Multi-scale computational model for understanding the mechanisms controlling tissue shape and structure in the shoot apical meristem of Arabidopsis thaliana

The shoot apical meristem (SAM) of Arabidopsis thaliana is a developmental organ that maintains a constant set of stem cells. It resides at the tip of the plant's growing stem and is responsible for all above-ground organ production. While SAM cells continually expand and divide throughout the plant’s life cycle, effluxing from the organ, the SAM maintains both a dome-like shape and a distinct layered structure of cells. Since plant cells are strongly adhered together and do not slip along one another, the principal factors influencing SAM shape and structure are placement of cell division planes and preferentially oriented anisotropic expansion of cells. Previous work has shown that there are multiple factors controlling these cell behaviors, including the plant hormones WUSCHEL and cytokinin. Since patterns of cell growth and division further influence cell shape and tensile forces, it becomes difficult to experimentally differentiate how cells respond to chemical and mechanical signaling, and what impact hypothesized growth mechanisms might have in maintaining SAM shape and structure. In an effort to understand this system, we constructed a mechanistic and data-calibrated multiscale subcellular element model in two dimensions, including both mechanical and chemical signaling. This model was used to generate several in silica cross-sections of the SAM whose cells followed various hypothesized cell behavior. Specifically, we tested whether WUSCHEL and cytokinin control both cells' anisotropic expansion and division plane placement, or whether patterns of cell division emerged from mechanical signaling. Our results revealed that the best match between model output and experimental data is when there is a layer-specific dependence of cell behavior on either chemical or mechanical signaling. Moreover, cells in the SAM's epidermal cell layers are known to experience substantial mechanical tension; the role of such an external source of tension in establishing the structure and shape of the SAM is currently not well understood. Preliminary simulations demonstrate that adequate peripherally-sourced tension is sufficient to recover the characteristic dome shape of the SAM.