Abstract
Morphogenesis is a precise and robust dynamic process during metazoan embryogenesis, consisting of both cell proliferation and cell migration. Despite the fact that much is known about specific regulations at molecular level, how cell proliferation and migration together drive the morphogenesis at cellular and organismic levels is not well understood. Using Caenorhabditis elegans as the model animal, we present a phase field model to compute early embryonic morphogenesis within a confined eggshell. With physical information about cell division obtained from three-dimensional time-lapse cellular imaging experiments, the model can precisely reproduce the early morphogenesis process as seen in vivo, including time evolution of location and morphology of each cell. Furthermore, the model can be used to reveal key cell-cell attractions critical to the development of C. elegans embryo. Our work demonstrates how genetic programming and physical forces collaborate to drive morphogenesis and provides a predictive model to decipher the underlying mechanism.
Highlights
The development of metazoan embryos consists of cell proliferation, cell migration, and cell differentiation, which is robust against perturbations and reproducible among individuals [1,2,3]
We present a phase field model combined with in vivo cell morphology data, to reconstruct the morphogenetic dynamics in early C. elegans embryogenesis and investigate the strategies and principles accounting for the stereotypic patterns
The C. elegans early development is divided into separate stages with exact cell numbers for step-bystep simulation, according to its invariant cell division sequence in vivo (Fig 1B) [2]
Summary
The development of metazoan embryos consists of cell proliferation, cell migration, and cell differentiation, which is robust against perturbations and reproducible among individuals [1,2,3]. The system evolves from a fertilized zygote to a multicellular structure with hundreds to thousands of cells and forms stereotypic three-dimensional spatial patterns [4,5,6] These morphogenetic dynamics are achieved by the precise control on cell divisions [7,8], mechanical interactions between cells [9,10], and other molecular-level regulations like cortical myosin flow, inhomogeneous cytomembrane adhesion, and active actomyosin contractility [11,12,13]. There are 4 cell types at 4-cell stage and 6 cell types at 8-cell stage—the cell types are diversified by the consecutive asymmetric divisions of the germline stem cell (i.e., P0, P1, P2, and P3) and the contact-based cell-cell signaling transductions (e.g., Wnt and Notch) [15,16,17] These cells of different sizes, shapes, and fates migrate, communicate and interact with each other, making the correctness of their positions and contacts extremely momentous
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