The potential of enhanced photosynthetic efficiency to help achieve the sustainable yield increases required to meet future demands for food and energy has spurred intense research towards understanding, modeling, and engineering photosynthesis. These current efforts, largely focused on the C3 model Arabidopsis thaliana or crop plants (e.g. rice, sorghum, maize, and wheat), could be intensified and broadened using model systems closely related to our food, feed, and energy crops and that allow rapid design-build-test-learn cycles. In this outlooking Opinion, we advocate for a concerted effort to expand our understanding and improve our ability to redesign carbon uptake, allocation, and utilization. We propose two specific research directions that combine enhanced photosynthesis with climate-smart metabolic attributes: (i) engineering pathways for flexible (facultative) C3-C4 metabolism where plants will operate either C3 or C4 photosynthesis based on environmental conditions such as temperature, light, and atmospheric CO2 levels; and (ii) increasing rhizospheric sink strength for carbon utilization, including strategies that allow for augmented transport of carbon to the soil for improved soil properties and carbon storage without jeopardizing aboveground crop biomass. We argue that such ambitious undertakings be first approached and demonstrated by exploring the full genomic potential of two model grasses, the C3Brachypodium distachyon and the C4Setaria viridis. The development of climate-smart crops could provide novel and bold solutions to increase crop productivity while reducing atmospheric carbon and nitrogen emissions.
