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Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’

Plants possess an essential ability to rapidly down-regulate light-harvesting in response to high light. This photoprotective process involves the formation of energy-quenching interactions between the chlorophyll and carotenoid pigments within the antenna of Photosystem II (PSII). The nature of the...

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Autores principales: Balevičius, Vytautas, Duffy, Christopher D. P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Netherlands 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7239839/
https://www.ncbi.nlm.nih.gov/pubmed/32266612
http://dx.doi.org/10.1007/s11120-020-00737-8
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author Balevičius, Vytautas
Duffy, Christopher D. P.
author_facet Balevičius, Vytautas
Duffy, Christopher D. P.
author_sort Balevičius, Vytautas
collection PubMed
description Plants possess an essential ability to rapidly down-regulate light-harvesting in response to high light. This photoprotective process involves the formation of energy-quenching interactions between the chlorophyll and carotenoid pigments within the antenna of Photosystem II (PSII). The nature of these interactions is currently debated, with, among others, ‘incoherent’ or ‘coherent’ quenching models (or a combination of the two) suggested by a range of time-resolved spectroscopic measurements. In ‘incoherent quenching’, energy is transferred from a chlorophyll to a carotenoid and is dissipated due to the intrinsically short excitation lifetime of the latter. ‘Coherent quenching’ would arise from the quantum mechanical mixing of chlorophyll and carotenoid excited state properties, leading to a reduction in chlorophyll excitation lifetime. The key parameters are the energy gap, [Formula: see text] and the resonance coupling, J, between the two excited states. Coherent quenching will be the dominant process when [Formula: see text] i.e., when the two molecules are resonant, while the quenching will be largely incoherent when [Formula: see text] One would expect quenching to be energetically unfavorable for [Formula: see text] The actual dynamics of quenching lie somewhere between these limiting regimes and have non-trivial dependencies of both J and [Formula: see text] Using the Hierarchical Equation of Motion (HEOM) formalism we present a detailed theoretical examination of these excitation dynamics and their dependence on slow variations in J and [Formula: see text] We first consider an isolated chlorophyll–carotenoid dimer before embedding it within a PSII antenna sub-unit (LHCII). We show that neither energy transfer, nor the mixing of excited state lifetimes represent unique or necessary pathways for quenching and in fact discussing them as distinct quenching mechanisms is misleading. However, we do show that quenching cannot be switched ‘on’ and ‘off’ by fine tuning of [Formula: see text] around the resonance point, [Formula: see text] Due to the large reorganization energy of the carotenoid excited state, we find that the presence (or absence) of coherent interactions have almost no impact of the dynamics of quenching. Counter-intuitively significant quenching is present even when the carotenoid excited state lies above that of the chlorophyll. We also show that, above a rather small threshold value of [Formula: see text] quenching becomes less and less sensitive to J (since in the window [Formula: see text] the overall lifetime is independent of it). The requirement for quenching appear to be only that [Formula: see text] Although the coherent/incoherent character of the quenching can vary, the overall kinetics are likely robust with respect to fluctuations in J and [Formula: see text] This may be the basis for previous observations of NPQ with both coherent and incoherent features. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s11120-020-00737-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-72398392020-05-27 Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’ Balevičius, Vytautas Duffy, Christopher D. P. Photosynth Res Original Article Plants possess an essential ability to rapidly down-regulate light-harvesting in response to high light. This photoprotective process involves the formation of energy-quenching interactions between the chlorophyll and carotenoid pigments within the antenna of Photosystem II (PSII). The nature of these interactions is currently debated, with, among others, ‘incoherent’ or ‘coherent’ quenching models (or a combination of the two) suggested by a range of time-resolved spectroscopic measurements. In ‘incoherent quenching’, energy is transferred from a chlorophyll to a carotenoid and is dissipated due to the intrinsically short excitation lifetime of the latter. ‘Coherent quenching’ would arise from the quantum mechanical mixing of chlorophyll and carotenoid excited state properties, leading to a reduction in chlorophyll excitation lifetime. The key parameters are the energy gap, [Formula: see text] and the resonance coupling, J, between the two excited states. Coherent quenching will be the dominant process when [Formula: see text] i.e., when the two molecules are resonant, while the quenching will be largely incoherent when [Formula: see text] One would expect quenching to be energetically unfavorable for [Formula: see text] The actual dynamics of quenching lie somewhere between these limiting regimes and have non-trivial dependencies of both J and [Formula: see text] Using the Hierarchical Equation of Motion (HEOM) formalism we present a detailed theoretical examination of these excitation dynamics and their dependence on slow variations in J and [Formula: see text] We first consider an isolated chlorophyll–carotenoid dimer before embedding it within a PSII antenna sub-unit (LHCII). We show that neither energy transfer, nor the mixing of excited state lifetimes represent unique or necessary pathways for quenching and in fact discussing them as distinct quenching mechanisms is misleading. However, we do show that quenching cannot be switched ‘on’ and ‘off’ by fine tuning of [Formula: see text] around the resonance point, [Formula: see text] Due to the large reorganization energy of the carotenoid excited state, we find that the presence (or absence) of coherent interactions have almost no impact of the dynamics of quenching. Counter-intuitively significant quenching is present even when the carotenoid excited state lies above that of the chlorophyll. We also show that, above a rather small threshold value of [Formula: see text] quenching becomes less and less sensitive to J (since in the window [Formula: see text] the overall lifetime is independent of it). The requirement for quenching appear to be only that [Formula: see text] Although the coherent/incoherent character of the quenching can vary, the overall kinetics are likely robust with respect to fluctuations in J and [Formula: see text] This may be the basis for previous observations of NPQ with both coherent and incoherent features. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s11120-020-00737-8) contains supplementary material, which is available to authorized users. Springer Netherlands 2020-04-08 2020 /pmc/articles/PMC7239839/ /pubmed/32266612 http://dx.doi.org/10.1007/s11120-020-00737-8 Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Original Article
Balevičius, Vytautas
Duffy, Christopher D. P.
Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’
title Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’
title_full Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’
title_fullStr Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’
title_full_unstemmed Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’
title_short Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’
title_sort excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7239839/
https://www.ncbi.nlm.nih.gov/pubmed/32266612
http://dx.doi.org/10.1007/s11120-020-00737-8
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