Differences in cellular mechanics and ECM dynamics shape differential development of wing and haltere in Drosophila

Abstract

Diverse organ shapes and sizes arise from the complex interplay between cellular properties, mechanical forces, and gene regulation. Drosophila wing-a flat structure and the globular haltere are two homologous flight appendages emerging from a similar group of progenitor cells. The activity of a single Hox transcription factor, Ultrabithorax (Ubx), governs the development of these two distinct organs-wing and haltere with different cell and organ morphologies. Our work reported here on differential development of wing and haltere suggest that the localization and abundance of actomyosin complexes, apical cell contractility, properties of extracellular matrix, and cell size and shape, which is a result of various cell intrinsic and extrinsic forces, plausibly influence the flat vs. globular geometry of these two organs. Loss of Ubx function led to wing cell-like cellular features in haltere discs, and corresponding changes at the level of adult organs. We also observed that RNAi-mediated downregulation of Atrophin or Pten, in the background of downregulated Expanded (or elevated Yki), gave rise to varying degrees of wing-like homeotic transformations at the cellular as well as adult organ levels. Finally, we employ a minimal vertex model to demonstrate that the observed differences in tissue architecture are physically sufficient to maintain and elaborate early shape differences and mimic flat wing-like or globular haltere-like morphologies. Together, these findings show how genetic and mechanical factors are integrated to generate organ-specific morphologies and provide a framework for understanding the evolution of organ shape.