ORCID IDs: 0000-0002-6129-4570 (A.M.); 0000-0001-8273-8022 (X.Y); 0000-0002-0607-4508 (J.H.); 0000-0003-4144-6028 (S.M.D.); 0000-0001-6011-7487 (J.M.); 0000-0003-2196-547X (P.C.S.).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 noncyclic 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 (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 CO 2 , to test predictions of the model under different experimental conditions. Simulations suggested that there are strong interactions between cyclic and noncyclic 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 is possible 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, ADP, and inorganic phosphate, and this facilitated an increase in nonphotochemical quenching and proton motive force under conditions where metabolism was limiting, such as low CO 2 , high light intensity, or combined high CO 2 and high light intensity. The model may be used as an in silico platform for future research on the regulation of photosynthetic electron transport.Plants face highly variable environmental conditions, with fluctuations of light intensity, temperature, humidity, and CO 2 that occur over a wide range of time scales, from seconds to seasons. Imbalances between the rate of light capture and CO 2 assimilation can lead to an excess of energy in the system. Under such conditions, photosynthesis faces three main challenges:1. To dissipate the excess of energy that could otherwise result in the production of reactive oxygen species (Foyer et al., 2011); 2. To couple the production and demand of ATP and NADPH in chloroplasts under a fluctuating environment (Noctor and Foyer, 2000); 3. To maintain an adequate redox state (Allen, 2004) of the photosynthetic electron transport chain (PETC).In this study, we use the term regulation to indicate those mechanisms that allow photosynthesis to achieve these goals. These goals must be met simultaneously, and several mechanisms have been identified as contributing (Kramer et al., 2004), including:1. Nonphotochemical quenching (NPQ) of excess energy absorbed by photosynthetic...