Specific expression and function of the Six3 optix in Drosophila serially homologous organs.

Amer Al Khatib,Nico Posnien,Antonella Iannini,Natalia Siomava,Fernando Casares

doi:10.1242/bio.023606

Abstract

ABSTRACTOrgan size and pattern results from the integration of two positional information systems. One global information system, encoded by the Hox genes, links organ type with position along the main body axis. Within specific organs, local information is conveyed by signaling molecules that regulate organ growth and pattern. The mesothoracic (T2) wing and the metathoracic (T3) haltere of Drosophila represent a paradigmatic example of this coordination. The Hox gene Ultrabithorax (Ubx), expressed in the developing T3, selects haltere identity by, among other processes, modulating the production and signaling efficiency of Dpp, a BMP2-like molecule that acts as a major regulator of size and pattern. However, the mechanisms of the Hox-signal integration in this well-studied system are incomplete. Here, we have investigated this issue by studying the expression and function of the Six3 transcription factor optix during Drosophila wing and haltere development. We find that in both organs, Dpp defines the expression domain of optix through repression, and that the specific position of this domain in wing and haltere seems to reflect the differential signaling profile among these organs. We show that optix expression in wing and haltere primordia is conserved beyond Drosophila in other higher diptera. In Drosophila, optix is necessary for the growth of wing and haltere. In the wing, optix is required for the growth of the most anterior/proximal region (the ‘marginal cell’) and for the correct formation of sensory structures along the proximal anterior wing margin; the halteres of optix mutants are also significantly reduced. In addition, in the haltere, optix is necessary for the suppression of sensory bristles.

Highlights

During development, several positioning systems inform cells of their location
The Six3 gene optix is differentially expressed in the wing and haltere discs Optix transcription, detected using RNA in situ hybridization, is found in both the wing and haltere imaginal discs of late third instar (L3) larvae (Organista et al, 2015; Seimiya and Gehring, 2000) (Fig. 1A) in the pouch regions of both discs
Since we have found that optix was expressed more laterally in the wing than in the haltere pouch, we asked whether the position of optix relative to the Dpp signaling gradient was different

Summary

Introduction

Several positioning systems inform cells of their location. The Hox code defines position along the anterior-posterior axis. In insects, this system generates segmental diversity along this body axis. The Drosophila wing and haltere primordia constitute a paradigm in which the integration of these two positional systems has been intensively investigated. In the Drosophila thorax (T), the second and third segments develop two serially homologous organs: the wing (in T2) and the haltere (in T3). The specific expression of the Hox gene Ultrabithorax (Ubx) in T3 is responsible for the specific morphology of the haltere, a small modified wing that acts as a balancing organ during Drosophila flight. Mutants that cause the loss of Ubx during haltere development cause its transformation into wing (Lewis, 1978), while ectopic expression of Ubx in the developing wing results in wings transformed into haltere-like appendages (Gonzalez-Gaitan et al, 1990)

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Conclusion