The role of photorespiration during the evolution of C photosynthesis in the genus Flaveria

C photosynthesis represents a most remarkable case of convergent evolution of a complex trait, which includes the reprogramming of the expression patterns of thousands of genes. Anatomical, physiological, and phylogenetic and analyses as well as computational modeling indicate that the establishment of a photorespiratory carbon pump (termed C photosynthesis) is a prerequisite for the evolution of C. However, a mechanistic model explaining the tight connection between the evolution of C and C photosynthesis is currently lacking. Here we address this question through comparative transcriptomic and biochemical analyses of closely related C, C-C, and C species, combined with Flux Balance Analysis constrained through a mechanistic model of carbon fixation. We show that C photosynthesis creates a misbalance in nitrogen metabolism between bundle sheath and mesophyll cells. Rebalancing nitrogen metabolism requires anaplerotic reactions that resemble at least parts of a basic C cycle. Our findings thus show how C photosynthesis represents a pre-adaptation for the C system, where the evolution of the C system establishes important C components as a side effect. © Mallmann et al.