During development, unique combinations of transcription factors and signaling pathways carve the nascent eye-antennal disc of the fruit fly Drosophila melanogaster into several territories that will eventually develop into the compound eye, ocelli, head epidermis, bristles, antenna and maxillary palpus of the adult head. Juxtaposed patterns of Hedgehog (Hh) and Decapentaplegic (Dpp) initiate compound eye development, while reciprocal domains of Dpp and Wingless (Wg) induce formation of the antennal and maxillary palp fields. Hh and Wg signaling, but not Dpp, contribute to the patterning of the dorsal head vertex. Here, we show that combinatorial reductions of the Pax6 transcription factor Twin of Eyeless and either the Wg pathway or the Mirror (Mirr) transcription factor trigger a transformation of the ocelli into a compound eye and the neighboring head epidermis into an antenna. These changes in fate are accompanied by the ectopic expression of Dpp, which might be expected to trigger these changes in fate. However, the transformation of the field cannot be replicated by increasing Dpp levels alone despite the recreation of adjacent Hh-Dpp and Wg-Dpp domains. As such, the emergence of these ectopic organs occurs through a unique regulatory path.

Author contributions

Conceptualization: G.T., B.M.W., A.J.O., J.P.K.; Methodology: G.T., B.M.W., A.J.O., B.P.W.; Formal analysis: G.T., B.M.W., J.P.K.; Investigation: G.T., B.M.W., B.P.W.; Writing - original draft: J.P.K.; Writing - review & editing: G.T., B.M.W., J.P.K.; Visualization: G.T., B.M.W.; Supervision: J.P.K.; Project administration: J.P.K.; Funding acquisition: J.P.K.

Funding

The work has been supported by the Robert Briggs Fellowship in Developmental Biology to G.T. and A.J.O., as well as National Eye Institute (NEI) grants (R01 EY014863 and EY030847) and funds from the Department of Biology, College of Arts and Sciences and the Office of the Vice Provost for Research at Indiana University to J.P.K. Deposited in PMC for release after 12 months.

Data availability

All relevant data can be found within the article and its supplementary information.

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