On the nature and function of organizers.

Alfonso Martinez Arias,Ben Steventon

doi:10.1242/dev.159525

Abstract

ABSTRACTOrganizers, which comprise groups of cells with the ability to instruct adjacent cells into specific states, represent a key principle in developmental biology. The concept was first introduced by Spemann and Mangold, who showed that there is a cellular population in the newt embryo that elicits the development of a secondary axis from adjacent cells. Similar experiments in chicken and rabbit embryos subsequently revealed groups of cells with similar instructive potential. In birds and mammals, organizer activity is often associated with a structure known as the node, which has thus been considered a functional homologue of Spemann's organizer. Here, we take an in-depth look at the structure and function of organizers across species and note that, whereas the amphibian organizer is a contingent collection of elements, each performing a specific function, the elements of organizers in other species are dispersed in time and space. This observation urges us to reconsider the universality and meaning of the organizer concept.

Highlights

In the context of an embryo, an ‘organizer’ refers to a group of cells that harbour the ability to instruct fates and morphogenesis in surrounding cells, steering their development into specific organs and tissues (Anderson et al, 2016)
We recognize that a slight modification of the Lane and Sheets revision of the amphibian embryo fate map generates a useful frame of reference that allows the comparison of pre-gastrulation embryos of different species and reveals the existence of heterochronies and heterotopographies and conserved modules
The amphibian organizer, which originates the concept, is a contingent collection of elements, each with a specific function that unfolds over time during gastrulation; it is a structure characteristic of amphibian embryos

Summary

Introduction

In the context of an embryo, an ‘organizer’ refers to a group of cells that harbour the ability to instruct fates and morphogenesis in surrounding cells, steering their development into specific organs and tissues (Anderson et al, 2016). The fate map resulting from these observations remains an oversimplification but emphasizes the difficulty of implementing a simple Cartesian mapping of body axes onto the gastrula stage embryo (for example, see Niehrs, 2010) It allows for an easier comparison with amniote fate maps which, either in a disc or cylinder arrangement, have the AP axis as their main reference (see Stern et al, 1992). With this in mind, from the perspective of trying to better understand Spemann’s organizer, we propose that the most appropriate comparison in terms of fate maps across species is a correspondence between a frog at the onset of gastrulation (stage 10) and a mouse embryo at the end of primary gastrulation [embryonic day (E) 7.5]. The inherently dynamic nature of the way the body axes unfold during gastrulation, and the associated variety of gastrulation modes, requires a precise analysis of when and where signalling and

A Xenopus

Head process

Conclusions and perspectives