Wnt/β-catenin regulates an ancient signaling network during zebrafish scale development

Andrew J Aman,Alexis N Fulbright,David M Parichy

doi:10.7554/elife.37001

Abstract

Understanding how patterning influences cell behaviors to generate three dimensional morphologies is a central goal of developmental biology. Additionally, comparing these regulatory mechanisms among morphologically diverse tissues allows for rigorous testing of evolutionary hypotheses. Zebrafish skin is endowed with a coat of precisely patterned bony scales. We use in-toto live imaging during scale development and manipulations of cell signaling activity to elucidate core features of scale patterning and morphogenesis. These analyses show that scale development requires the concerted activity of Wnt/β-catenin, Ectodysplasin (Eda) and Fibroblast growth factor (Fgf) signaling. This regulatory module coordinates Hedgehog (HH) dependent collective cell migration during epidermal invagination, a cell behavior not previously implicated in skin appendage morphogenesis. Our analyses demonstrate the utility of zebrafish scale development as a tractable system in which to elucidate mechanisms of developmental patterning and morphogenesis, and suggest a single, ancient origin of skin appendage patterning mechanisms in vertebrates.

Highlights

Developmental patterning generates distinct gene expression regimes that regulate morphogenetic cell behaviors
These analyses show that scale development relies on signaling interactions similar to interactions that regulate the patterning and morphogenesis of amniote skin appendages such as hair and feathers, and support a model in which diverse skin appendages of vertebrates arose from a common archetype
We find that zebrafish squamation proceeds through an invariant sequence of row and column addition (Figure 7A), this differs from previous reports based on fixed specimens that inferred a sequential spread of scales from posterior to

Summary

Introduction

Developmental patterning generates distinct gene expression regimes that regulate morphogenetic cell behaviors. We use conditional-genetic manipulations, live imaging and gene expression assays optimized for post-embryonic fish to show that multiple signaling pathways, including Wnt/b-catenin, Eda, Fgf and Shh regulate scale patterning and morphogenesis. These analyses show that scale development relies on signaling interactions similar to interactions that regulate the patterning and morphogenesis of amniote skin appendages such as hair and feathers, and support a model in which diverse skin appendages of vertebrates arose from a common archetype. Our analyses establish the fundamental parameters that govern scale initiation and morphogenesis and lay the groundwork for exploiting zebrafish scale development as a system in which to discern general principles of developmental patterning, regulation of morphogenetic cell behaviors, and the evolution of genetic regulatory mechanisms

Results

Discussion

Materials and methods

Findings

Funding Funder National Institutes of Health