Abstract

Although many of the core components of the embryonic cell-cycle network have been elucidated, the question of how embryos achieve robust, synchronous cellular divisions post-fertilization remains unexplored. What are the different schemes that could be implemented by the embryo to achieve synchronization? By extending a cell-cycle model previously developed for embryos of the frog Xenopus laevis to include the spatial dimensions of the embryo, we establish a novel role for the rapid, fertilization-initiated calcium wave that triggers cell-cycle oscillations. Specifically, in our simulations a fast calcium wave results in synchronized cell cycles, while a slow wave results in full-blown spatio-temporal chaos. We show that such chaos would ultimately lead to an unpredictable patchwork of cell divisions across the embryo. Given this potential for chaos, our results indicate a novel design principle whereby the fast calcium-wave trigger following embryo fertilization synchronizes cell divisions.

Highlights

  • The early stages of embryo development require the integration of two separate design principles: a network that generates sustained oscillations and a control mechanism that produces robust spatial synchronization

  • Simple diffusion alone is insufficient to communicate the stage of the cell cycle over typical embryonic length scales (0.1–1 mm), it has been proposed that the combination of certain molecular species in a developing embryo may be regarded as an active medium [2]

  • What would be the biological consequences of this behavior? How do embryos avoid chaos? Our work provides potential answers to these questions: Chaos would lead to an unpredictable patchwork of cell divisions across the embryo - clearly a fatal defect in development

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Summary

Introduction

The early stages of embryo development require the integration of two separate design principles: a network that generates sustained oscillations and a control mechanism that produces robust spatial synchronization. Simple diffusion alone is insufficient to communicate the stage of the cell cycle over typical embryonic length scales (0.1–1 mm), it has been proposed that the combination of certain molecular species in a developing embryo may be regarded as an active medium [2]. Active media allow for the transmission of information over large length scales at rates far greater than allowed by simple diffusion. The existence of an active medium coupled to an oscillatory system does not guarantee spatial synchrony: active media can give rise to complex spatial patterns, including chaos [5]. If the embryo functions as an active medium during development, what guarantees that oscillations will be uniform and not spatially patterned or even chaotic?

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