Computational modelling predicts substantial carbon assimilation gains for C(3) plants with a single-celled C(4) biochemical pump

Achieving global food security for the estimated 9 billion people by 2050 is a major scientific challenge. Crop productivity is fundamentally restricted by the rate of fixation of atmospheric carbon. The dedicated enzyme, RubisCO, has a low turnover and poor specificity for CO(2). This limitation of C(3) photosynthesis (the basic carbon-assimilation pathway present in all plants) is alleviated in some lineages by use of carbon-concentrating-mechanisms, such as the C(4) cycle—a biochemical pump that concentrates CO(2) near RubisCO increasing assimilation efficacy. Most crops use only C(3) photosynthesis, so one promising research strategy to boost their productivity focuses on introducing a C(4) cycle. The simplest proposal is to use the cycle to concentrate CO(2) inside individual chloroplasts. The photosynthetic efficiency would then depend on the leakage of CO(2) out of a chloroplast. We examine this proposal with a 3D spatial model of carbon and oxygen diffusion and C(4) photosynthetic biochemistry inside a typical C(3)-plant mesophyll cell geometry. We find that the cost-efficiency of C(4) photosynthesis depends on the gas permeability of the chloroplast envelope, the C(4) pathway having higher quantum efficiency than C(3) for permeabilities below 300 μm/s. However, at higher permeabilities the C(4) pathway still provides a substantial boost to carbon assimilation with only a moderate decrease in efficiency. The gains would be capped by the ability of chloroplasts to harvest light, but even under realistic light regimes a 100% boost to carbon assimilation is possible. This could be achieved in conjunction with lower investment in chloroplasts if their cell surface coverage is also reduced. Incorporation of this C(4) cycle into C(3) crops could thus promote higher growth rates and better drought resistance in dry, high-sunlight climates.