Abstract

In animals, body axis patterning is based on the concentration-dependent interpretation of graded morphogen signals, which enables correct positioning of the anatomical structures. The most ancient axis patterning system acting across animal phyla relies on β-catenin signaling, which directs gastrulation, and patterns the main body axis. However, within Bilateria, the patterning logic varies significantly between protostomes and deuterostomes. To deduce the ancestral principles of β-catenin-dependent axial patterning, we investigate the oral–aboral axis patterning in the sea anemone Nematostella—a member of the bilaterian sister group Cnidaria. Here we elucidate the regulatory logic by which more orally expressed β-catenin targets repress more aborally expressed β-catenin targets, and progressively restrict the initially global, maternally provided aboral identity. Similar regulatory logic of β-catenin-dependent patterning in Nematostella and deuterostomes suggests a common evolutionary origin of these processes and the equivalence of the cnidarian oral–aboral and the bilaterian posterior–anterior body axes.

Highlights

  • In animals, body axis patterning is based on the concentration-dependent interpretation of graded morphogen signals, which enables correct positioning of the anatomical structures

  • Graded morphogen signals comprise the top tier of the axial patterning cascades in Bilateria and their phylogenetic sister group Cnidaria[1,2,3]

  • We argue that this represents the ancestral regulatory logic of β-catenin-dependent axial patterning conserved since before the cnidarian–bilaterian split and discuss the implications of this on our understanding of the correspondence of the cnidarian and bilaterian body axes

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Summary

Introduction

Body axis patterning is based on the concentration-dependent interpretation of graded morphogen signals, which enables correct positioning of the anatomical structures. We show that the regulatory logic based on repression of the more aborally expressed β-catenin signaling target genes by the more orally expressed β-catenin signaling target genes is responsible for setting up gene expression domain boundaries along the entire O–A axis and identify Sp6-9 as a “transcriptional repressor Y” setting up the midbody/aboral boundary. We argue that this represents the ancestral regulatory logic of β-catenin-dependent axial patterning conserved since before the cnidarian–bilaterian split and discuss the implications of this on our understanding of the correspondence of the cnidarian and bilaterian body axes

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