Other ; This is the author accepted manuscript. The final version is available from the Nature Publishing Group via http://dx.doi.org/10.1038/nplants.2016.161 ; Abstract ; C$_{4}$ photosynthesis acts as a carbon concentrating mechanism that leads to large increases in photosynthetic efficiency. The C$_{4}$ pathway is found in more than 60 plant lineages but the molecular enablers of this evolution are poorly understood. In particular, it is unclear how non-photosynthetic proteins in the ancestral C$_{3}$ system have repeatedly become strongly expressed and integrated into photosynthesis gene regulatory networks in C$_{4}$ leaves. Here, we provide clear evidence that in C$_{3}$ leaves, genes encoding key enzymes of the C$_{4}$ pathway are already co-regulated with photosynthesis genes and are controlled by both light and chloroplast-to-nucleus signalling. In C$_{4}$ leaves this regulation becomes increasingly dependent on the chloroplast. We propose that regulation of C$_{4}$ cycle genes by light and the chloroplast in the ancestral C$_{3}$ state has facilitated the repeated evolution of the complex and convergent C$_{4}$ trait. ; Other ; The work was funded by the European Union 3to4 project and Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/J011754/1. I.G.-M. was supported by the Amgen Foundation. Research on chloroplast signalling by M.J.T. was supported by BBSRC grant (BB/J018139/1).