Drosophila female-specific Ilp7 motoneurons are generated by Fruitless-dependent cell death in males and a double-assurance survival role for Transformer in females [RESEARCH ARTICLE]

Sarah Rose C. Garner, Monica C. Castellanos, Katherine Baillie, Tianshun Lian, and Douglas W. Allan

Female-specific Ilp7 neuropeptide-expressing motoneurons (FS-Ilp7 motoneurons) are required in Drosophila for oviduct function in egg-laying. Here, we uncover cellular and genetic mechanisms underlying their female-specific generation. We demonstrate that programmed cell death (PCD) eliminates FS-Ilp7 motoneurons in males, and that this requires male-specific splicing of the sex determination gene fruitless (fru) into the Fru^MC isoform. However, in females, fru alleles that only generate Fru^M isoforms failed to kill FS-Ilp7 motoneurons. This blockade of Fru^M-dependent PCD was not attributable to doublesex gene function but to a non-canonical role for transformer (tra), a gene encoding the RNA splicing activator of fru and dsx gene transcripts that is only functional in females and prevents splicing into the Fru^M protein isoform. However, in both sexes, we show that Tra prevents PCD even in the presence of constitutive Fru^M isoform generation. In addition, we found that Fru^MC eliminated FS-Ilp7 motoneurons in both sexes, but only when Tra is absent. Thus, Fru^MC-dependent PCD eliminates female-specific neurons in males, and Tra plays a double-assurance function in females to establish and reinforce the decision to generate female-specific neurons.

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