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Embryonic expression of priapulid Wnt genes - PubMed

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Embryonic expression of priapulid Wnt genes

Mattias Hogvall et al. Dev Genes Evol. 2019 Jul.

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.

Keywords: Ecdysozoan ancestor; Evolution; Penis worm; Posterior elongation; Wnt signalling.

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Figures

Fig. 1
Fig. 1

(A) Simplified cladogram representing the phylogenetic relationships of different ecdysozoan groups (after Campbell et al. 2011). (B) Adult specimen of the priapulid worm Priapulus caudatus next to a centimetre scale bar. Note subdivision of the adult body into the anterior introvert, the trunk and the posterior caudal appendage

Fig. 2
Fig. 2

(A) Phylogenetic analysis of Wnt genes. Bayesian analysis of Wnt amino acid sequences. Support of each node is given as posterior probability. Included species are as follows: Achaearanea (syn. Parasteatoda) tepidariorum (At), Acyrthosiphon pisum (Ap), Cupiennius salei (Cs), Daphnia pulex (Dp), Drosophila melanogaster (Dm), Euperipatoides kanangrensis (Ek), Glomeris marginata (Gm), Halicryptus spinulosus (Hspi), Homo sapiens (Hs), Ixodes scapularis (Is), Platynereis dumerilii (Pd), Priapulus caudatus (Pc) and Tribolium castaneum (Tc). (B) Wnt gene complement in arthropods, an onychophoran and priapulids. Grey boxes indicate lost Wnt subfamilies. Question marks in grey boxes indicate Wnts that have not been found in sequenced embryonic transcriptomes. Duplicated Wnts are represented by overlapping boxes. (E) Unpublished embryonic expression pattern (R. Janssen); E, published embryonic expression pattern; e, embryonic expression has been investigated but specific expression patterns were not detected; F, functional data are available

Fig. 3
Fig. 3

Expression of Wnt genes during P. caudatus embryogenesis. The estimated counts were averaged between replicates and summed between putative isoforms, and log transformed to visualise the gene-level abundances across developmental stages

Fig. 4
Fig. 4

Embryonic expression patterns of Priapulus caudatus Wnt genes. In all panels, asterisks mark the posterior pole of the embryo. The first column shows embryos in posterior view (A, E, I, M, Q, U); the second column shows embryos in lateral view (B, F, J, N, R, V); the third column shows schematic expression in lateral view (cf. second column); the fourth column shows schematic expression in posterior–lateral view (the white arrows indicate the AP axis). Roman numerals in panel E indicate six dot-like expression domains surrounding the posterior pole of the embryo. In all data panels, the developmental stage is indicated. The arrows in panels showing the introvertula stage in lateral viewpoint to the groove separating the introvert from the trunk

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