Mapping light-harvesting and photoprotection responses in the Photosystem II antenna system of higher plants

Optimal photosynthetic performance of plants requires a balance between light energy capture and its use in downstream reactions. The process of light harvesting and its regulation are mediated by a complex array of antenna proteins, whose conservation throughout evolution suggests each complex serves a specific function in the diverse growth conditions in the natural subaerial environment. However, the specific roles of individual gene products in various antenna functions remain poorly understood. In this study, we investigated the Photosystem II antenna system by employing genome editing techniques targeted at subsets of LHCB genes and characterized Arabidopsis thaliana mutants missing specific components of the Photosystem II antenna: namely, the trimeric LHCII, the monomeric LHC, or both. The focus was on light-harvesting capabilities and photoprotective functions, which included exciton trapping cooperativity, non-photochemical quenching (NPQ) of excess excitation energy, and overall resistance to photoinhibition under excess irradiation, aiming to pinpoint the site(s) of the photoprotective responses. NPQ activity was present in all genotypes, indicating that each pigment-binding protein contributes to the overall quenching response. Within each antenna subgroup, NPQ activity did not rely on lutein, whereas zeaxanthin proved essential. Although trimeric LHCII provided the largest contribution to NPQ, the presence of monomeric Lhcbs was associated with enhanced Photosystem II phototolerance under excess light exposure. We conclude that the assembly of Photosystem II supercomplexes, including monomeric Lhcbs, is vital for maintaining PSII stability and functional integrity, playing a key role in preventing photoinhibition.The functional topology of photoprotection responses shows that monomeric antennae enhance PSII connectivity and phototolerance, while the major antenna LHCII is crucial in thermal energy dissipation.