Adapting C4 photosynthesis to atmospheric change and increasing productivity by elevating Rubisco content in Sorghum and Sugarcane

Meta-analyses and theory show that with rising atmospheric [CO2], Rubisco has become the greatest limitation to light-saturated leaf CO2 assimilation rates (Asat) in C4 crops. So would transgenically increasing Rubisco increase Asat and result in increased productivity in the field? Here, we successfully overexpressed the Rubisco small subunit (RbcS) with Rubisco accumulation factor 1 (Raf1) in both sorghum and sugarcane, resulting in significant increases in Rubisco content of 13-25% and up to 90% respectively. Asat increased 12-15% and Rubisco enzyme activity [~]40% in three independent transgenic events of both species. Sorghum plants also showed increased speeds of photosynthetic induction and decreased bundle sheath leakiness. These improvements translated into average increases of 15.5% in biomass in field-grown sorghum and a 37-81% increase in greenhouse-grown sugarcane. This suggests a potential opportunity to achieve substantial increases in productivity of this key economically important clade of C4 crops, future proofing their value under global atmospheric change. Significance StatementThe world is projected to need a 60% increase in food supply by 2050 (UN), and this must be achieved under conditions of global change without expanding onto yet more land. C4 crops, while few in number, account for a large proportion of agricultural productivity. We reason that rising atmospheric [CO2] has very recently made Rubisco, the enzyme used for all carbon fixation in plants, the greatest limitation to light saturated photosynthesis in C4 crops. We demonstrate that transgenically increasing Rubisco content in sorghum and sugarcane, increases their photosynthetic efficiency and productivity, including in a field trial of sorghum. This shows a means to sustainably increase the productivity of this key group of crops.