010 .

[59]  Stephen B. Powles,et al.  Photoinhibition of Photosynthesis Induced by Visible Light , 1984 .