Ancient role of ten-m/odz in segmentation and the transition from sequential to syncytial segmentation

Axel Hunding,Stefan Baumgartner

doi:10.1186/s41065-017-0029-1

Axel Hunding, Stefan Baumgartner

Open Access

https://doi.org/10.1186/s41065-017-0029-1

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Journal: Hereditas	Publication Date: Apr 27, 2017
Citations: 8	License type: open-access

Affiliation: University of Copenhagen, Lund University

Abstract

BackgroundUntil recently, mechanisms of segmentation established for Drosophila served as a paradigm for arthropod segmentation. However, with the discovery of gene expression waves in vertebrate segmentation, another paradigm based on oscillations linked to axial growth was established. The Notch pathway and hairy delay oscillator are basic components of this mechanism, as is the wnt pathway. With the establishment of oscillations during segmentation of the beetle Tribolium, a common segmentation mechanism may have been present in the last common ancestor of vertebrates and arthropods. However, the Notch pathway is not involved in segmentation of the initial Drosophila embryo. In arthropods, the engrailed, wingless pair has a much more conserved function in segmentation than most of the hierarchy established for Drosophila.ResultsHere, we work backwards from this conserved pair by discussing possible mechanisms which could have taken over the role of the Notch pathway. We propose a pivotal role for the large transmembrane protein Ten-m/Odz. Ten-m/Odz may have had an ancient role in cell-cell communication, parallel to the Notch and wnt pathways. The Ten-m protein binds to the membrane with properties which resemble other membrane-based biochemical oscillators.ConclusionWe propose that such a simple transition could have formed the initial scaffold, on top of which the hierarchy, observed in the syncytium of dipterans, could have evolved.

Highlights

Until recently, mechanisms of segmentation established for Drosophila served as a paradigm for arthropod segmentation
For more than a decade, in attempts to understand sequential segmentation in other arthropods, the paradigm for Drosophila segmentation was used to explain the mechanisms of sequential segmentation
Synthesis of hairy mRNA is inhibited by Hairy protein, which is itself translated from the mRNA

Summary

Introduction

Mechanisms of segmentation established for Drosophila served as a paradigm for arthropod segmentation. With the establishment of oscillations during segmentation of the beetle Tribolium, a common segmentation mechanism may have been present in the last common ancestor of vertebrates and arthropods. Periodically-arising gene-expression waves, first established in chicken embryos [7], arise from the elongating posterior end of the embryo and run towards the anterior where they gradually stop, thereby adding a segment per period. This was interpreted as an oscillation under control of the chicken Hairy protein. This process repeats itself when the group of cells come to a halt during their oscillation, and segments form sequentially (from anterior towards posterior)

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