Journal Article

Anteroposterior axis patterning by early canonical Wnt signaling during hemichordate development

Hurley, Imogen A., Osovitz, Michelle, Terasaki, Mark, Fritzenwanker, Jens H., Gerhart, John C., Pani, Ariel M., Aronowicz, Jochanan, Norris, Rachael P., Wu, Mike, Lowe, Christopher J., Uhlinger, Kevin R., Darras, Sébastien, Farrelly, Ellyn, Kirschner, Marc

2018

Overview

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.

• Publisher: Public Library of Science,Public Library of Science (PLoS)
• Subject: Animals / Antagonists / Autonomy / Biological Transport / Biology and Life Sciences / Blastula / Body Patterning - physiology / Cell Lineage - physiology / Cellular biology / Cellular signal transduction / Computer and Information Sciences / Developmental biology / Ectoderm / Embryogenesis / Embryonic Development - physiology / Embryonic growth stage / Embryos / Frizzled protein / Frizzled Receptors - physiology / Funding / Gene expression / Gene Expression Regulation, Developmental - physiology / Genes, Homeobox / Genetic aspects / Genetic engineering / Growth / Hemichordates / Homeostasis / Hypotheses / Life Sciences / Ligands / Organismal biology / Patterning / Physiological aspects / Planarians / Polychaeta - embryology / Polychaeta - physiology / Promotion / Proteins / Regeneration / Saccoglossus kowalevskii / Signaling / Specifications / Studies / Vertebrates / Wnt protein / Wnt Signaling Pathway - physiology / Xenopus