Abstract

BackgroundConservation of orthologous regulatory gene expression domains, especially along the neuroectodermal anterior-posterior axis, in animals as disparate as flies and vertebrates suggests that common patterning mechanisms have been conserved since the base of Bilateria. The homology of axial patterning is far less clear for the many marine animals that undergo a radical transformation in body plan during metamorphosis. The embryos of these animals are microscopic, feeding within the plankton until they metamorphose into their adult forms.ResultsWe describe here the localization of 14 transcription factors within the ectoderm during early embryogenesis in Patiria miniata, a sea star with an indirectly developing planktonic bipinnaria larva. We find that the animal-vegetal axis of this very simple embryo is surprisingly well patterned. Furthermore, the patterning that we observe throughout the ectoderm generally corresponds to that of "head/anterior brain" patterning known for hemichordates and vertebrates, which share a common ancestor with the sea star. While we suggest here that aspects of head/anterior brain patterning are generally conserved, we show that another suite of genes involved in retinal determination is absent from the ectoderm of these echinoderms and instead operates within the mesoderm.ConclusionsOur findings therefore extend, for the first time, evidence of a conserved axial pattering to echinoderm embryos exhibiting maximal indirect development. The dissociation of head/anterior brain patterning from "retinal specification" in echinoderm blastulae might reflect modular changes to a developmental gene regulatory network within the ectoderm that facilitates the evolution of these microscopic larvae.

Highlights

  • Conservation of orthologous regulatory gene expression domains, especially along the neuroectodermal anterior-posterior axis, in animals as disparate as flies and vertebrates suggests that common patterning mechanisms have been conserved since the base of Bilateria

  • These hypotheses, in which a microscopic larval stage is assumed ancestral to the entire deuterostome clade, propose that a centralized nervous system evolved from an infolding of the larval ciliary bands [10,11,12]

  • We suggest that the sea urchin embryo may undergo a relatively more rapid specification of these territories, with an associated loss of intermediate domains that we observe in the sea star

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Summary

Introduction

Conservation of orthologous regulatory gene expression domains, especially along the neuroectodermal anterior-posterior axis, in animals as disparate as flies and vertebrates suggests that common patterning mechanisms have been conserved since the base of Bilateria. The homology of axial patterning is far less clear for the many marine animals that undergo a radical transformation in body plan during metamorphosis The embryos of these animals are microscopic, feeding within the plankton until they metamorphose into their adult forms. Within the Ambulacraria, the free-swimming, bilaterally symmetric larvae of echinoderms, especially the bipinnaria larva of sea stars and the auricularia larva of sea cucumbers, share many similarities with the tornaria larva of indirectly developing hemichordates These microscopic larvae have an apical concentration of serotonergic neurons [6] and one or two concentrations, or bands, of cilia used to feed and swim in the plankton [7,8]. These hypotheses, in which a microscopic larval stage is assumed ancestral to the entire deuterostome clade, propose that a centralized nervous system evolved from an infolding of the larval ciliary bands [10,11,12]

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