Photoprotective Energy Dissipation Involves the Reorganization of Photosystem II Light-Harvesting Complexes in the Grana Membranes of Spinach Chloroplasts

Johnson, Matthew P.; Góral, Tomasz; Duffy, Christopher D. P.; Brain, Anthony P.R.; Mullineaux, Conrad W.; Ruban, Alexander V.

doi:10.1105/tpc.110.081646

Cited by 321 publications

(345 citation statements)

References 73 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: 65%

“…26−28 The bulk of the Zea may facilitate other quenching processes, such as LHCII migration or quenching of reactive oxygen species, as suggested previously. 16,29 Accordingly, we suggest that the Zea •+ formation is not simply proportional to the concentration of Zea but is rather controlled by ΔpH or ΔpH-triggered mechanisms such as activation of the PSII subunit S (PsbS) protein. 30 It is well-accepted that qE mechanisms require activation of PsbS, which is initiated by ΔpH across the thylakoid membrane.…”

Section: * S Supporting Informationmentioning

confidence: 93%

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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: 65%

Section: * S Supporting Informationmentioning

confidence: 93%

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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“…An important role of light-induced LHCII reorganization in photoprotection against light-induced damage has emerged from several studies, both in vivo and in vitro (Barzda et al, 1996;Dobrikova et al, 2003;Cseh et al, 2005;Holm et al, 2005;Gruszecki et al, 2009b;Johnson et al, 2011). Most of these data suggest that the primary site of light-induced reorganizations is on the outer loop segments of LHCII, affecting the phosphorylation (Zer et al, 1999), the cation binding sites (Cseh et al, 2000;Garab and Mustardy, 2000), and the ability of stacking and lateral reorganizations (Dobrikova et al, 2003;Gruszecki et al, 2009b).…”

Section: Discussionmentioning

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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“…In this respect, recent findings of large-scale protein reorganizations in grana associated with high-energy quenching are interesting. 43,44 These studies on intact thylakoid membranes show that the protein packing density in grana changes in the course of qE induction. Interestingly, these ultrastructural changes in grana depend on the presence of the PsbS protein, 43 a key player for establishing qE.…”

Section: ■ Discussionmentioning

confidence: 99%

Carotenoid–Chlorophyll Coupling and Fluorescence Quenching Correlate with Protein Packing Density in Grana-Thylakoids

et al. 2013

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ABSTRACT:The regulation of light-harvesting in photosynthesis under conditions of varying solar light irradiation is essential for the survival and fitness of plants and algae. It has been proposed that rearrangements of protein distribution in the stacked grana region of thylakoid membranes connected to changes in the electronic pigment-interaction play a key role for this regulation. In particular, carotenoid−chlorophyll interactions seem to be crucial for the downregulation of photosynthetic light-harvesting. So far, it has been difficult to determine the influence of the dense protein packing found in native photosynthetic membrane on these interactions. We investigated the changes of the electronic couplings between carotenoids and chlorophylls and the quenching in grana thylakoids of varying protein packing density by two-photon spectroscopy, conventional chlorophyll fluorometry, low-temperature fluorescence spectroscopy, and electron micrographs of freeze-fracture membranes. We observed an increasing carotenoid−chlorophyll coupling and fluorescence quenching with increasing packing density. Simultaneously, the antennas size and excitonic connectivity of Photosystem II increased with increasing quenching and carotenoid−chlorophyll coupling whereas isolated, decoupled LHCII trimers decreased. Two distinct quenching data regimes could be identified that show up at different protein packing densities. In the regime corresponding to higher protein packing densities, quenching is strongly correlated to carotenoid−chlorophyll interactions whereas in the second regime, a weak correlation is apparent with low protein packing densities. Native membranes are in the strong-coupling data regime. Consequently, PSII and LHCII in grana membranes of plants are already quenched by protein crowding. We concluded that this ensures efficient electronic connection of all pigment−protein complexes for intermolecular energy transfer to the reaction centers and allows simultaneously sensitive regulation of light harvesting by only small changes in the protein packaging. ■ INTRODUCTIONPhotosynthesis in higher plants and algae is initiated by the harvesting of sunlight through a series of pigment−protein complexes located in the thylakoid membranes of chloroplasts. Starting from these light harvesting complexes (LHCs), the absorbed energy is efficiently transferred from one complex to the other. These transfer processes end up in the photosystem reaction centers where the energy is converted into redox energy. However, plants are exposed to changing light intensities on a daily basis that can vary over several orders of magnitude. 1 Thus, a regulation mechanism is necessary that assures effective usage of sunlight energy under low-light conditions but avoids photo-oxidative damage to the reaction centers or other parts of the photosynthetic apparatus if the absorbed light exceeds its capacity. A main mechanism that evolved to minimize photo-oxidative damage in plants is called high-energy quenching (qE). qE enables the dissipation ...

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Photoprotective Energy Dissipation Involves the Reorganization of Photosystem II Light-Harvesting Complexes in the Grana Membranes of Spinach Chloroplasts

Cited by 321 publications

References 73 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

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

Carotenoid–Chlorophyll Coupling and Fluorescence Quenching Correlate with Protein Packing Density in Grana-Thylakoids

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