On the evolution of morphogenetic models: mechano‐chemical interactions and an integrated view of cell differentiation, growth, pattern formation and morphogenesis

Abstract

In the 1950s, embryology was conceptualized as four relatively independent problems: cell differentiation, growth, pattern formation and morphogenesis. The mechanisms underlying the first three traditionally have been viewed as being chemical in nature, whereas those underlying morphogenesis have usually been discussed in terms of mechanics. Often, morphogenesis and its mechanical processes have been regarded as subordinate to chemical ones. However, a growing body of evidence indicates that the biomechanics of cells and tissues affect in striking ways those phenomena often thought of as mainly under the control of cell-cell signalling. This accumulation of data has led to a revival of the mechano-transduction concept in particular, and of complexity in general, causing us now to consider whether we should retain the traditional conceptualization of development. The researchers' semantic preferences for the terms 'patterning', 'pattern formation' or 'morphogenesis' can be used to describe three main 'schools of thought' which emerged in the late 1970s. In the 'molecular school', the term patterning is deeply tied to the positional information concept. In the 'chemical school', the term 'pattern formation' regularly implies reaction-diffusion models. In the 'mechanical school', the term 'morphogenesis' is more frequently used in relation to mechanical instabilities. Major differences among these three schools pertain to the concept of self-organization, and models can be classified as morphostatic or morphodynamic. Various examples illustrate the distorted picture that arises from the distinction among differentiation, growth, pattern formation and morphogenesis, based on the idea that the underlying mechanisms are respectively chemical or mechanical. Emerging quantitative approaches integrate the concepts and methods of complex sciences and emphasize the interplay between hierarchical levels of organization via mechano-chemical interactions. They draw upon recent improvements in mathematical and numerical morphogenetic models and upon considerable progress in collecting new quantitative data. This review highlights a variety of such models, which exhibit important advances, such as hybrid, stochastic and multiscale simulations.

Mechano-Chemical Aspects of Organ Formation in Arabidopsis thaliana: The Relationship between Auxin and Pectin

“…This type of patterning mechanism, requiring the active directional transport of an instructive chemical signal and the mechanical changes it induces, both invokes historical ideas and inspires future directions; indeed, further exploration of mechano-chemical regulatory loops in developmental biology will likely provide a rich landscape of interdisciplinary hypotheses [4], [5], [60].…”

“…As exemplified by the seminal work of Alan Turing [1], scientists of diverse disciplines have all attempted to explain biological patterns within their own frameworks [2]. Within the field of developmental biology, these disciplines have been interacting more and more to provide richer details for patterning mechanisms, a trend which will surely continue [3], [4], [5]. One of the most riveting proposals of Turing is that models explaining morphogenesis should consist of 'two parts, the mechanical and the chemical' [1], [4]; using this simple statement as a starting point, we have undertaken to examine how a chemical signal, it's chemical responses, and it's mechanical outputs combine in plant patterning to provide a mechano-chemical regulatory loop.…”

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

“…Since the discovery of embryonic induction, which revealed that secreted molecules are capable of instructing and organizing cells in surrounding tissues (Waddington 1940;Spemann and Mangold 2001), cell-cell signaling has become a sine qua non mechanism of pattern formation in many (if not most) developmental systems (Meyerowitz 2002;Rogers and Schier 2011;Urdy 2012;Kicheva and Briscoe 2015). Experimental manipulations of extracellular signals can impact tissue patterning at a distance (Salazar-Ciudad 2006;Nahmad Bensusan 2011;Perrimon et al 2012;Urdy et al 2016).…”

Theoretical Modelling of the Molluscan Shell: What has been Learned From the Comparison Among Molluscan Taxa?

“…The first type belongs to the class of lateral inhibition models and the second type belongs to the class of mechanical models. The similarities and differences between these two classes of models-as well as their historical roots-are discussed at length in Urdy (2012), using various examples from developmental biology.…”