Embryonic expression of priapulid Wnt genes

Mattias Hogvall,Ralf Janssen,Andreas Hejnol,Graham E Budd,Bruno C Vellutini,José M Martín-Durán

doi:10.1007/s00427-019-00636-6

Abstract

Posterior elongation of the developing embryo is a common feature of animal development. One group of genes that is involved in posterior elongation is represented by the Wnt genes, secreted glycoprotein ligands that signal to specific receptors on neighbouring cells and thereby establish cell-to-cell communication. In segmented animals such as annelids and arthropods, Wnt signalling is also likely involved in segment border formation and regionalisation of the segments. Priapulids represent unsegmented worms that are distantly related to arthropods. Despite their interesting phylogenetic position and their importance for the understanding of ecdysozoan evolution, priapulids still represent a highly underinvestigated group of animals. Here, we study the embryonic expression patterns of the complete sets of Wnt genes in the priapulids Priapulus caudatus and Halicryptus spinulosus. We find that both priapulids possess a complete set of 12 Wnt genes. At least in Priapulus, most of these genes are expressed in and around the posterior-located blastopore and thus likely play a role in posterior elongation. Together with previous work on the expression of other genetic factors such as caudal and even-skipped, this suggests that posterior elongation in priapulids is under control of the same (or very similar) conserved gene regulatory network as in arthropods.

Highlights

Wnt signalling is crucial for animal development, as it is involved in the regulation of numerous developmental processes such as cell proliferation and cell migration, organogenesis and pattern formation
Of the 12 priapulid Wnt genes identified in sequenced transcriptomes, nine are expressed during embryonic development until 9 days after fertilisation (the first larval stage is reached at approximately 10 days after fertilisation (Wennberg et al 2008))
The only Wnt genes that show expression in the stage-specific RNA-seq time course, and for which we could not obtain any in situ hybridisation signal, are Wnt2 and Wnt5

Summary

Introduction

Wnt signalling is crucial for animal development, as it is involved in the regulation of numerous developmental processes such as cell proliferation and cell migration, organogenesis and pattern formation. One of the key functions of Wnt signalling is its general involvement in posterior growth in animals In “overtly segmented” animals, i.e. vertebrates, annelids and panarthropods, Wnt signalling is a key component of posterior segment addition (reviewed in Aulehla and Herrmann 2004, Murat et al 2010, Cho et al 2010, Janssen et al 2010, Pruitt et al 2014). While the specific gene regulatory networks (GRN) controlling posterior growth and segmentation can differ between different groups of animals, and in some cases even between closely related species of the same group, Wnt signalling seems to be always involved. In arthropods for example, several Wnt genes are frequently expressed in the posterior-located segment addition zone from where new segments are added to the growing embryo (e.g. Janssen et al 2010; Hayden and Arthur 2014; Constantinou et al 2016), and functional studies revealed that at least some of them (as well as other factors of Wnt signalling) likely fulfil combinatorial and/or redundant function(s) in posterior elongation and segmentation (e.g. Bolognesi et al 2008; Beermann et al 2011; Murat et al 2010)

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Conclusion