A New Perspective for Nonphotochemical Quenching in Plant Antenna Complexes

Light-harvesting complexes (LHCs) of plants exert a dual function of light-harvesting and photoprotection. While LH processes are relatively well characterized, those involved in photoprotection are less understood. The main mechanism involved in photoprotection is to dissipate the energy absorbed by chlorophylls into harmless heat through processes collectively called nonphotochemical quenching (NPQ). Here, we characterize the quenching mechanisms of CP29, a minor LHC of plants with an important role in photoprotection, through 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 analysis reveals that the mechanism 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 pair of pigments is not sufficient but many pigments 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.