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Review
. 2018 Mar 9;145(5):dev159525.
doi: 10.1242/dev.159525.

On the nature and function of organizers

Affiliations
Review

On the nature and function of organizers

Alfonso Martinez Arias et al. Development. .

Abstract

Organizers, 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.

Keywords: Axial organization; Body plan; Neural induction; Organizer; Spemann; Vertebrate embryo.

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Conflict of interest statement

Competing interestsThe authors declare no competing or financial interests.

Figures

Fig. 1.
Fig. 1.
Unfolding of the principal body axes during gastrulation in Xenopus and mice. (A) Xenopus embryos at progressive developmental stages (st. 10-12) positioned with the blastopore lip on the right and the animal pole to the top. The prospective neural plate is shown in colours ranging from red (anterior) to yellow (posterior). Involuted mesodermal tissue is shown in green. Non-involuted mesodermal tissue is not shown. (B) Progressive emergence of the body axes in mouse. Mouse embryos are depicted at progressive stages of gastrulation, with proximal to the top and distal to the bottom. Lateral view, with the approximate future axes shown on the right. Note two important features of mammalian gastrulation, namely the impossibility of mapping the dorsoventral (DV) axis onto early gastrula stage embryos, and the progressive increase in the size of the embryo during gastrulation (not to scale). In both species, prospective head mesodermal cells arise from the non-involuted marginal zone/primitive streak and move anteriorly as anterior neural tissue is becoming specified in the overlying ectoderm/epiblast.
Fig. 2.
Fig. 2.
Similarities between the mouse node and the Xenopus blastoporal lip. Diagrams depicting sagittal transverse sections through the Xenopus blastoporal lip region (left) and the mouse node (right) at successive stages of gastrulation. Cells are colour coded to highlight homologies between tissues and their fates (see key). Species-specific structures are colour coded and labelled on the figure. These include bottle cells in Xenopus that drive the primary invagination of cells at the blastopore lip, and an epithelial indentation in the mouse node region, often referred to as the ‘pit’, that has motile cilia and acts as the source of the prechordal plate and the notochord. Posterior to the pit is a bulging structure often referred to as the ‘crown’, which gives rise to the postanal component of the notochord. Note that because of these two related structures, there is often some confusion in the literature as to what is considered the ‘node’ proper; the term has been used to refer to either the pit or both the pit and the crown. Here we use the term ‘node’ to refer to both structures, which are often transplanted together.
Fig. 3.
Fig. 3.
Heterochrony in gastrulation processes between mouse and Xenopus embryos. The diagrams on the left show Xenopus embryos at progressive stages of gastrulation with the prospective anterior to the left and posterior to the right. On the right are diagrams of mouse, shown with anterior to the left and posterior to the right, to follow convention. In both cases, the prospective neural plate is shown in colours ranging from red (anterior) to yellow (posterior). Involuted mesodermal tissue is in green. Non-involuted mesodermal tissue is not shown. Coloured bars indicate the principal cellular processes associated with gastrulation and how they map to different stages when comparing the two species. Note how these processes overlap in time in Xenopus but are temporally separate in mouse. EMT, epithelial-mesenchymal transition.

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