Energy dependent non-photoshemical quenching: PsbS, LhcSR and other players

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Abstract

The photosynthetic apparatus of plants is capable of capturing even weak fluxes of light energy. Hence, strong and rapid increase in irradiance should be dangerous for plants. To solve the problems caused by fluctuations of incident radiation (up to excessive), plants have developed a number of protective mechanisms, including non-photochemical quenching (NPQ) of excited chlorophyll states. NPQ is a set of mechanisms that shorten the lifetime of excited chlorophyll states in the photosynthetic antenna, thereby reducing dangerous effects of light. The most rapid mechanism of NPQ is energy-dependent quenching (qE) triggered by the proton potential formation on the thylakoid transmembrane. The main molecular players of qE are xanthophylls (oxygen-containing carotenoids) and proteins of the thylakoid membrane: antenna component LhcSR in algae and mosses and photosystem II component PsbS in higher plants and some groups of “green lineage” alga. This review discusses molecular mechanisms of qE, with a special focus on the PsbS-dependent quenching. The discovery that PsbS does not bind pigments has led to the hypothesis of PsbS-dependent indirect activation of quenching, in which PsbS acts as a relay switching on the quenching sites in the major (LHCII) and/or minor photosynthetic antennae. The suggested mechanisms include the effect of PsbS on carotenoid conformation and/or pKa values of amino acid residues in PSII antennae. PsbS can also act as a membrane “lubricant” that ensures migration of the major antenna LHCII in the thylakoid membrane and its aggregation followed by transition to the quenched state.

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V. V. Ptushenko

Lomonosov Moscow State University; N. M. Emanuel Institute of Biochemical Physics of the Russian Academy of Sciences

Author for correspondence.
Email: ptush@belozersky.msu.ru

A. N. Belozersky Institute of Physico-Chemical Biology

Russian Federation, 119992 Moscow; 119334 Moscow

A. P. Razjivin

Lomonosov Moscow State University

Email: ptush@belozersky.msu.ru

A. N. Belozersky Institute of Physico-Chemical Biology

Russian Federation, 119992 Moscow

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Supplementary files

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2. Fig. 1. Schematic illustrating the pathways for deactivation of the excited state of Chl antenna. The pathways for deactivation and their effective constants for the entire pool of Chl molecules in the antenna are shown: via a photochemical reaction (kP, green curved arrow), nonradiative thermal dissipation (kD, black wavy arrow), and fluorescence (kF, vertical red arrow). The blue vertical arrow pointing upward shows the transition of Chl to an excited state upon absorption of a quantum of light.

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3. Fig. 2. Schematic representation of the PS2 supercomplex, C2S2M2L2, comprising a dimer of PS2 complexes (denoted C) and a pair each of tightly (S), moderately (M), and loosely bound (L) LHCII major antenna complexes.

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4. Fig. 3. Schematic representation of the PS1 supercomplex (in the literature designated as PSI–LHCI–LHCII), including the PS1 complex, several LHCI antenna complexes (products of the lhca1–lhca9 genes) and two main PS2 antenna complexes, LHCII; view in the plane of the membrane. Depending on the species and illumination conditions, PS1 supercomplexes may contain a smaller number of antennae. The diagram is based on cryoelectron microscopy data on the structure of the supercomplex from C. reinhardtii (PDB code: 7D0J [28])

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5. Fig. 4. Scheme of interaction of pigments of the violaxanthin cycle with Chl antenna according to the model of molecular gear switching of Frank et al. [38]. The arched arrows show the transfer of neutral excitation between pigment molecules, in which the excited donor molecule passes to the ground state, and the unexcited acceptor molecule passes to the excited state. According to the model, the energy transfer between the considered pigments (Chl, Vio and Zea) occurs predominantly in the direction Vio → Chl → Zea. The wavy arrow shows the nonradiative and energy-transfer-free transition of Zea* to the ground state (thermal dissipation of excitation energy).

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6. Fig. 5. Structure of the S subunit of PSII, PsbS (a), according to X-ray diffraction analysis (PDB code: 4RI2 [62]), and of the monomer of the LHCII main antenna complex, Lhcb1 (b), according to cryo-electron microscopy data (PDB code: 8IX0 [63]); the sequence of the proteins that make up LHCII is close to the sequence of LhcSR, for which an experimental three-dimensional structure has not yet been obtained. The helical regions (α and 310) are shown as cylinders and labeled for both proteins (TM1–TM4 are transmembrane helices, H1–H3 are amphiphilic helices of PsbS; for Lhcb1, their generally accepted designations are A–C and E–D, respectively). Chl molecules bound to Lhcb1 are highlighted in green (Chl a) or turquoise (Chl b; phytol "tails" are shown as a thin line), carotenoids are yellow (lutein), orange (neoxanthin) and red (violaxanthin)

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7. Fig. 6. Structure of Lhcb1, as determined by cryo-electron microscopy (PDB code: 8IX0 [63]); only the cluster of chlorophylls Chl a 610, -611, -612 and lutein (at the Lut1 binding site), presumably forming the quenching center, are shown. The side chains of Glu-94, Lys-99 and Gln-103, presumably associated with the transition of LHCII to the quenched state, are shown in color. For further explanations, see the legend to Fig. 5.

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8. Fig. 7. Schematic representation of the main concepts of the mechanism of PsbS- (a) and LhcSR-dependent quenching (b).

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