Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae)

Abstract

The Drosophila gene bicoid functions at the beginning of a gene cascade that specifies anterior structures in the embryo. Its transcripts are localized at the anterior pole of the oocyte, giving rise to a Bicoid protein gradient, which regulates the spatially restricted expression of target genes along the anterior-posterior axis of the embryo in a concentration-dependent manner. The morphogen function of Bicoid requires the coactivity of the zinc finger transcription factor Hunchback, which is expressed in a Bicoid-dependent fashion in the anterior half of the embryo. Whereas hunchback is conserved throughout insects, bicoid homologs are known only from cyclorrhaphan flies. Thus far, identification of hunchback and bicoid homologs rests only on sequence comparison. In this study, we used double-stranded RNA interference (RNAi) to address the function of bicoid and hunchback homologs in embryos of the lower cyclorrhaphan fly Megaselia abdita (Phoridae). Megaselia-hunchback RNAi causes hunchback-like phenotypes as observed in Drosophila, but Megaselia-bicoid RNAi causes phenotypes different from corresponding RNAi experiments in Drosophila and bicoid mutant embryos. Megaselia-bicoid is required not only for the head and thorax but also for the development of four abdominal segments. This difference between Megaselia and Drosophila suggests that the range of functional bicoid activity has been reduced in higher flies.

Evidence for a composite anterior determinant in the hover flyEpisyrphus balteatus(Syrphidae), a cyclorrhaphan fly with an anterodorsal serosa anlage

“…It features an anterodorsal serosa anlage, strong influence of caudal on the AP axis, a (nearly) ubiquitous early zygotic activation of hunchback, as well as hunchback expression in the serosa anlage, which has been reported for non-cyclorrhaphan insects (Goltsev et al, 2004;Pultz et al, 2005;Rohr et al, 1999;Wolff et al, 1995) and is absent in Drosophila, Musca and Megaselia (Sommer and Tautz, 1991;Stauber et al, 2000;Tautz and Pfeifle, 1989). During late embryonic development, Engrailed expression in the hindgut of Episyrphus embryos is narrow and ring-shaped (S.L.…”

“…Fragments of Episyrphus homologs have been obtained by PCR using degenerate primers for hunchback (Stauber et al, 2000), nanos (5Ј-TGYGTGTTYTGYRARAAYAA/5Ј-GGYTTYTTNGGRCARTAYTT), caudal and orthodenticle (5Ј-GGRTTYYCNC -AAGGTATGTGGG/5Ј-ACCTGWACTCKWGATTCNGG). A fragment of the Eba-otd homeodomain was also obtained with degenerate bicoid primers (5Ј-TNGTNATGMGNMGNMGNMGNAC/5Ј-CKNCKRTTYT -TR AAC CA).…”

“…In many other cyclorrhaphan flies, this fundamental role of bicoid is probably conserved, because in Megaselia, a basal cyclorrhaphan taxon, suppression of bicoid results in a mirror image duplication of the posterior abdomen, i.e. the loss of global AP polarity Stauber et al, 2000).…”

Divergence évolutive extrême d’un gène homéotique : le cas bicoid

“…La conservation fonctionnelle suggérée par ces résultats fut même testée pour bicoid, grâce à la technique d'interférence par l'ARN qui permet de produire des phéno-copies 2 de type perte de fonction d'un gène par inactivation avec l'ARN double brin correspondant. Ainsi, que ce soit chez la mouche domestique (Musca) [8] ou bien chez un autre cyclorrhaphe issu d'une lignée plus basale (Megaselia) [10], l'interférence ARN permit d'obtenir des phénocopies ressemblant aux phénotypes mutants de bicoid décrits chez la drosophile. Par conséquent, la fonction de bicoid ne présente aucune divergence majeure parmi les diptères cyclorrhaphes.…”

Evo‐Devo aspects of classical and molecular data in a historical perspective

“…This interpretation, together with the fact that in the lower cyclorrhaphan fly Megaselia bicoid has an essentially conserved function (Stauber et al, 2000), predicts that bicoid-specific functions originated during the very early radiation of this group of higher flies. As before that time the flies developed heads as well, the novel functions of bicoid must have replaced or enslaved specific functions of another gene (or genes) previously serving to initate anterior pattern formation.…”