C4 photosynthesis occurs in the most productive crops and vegetation on the planet, and has become widespread because it allows increased rates of photosynthesis compared with the ancestral C3 pathway. Leaves of C4 plants typically possess complicated alterations to photosynthesis, such that its reactions are compartmented between mesophyll and bundle sheath cells. Despite its complexity, the C4 pathway has arisen independently in 62 separate lineages of land plants, and so represents one of the most striking examples of convergent evolution known. We demonstrate that elements in untranslated regions (UTRs) of multiple genes important for C4 photosynthesis contribute to the metabolic compartmentalization characteristic of a C4 leaf. Either the 5′ or the 3′ UTR is sufficient for cell specificity, indicating that functional redundancy underlies this key aspect of C4 gene expression. Furthermore, we show that orthologous PPDK and CA genes from the C3 plant Arabidopsis thaliana are primed for recruitment into the C4 pathway. Elements sufficient for M-cell specificity in C4 leaves are also present in both the 5′ and 3′ UTRs of these C3A. thaliana genes. These data indicate functional latency within the UTRs of genes from C3 species that have been recruited into the C4 pathway. The repeated recruitment of pre-existing cis-elements in C3 genes may have facilitated the evolution of C4 photosynthesis. These data also highlight the importance of alterations in trans in producing a functional C4 leaf, and so provide insight into both the evolution and molecular basis of this important type of photosynthesis.