A possible molecular basis for photoprotection in the minor antenna proteins of plants

Fox, Kieran F.; Ünlü, Caner; Balevičius, Vytautas; Ramdour, Baboo Narottamsing; Kern, Carina; Pan, Xiaowei; Li, Mei; Amerongen, Herbert van; Duffy, Christopher D. P.

doi:10.1016/j.bbabio.2018.03.015

Cited by 27 publications

(44 citation statements)

References 65 publications

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“…In our analysis, we use the same kinetic model established in Ref. 28 for the X-ray structure of CP29 [31], Enlarged view of the significant Chl-Car interaction domains within the CP29 complex, namely L1, L2 and N1 sites. (d)-(e) Structural differences between (d) the CP29 X-ray structure [31] and (e) the recently resolved Cryo-EM structure [33].…”

Section: The All-pigment Eet Modelmentioning

confidence: 99%

“…A newer model was developed with a more realistic spectral density for carotenoids (obtained by fitting the twophoton spectrum of Lut), and some QM optimization of the pigment geometries [27]. The same method was finally applied to CP29 [28]. Other models (for LHCII) instead used molecular dynamics (MD) simulations prior to coupling estimation but considered only luteins [29] or only the lutein in site L1 [30].…”

Section: Introductionmentioning

confidence: 99%

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The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

Lapillo

Cignoni

Cupellini

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Antenna complexes in photosystems of plants and green algae are able to switch between a light-harvesting unquenched conformation and a quenched conformation so to avoid photodamage. When the switch is activated, nonphotochemical quenching (NPQ) mechanisms take place for an efficient deactivation of excess excitation energy. The molecular details of these mechanisms have not been fully clarified but different hypotheses have been proposed. Among them, a popular one involves excitation energy transfer (EET) from the singlet excited Chls to the lowest singlet state (S 1) of carotenoids. In this work, we combine such model with µs-long molecular dynamics simulations of the CP29 minor antenna complex to investigate how conformational fluctuations affect the electronic couplings and the final EET quenching. The computational framework is applied to both CP29 embedding violaxanthin and zeaxantin in its L2 site. Our results demonstrate that the EET model is rather insensitive to physically reasonable variations in single chlorophyll-carotenoid couplings, and that very large conformational changes would be needed to see the large variation of the complex lifetime expected in the switch from light-harvesting to quenched state. We show, however, that a major role in regulating the EET quenching is played by the S 1 energy of the carotenoid, in line with very recent spectroscopy experiments.

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Section: The All-pigment Eet Modelmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

Lapillo

Cignoni

Cupellini

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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“…Only few research groups have investigated these phenomena using atomistic models. In particular, Duffy and coworkers have extensively studied carotenoid-mediated quenching mechanisms using semiempirical QM methods [131,132]. They have also combined the same approach with MD trajectories for investigating the role of the protein dynamics in the quenching of the excited chlorophylls by energy transfer to carotenoids in major and minor LH complexes of plants [133].…”

Section: From the Lh Function To Its Photoregulationmentioning

confidence: 99%

Successes & challenges in the atomistic modeling of light-harvesting and its photoregulation

Cupellini

Bondanza

Nottoli

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Light-harvesting is a crucial step of photosynthesis. Its mechanisms and related energetics have been revealed by a combination of experimental investigations and theoretical modeling. The success of theoretical modeling is largely due to the application of atomistic descriptions combining quantum chemistry, classical models and molecular dynamics techniques. Besides the important achievements obtained so far, a complete and quantitative understanding of how the many different light-harvesting complexes exploit their structural specificity is still missing. Moreover, many questions remain unanswered regarding the mechanisms through which light-harvesting is regulated in response to variable light conditions. Here we show that, in both fields, a major role will be played once more by atomistic descriptions, possibly generalized to tackle the numerous time and space scales on which the regulation takes place: going from the ultrafast electronic excitation of the multichromophoric aggregate, through the subsequent conformational changes in the embedding protein, up to the interaction between proteins.

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“…In order to asses the efficiency of quenching within the dimer and LHCII a suitable measure is needed. Here, as previously (Chmeliov et al 2015;Fox et al 2017Fox et al , 2018Balevičius Jr. et al 2017), we consider the 'mean excitation lifetime', exc . This is an observable quantitiy (through fluorescence lifetime/yield measurements) and is therefore basis-independant.…”

Section: Excitation Lifetimes and Dynamics Within A Coupled System Ofmentioning

confidence: 99%

“…Two-photon absorption on Lut in native LHCII gives a value ∼ 15,300 cm −1 although this is taken from fitting a single line to the sharpest peak in the data (a higher energy vibronic peak) (Walla et al 2000). Fitting the cleaner two-photon spectrum of Lut in octanol (Walla et al 2002) we previously obtained a value of ∼ 14,000 cm −1 (with a second vibronic peak at ∼ 15,300 cm −1 ) (Fox et al 2018) which matches values obtained from S 1 excited state absorption (Polívka and Sundström 2004). Although the precise value is not well defined it is reasonable to assume that Chl a Q y lies somewhere between the S 1 0-0 and first vibronic transitions.…”

Section: Contribution Of Excitonic Quenching To the Npq Mechanismmentioning

confidence: 99%

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

Balevičius

Duffy

2020

Photosynth Res

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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, Δ = Car − Chl , and the resonance coupling, J, between the two excited states. Coherent quenching will be the dominant process when −J < Δ < J, i.e., when the two molecules are resonant, while the quenching will be largely incoherent when Chl > ( Car + J). One would expect quenching to be energetically unfavorable for Chl < ( Car − J). The actual dynamics of quenching lie somewhere between these limiting regimes and have non-trivial dependencies of both J and Δ . 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 Δ . We first consider an isolated chlorophyllcarotenoid 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 Δ around the resonance point, Δ = 0. 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. Counterintuitively 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 J > 10 cm −1 quenching becomes less and less sensitive to J (since in the window −J < Δ < J the overall lifetime is independent of it). The requirement for quenching appear to be only that J > 0. Although the coherent/incoherent character of the quenching can vary, the overall kinetics are likely robust with respect to fluctuations in J and Δ . This may be the basis for previous observations of NPQ with both coherent and incoherent features. energy gap, Δ , and resonance coupling, J. The solid lines are contours indicating points where the lifetime of the state is the same. e The same for the short-lived Car-like state ( |ex2 >). f, g are a clearer representation of the data in (d, e) for re...

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A possible molecular basis for photoprotection in the minor antenna proteins of plants

Cited by 27 publications

References 65 publications

The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

Successes & challenges in the atomistic modeling of light-harvesting and its photoregulation

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

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