1. Introduction
Embryonic development is a process which happens across scales, requiring temporal and spatial coordination across multiple levels of organization. At the smallest scale, individual cells must make numerous cell fate decisions as they acquire their final fates. This must be organized in such a way that coordination between cells produces patterns that, at the multi-cellular and tissue scale have organization and coherence.
Ultimately, the well-orchestrated development of multiple tissues lead to a reproducible development of embryos into their final adult form. A key question in developmental biology therefore relates to how information is propagated across these scales, both in terms of developmental emergence (i.e. how alterations within cells result in the emergence of tissue patterning and morphogenesis), and downward causation (i.e. how information is relayed downwards from alterations at the organismal and multi-tissue level to the regulation of dynamic individual cellular processes). How such multi-level interactions lead to the timing of developmental processes has been reviewed recently [1]. Here, we focus on how patterning (the generation of discernible patterns of gene expression) and morphogenesis (tissue shaping) act together.
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Cellular movements are a critical feature of embryogenesis, as it is the driving force of morphogenesis, which shapes the embryo into its final form. By regularly reorganizing cells and tissues in space, this results in the frequent rearrangement and repositioning of signalling centres which in turn can function either to further develop the pattern being produced by exposing cells differently to signalling, or to disrupt it by blurring the boundaries between domains of gene expression. As the pattern of gene expression within a tissue is a function of both the dynamics of gene expression intrinsic to the cells and the temporal exposure to extrinsic signals, cell movements probably act as an important additional component in the regulation of pattern emergence. In addition to this, mechanochemical signals can also impact the regulation of gene expression by triggering the activity signalling cascades in response to an altered mechanical environment [1]. Given these observations, we propose that by the explicit incorporation of cell movement into our understanding of pattern emergence, new mechanisms of this fundamental problem in biology are likely to emerge. This will build on our current understanding of how fate decisions in individual cells result in tissue-level molecular patterns that have largely been derived from studies in tissues with limited cell movement. Such studies have clearly demonstrated how, for example, morphogen gradients are able to inform cells of their position within a tissue and how cell fates are resolved as a result [2-6].
The aim of this review is to draw attention to the largely unappreciated role of cell movements in pattern formation. To this end, we will briefly review some of the landmark studies of pattern formation in tissues with limited cell movement to emphasize how in such systems pattern formation is an emergent property of signalling and gene regulatory networks (GRNs) alone, and briefly consider how research in these systems has shaped our current notions of patterning precision. We then move on to review pattern formation in developing tissues with extensive cell movements to propose that in such cases, pattern formation is no longer an emergent property of signalling and GRNs alone, but of signalling, GRNs and cell movements. We go further to suggest that cell movements themselves may play an important and often overlooked generative role in patterning, rather than being merely a source of noise to be buffered. Finally, we will consider how this broader conceptualization of the drivers of pattern formation might help us understand how developmental patterning might evolve by modifying not only signalling environments and GRN interactions across phylogeny, but also the geometry of body plans, with different cell and tissue morphogeneses.
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