The dorsoventral patterning of Musca domestica embryos: insights into BMP/Dpp evolution from the base of the lower cyclorraphan flies

Abstract

BackgroundIn the last few years, accumulated information has indicated that the evolution of an extra-embryonic membrane in dipterans was accompanied by changes in the gene regulatory network controlled by the BMP/Dpp pathway, which is responsible for dorsal patterning in these insects. However, only comparative analysis of gene expression levels between distant species with two extra-embryonic membranes, like A. gambiae or C. albipunctata, and D. melanogaster, has been conducted. Analysis of gene expression in ancestral species, which evolved closer to the amnioserosa origin, could provide new insights into the evolution of dorsoventral patterning in dipterans.ResultsHere we describe the spatial expression of several key and downstream elements of the Dpp pathway and show the compared patterns of expression between Musca and Drosophila embryos, both dipterans with amnioserosa. Most of the analyzed gene showed a high degree of expression conservation, however, we found several differences in the gene expression pattern of M. domestica orthologs for sog and tolloid. Bioinformatics analysis of the promoter of both genes indicated that the variations could be related to the gain of several binding sites for the transcriptional factor Dorsal in the Md.tld promoter and Snail in the Md.sog enhancer. These altered expressions could explain the unclear formation of the pMad gradient in the M. domestica embryo, compared to the formation of the gradient in D. melanogaster.ConclusionGene expression changes during the dorsal–ventral patterning in insects contribute to the differentiation of extra-embryonic tissues as a consequence of changes in the gene regulatory network controlled by BMP/Dpp. In this work, in early M. domestica embryos, we identified the expression pattern of several genes members involved in the dorsoventral specification of the embryo. We believe that these data can contribute to understanding the evolution of the BMP/Dpp pathway, the regulation of BMP ligands, and the formation of a Dpp gradient in higher cyclorraphan flies.Electronic supplementary materialThe online version of this article (10.1186/s13227-018-0102-5) contains supplementary material, which is available to authorized users.

A pro-BMP function exerted by Rhodnius prolixus short gastrulation reveals great diversity in the role of BMP modulators during embryonic patterning

“…In Drosophila DV patterning, Sog and Tsg inhibit Dpp autoactivation in the lateral neuroectoderm [ 53 ], and also shuttle Dpp against its source in the dorsal part of the embryo to concentrate a sharp field of Dpp activity required for amnioserosa formation [ 54 ]. A shuttling function for Sog has also been suggested in the induction of Clogmia and Musca dorsal extraembryonic tissue [ 5 , 55 ]. Likewise, T. castaneum Sog inhibits BMP function in the neuroectoderm and shuttles Dpp for serosa formation [ 6 ].…”

“…In some insect groups, loss-of-function for the BMP2/4 homologue decapentaplegic ( dpp ) results in the restricted loss of dorsal elements, such as the extraembryonic tissues in the diptera Drosophila melanogaster [ 4 ] and Musca domestica [ 5 ], as well as in the beetle Tribolium castaneum [ 6 ] and the cricket Gryllus bimaculatus [ 7 ]. In other species, however, loss of BMP function results in broad alterations in patterning, as revealed with knockdown assays for BMP encoding genes in the wasp Nasonia vitripennis [ 8 ] and the bug Oncopeltus fasciatus [ 9 ], where all DV patterning is lost.…”

Extraembryonic tissue in chelicerates: a review and outlook

“…Further genes that are expressed in the insect EEMs include developmental genes like Dorsocross (Doc), pebbled/hindsight, iroquois, pannier and tailup (e.g. [49][50][51][52]). However, the evolutionary conservation of these factors in the establishment of putative extraembryonic tissues in chelicerates is unclear: the zenhomologue Hox3 is not expressed in the dorsal field or the contra-orbital cells [53,54], and the expression and function of Doc, hindsight, iroquois, pannier and tailup have not yet been studied in chelicerates, whereas BMP signalling appears to be involved in the formation of the dorsal field in spiders (see below).…”