Elsevier

Biosystems

Volume 109, Issue 3, September 2012, Pages 262-279
Biosystems

Morphogenesis as a macroscopic self-organizing process

https://doi.org/10.1016/j.biosystems.2012.05.003Get rights and content

Abstract

We start from reviewing different epistemological constructions used for explaining morphogenesis. Among them, we explore the explanatory power of a law-centered approach which includes top-down causation and the basic concepts of a self-organization theory. Within such a framework, we discuss the morphomechanical models based upon the presumption of feedbacks between mechanical stresses imposed onto a given embryo part from outside and those generated within the latter as a kind of active response. A number of elementary morphogenetic events demonstrating that these feedbacks are directed towards hyper-restoration (restoration with an overshoot) of the initial state of mechanical stresses are described. Moreover, we show that these reactions are bound together into the larger scale feedbacks. That permits to suggest a reconstruction of morphogenetic successions in early Metazoan development concentrated around two main archetypes distinguished by the blastopores geometry. The perspectives of applying the same approach to cell differentiation are outlined. By discussing the problem of positional information we suggest that the developmental pathway of a given embryo part depends upon its preceded deformations and the corresponding mechanical stresses rather than upon its static position at any moment of development.

Section snippets

Introduction: from classical to top-down causation

We define morphogenesis, in the broadest meaning of this term, as formation of new spatial structures during the development of organisms. Let us define any structure as a new one if its formation is associated with the changes (in most cases with the reduction) of a symmetry order. Our next step will be to classify these structures according to their spatial dimensions. What we see here first of all is a sharp distinction between two categories of structures: macroscopic, created by a

Morphomechanical feedbacks: models and experiments

A most general feature of morphogenesis is that it is associated with a series of symmetry breaks of embryonic bodies which, in the overwhelming majority of cases cannot be regarded as being imprinted from outside. Most obvious examples are the reductions of translational symmetry (metamerization: subdivision of a body into similar or non-similar parts); even if these events require any external inductors, the latter's symmetry order is always higher than that of the resulted structures. As

HR-based general morphomechanical scheme of early metazoans development

In this section we want to show that HR reactions until now described separately from each other can be combined into prolonged enough developmental successions. Moreover, we hope to demonstrate that such an approach gives new breath to the old idea of the developmental archetypes, postulating the existence of quite a restricted number of the main developmental pathways embracing at least in broad outlines the development of most Metazoans. More concrete, we would like to show the following:

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Cell differentiation: a place for self-organization and morphomechanics

By a routine view, cell differentiation is regarded as a classical cause-effect transition, unambiguously determined by specific molecular signals. It becomes increasingly evident however that such an interpretation greatly oversimplifies the real situation. As it was numerously shown (for a detailed analysis see Kupiec, 2009) an absolute specificity is lost already in the first steps of the signaling pathways and can be restored within a reacting cell only by a secondary selection of the

A brief review of unsolved problems

Although about one and a half century passed since a valiant Wilhelm His (1878) claim that the heredity without mechanics belongs to a “non-scientific mysticism”, a morphomechanics is making just its first steps and only few developmental problems has been properly analyzed from this point of view. Below is given a very brief list of unsolved problems. Most of them are dealing with morphomechanics of freely moving mesenchyme type cells. By many evidences, their developmental fates largely

Acknowledgement

This work was supported by the Russian Foundation for Basic Research, grant # 11-04-01718.

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