Drosophila Hox and Sex-Determination Genes Control Segment Elimination through EGFR and extramacrochetae Activity

David Foronda,Paloma Martín,Ernesto Sánchez-Herrero

doi:10.1371/journal.pgen.1002874

David Foronda, Paloma Martín + Show 1 more

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https://doi.org/10.1371/journal.pgen.1002874

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Abstract

The formation or suppression of particular structures is a major change occurring in development and evolution. One example of such change is the absence of the seventh abdominal segment (A7) in Drosophila males. We show here that there is a down-regulation of EGFR activity and fewer histoblasts in the male A7 in early pupae. If this activity is elevated, cell number increases and a small segment develops in the adult. At later pupal stages, the remaining precursors of the A7 are extruded under the epithelium. This extrusion requires the up-regulation of the HLH protein Extramacrochetae and correlates with high levels of spaghetti-squash, the gene encoding the regulatory light chain of the non-muscle myosin II. The Hox gene Abdominal-B controls both the down-regulation of spitz, a ligand of the EGFR pathway, and the up-regulation of extramacrochetae, and also regulates the transcription of the sex-determining gene doublesex. The male Doublesex protein, in turn, controls extramacrochetae and spaghetti-squash expression. In females, the EGFR pathway is also down-regulated in the A7 but extramacrochetae and spaghetti-squash are not up-regulated and extrusion of precursor cells is almost absent. Our results show the complex orchestration of cellular and genetic events that lead to this important sexually dimorphic character change.

Highlights

A major change during evolution is the disappearance of a particular organ or structure
The expression driven by a escargot-Gal4 line [17] in the abdomen marks the histoblasts, which can be distinguished from surrounding larval epidermal cells (LECs) because they are diploid whereas the LECs are polytenic
We have found that the expression of spitz, a ligand of the Epidermal growth factor receptor (EGFR) pathway present both in histoblasts and LECs [19], and of argos, a target of the pathway [23], are reduced in the male A7 as compared to that of more anterior nests (Figure 1D–D0; Figure S1I, I9; the reduction is weakly detected in some cases)

Summary

Introduction

A major change during evolution is the disappearance of a particular organ or structure This event is sometimes restricted to one sex, and needs the coordination between sexdetermination genes and those that control pattern [1], such as the Hox genes, a group of genes that specify different structures along the antero-posterior axis [2]. One example of such coordination is the control of pigmentation in the Drosophila melanogaster posterior abdomen, uniformly pigmented in males but not in females. The histoblasts proliferate and spread, whereas the larval epidermal cells that are contiguous to them die and are extruded, until the whole abdominal region is covered by the histoblasts, which secrete the adult cuticle [11,12,13,14]

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