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

Abstract

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-offunction 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.

Antero-posterior patterning of Drosophila ocelli requires an anti-repressor mechanism within the hh-pathway mediated by the Six3 gene Optix

“…Here, we have shown that in Drosophila the expression domain of Optix in eye discs, which runs along the anteriormost medial disc region, maps to the anterior medial dorsal head, where it is required. In addition, OptixNP2631>OptixRNAi adults show defects in the clypeal skeleton (not shown), recapitulating the defects seen in larvae (Coiffier et al, 2008). Therefore, all these results point to six3/Optix as a medial head-patterning gene also during eyeantennal disc development.…”

“…segment in Drosophila and the labral and middle head regions in Tribolium. Accordingly, six3/Optix mutant Drosophila larvae show reduced or absent labral-derived head skeletal elements, such as the labral organ and the maxillary segment-derived mouth hooks in Drosophila (Coiffier et al, 2008) and loss of the labrum and anterior vertex bristle in Tribolium (Posnien et al, 2009(Posnien et al, , 2011. Here, we have shown that in Drosophila the expression domain of Optix in eye discs, which runs along the anteriormost medial disc region, maps to the anterior medial dorsal head, where it is required.…”

“…The expression pattern and function of six3/Optix have been studied in Drosophila (Seimiya and Gehring, 2000;Coiffier et al, 2008) and Tribolium (Posnien et al, 2009(Posnien et al, , 2011Kittelmann et al, 2013) embryos. In both insects, six3/Optix expression is restricted to the head region, and includes the clypeolabrum and maxillary (A) Initially, broad wg expression maintains otd in the anterior dorsal eye disc region.…”

boudinis required for septate junction organisation inDrosophilaand codes for a diffusible protein of the Ly6 superfamily

“…To bypass embryonic lethality and recover bou let mutant larvae, we expressed wild-type HA-Bou in bou let embryos using nulloGAL4, a driver only active at the blastoderm stage (Coiffier et al, 2008). In this way, we obtained bou let mutants now dying at pupariation and presenting discs with reduced size and abnormal shape.…”

Dissecting the functional specificities of two Hox proteins

“…Repression of Distalless (Dll) by abdominal Hox genes (Vachon et al 1992;Gebelein et al 2002), but not more anterior Hox genes, represents a semiparalog-specific target gene (Mann et al 2009). In contrast, the head-specifying gene optix is repressed by most Hox genes, and provides an example of a shared Hox function (Coiffier et al 2008). In principle, because a high degree of specificity is required for only paralog-specific target gene regulation, the types of binding sites used by Hox proteins to regulate these distinct types of target genes may be different (Mann et al 2009).…”