LADYBIRD, A TANDEM OF HOMEOBOX GENES THAT MAINTAIN LATE WINGLESS EXPRESSION IN TERMINAL AND DORSAL EPIDERMIS OF THE DROSOPHILA EMBRYO

ladybird early and ladybird late genes, tandemly located in the Drosop hila 93E homeobox gene cluster, encode highly related homeodomain-cont aining transcription factors. Here we report the cloning of the comple te cDNA sequences of both genes and a study of their expression and re gulatory interactions with the segment polarity gene wingless in the e pidermis. ladybird genes are co-expressed with wingless in epidermal c ells close to the posterior parasegmental boundaries and in terminal r egions of the body. In mutant embryos with altered wingless function, transcription of ladybird early and ladybird late is changed; it disap pears completely from the epidermis in wingless(-) embryos, indicating wingless-dependence. After 6 hours of development, wingless expressio n is maintained by gooseberry in the ventral epidermis. However, in th e dorsal epidermis and the terminal regions of the body, expression of wingless is independent of gooseberry but requires a wingless-ladybir d regulatory feedback loop. Loss of ladybird function reduces the numb er of wingless-expressing cells in dorsal epidermis and leads to compl ete inactivation of wingless in the anal plate. Consequently, mutant l adybird embryos fail to develop anal plates and ubiquitous embryonic e xpression of either one or both ladybird genes leads to severe defects of the dorsal cuticle. Lack of late wingless expression and anal plat e formation can be rescued with the use of a heat-shock-ladybird trans gene.