The transcription factor optomotor-blind antagonizes Drosophila haltere growth by repressing decapentaplegic and hedgehog targets.

Eléanor Simon,Isabel Guerrero

doi:10.1371/journal.pone.0121239

Eléanor Simon, Isabel Guerrero

Open Access

https://doi.org/10.1371/journal.pone.0121239

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Abstract

In Drosophila, decapentaplegic, which codes for a secreted signaling molecule, is activated by the Hedgehog signaling pathway at the anteroposterior compartment border of the two dorsal primordia; the wing and the haltere imaginal discs. In the wing disc, Decapentaplegic and Hedgehog signaling targets are implicated in cell proliferation and cell survival. However, most of their known targets in the wing disc are not expressed in the haltere disc due to their repression by the Hox gene Ultrabithorax. The T-box gene optomotor-blind escapes this repression in the haltere disc, and therefore is expressed in both the haltere and wing discs. Optomotor-blind is a major player during wing development and its function has been intensely investigated in this tissue, however, its role in haltere development has not been reported so far. Here we show that Optomotor-blind function in the haltere disc differs from that in the wing disc. Unlike its role in the wing, Optomotor-blind does not prevent apoptosis in the haltere but rather limits growth by repressing several Decapentaplegic and Hedgehog targets involved both in wing proliferation and in modulating the spread of morphogens similar to Ultrabithorax function but without disturbing Ultrabithorax expression.

Highlights

Drosophila wings and halteres are homologous dorsal structures located in the second and third thoracic segments, respectively
The acquisition of wing vs. haltere-specific features is controlled by the differential expression of the Hox gene, Ultrabithorax (Ubx), which is expressed in the haltere disc but absent in the wing disc [1, 2]
In the wing imaginal disc (Fig. 1A shows wing disc organization), omb is expressed in a large domain around the anteroposterior (A/P) axis in the wing pouch and the presumptive hinge (Fig. 1B, B’)

Summary

Introduction

Drosophila wings and halteres are homologous dorsal structures located in the second and third thoracic segments, respectively. The primordia of wing and haltere are sacs of epithelial sheets called imaginal discs. Both structures differ in shape and size; they share a common developmental program. Morphogens involved in developmental programs are expressed in a similar fashion in both discs. The acquisition of wing vs haltere-specific features is controlled by the differential expression of the Hox gene, Ultrabithorax (Ubx), which is expressed in the haltere disc but absent in the wing disc [1, 2]. Ubx acts as a haltere identity selector, by impeding the activation of several downstream target genes which are part

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