Pre-bilaterian origin of the blastoporal axial organizer.

Yulia Kraus,Ulrich Technau,Grigory Genikhovich,Andy Aman

doi:10.1038/ncomms11694

Yulia Kraus, Ulrich Technau + Show 2 more

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https://doi.org/10.1038/ncomms11694

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Abstract

The startling capacity of the amphibian Spemann organizer to induce naïve cells to form a Siamese twin embryo with a second set of body axes is one of the hallmarks of developmental biology. However, the axis-inducing potential of the blastopore-associated tissue is commonly regarded as a chordate feature. Here we show that the blastopore lip of a non-bilaterian metazoan, the anthozoan cnidarian Nematostella vectensis, possesses the same capacity and uses the same molecular mechanism for inducing extra axes as chordates: Wnt/β-catenin signaling. We also demonstrate that the establishment of the secondary, directive axis in Nematostella by BMP signaling is sensitive to an initial Wnt signal, but once established the directive axis becomes Wnt-independent. By combining molecular analysis with experimental embryology, we provide evidence that the emergence of the Wnt/β-catenin driven blastopore-associated axial organizer predated the cnidarian-bilaterian split over 600 million years ago.

Highlights

The startling capacity of the amphibian Spemann organizer to induce naıve cells to form a Siamese twin embryo with a second set of body axes is one of the hallmarks of developmental biology
Since only the blastopore lip is capable of inducing a second axis upon transplantation[2], our search for a candidate Wnt was restricted to Wnt genes, which are expressed in the blastopore lip of the Nematostella mid-gastrula
In this paper, we showed that the key molecules conveying the inductive capacity to the Nematostella organizer are Wnt[1] and Wnt[3]. Their co-expression in any region of the ectoderm of the gastrula following the single blastomere injection appears to be sufficient for the tissue to acquire axial organizer properties

Summary

Introduction

The startling capacity of the amphibian Spemann organizer to induce naıve cells to form a Siamese twin embryo with a second set of body axes is one of the hallmarks of developmental biology. Axis-forming blastoporal organizers were long thought to be a chordate-specific feature, transplantation of a fragment of the mid-gastrula blastopore lip in the sea anemone Nematostella vectensis, a member of the early branching non-bilaterian phylum Cnidaria (which, in addition to sea anemones, includes corals, hydroids and jellyfish), resulted in the formation of an ectopic body axis[2], just like the Mangold-Spemann organizer in amphibians Whether this similarity reflects the homologous or convergent origin of the cnidarian and vertebrate blastoporal axial organizers remained unclear, since the molecular nature of the signal conveying axial organizer properties to an embryonic tissue has not been determined outside deuterostomes. In order to test whether the progeny of the EF1a::Wnt1/EF1a::Wnt[3] injected blastomere becomes part of the induced ectopic axis, we added the EF1a::mOrange[2] plasmid to the injection mix and showed that the mOrange2-expressing tissue contributes to the pharynx and the hypostome of the induced secondary head (Fig. 1f)

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