Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein

Ahn, Tae Kyu; Avenson, Thomas J.; Ballottari, Matteo; Cheng, Yuan‐Chung; Niyogi, Krishna; Bassi, Roberto; Fleming, Graham R.

doi:10.1126/science.1154800

Cited by 501 publications

(534 citation statements)

References 29 publications

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“…We suggest that this is due to trimeric LHCII migration away from the photosystem II (PSII) supercomplex, which is proposed to occur within 5 min of high light exposure. 15,16 If, as suggested previously, 11,12,17 CT quenching occurs in the monomeric LHCII, this reduces the amount of excitation energy funneled to the CT quenching site. It is noteworthy that the Zea •+ TA signal slowly decreased in dark periods despite the near-constant Zea concentration, indicative of asymmetric induction-relaxation of the CT quenching mechanism.…”

Section: * S Supporting Informationmentioning

confidence: 78%

“…6 However, these thylakoids had been high-light-acclimated for over 30 min before measurement, which does not indicate whether CT quenching is activated within the first few minutes of high light exposure, the time scale of qE activation. Zea •+ has also been observed in isolated minor (monomeric) light-harvesting complexes containing Zea, 11,12 but these protein conditions may not be indicative of in vivo behavior, and once again, do not give information about when CT quenching turns on during light acclimation. In a recent study, Dall'Osto and coworkers concluded that the trimeric light-harvesting complex II (LHCII) is the location of a more slowly activated (several minutes) quenching mechanism that does not involve formation of Zea •+ in vivo.…”

Section: * S Supporting Informationmentioning

confidence: 99%

“…Pump−probe spectroscopy for TA measurements has been described in previous literature. 6,11 A Ti:sapphire oscillator (Coherent MIRA Seed) was used to seed a regenerative amplifier (Coherent RegA 9050) with an external stretcher/compressor, generating an 800 nm pulse with a repetition rate of 250 kHz. A portion of the pulses pumped an optical parametric amplifier (OPA, Coherent 9450) which was tuned to 650 nm for Chl b Q y transition.…”

Section: ■ Experimental Methodsmentioning

confidence: 99%

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Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes

Park

Fischer

et al. 2017

J. Phys. Chem. Lett.

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Nonphotochemical quenching mechanisms regulate light harvesting in oxygenic photosynthesis. Measurement techniques for nonphotochemical quenching have typically focused on downstream effects of quenching, such as measuring reduced chlorophyll fluorescence. Here, to directly measure a species involved in quenching, we report snapshot transient absorption (TA) spectroscopy, which rapidly tracks carotenoid radical cation signals as samples acclimate to excess light. The formation of zeaxanthin radical cations, which is possible evidence of zeaxanthin–chlorophyll charge-transfer (CT) quenching, was investigated in spinach thylakoids. Together with fluorescence lifetime snapshot data and time-resolved high-performance liquid chromatography (HPLC) measurements, snapshot TA reveals that Zea•+ formation is closely related to energy-dependent quenching (qE) in nonphotochemical quenching. Quantitative and dynamic information on CT quenching discussed in this work give insight into the design principles of photoprotection in natural photosynthesis.

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Section: * S Supporting Informationmentioning

confidence: 78%

Section: * S Supporting Informationmentioning

confidence: 99%

Section: ■ Experimental Methodsmentioning

confidence: 99%

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Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes

Park

Fischer

et al. 2017

J. Phys. Chem. Lett.

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“…In LHCII trimers this is accomplished by conformational switching between a light-harvesting and a dissipating state (32,33), whereas in the minor antennae formation of a carotenoid radical cation was suggested to be involved (34,35). Although a photoprotective role has been suggested for Lhca complexes as well (36), little is known about the nature of this process in Lhcas, in particular whether the red Chls play an active role.…”

