Roles of multiple TEF30-associated intermediate complexes in the repair and reassembly of photosystem II in Chlamydomonas reinhardtii

During oxygenic photosynthesis, photosystem II (PSII) uses light energy for oxidizing water and reducing plastoquinone. It is susceptible to photodamage, and the damaged PSII is repaired through a sophisticated biological process assisted by numerous auxiliary proteins. Here we report the cryogenic electron microscopy structures of four PSII-repair complexes from Chlamydomonas reinhardtii associated with the Thylakoid Enriched Fraction 30 (TEF30, an orthologue of plant MET1) protein—namely, a TEF30–PSII core monomer (TEF30-C), two types of TEF30–PSII core dimers (types I and II, TEF30₂-C₂-I and TEF30₂-C₂-II) and a TEF30-C₂S-type PSII–LHCII supercomplex (TEF30-C₂S; S, strongly associated light-harvesting complex II trimer). TEF30 mediates the assembly of CP43 with the RC47 module by clamping on the stromal surfaces and prevents the premature association of peripheral antennae with PSII-C. In the transition from TEF30₂-C₂-I to TEF30₂-C₂-II, TEF30-C₂S and mature C₂S₂, one PSII core slides along the dimerization interface against the adjacent one by 22–35 Å, generating a zigzagged surface for accommodating the peripheral antennae. These results suggest that the PSII repair process undergoes multiple TEF30-mediated intermediate states to form intact PSII–LHCII supercomplexes.