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'.