Plants in natural environments receive light through sunflecks, the duration and distribution of these being highly variable across the day. Consequently, plants need to adjust their photosynthetic processes to avoid photoinhibition and maximize yield. Changes in the composition of the photosynthetic apparatus in response to sustained changes in the environment are referred to as photosynthetic acclimation, a process that involves changes in protein content and composition. Considering this definition, acclimation differs from regulation, which involves processes that alter the activity of individual proteins over short-time periods, without changing the abundance of those proteins. The interconnection and overlapping of the short- and long-term photosynthetic responses, which can occur simultaneously or/and sequentially over time, make the study of long-term acclimation to fluctuating light in plants challenging. In this review we identify short-term responses of plants to fluctuating light that could act as sensors and signals for acclimation responses, with the aim of understanding how plants integrate environmental fluctuations over time and tailor their responses accordingly. Mathematical modelling has the potential to integrate physiological processes over different timescales and to help disentangle short-term regulatory responses from long-term acclimation responses. We review existing mathematical modelling techniques for studying photosynthetic responses to fluctuating light and propose new methods for addressing the topic from a holistic point of view.