Recruitment of pre-existing networks during the evolution of C4 photosynthesis

During C-4 photosynthesis, CO2 is concentrated around the enzyme RuBisCO. The net effect is to reduce photorespiration while increasing water and nitrogen use efficiencies. Species that use C-4 photosynthesis have evolved independently from their C-3 ancestors on more than 60 occasions. Along with mimicry and the camera-like eye, the C-4 pathway therefore represents a remarkable example of the repeated evolution of a highly complex trait. In this review, we provide evidence that the polyphyletic evolution of C-4 photosynthesis is built upon pre-existing metabolic and genetic networks. For example, cells around veins of C-3 species show similarities to those of the C-4 bundle sheath in terms of C-4 acid decarboxylase activity and also the photosynthetic electron transport chain. Enzymes of C-4 photosynthesis function together in gluconeogenesis during early seedling growth of C-3 Arabidopsis thaliana. Furthermore, multiple C-4 genes appear to be under control of both light and chloroplast signals in the ancestral C-3 state. We, therefore, hypothesize that relatively minor rewiring of pre-existing genetic and metabolic networks has facilitated the recurrent evolution of this trait. Understanding how these changes are likely to have occurred could inform attempts to install C-4 traits into C-3 crops. This article is part of the themed issue 'Enhancing photosynthesis in crop plants: targets for improvement'.