Common functions of central and posterior Hox genes for the repression of head in the trunk of Drosophila

Hox genes are localised in complexes, encode conserved homeodomain transcription factors and have mostly been studied for their specialised functions: the formation of distinct structures along the anteroposterior axis. They probably derived via duplication followed by divergence, from a unique gene, suggesting that Hox genes may have retained a common function. The comparison of their homeodomain sequences groups Hox proteins into Anterior, Central and Posterior classes, reflecting their expression patterns in the head, trunk and tail, respectively. However, functional data supporting this classification are rare. Here, we re-examine a common activity of Hox genes in Drosophila: the repression of head in the trunk. First, we show that central and posterior Hox genes prevent the expression of the head specific gene optix in the trunk, providing a functional basis for the classification. Loss-of-function mutations of optix affect embryonic head development, whereas ectopic Optix expression strongly perturbs trunk development. Second, we demonstrate that the non-Hox genes teashirt, extradenticle and homothorax are required for the repression of optix and that Wingless signalling and Engrailed contribute to this repression. We propose that an evolutionary early function of Hox genes was to modify primitive head morphology with novel functions specialising the trunk appearing later on.