Notch-dependent epithelial fold determines boundary formation between developmental fields in the Drosophila antenna.

Hui-Yu Ku,Y Henry Sun

doi:10.1371/journal.pgen.1006898

Abstract

Compartment boundary formation plays an important role in development by separating adjacent developmental fields. Drosophila imaginal discs have proven valuable for studying the mechanisms of boundary formation. We studied the boundary separating the proximal A1 segment and the distal segments, defined respectively by Lim1 and Dll expression in the eye-antenna disc. Sharp segregation of the Lim1 and Dll expression domains precedes activation of Notch at the Dll/Lim1 interface. By repressing bantam miRNA and elevating the actin regulator Enable, Notch signaling then induces actomyosin-dependent apical constriction and epithelial fold. Disruption of Notch signaling or the actomyosin network reduces apical constriction and epithelial fold, so that Dll and Lim1 cells become intermingled. Our results demonstrate a new mechanism of boundary formation by actomyosin-dependent tissue folding, which provides a physical barrier to prevent mixing of cells from adjacent developmental fields.

Highlights

During development, an organism is progressively divided into discrete fields that develop into different organs or parts of an organ
We focused our analysis on the antennal A1 fold that separates the A1 and A2-Ar segments, corresponding to the evolutionarily conserved segregation between coxopodite and telopodite segments of arthropod appendages
We found that Notch activation at the boundary between adjacent fields of selector gene expression triggers actomyosin-mediated cell apical constriction, which induces the formation of an epithelial fold and prevents intermixing of cells from adjacent fields

Summary

Introduction

An organism is progressively divided into discrete fields that develop into different organs or parts of an organ. The adjacent developmental fields develop distinct morphological, functional and molecular characteristics and are often divided by a sharp boundary that function to prevent lineage-related cells originating from one compartment from crossing into the adjacent compartment. Such lineage-restricting boundaries were first described in the fruitfly Drosophila wing and the milkweed bug Oncopeltus abdomen, using mitotic clones and cuticle markers to trace lineage distributions [1, 2]. Compartment boundaries generally coincide with the expression borders of the selector genes that determine the fates of developmental fields. We define ‘boundary’ as indicating lineage restriction, ‘compartment boundary’ to indicate absolute lineage restriction, ‘field boundary’ for incomplete lineage restriction, and ‘border’ to refer to expression domains

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