Metabolic Network Constrains Gene Regulation of C(4) Photosynthesis: The Case of Maize

Engineering C(3) plants to increase their efficiency of carbon fixation as well as of nitrogen and water use simultaneously may be facilitated by understanding the mechanisms that underpin the C(4) syndrome. Existing experimental studies have indicated that the emergence of the C(4) syndrome requires co-ordination between several levels of cellular organization, from gene regulation to metabolism, across two co-operating cell systems—mesophyll and bundle sheath cells. Yet, determining the extent to which the structure of the C(4) plant metabolic network may constrain gene expression remains unclear, although it will provide an important consideration in engineering C(4) photosynthesis in C(3) plants. Here, we utilize flux coupling analysis with the second-generation maize metabolic models to investigate the correspondence between metabolic network structure and transcriptomic phenotypes along the maize leaf gradient. The examined scenarios with publically available data from independent experiments indicate that the transcriptomic programs of the two cell types are co-ordinated, quantitatively and qualitatively, due to the presence of coupled metabolic reactions in specific metabolic pathways. Taken together, our study demonstrates that precise quantitative coupling will have to be achieved in order to ensure a successfully engineered transition from C(3) to C(4) crops.