Extended differentiation of veins and stomata is essential for the expansion of large leaves in Rheum rhabarbarum

Premise of the Study The densities of veins and stomata govern leaf water supply and gas exchange. They are coordinated to avoid overproduction of either veins or stomata. In many species, where leaf area is greater at low light, this coordination is primarily achieved through differential cell expansion, resulting in lower stomatal and vein density in larger leaves. This mechanism would, however, create highly inefficient leaves in species in which leaf area is greater at high light. Here we investigate the role of cell expansion and differentiation as regulators of vein and stomatal density in Rheum rhabarbarum, which produces large leaves under high light. Methods Rheum rhabarbarum plants were grown under full sunlight and 7% of full sunlight. Leaf area, stomatal density, and vein density were measured from leaves harvested at different intervals. Key Results Leaves of R. rhabarbarum expanded at high light were six times larger than leaves expanded at low light, yet vein and stomatal densities were similar. In high light‐expanded leaves, minor veins were continuously initiated as the leaves expanded, while an extended period of stomatal initiation, compared to leaves expanded at low light, occurred early in leaf development. Conclusions We demonstrate that R. rhabarbarum adjusts the initiation of stomata and minor veins at high light, allowing for the production of larger leaves uncoupled from lower vein and stomatal densities. We also present evidence for an independent control of vein and stomatal initiation, suggesting that this adjustment must involve some unknown developmental mechanism.