Updated project metadata. Plants respond to seasonal cues such as the photoperiod, to adapt to current conditions and to prepare for environmental changes in the season to come. To assess photoperiodic responses at the protein level, we quantified the proteome of the model plant Arabidopsis thaliana by mass spectrometry across four photoperiods. This revealed coordinated changes of abundance in the proteins of photosynthesis, primary metabolism and secondary metabolic processes such as pigment biosynthesis, consistent with higher metabolic activity in long photoperiods. Higher translation rates during the day than during the night likely contribute to these changes, but rhythmic RNA profiles will alter their effects. Photoperiodic control of protein levels might be greatest if high translation rates only coincide with high transcript levels in some photoperiods. We term this mechanism ‘translational coincidence’, mathematically model its components, and demonstrate its effect on the Arabidopsis proteome. Datasets from a green alga and a cyanobacterium suggest that this mechanism is general, contributing to the seasonal control of the proteome in many phototrophic organisms, and favouring RNA rhythms even for stable proteins.