The Drosophila egg chamber-a new spin on how tissues elongate

Abstract

During development, tissues undergo complex cellular rearrangements and changes in shape that produce a diversity of body plans and the functional organs therein. The Drosophila egg chamber has emerged as an exciting and highly tractable model in which to investigate novel mechanisms driving the elongation of tissues. Egg chambers are multicellular assemblies within flies' ovaries that will each give rise to a single egg. Although initially spherical, these simple organ-like structures lengthen as they grow. This transformation depends on an unusual form of planar polarity in the egg chamber's outer epithelial layer, in which arrays of linear actin bundles and fibril-like structures in the basement membrane both align perpendicular to the axis of elongation. The resulting circumferential arrangement of structural molecules is then thought to act as a "molecular corset" that directionally biases growth of the egg chamber. I will explore four fundamental questions about this system: (1) How is the circumferential pattern generated in the follicular epithelium? (2) What is the physical nature of the corset? (3) How does a corset-type mechanism lead to the cellular rearrangements necessary for the elongation of tissues? and (4) To what extent are the cellular mechanisms controlling egg chamber elongation conserved in other systems? For each topic, I will present insights gleaned from the recent literature and highlight fertile areas for future investigation.

Fig. 1

Overview of egg chamber elongation. (A) Micrograph showing a developmental array of egg chambers (ovariole) with the germarium at the anterior end. Egg chambers progressively elongate along their AP axes as they grow. Numbers indicate developmental stage. (B) Overview of the structure of an egg chamber. (C) The circumferential organization of basal actin bundles and the basement membrane is thought to function as a two-component molecular corset controlling egg chamber elongation. The vertical green lines represent basement membrane fibrils in the corset pattern on the egg chamber’s surface. The blue arrows represent how growth is preferentially channeled along the AP axis. (D) Illustrations of a rotating egg chamber that has been cut in half and tilted toward the viewer. The follicle cells collectively migrate along the inner surface of the basement membrane, which causes the entire egg chamber to rotate within the stationary matrix. Red dots mark the same four follicle cells over time. (E) The three major phases of egg chamber elongation.

Fig. 2

Relationship between the basal actin pattern and final egg shape. (A–B) Organization of contractile actin bundles at the basal surface of the follicular epithelium at stage 12. The F-actin is visualized with rhodamine phalloidin. (A) In a wild-type epithelium, the basal actin bundles are oriented perpendicular to the AP axis, which creates a circumferential pattern around the egg chamber. (B) Under certain mutant conditions, the basal actin bundles are still largely aligned within individual cells, but their tissue-level organization is lost. (C–D) Dorsal views of mature eggs. (C) A wild-type, elongated egg. (D) The rounded egg shape that arises from the disrupted tissue pattern shown in (B).

Fig. 3

Organization of the basal actin and basement membrane at early stages. (A) The basal actin bundles first show a circumferential organization in the germarium (A) optical cross-section through a germarium. (A′) Basal view of the same germarium showing the actin pattern. (B) The basal actin bundles show a robust circumferential organization during the period that the egg chamber is rotating. (A–B) The F-actin is visualized with rhodamine phalloidin. (C) Fibril-like structures in the basement membrane show a similar organization as that of the basal actin. The basement membrane in visualized with Collagen IV-GFP.