Mesophyll Development in 3D: Pressure, Plasticity, and Porosity

Despite their myriad macroscopic shapes, almost all plant leaves consist of four layers of tissue: a top epidermal layer, followed by two layers of mesophyll tissue, the more ordered, denser, palisade mesophyll, and the more disordered and porous, spongy mesophyll, and finally a bottom epidermal layer. Even though spongy mesophyll exists in almost every terrestrial plant species and is critical in the structure and photosynthetic function of leaves, the physics of the morphogenesis of this tissue remains poorly understood. During development, spongy mesophyll cells transform from a dense packing of polyhedral cells to a disordered network of highly aspherical cells. We develop novel 3D discrete element method simulations to model spongy mesophyll development in arabidopsis thaliana. We probe the competing roles of turgor pressure, cell wall plasticity, and cell-cell adhesion during tissue development and find the necessary conditions for stable, porous, spongy mesophyll tissue. The predictions from the model for the cell shape, cell volume expansion, and tissue porosity match those found in experimental microcomputed tomography and confocal microscopy images of spongy mesophyll in arabidopsis thaliana.