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confidence: 99%

Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes

Krüger

Wientjes

Croce

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

104

125

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The light-harvesting complexes of photosystem I and II (Lhcas and Lhcbs) of plants display a high structural homology and similar pigment content and organization. Yet, the spectroscopic properties of these complexes, and accordingly their functionality, differ substantially. This difference is primarily due to the charge-transfer (CT) character of a chlorophyll dimer in all Lhcas, which mixes with the excitonic states of these complexes, whereas this CT character is generally absent in Lhcbs. By means of single-molecule spectroscopy near room temperature, we demonstrate that the presence or absence of such a CT state in Lhcas and Lhcbs can occasionally be reversed; i.e., these complexes are able to interconvert conformationally to quasi-stable spectral states that resemble the Lhcs of the other photosystem. The high structural similarity of all the Lhca and Lhcb proteins suggests that the stable conformational states that give rise to the mixed CT-excitonic state are similar for all these proteins, and similarly for the conformations that involve no CT state. This indicates that the specific functions related to Lhca and Lhcb complexes are realized by different stable conformations of a single generic protein structure. We propose that this functionality is modulated and controlled by the protein environment.protein multifunctionality | red forms A lthough conformational changes are essential for the function of proteins, little is known about their complex structural dynamics. Protein motions can partially be described by dynamic disorder in the crystalline, glass-like, or liquid states of matter (1-3). A feasible conceptual framework has been developed to visualize these dynamics as transitions between hierarchically ordered minima in the high-dimensional energy landscape of the protein (4, 5). Such a landscape represents all possible energy states as a function of the protein's conformation. The local minima, which signify conformational substates (CSs), are divided by energy barriers into different tiers. The order of a tier is characterized by an average barrier height, a higher barrier of which corresponds to a lower rate of conformational transitions (6). Protein-embedded pigments often serve as effective probes of conformational changes. In particular, strong intrapigment interactions in pigment aggregates can considerably increase the sensitivity of the pigments to the local environment (7). As a result, transitions between CSs are reflected as changes in the pigment electronic states and can be observed as distinct shifts in their absorption and emission energies. In conventional spectroscopy on large ensembles of proteins, energy equilibration after an excitation perturbation is monitored as the average of a very large number of possible trajectories on the energy landscapes of many similar proteins. In contrast, in single-molecule spectroscopy (SMS), the energy landscape of a single protein can be probed. For various pigment-protein complexes, this technique has proven successful to identify conform...

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“…Different molecular mechanisms of excitation quenching via zeaxanthin have been proposed. Among those mechanisms are the direct, singlet-singlet energy transfer from chlorophyll (Frank et al, 2000) and the formation of zeaxanthin-chlorophyll charge transfer complexes (Ahn et al, 2008). The indirect effect of zeaxanthin on excitation quenching in LHCII has also been proposed, based on the effect in molecular organization of LHCII supramolecular structures (Ruban et al, 1997;Gruszecki et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Molecular Architecture of Plant Thylakoids under Physiological and Light Stress Conditions: A Study of Lipid-Light-Harvesting Complex II Model Membranes

et al. 2013

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In this study, we analyzed multibilayer lipid-protein membranes composed of the photosynthetic light-harvesting complex II (LHCII; isolated from spinach [Spinacia oleracea]) and the plant lipids monogalcatosyldiacylglycerol and digalactosyldiacylglycerol. Two types of pigment-protein complexes were analyzed: those isolated from dark-adapted leaves (LHCII) and those from leaves preilluminated with high-intensity light (LHCII-HL). The LHCII-HL complexes were found to be partially phosphorylated and contained zeaxanthin. The results of the x-ray diffraction, infrared imaging microscopy, confocal laser scanning microscopy, and transmission electron microscopy revealed that lipid-LHCII membranes assemble into planar multibilayers, in contrast with the lipid-LHCII-HL membranes, which form less ordered structures. In both systems, the protein formed supramolecular structures. In the case of LHCII-HL, these structures spanned the multibilayer membranes and were perpendicular to the membrane plane, whereas in LHCII, the structures were lamellar and within the plane of the membranes. Lamellar aggregates of LHCII-HL have been shown, by fluorescence lifetime imaging microscopy, to be particularly active in excitation energy quenching. Both types of structures were stabilized by intermolecular hydrogen bonds. We conclude that the formation of trans-layer, rivet-like structures of LHCII is an important determinant underlying the spontaneous formation and stabilization of the thylakoid grana structures, since the lamellar aggregates are well suited to dissipate excess energy upon overexcitation.

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Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein

Cited by 501 publications

References 29 publications

Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes

Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes

Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes

Molecular Architecture of Plant Thylakoids under Physiological and Light Stress Conditions: A Study of Lipid-Light-Harvesting Complex II Model Membranes

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