Neuronal patterning of the tubular collar cord is highly conserved among enteropneusts but dissimilar to the chordate neural tube

Sabrina Kaul-Strehlow,Andreas Wanninger,Daniela Praher,Makoto Urata

doi:10.1038/s41598-017-07052-8

Sabrina Kaul-Strehlow, Andreas Wanninger + Show 2 more

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https://doi.org/10.1038/s41598-017-07052-8

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Abstract

A tubular nervous system is present in the deuterostome groups Chordata (cephalochordates, tunicates, vertebrates) and in the non-chordate Enteropneusta. However, the worm-shaped enteropneusts possess a less complex nervous system featuring only a short hollow neural tube, whereby homology to its chordate counterpart remains elusive. Since the majority of data on enteropneusts stem from the harrimaniid Saccoglossus kowalevskii, putative interspecific variations remain undetected resulting in an unreliable ground pattern that impedes homology assessments. In order to complement the missing data from another enteropneust family, we investigated expression of key neuronal patterning genes in the ptychoderid Balanoglossus misakiensis. The collar cord of B. misakiensis shows anterior Six3/6 and posterior Otx + Engrailed expression, in a region corresponding to the chordate brain. Neuronal Nk2.1/Nk2.2 expression is absent. Interestingly, we found median Dlx and lateral Pax6 expression domains, i.e., a condition that is reversed compared to chordates. Comparative analyses reveal that adult nervous system patterning is highly conserved among the enteropneust families Harrimaniidae, Spengelidae and Ptychoderidae. BmiDlx and BmiPax6 have no corresponding expression domains in the chordate brain, which may be indicative of independent acquisition of a tubular nervous system in Enteropneusta and Chordata.

Highlights

The evolution of the nervous system in Bilateria and Deuterostomia in particular has been hotly debated for decades[1,2,3,4,5,6]
In order to obtain an overview of the developing adult nervous system of Balanoglossus misakiensis, we first examined the expression of Elav, an RNA-binding protein that marks differentiating neurons[22,23,24]
BmiElav is expressed in the epidermis of the metamorphosing larva (Agassiz stage) of B. misakiensis as a stripe along the entire dorsal midline and extends circumferentially to the posterior base of the proboscis (Fig. 1A,B,D)

Summary

Introduction

The evolution of the nervous system in Bilateria and Deuterostomia in particular has been hotly debated for decades[1,2,3,4,5,6]. We focused on the expression patterns in the developing collar cord of anteroposterior (Six3/6, Otx, and Engrailed) as well as putative mediolateral patterning genes (Pax[6], Dlx, Nk2.1, Nk2.2) The latter have been reported to form abutting domains of Nk and Pax genes in the annelid ventral nerve cord and in the vertebrate dorsal neural tube[2, 19]. In each of these progenitor domains specific neuronal cell types are formed The 2nd objective of this study is to compare the collar cord with the chordate neural tube, in order to elucidate the evolution of tubular nervous systems in Deuterostomia

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