Maternal activation of gap genes in the hover flyEpisyrphus

Abstract

The metameric organization of the insect body plan is initiated with the activation of gap genes, a set of transcription-factor-encoding genes that are zygotically expressed in broad and partially overlapping domains along the anteroposterior (AP) axis of the early embryo. The spatial pattern of gap gene expression domains along the AP axis is generally conserved, but the maternal genes that regulate their expression are not. Building on the comprehensive knowledge of maternal gap gene activation in Drosophila, we used loss- and gain-of-function experiments in the hover fly Episyrphus balteatus (Syrphidae) to address the question of how the maternal regulation of gap genes evolved. We find that, in Episyrphus, a highly diverged bicoid ortholog is solely responsible for the AP polarity of the embryo. Episyrphus bicoid represses anterior zygotic expression of caudal and activates the anterior and central gap genes orthodenticle, hunchback and Krüppel. In bicoid-deficient Episyrphus embryos, nanos is insufficient to generate morphological asymmetry along the AP axis. Furthermore, we find that torso transiently regulates anterior repression of caudal and is required for the activation of orthodenticle, whereas all posterior gap gene domains of knirps, giant, hunchback, tailless and huckebein depend on caudal. We conclude that all maternal coordinate genes have altered their specific functions during the radiation of higher flies (Cyclorrhapha).

Maternal Co-ordinate Gene Regulation and Axis Polarity in the Scuttle Fly Megaselia abdita

“…abdita , similar to E . balteatus [38]. Our evidence does not conclusively establish whether this interaction is direct.…”

“…melanogaster [51] and in bcd RNAi-treated embryos of E . balteatus [38]. In both of these cases, the anterior cap of hb expression has been interpreted as an anterior mirror duplication of the posterior hb domain [38,51].…”

“…balteatus [38]. In both of these cases, the anterior cap of hb expression has been interpreted as an anterior mirror duplication of the posterior hb domain [38,51]. The posterior hb domain is also conserved in M .…”

“…The hoverfly Episyrphus balteatus , for example, has secondarily lost maternal hb expression (Fig. 1) [38,44]. Consequently, knock-down of bcd by RNA interference (RNAi) leads to bicaudal phenotypes in this species [38].…”

New genes as drivers of phenotypic evolution

“…For example, HOX genes and apoptotic genes (such as apoptotic protease-activating factor 1 ( APAF1 ), BCL2 and caspase genes) 40 are ancient metazoan developmental genes that arose ~500–900 MYA. bicoid originated in insects ~100–300 MYA as a duplicate of Hox3 , and rapidly evolved as an essential maternal-effect morphogen in the control of gap genes, which are crucial for the initial set-up of the body axis in the D. melanogaster embryo 41,42 and in embryos in higher insect taxa 43 . Therefore, organism body plans have been remodelled as a result of the expansion in the repertoire of developmental genes, and it is interesting to consider the importance and evolution of newly arisen developmental genes.…”