The effect of 3-(3,4-dichlorophenyl)-1,1-dimethyl urea (diuron) binding at the secondary quinone (QB) binding site of reaction center II (RCII), on the high-light-induced degradation of the RCII proteins D1 and D2, and the core proteins CP43 and CP47 was investigated in vivo in Chlamydomonas reinhardtii. The degradation of the RCII-D2 and the CP43 proteins shows a short lag relative to that of the RCII-D1 protein. Diuron retards but does not prevent the degradation of RCII-D1, D2 and CP43 proteins. The degradation of the CP47 protein is not retarded by diuron. The RCII-D1 protein present in cells photoinactivated in the presence of diuron is subsequently degraded in cells transferred to low light or to darkness. The protein can be replaced (turnover) at least partially under both conditions. The RCII-D1 protein is not degraded during photoinactivation of a cytochrome-bf-defective mutant. Degradation occurs however when the cells are returned to low light permitting slow reoxidation of plastoquinol [Zer, H., Prasil, O. & Ohad, I. (1994) J. Biol. Chem. 269, 17,670-17,676]. Addition of diuron does not prevent the degradation of the protein at this stage. Tryptic digestion of the RCII-D1 protein is partially inhibited by diuron in isolated thylakoids [Trebst, A., Depka, B., Kraft, B. & Johanningmeier, U. (1988) Photosynth. Res. 18, 163-177] but not in thylakoids obtained from photoinactivated cells. We conclude that photoinactivation induces a series of sequential changes in RCII exposing the cleavage site of the RCII-D1 protein to degradation and abolishing the regulatory role of the QB site occupancy by plastoquinone or analog ligands on the cleavage process. The degradation of the RCII-D2 and CP43 proteins may be a secondary process following modification and/or loss of the RCII-D1 protein.