Polycomb and Hox Genes Control JNK-Induced Remodeling of the Segment Boundary during Drosophila Morphogenesis

In segmented tissues, anterior and posterior compartments represent independent morphogenetic domains, which are made of distinct lineages separated by boundaries. During dorsal closure of the Drosophila embryo, specific “mixer cells” (MCs) are reprogrammed in a JNK-dependent manner to express the posterior determinant engrailed (en) and cross the segment boundary. Here, we show that JNK signaling induces de novo expression of en in the MCs through repression of Polycomb (Pc) and release of the en locus from the silencing PcG bodies. Whereas reprogramming occurs in MCs from all thoracic and abdominal segments, cell mixing is restricted to the central abdominal region. We demonstrate that this spatial control of MC remodeling depends on the antagonist activity of the Hox genes abdominal-A and Abdominal-B. Together, these results reveal an essential JNK/en/Pc/Hox gene regulatory network important in controlling both the plasticity of segment boundaries and developmental reprogramming. [Display omitted] •JNK controls Mixer cell reprogramming through Polycomb downregulation•HOX genes spatially regulate cell mixing at segment boundaries•Abdominal-A acts as a pro-mixing factor•Abdominal-B is a prevalent, negative regulator of cell mixing Roumengous et al. identify a gene regulatory network involving JNK, Polycomb, engrailed, and Hox genes that is important for developmental reprogramming and cell remodeling during tissue morphogenesis.