Abstract
The Wnt family of secreted proteins has been proposed to play a conserved role in early specification of the bilaterian anteroposterior (A/P) axis. This hypothesis is based predominantly on data from vertebrate embryogenesis as well as planarian regeneration and homeostasis, indicating that canonical Wnt (cWnt) signaling endows cells with positional information along the A/P axis. Outside of these phyla, there is strong support for a conserved role of cWnt signaling in the repression of anterior fates, but little comparative support for a conserved role in promotion of posterior fates. We further test the hypothesis by investigating the role of cWnt signaling during early patterning along the A/P axis of the hemichordate Saccoglossus kowalevskii. We have cloned and investigated the expression of the complete Wnt ligand and Frizzled receptor complement of S. kowalevskii during early development along with many secreted Wnt modifiers. Eleven of the 13 Wnt ligands are ectodermally expressed in overlapping domains, predominantly in the posterior, and Wnt antagonists are localized predominantly to the anterior ectoderm in a pattern reminiscent of their distribution in vertebrate embryos. Overexpression and knockdown experiments, in combination with embryological manipulations, establish the importance of cWnt signaling for repression of anterior fates and activation of mid-axial ectodermal fates during the early development of S. kowalevskii. However, surprisingly, terminal posterior fates, defined by posterior Hox genes, are unresponsive to manipulation of cWnt levels during the early establishment of the A/P axis at late blastula and early gastrula. We establish experimental support for a conserved role of Wnt signaling in the early specification of the A/P axis during deuterostome body plan diversification, and further build support for an ancestral role of this pathway in early evolution of the bilaterian A/P axis. We find strong support for a role of cWnt in suppression of anterior fates and promotion of mid-axial fates, but we find no evidence that cWnt signaling plays a role in the early specification of the most posterior axial fates in S. kowalevskii. This posterior autonomy may be a conserved feature of early deuterostome axis specification.
Highlights
The Wnt family of secreted ligand proteins is involved in a wide range of developmental functions during animal development, from embryonic induction to cell fate specification and the generation of cell polarity [1,2]
The widely accepted model for the role of Wnt signalling in A/P axis specification is by the establishment of a simple activity gradient whereby high levels of Wnt lead to posterior fates and low levels to anterior fates
In this study we further test this model, examining the role of Wnt signaling in the acorn worm, a representative of hemichordates that belongs to the superphylum Deuterostomia along with chordates
Summary
The Wnt family of secreted ligand proteins is involved in a wide range of developmental functions during animal development, from embryonic induction to cell fate specification and the generation of cell polarity [1,2]. The presence of Wnt ligands, receptors, and Wnt antagonists in cnidarians, sponges, and ctenophores indicates an early origin and diversification of the Wnt pathway during the radiation of metazoan phyla, before the emergence of bilaterians [3,4,5,6,7]. The canonical Wnt (cWnt) or Wnt-β-catenin pathway is the best studied and involves ligand binding of both the Frizzled (Fz) receptor and Lrp5/6 coreceptor. Activation of this pathway leads to stabilization of β-catenin and trafficking to the nucleus where it activates downstream targets in cooperation with Tcell factor/lymphoid enhancer factor (Tcf/lef) transcription factors. Comparative studies have proposed conserved roles of cWnt signaling in basic axial patterning of metazoan embryos, suggesting that cWnt signaling played a fundamental role in the early establishment of metazoan axis formation [3,4,8,9,10,11,12,13,14]
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