We present a new simulation model of the reactions in the photosynthetic electron transport chain of C3 species. We show that including recent insights about the regulation of the thylakoid proton motive force, ATP/NADPH balancing mechanisms (cyclic and non-cyclic alternative electron transport), and regulation of Rubisco activity, leads to emergent behaviors that may affect the operation and regulation of photosynthesis under different dynamic environmental conditions. The model was parameterized with experimental results in the literature, with a focus on Arabidopsis thaliana. A dataset was constructed from multiple sources, including measurements of steady-state and dynamic gas exchange, chlorophyll fluorescence and absorbance spectroscopy under different light intensities and CO2. This dataset was used to test predictions of the model under different experimental conditions. Simulations suggested that there are strong interactions between cyclic and non-cyclic alternative electron transport and that an excess capacity for alternative electron transport is required to ensure adequate redox state and lumen pH. Furthermore, the model predicted that, under specific conditions, reduction of ferredoxin by plastoquinol was possible, especially after a rapid increase in light intensity. Further analysis also revealed that the relationship between ATP synthesis and proton motive force was highly regulated by the concentrations of ATP and ADP, and this facilitated an increase in non-photochemical quenching under conditions where metabolism was limiting, such as low CO2 or high light intensity. The model may be used as an in silico platform for future research on the regulation of photosynthetic electron transport.