Abstract

IntroductionSomites, blocks of mesoderm tissue located on either side of the neural tube in the developing vertebrate embryo, are derived from mesenchymal cells in the presomitic mesoderm (PSM) and are a defining characteristic of vertebrates. In vertebrates, the somite segmental boundary is determined by Notch signalling and the antagonistic relationship of the downstream targets of Notch, Lfng, and Delta1 in the anterior PSM. The presence of somites in the basal chordate amphioxus (Branchiostoma floridae) indicates that the last common ancestor of chordates also had somites. However, it remains unclear how the genetic mechanisms underlying somitogenesis in vertebrates evolved from those in ancestral chordates.ResultsWe demonstrate that during the gastrula stages of amphioxus embryos, BfFringe expression in the endoderm of the archenteron is detected ventrally to the ventral limit of BfDelta expression in the presumptive rostral somites along the dorsal/ventral (D/V) body axis. Suppression of Notch signalling by DAPT (a γ-secretase inhibitor that indirectly inhibits Notch) treatment from the late blastula stage reduced late gastrula stage expression of BfFringe in the endodermal archenteron and somite markers BfDelta and BfHairy-b in the mesodermal archenteron. Later in development, somites in the DAPT-treated embryo did not separate completely from the dorsal roof of the archenteron. In addition, clear segmental boundaries between somites were not detected in DAPT-treated amphioxus embryos at the larva stage. Similarly, in vertebrates, DAPT treatment from the late blastula stage in Xenopus (Xenopus laevis) embryos resulted in disruption of somite XlDelta-2 expression at the late gastrula stage. At the tail bud stage, the segmental expression of XlMyoD in myotomes was diminished.ConclusionsWe propose that Notch signalling and the Fringe/Delta cassette for dorso-ventral boundary formation in the archenteron that separates somites from the gut in an amphioxus-like ancestral chordate were co-opted for anteroposterior segmental boundary formation in the vertebrate anterior PSM during evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-015-0033-0) contains supplementary material, which is available to authorized users.

Highlights

  • Somites, blocks of mesoderm tissue located on either side of the neural tube in the developing vertebrate embryo, are derived from mesenchymal cells in the presomitic mesoderm (PSM) and are a defining characteristic of vertebrates

  • We propose that Notch signalling and the Fringe/Delta cassette for dorso-ventral boundary formation in the archenteron that separates somites from the gut in an amphioxus-like ancestral chordate were co-opted for anteroposterior segmental boundary formation in the vertebrate anterior PSM during evolution

  • Dorso-ventral boundary formation between the rostral somites and the gut is controlled by Notch signalling In vertebrates, lunatic fringe (Lfng) suppresses Notch signalling in the anterior PSM and controls segmental boundary determination of future somites [33]

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Summary

Introduction

Blocks of mesoderm tissue located on either side of the neural tube in the developing vertebrate embryo, are derived from mesenchymal cells in the presomitic mesoderm (PSM) and are a defining characteristic of vertebrates. The presence of somites in the basal chordate amphioxus (Branchiostoma floridae) indicates that the last common ancestor of chordates had somites. It remains unclear how the genetic mechanisms underlying somitogenesis in vertebrates evolved from those in ancestral chordates. Segmented structures composed of repetitive units, called somites, that arise transiently during embryogenesis are a key feature of the vertebrate body plan. In amphioxus, the rostral somites develop from the dorsal mesoderm during early embryogenesis. The mesoderm is a single layer located in the dorsal roof of the archenteron

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