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

During C4 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 C4 photosynthesis have evolved independently from their C3 ancestors on more than 60 occasions. Along with mimicry and the camera-like eye, the C4 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 C4 photosynthesis is built upon pre-existing metabolic and genetic networks. For example, cells around veins of C3 species show similarities to those of the C4 bundle sheath in terms of C4 acid decarboxylase activity and also the photosynthetic electron transport chain. Enzymes of C4 photosynthesis function together in gluconeogenesis during early seedling growth of C3Arabidopsis thaliana Furthermore, multiple C4 genes appear to be under control of both light and chloroplast signals in the ancestral C3 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 C4 traits into C3 crops.This article is part of the themed issue 'Enhancing photosynthesis in crop plants: targets for improvement'.