Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate

Stanislav Kremnyov,Kristine Henningfeld,Nikoloz Tsikolia,Christoph Viebahn

doi:10.1186/s13227-017-0090-x

Abstract

BackgroundThe notochord has organizer properties and is required for floor plate induction and dorsoventral patterning of the neural tube. This activity has been attributed to sonic hedgehog (shh) signaling, which originates in the notochord, forms a gradient, and autoinduces shh expression in the floor plate. However, reported data are inconsistent and the spatiotemporal development of the relevant shh expression domains has not been studied in detail. We therefore studied the expression dynamics of shh in rabbit, chicken and Xenopus laevis embryos (as well as indian hedgehog and desert hedgehog as possible alternative functional candidates in the chicken).ResultsOur analysis reveals a markedly divergent pattern within these vertebrates: whereas in the rabbit shh is first expressed in the notochord and its floor plate domain is then induced during subsequent somitogenesis stages, in the chick embryo shh is expressed in the prospective neuroectoderm prior to the notochord formation and, interestingly, prior to mesoderm immigration. Neither indian hedgehog nor desert hedgehog are expressed in these midline structures although mRNA of both genes was detected in other structures of the early chick embryo. In X. laevis, shh is expressed at the beginning of gastrulation in a distinct area dorsal to the dorsal blastopore lip and adjacent to the prospective neuroectoderm, whereas the floor plate expresses shh at the end of gastrulation.ConclusionsWhile shh expression patterns in rabbit and X. laevis embryos are roughly compatible with the classical view of “ventral to dorsal induction” of the floor plate, the early shh expression in the chick floor plate challenges this model. Intriguingly, this alternative sequence of domain induction is related to the asymmetrical morphogenesis of the primitive node and other axial organs in the chick. Our results indicate that the floor plate in X. laevis and chick embryos may be initially induced by planar interaction within the ectoderm or epiblast. Furthermore, we propose that the mode of the floor plate induction adapts to the variant topography of interacting tissues during gastrulation and notochord formation and thereby reveals evolutionary plasticity of early embryonic induction.

Highlights

The notochord has organizer properties and is required for floor plate induction and dorsoventral pat‐ terning of the neural tube
As inductive interactions belong to central concepts in developmental biology [76], the early role of the notochord serves as a paradigmatic example of induction by organizers, which are defined by their ability to induce and pattern adjacent tissue [3]
Axial expression of hedgehog genes in the chick In HH stage 5 [29] chicken embryos, which are at the beginning of notochord formation and concomitant primitive streak regression, a shh-positive area appears as a stripe-like expression in the midline anterior to the node (Fig. 1a and Additional file 1: Fig. 1A), whereas the node domain displays progressive left–right asymmetry [86]

Summary

Introduction

The notochord has organizer properties and is required for floor plate induction and dorsoventral pat‐ terning of the neural tube. This activity has been attributed to sonic hedgehog (shh) signaling, which originates in the notochord, forms a gradient, and autoinduces shh expression in the floor plate. Studies in amphibian embryos suggested that the notochord is required for correct morphological dorsoventral patterning of the neural tube [37], while other observations indicated, that a more cautious interpretation is needed [38, 75]. The notochord in the chick was shown to be required for floor plate development as well for its specific inductive function [59, 90]. Implantation of the notochord lateral to the neural tube causes ventralization of the lateral tube wall and formation of ectopic floor plate, as seen by cell shape change or ectopic axon outgrowth [59, 91]

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