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Zoological Lett. 2015 Nov 26;1:33. doi: 10.1186/s40851-015-0033-0. eCollection 2015.

On the origin of vertebrate somites.

Zoological letters

Takayuki Onai, Toshihiro Aramaki, Hidehiko Inomata, Tamami Hirai, Shigeru Kuratani

Affiliations

  1. Kuratani Evolutionary Morphology Laboratory, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-Minamimachi, Chuo-ku Kobe, 650-0047 Japan.
  2. Pattern Formation Group, Graduate School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, Osaka 565-0871 Japan.
  3. Laboratory for Axial Pattern Dynamics, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-Minamimachi, Chuo-ku Kobe, 650-0047 Japan.

PMID: 26613046 PMCID: PMC4660845 DOI: 10.1186/s40851-015-0033-0

Abstract

INTRODUCTION: 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. 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.

RESULTS: We 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.

CONCLUSIONS: 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.

Keywords: Amphioxus; Enterocoel theory; Notch signalling; Origin of vertebrates; Somites

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