Sequential pattern formation governed by signaling gradients

Abstract

Rhythmic and sequential segmentation of the embryonic body plan is a vital developmental patterning process in all vertebrate species. However, a theoretical framework capturing the emergence of dynamic patterns of gene expression from the interplay of cell oscillations with tissue elongation and shortening and with signaling gradients, is still missing. Here we show that a set of coupled genetic oscillators in an elongating tissue that is regulated by diffusing and advected signaling molecules can account for segmentation as a self-organized patterning process. This system can form a finite number of segments and the dynamics of segmentation and the total number of segments formed depend strongly on kinetic parameters describing tissue elongation and signaling molecules. The model accounts for existing experimental perturbations to signaling gradients, and makes testable predictions about novel perturbations. The variety of different patterns formed in our model can account for the variability of segmentation between different animal species.

Positional information encoded in the dynamic differences between neighbouring oscillators during vertebrate segmentation

“…These results suggest the possibility that Wnt activity link the properties of the oscillators such as the characteristic time scale of the amplitude and period gradients (α and β) with the growth rate. The coupling between the properties of the oscillators and growth has previously been shown to lead to a segmentation process that can account for PSM shrinking and growth termination (Jörg et al, 2015; Jörg et al, 2016), and in our model, it is required in order to fit data from different species (Figure 5). Moreover, such coupling suggests a possible developmental mechanism of somite size control.…”

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

“…Some iterations abandon the notion of the importance of global positional information via gradients altogether, in favor of an oscillatory reaction–diffusion mechanism . Importantly, however, only by explicitly including termination of elongation and patterning in these models will the true evolutionary diversity in vertebral formulas be accounted for . This would further entail the control to balance segmentation speed and progenitor pool size, as well as incorporating the temporal and spatial effects of an axial Hox code on progenitor proliferation and somite identity .…”

“…112 Importantly, however, only by explicitly including termination of elongation and patterning in these models will the true evolutionary diversity in vertebral formulas be accounted for. 113 This would further entail the control to balance segmentation speed and progenitor pool size, 114 as well as incorporating the temporal and spatial effects of an axial Hox code on progenitor proliferation and somite identity. [115][116][117][118] Intriguingly, either modulations in the speed of the segmentation clock or, alternatively, changing the duration of progenitor pool persistence have been shown to alter the eventual number of segments in the vertebral column of different species.…”

A unified mechanism for spatiotemporal patterns in somitogenesis

“…These primarily include molecules belonging to the FGF [46,47], RA [48,49] and Wnt families [50][51][52]. Even though the role of gradients on the overall dynamics has been explored [53][54][55][56], there is to date no consensus as to the explicit mechanism through which they contribute to somite formation. Our model demonstrates (a) Schematic diagram depicting the zebrafish pre-somitic mesoderm (PSM) and the dynamical states exhibited by the cells over the course of somitogenesis.…”