REGULATION OF THE TRIBOLIUM HOMOLOGS OF CAUDAL AND HUNCHBACK IN DROSOPHILA - EVIDENCE FOR MATERNAL GRADIENT SYSTEMS IN A SHORT GERM EMBRYO

In short germ embryos, the germ rudiment forms at the posterior ventra l side of the egg, while the anterior-dorsal region becomes the extra- embryonic serosa, It is difficult to see how an anterior gradient like that of bicoid in Drosophila could in these embryos be directly invol ved in patterning of the germ rudiment. Moreover, since it has not yet been possible to recover a bicoid homologue from any species outside the diptera, it has been speculated that the anterior bicoid gradient could be a late addition during insect evolution. We addressed this qu estion by analysing the regulation of potential target genes of bicoid in the short germ embryo of Tribolium castaneum. We demonstrate that homologues of caudal and hunchback from Tribolium are regulated by Dro sophila bicoid, In Drosophila, maternal caudal RNA is translationally repressed by bicoid, We find that Tribolium caudal RNA is also transla tionally repressed by bicoid, when it is transferred into Drosophila e mbryos under a maternal promoter. This strongly suggests that a functi onal bicoid homologue must exist in Tribolium, The second target gene, hunchback, is transcriptionally activated by bicoid in Drosophila. Tr ansfer of the regulatory region of Tribolium hunchback into Drosophila also results in regulation by early maternal factors, including bicoi d, but in a pattern that is more reminiscent of Tribolium hunchback ex pression, namely in two early blastoderm domains. Using enhancer mappi ng constructs and footprinting, we show that caudal activates the post erior of these domains via a specific promoter. Our experiments sugges t that a major event in the evolutionary transition from short to long germ embryogenesis was the switch from activation of the hunchback ga p domain by caudal to direct activation by bicoid, This regulatory swi tch can explain how this domain shifted from a posterior location in s hort germ embryos to its anterior position in long germ insects, and i t also suggest how an anterior gradient can pattern the germ rudiment in short germ embryos, i.e. by regulating the expression of caudal.