Post-Turing tissue pattern formation: Advent of mechanochemistry

Chemical and mechanical pattern formation is fundamental during embryogenesis and tissue development. Yet, the underlying molecular and cellular mechanisms are still elusive in many cases. Most current theories assume that tissue development is driven by chemical processes: either as a sequence of chemical patterns each depending on the previous one, or by patterns spontaneously arising from specific chemical interactions (such as “Turing-patterns”). Within both theories, mechanical patterns are usually regarded as passive by-products of chemical pre-patters. However, several experiments question these theories, and an increasing number of studies shows that tissue mechanics can actively influence chemical patterns during development. In this study, we thus focus on the interplay between chemical and mechanical processes during tissue development. On one hand, based on recent experimental data, we develop new mechanochemical simulation models of evolving tissues, in which the full 3D representation of the tissue appears to be critical for obtaining a realistic mechanochemical behaviour. The presented modelling approach is flexible and numerically studied using state of the art finite element methods. Thus, it may serve as a basis to combine simulations with new experimental methods in tissue development. On the other hand, we apply the developed approach and demonstrate that even simple interactions between tissue mechanics and chemistry spontaneously lead to robust and complex mechanochemical patterns. Especially, we demonstrate that the main contradictions arising in the framework of purely chemical theories are naturally and automatically resolved using the mechanochemical patterning theory.Author summary: During embryogenesis, biological tissues gradually increase their complexity by self-organised creation of diverse chemical and mechanical patterns. Detailed mechanisms driving and controlling these patterns are not well understood. Previous theories mostly assume that these patterns are driven by chemical processes. Based on these theories, mechanical patterns are usually considered being mainly determined by chemical pre-patterns. However, experimental evidence for these theories is sparse, and several inconsistencies have been discovered. Furthermore, an increasing amount of data shows that tissue mechanics plays an important role in pattern formation. In this study, we present 3D computer simulations of evolving tissues to investigate the capacity of mechanochemical interactions for pattern formation. We show that even simple interactions between tissue mechanics and tissue chemistry spontaneously lead to robust chemical and mechanical pattern formation. We additionally demonstrate that main contradictions arising in the framework of purely chemical theories are naturally and automatically resolved using the mechanochemical patterning theory. The presented modelling approach can be used to combine simulations with recent experimental developments, to help unravel one of the big mysteries in biology: The mechanisms of self-organised pattern formation during embryogenesis.