Maximum CO₂ diffusion inside leaves is limited by the scaling of cell size and genome size

Summary

Maintaining high rates of photosynthesis in leaves requires efficient movement of CO₂ from the atmosphere to the chloroplasts inside the leaf where it is converted into sugar. Throughout the evolution of vascular plants, CO₂ diffusion across the leaf surface was maximized by reducing the sizes of the guard cells that form stomatal pores in the leaf epidermis^1,2. Once inside the leaf, CO₂ must diffuse through the intercellular airspace and into the mesophyll cells where photosynthesis occurs^3,4. However, the diffusive interface defined by the mesophyll cells and the airspace and its coordinated evolution with other leaf traits are not well described⁵. Here we show that among vascular plants variation in the total amount of mesophyll surface area per unit mesophyll volume is driven primarily by cell size, the lower limit of which is defined by genome size. The higher surface area enabled by smaller cells allows for more efficient CO₂ diffusion into photosynthetic mesophyll cells. Our results demonstrate that genome downsizing among the flowering plants⁶ was critical to restructuring the entire pathway of CO₂ diffusion, facilitating high rates of CO₂ supply to the leaf mesophyll cells despite declining atmospheric CO₂ levels during the Cretaceous.