On Earth, solar irradiance varies as the sun rises and sets over the
horizon, and sunlight is thus in constant fluctuation, following a slow
dark–low–high–low–dark curve. Optimal plant growth and development are
dependent on the capacity of plants to acclimate and regulate
photosynthesis in response to these changes of light. Little is known of
regulative processes for photosynthesis during nocturnal events. The
nucleus-encoded plant lineage-specific protein PSB33 has been described
as stabilizing the photosystem II complex, especially under light stress
conditions, and plants lacking PSB33 have a dysfunctional state
transition. To clarify the localization and function of this protein, we
used phenomic, biochemical and proteomics approaches in the model plant
Arabidopsis. We report that PSB33 is predominantly located in
non-appressed thylakoid regions and dynamically associates with a
thylakoid protein complex in a light-dependent manner. Moreover, plants
lacking PSB33 show an accelerated D1 protein degradation in nocturnal
periods, and show severely stunted growth when challenged with
fluctuating light. We further show that the function of PSB33 precedes
the STN7 kinase to regulate or balance the excitation energy of
photosystems I and II in fluctuating light conditions.