A different perspective for nonphotochemical quenching in plant antenna complexes

Abstract

Light-harvesting complexes of plants exert a dual function of light-harvesting (LH) and photoprotection through processes collectively called nonphotochemical quenching (NPQ). While LH processes are relatively well characterized, those involved in NPQ are less understood. Here, we characterize the quenching mechanisms of CP29, a minor LHC of plants, through the integration of two complementary enhanced-sampling techniques, dimensionality reduction schemes, electronic calculations and the analysis of cryo-EM data in the light of the predicted conformational ensemble. Our study reveals that the switch between LH and quenching state is more complex than previously thought. Several conformations of the lumenal side of the protein occur and differently affect the pigments’ relative geometries and interactions. Moreover, we show that a quenching mechanism localized on a single chlorophyll-carotenoid pair is not sufficient but many chlorophylls are simultaneously involved. In such a diffuse mechanism, short-range interactions between each carotenoid and different chlorophylls combined with a protein-mediated tuning of the carotenoid excitation energies have to be considered in addition to the commonly suggested Coulomb interactions.

A perspective on the major light-harvesting complex dynamics under the effect of pH, salts, and the photoprotective PsbS protein

“…2), in line with previous suggestions in the literature (Yan et al 2007;Liguori et al 2015;Papadatos et al 2017;Daskalakis et al 2019a;Cupellini et al 2020;Li et al 2020). A recent study on the CP29 minor antenna (Cignoni et al 2021) confirms that helix A/B and helix-D subtle conformational changes are transitions that are evident in the LHC protein scaffold by employing enhanced sampling molecular dynamics techniques. In detail, α scissoring motion of helices A and B of the major LHCII, along with the movement of helix-D (Fig.…”

Trivial Excitation Energy Transfer to Carotenoids Is an Unlikely Mechanism for Non-photochemical Quenching in LHCII

“…Cignoni et al provide a possible answer via a detailed QM/MM study of CP29 in which short-range interactions (exchange, overlap, etc.) were found to make large contributions to the Chl-Cart couplings (Cignoni et al, 2021 ). These are naturally far more sensitive to minor conformational changes than the long-range Coulomb interactions.…”

The major trimeric antenna complexes serve as a site for qH-energy dissipation in plants

“…Small changes in the conformation of the trimer modifying the protein environment of Chls or their orientation and/or distance with each other could enable qH, and the work reported here will enable to identify this fine-tuning. Such changes of the conformational space of proteins or carotenoids have recently been studied for qE experimentally or through molecular dynamics simulations (Liguori et al, 2017, Cignoni et al, 2021 and highlighted that several conformers would underlie light-harvesting and energy-dissipation states providing a more complex picture than previously thought for NPQ regulation. It could also be that qH is due to altered chlorophyll-amino acid or chlorophyll-hydrophobic molecule interaction; for a recent review of Chl quenching mechanisms, see (Ruban & Saccon, 2022).…”