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      Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants

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          Abstract

          The photosynthetic apparatus of higher plants can dissipate excess excitation energy during high light exposure, by deactivating excited chlorophylls through a mechanism called nonphotochemical quenching (NPQ). However, the precise molecular details of quenching and the mechanism regulating the quenching level are still not completely understood. Focusing on the major light-harvesting complex LHCII of Photosystem II, we show that a charge transfer state involving Lutein can efficiently quench chlorophyll excitation, and reduce the excitation lifetime of LHCII to the levels measured in the deeply quenched LHCII aggregates. Through a combination of molecular dynamics simulations, multiscale quantum chemical calculations, and kinetic modeling, we demonstrate that the quenching level can be finely tuned by the protein, by regulating the energy of the charge transfer state. Our results suggest that a limited conformational rearrangement of the protein scaffold could act as a molecular switch to activate or deactivate the quenching mechanism.

          Abstract

          The plant photosynthetic machinery quenches excess excitation energy to avoid photodamage. Here, via molecular dynamics and quantum chemical calculations, Cupellini et al. show that lutein/chlorophyll pairs in light-harvesting complex II can quench excess energy via a transient charge transfer state.

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          Most cited references53

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          The photoprotective molecular switch in the photosystem II antenna.

          We have reviewed the current state of multidisciplinary knowledge of the photoprotective mechanism in the photosystem II antenna underlying non-photochemical chlorophyll fluorescence quenching (NPQ). The physiological need for photoprotection of photosystem II and the concept of feed-back control of excess light energy are described. The outline of the major component of nonphotochemical quenching, qE, is suggested to comprise four key elements: trigger (ΔpH), site (antenna), mechanics (antenna dynamics) and quencher(s). The current understanding of the identity and role of these qE components is presented. Existing opinions on the involvement of protons, different LHCII antenna complexes, the PsbS protein and different xanthophylls are reviewed. The evidence for LHCII aggregation and macrostructural reorganization of photosystem II and their role in qE are also discussed. The models describing the qE locus in LHCII complexes, the pigments involved and the evidence for structural dynamics within single monomeric antenna complexes are reviewed. We suggest how PsbS and xanthophylls may exert control over qE by controlling the affinity of LHCII complexes for protons with reference to the concepts of hydrophobicity, allostery and hysteresis. Finally, the physics of the proposed chlorophyll-chlorophyll and chlorophyll-xanthophyll mechanisms of energy quenching is explained and discussed. This article is part of a Special Issue entitled: Photosystem II. © 2011 Elsevier B.V. All rights reserved.
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            Carotenoid cation formation and the regulation of photosynthetic light harvesting.

            Photosynthetic light harvesting in excess light is regulated by a process known as feedback deexcitation. Femtosecond transient absorption measurements on thylakoid membranes show selective formation of a carotenoid radical cation upon excitation of chlorophyll under conditions of maximum, steady-state feedback deexcitation. Studies on transgenic Arabidopsis thaliana plants confirmed that this carotenoid radical cation formation is correlated with feedback deexcitation and requires the presence of zeaxanthin, the specific carotenoid synthesized during high light exposure. These results indicate that energy transfer from chlorophyll molecules to a chlorophyllzeaxanthin heterodimer, which then undergoes charge separation, is the mechanism for excess energy dissipation during feedback deexcitation.
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              Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis.

              All photosynthetic organisms need to regulate light harvesting for photoprotection. Three types of flexible non-photochemical quenching (NPQ) mechanisms have been characterized in oxygenic photosynthetic cyanobacteria, algae, and plants: OCP-, LHCSR-, and PSBS-dependent NPQ. OCP-dependent NPQ likely evolved first, to quench excess excitation in the phycobilisome (PB) antenna of cyanobacteria. During evolution of eukaryotic algae, PBs were lost in the green and secondary red plastid lineages, while three-helix light-harvesting complex (LHC) antenna proteins diversified, including LHCSR proteins that function in dissipating excess energy rather than light harvesting. PSBS, an independently evolved member of the LHC protein superfamily, seems to have appeared exclusively in the green lineage, acquired a function as a pH sensor that turns on NPQ, and eventually replaced LHCSR in vascular plants. Copyright © 2013 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                lorenzo.cupellini@unipi.it
                benedetta.mennucci@unipi.it
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                31 January 2020
                31 January 2020
                2020
                : 11
                : 662
                Affiliations
                [1 ]ISNI 0000 0004 1757 3729, GRID grid.5395.a, Università di Pisa, Dipartimento di Chimica e Chimica Industriale, ; Via G. Moruzzi 13, 56124 Pisa, (PI) Italy
                [2 ]GRID grid.4817.a, Laboratoire CEISAM-UMR CNRS 6230, , Université de Nantes, ; 2 Rue de la Houssiniere, BP-92208, F-44322 Cedex 3, Nantes, France
                Author information
                http://orcid.org/0000-0003-0848-2908
                http://orcid.org/0000-0002-3106-4061
                http://orcid.org/0000-0002-4217-0708
                http://orcid.org/0000-0002-4394-0129
                Article
                14488
                10.1038/s41467-020-14488-6
                6994720
                32005811
                80c89a6b-f958-4848-bd2c-a0dbef516291
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 14 November 2019
                : 9 January 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/100010663, EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council);
                Award ID: ERC-AdG- 786714
                Award Recipient :
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                © The Author(s) 2020

                Uncategorized
                bioenergetics,non-photochemical quenching,computational chemistry,molecular dynamics

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