Computational modeling of the evolutionary transition from C3 to C4 photosynthesis

C4 photosynthesis is an evolutionary adaptation that minimizes the adverse effects of the high photorespiration rate. Although it is widely accepted that the C4 plants are evolved from C3 ancestors, the knowledge about the details of this process is yet to be complete. One application of constraint-based metabolic network modeling is to simulate evolutionary trajectories that an organism endures under a certain selective pressure. However, this approach is barely used to predict the evolution of a complex trait in eukaryotes. Here, we utilized a genetic algorithm combined with a constraint-based metabolic network model of Arabidopsis thaliana to simulate the trajectories of C3 to C4 conversion under high photorespiration rate conditions combined with different environmental conditions. Our modeling predicted that the C3-C4 intermediates and C4 strategies are superior to C3 photosynthesis in these environmental conditions. Besides, resource scarcities drive different evolutionary trajectories toward the emergence of C4 photosynthesis. AUTHOR SUMMARYIt is estimated that high photorespiration reduces C3 crops productivity up to 50% [1]. Carbon concentrating mechanisms have evolved in many plants to overcome adverse effects of high photorespiration rate in especial environments. C4 photosynthesis is one of these adaptations that separate carbon assimilation reactions spatially between mesophyll and bundle sheath cells of the leaves. It is reported that C4 photosynthesis is evolved more than 65 times in 19 different families of angiosperms independently from C3 ancestors. Therefore, it is hypothesized that the potential modules, at the level of metabolism, anatomy, and gene regulation, which are needed to perform C4 photosynthesis are present in C3 plants. Since C4 plants grow better than C3 plants in hot and dry environments, scientists are working on converting C3 crops such as rice to C4 plants. However, several challenges, including a lack of understanding of the evolutionary paths toward manifestation of C4 trait, have hampered the C3-to-C4 engineering ([2]). Here, we used a metabolic network model of Arabidopsis thaliana as a C3 model plant and attempted to understand the possible evolutionary events leading to emerging of C4 photosynthesis in various scenarios and examined the results.