Abstract
Maintaining high rates of photosynthesis in leaves requires efficient movement of CO2 from the atmosphere to the mesophyll cells inside the leaf where CO2 is converted into sugar. CO2 diffusion inside the leaf depends directly on the structure of the mesophyll cells and their surrounding airspace, which have been difficult to characterize because of their inherently three-dimensional organization. Yet faster CO2 diffusion inside the leaf was probably critical in elevating rates of photosynthesis that occurred among angiosperm lineages. Here we characterize the three-dimensional surface area of the leaf mesophyll across vascular plants. We show that genome size determines the sizes and packing densities of cells in all leaf tissues and that smaller cells enable more mesophyll surface area to be packed into the leaf volume, facilitating higher CO2 diffusion. Measurements and modelling revealed that the spongy mesophyll layer better facilitates gaseous phase diffusion while the palisade mesophyll layer better facilitates liquid-phase diffusion. Our results demonstrate that genome downsizing among the angiosperms was critical to restructuring the entire pathway of CO2 diffusion into and through the leaf, maintaining high rates of CO2 supply to the leaf mesophyll despite declining atmospheric CO2 levels during the Cretaceous.
Highlights
The primary limiting enzyme in photosynthesis, rubisco, functions poorly under low CO2 concentrations
The importance of maintaining efficient CO2 diffusion into the leaf is reflected in the evolutionary history of leaf anatomy; leaf surface conductance has increased during periods of declining atmospheric CO2 concentration [1], primarily due to increasing the density and reducing the sizes of stomatal guard cells that form the pores in the epidermis through which CO2 diffuses [2,3,4,5]
For 86 species spanning the extant diversity of vascular plants, we quantified from microcomputed tomography (microCT) images the sizes of spongy and palisade mesophyll cells and stomatal guard cells, as well as the packing densities per unit leaf area of veins, stomata and palisade mesophyll cells
Summary
The primary limiting enzyme in photosynthesis, rubisco, functions poorly under low CO2 concentrations. The surface area of the mesophyll per tissue volume (SAmes/Vmes; electronic supplementary material, figure S2), is the primary tissue-level structural trait limiting CO2 diffusion from the intercellular airspace into the hydrated cell walls of the mesophyll.
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