State transitions involve the phosphorylation and dephosphorylation of light-harvesting complex II, catalyzed by the thylakoid kinase STN7 and the phosphatase TAP38/PPH1 in algae and higher plants. These transitions enable algae and plants to coordinate the activation of photosystem I and II. However, the impact of state transitions on the turnover of thylakoid proteins remains unclear. In this study, we systematically measured the in vivo turnover rates of thylakoid proteins in stn7-1 and tap38-1 knockout mutants, which are locked in permanent State I and State II, respectively, and compared these rates to those in wild-type Arabidopsis. Notably, photosynthetic proteins such as D1, LHCII, and PSAB exhibited opposing turnover rates in the two mutant lines, suggesting that State I and State II regulate their turnover antagonistically. Strikingly, these changes in turnover did not correspond to changes in protein abundance but correlate with distribution of activation energy and intensity of electron flows, highlighting the role of activation energy and electron flow in protein turnover and homeostasis maintenance. Overall, this study elucidates a novel role of state transitions in regulation of the turnover of photosynthetic electron transport chain protein complexes, providing new insights into the reason for existence of state transition in plants, most likely through regulating energy distribution associated electron flows.