Patterning potential of the terminal system in the Drosophila embryo

Abstract

Segmentation of the Drosophila embryo is initiated by localized maternal signals. In this context, anteriorly localized Bicoid activates the gap genes in the anterior half of the embryo while posteriorly localized Nanos represses the translation of maternal hunchback mRNA to pattern the posterior half. The non-segmented termini are patterned by the localized activation of mitogen-activated protein kinase. Yet, the spatial extent of the terminal patterning system in regulating gap genes beyond poles remains unknown. We investigated the patterning potential of the terminal system using mutagenized embryos that lack both the anterior and the posterior maternal signaling systems. Using a combination of quantitative imaging and mathematical modeling, we analyzed the spatial patterns of gap genes in the early Drosophila embryo. We found that this mutant embryo develops symmetric cuticle patterns along the anteroposterior axis with two segments on each side. Notably, the terminal system can affect the expression of Kruppel in the torso region. Our mathematical model recapitulates the experimental data and reveals the potential bistability in the terminal patterning system. Collectively, our study suggests that the terminal system can act as a long-range inductive signal and establish multiple gene expression boundaries along the anteroposterior axis of the developing embryo.