Dynamical and allosteric regulation of photoprotection in light harvesting complex II

Major light-harvesting complex of photosystem II (LHCII) plays a dual role in light-harvesting and excited energy dissipation to protect photodamage from excess energy. The regulatory switch is induced by increased acidity, temperature or both. However, the molecular origin of the protein dynamics at the atomic level is still unknown. We carried out temperature-jump time-resolved infrared spectroscopy and molecular dynamics simulations to determine the energy quenching dynamics and conformational changes of LHCII trimers. We found that the spontaneous formation of a pair of local α-helices from the 3₁₀-helix E/loop and the C-terminal coil of the neighboring monomer, in response to the increased environmental temperature and/or acidity, induces a scissoring motion of transmembrane helices A and B, shifting the conformational equilibrium to a more open state, with an increased angle between the associated carotenoids. The dynamical allosteric conformation change leads to close contacts between the first excited state of carotenoid lutein 1 and chlorophyll pigments, facilitating the fluorescence quenching. Based on these results, we suggest a unified mechanism by which the LHCII trimer controls the dissipation of excess excited energy in response to increased temperature and acidity, as an intrinsic result of intense sun light in plant photosynthesis.