Abstract
Development encompasses processes that occur at multiple length scales, including gene-regulatory interactions, cell movements and reorganization, cell signalling and growth. It is essential that the timing of events in all of these different processes is coordinated to generate well-patterned tissues and organs. However, how the timing of intrinsic cell state changes is coordinated with events occurring at the multi-tissue and whole-organism level is unknown. Here, we argue that an important mechanism that accounts for the integration of timing across levels of organization is provided by tissue tectonics, i.e. how morphogenetic events driving tissue shape changes result in the relative displacement of signalling and responding tissues and coordinate developmental timing across scales. In doing so, tissue tectonics provides a mechanism by which the cell specification events intrinsic to cells can be modulated by the temporal exposure to extracellular signals. This exposure is in turn regulated by higher-order properties of the embryo, such as their physical properties, rates of growth and the combination of dynamic cell behaviours, impacting tissue morphogenesis. Tissue tectonics creates a downward flow of information from higher to lower levels of biological organization, providing an instance of downward causation in development.
Highlights
Time is central to biological phenomena: all biological processes are inherently dynamic, and this is true across fields
We propose that tissue tectonics is an essential consideration in understanding the mechanisms of downward causation in development, because downward causation is intimately associated with signalling between cells
Cell-intrinsic and cellextrinsic timer mechanisms both contribute to the overall timing of events during development, and we have described the utility of experimental embryology in distinguishing between these modes of developmental timer control
Summary
Time is central to biological phenomena: all biological processes are inherently dynamic, and this is true across fields. We will focus in this review on how the absolute timing of a given event in development is controlled and propose a mechanism by which timing may be coordinated across different levels of organization in the embryo. We will highlight how the reverse can be true, such that the dynamics of lowerlevel processes are regulated by alterations at higher levels, through downward causation. While this viewpoint abdicates the search for a single causative source of a developmental timer, we believe this holistic view to be essential for the development of meaningful explanations for core developmental (a) intrinsic timer (b) extrinsic timer royalsocietypublishing.org/journal/rsfs Interface Focus 11: 20200057. Which intrinsic timers are modulated by the local signalling environment that they encounter during development
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