Evolution and expression of BMP genes in flies

Abstract

Bone morphogenetic proteins (BMPs) play key roles in development. In Drosophila melanogaster, there are three BMP-encoding genes: decapentaplegic (dpp), glass bottom boat (gbb) and screw (scw). dpp and gbb are found in all groups of insects. In contrast, the origin of scw via duplication of an ancestral gbb homologue is more recent, with new evidence placing it within the Diptera. Recent studies show that scw appeared basal to the Schizophora, since scw orthologues exist in aschizan cyclorrhaphan flies. In order to further localise the origin of scw, we have utilised new genomic resources for the nematoceran moth midge Clogmia albipunctata (Psychodidae). We identified the BMP subclass members dpp and gbb from an early embryonic transcriptome and show that their expression patterns in the blastoderm differ considerably from those seen in cyclorrhaphan flies. Further searches of the genome of C. albipunctata were unable to identify a scw-like gbb duplicate, but confirm the presence of dpp and gbb. Our phylogenetic analysis shows these to be clear orthologues of dpp and gbb from other non-cyclorrhaphan insects, with C. albipunctata gbb branching ancestrally to the cyclorrhaphan gbb/scw split. Furthermore, our analysis suggests that scw is absent from all Nematocera, including the Bibionomorpha. We conclude that the gbb/scw duplication occurred between the separation of the lineage leading to Brachycera and the origin of cyclorrhaphan flies 200-150 Ma ago.

Fig. 1

Schematic tree of organisms discussed in the text. The relationships of the class Insecta are shown including the orders Phthiraptera, Hemiptera, Hymenoptera, Coleoptera and Diptera. The Diptera are traditionally classified into two suborders, the monophyletic Brachycera and an assemblage of basally branching lineages, the Nematocera. The Nematocera include the infraorders Tipulomorpha (not shown), Culicomorpha, Psychodomorpha and Bibionomorpha. The Bibionomorpha are the likely sister group to the Brachycera and together they form the Neodiptera, whose sister group in turn is likely to be the Psychodomorpha. The Brachycera are classified into the infraorders Cyclorrhapha and the basally branching lineages of the non-cyclorrhaphan Brachycera. These include the more closely related infraorders of Asiloidea, Stratiomyomorpha and Tabanomorpha and the likely sister group of the Cyclorrhapha, the Empidoidea. The Cyclorrhapha are in turn divided into the Schizophora with the basally branching lineages of the Cyclorrhapha forming the paraphyletic assemblage of the Aschiza. Previous studies have confirmed the presence of gbb and scw in the Cyclorrhapha (bold lines) indicating the gbb/scw duplication occurred somewhere between the origin of this lineage and the splitting of the Psychodomorpha

Fig. 2

Phylogenetic analysis of C. albipunctata BMP sequences. The tree is rooted using anti-dorsalizing morphogenetic protein (admp) sequence from the chordate amphioxus (Branchiostoma). Previous analyses have suggested that admp belongs to a family within the BMPs outside of the BMP2/4 and BMP5678 families (Van der Zee et al. 2008). dpp sequences form one group with strong bootstrap support (98), with a second group consisting of gbb, and gbb duplicates, forming another strongly supported group (bootstrap, 100). Within the dpp group, C. albipunctata dpp branches with other dipteran sequences. The second C. albipunctata sequence branches basally to M. destructor gbb, and both branch basally to the cyclorrhaphan gbb/scw genes indicating that they did not take part in this duplication event

Fig. 3

In situ hybridisation of BMP transcripts from C. albipunctata. Expression patterns for C. albipunctata dpp (a, a′, b, b′) and gbb (c, c′, d, d′) genes at blastoderm (a, a′, c, c′) and extended germ band stages (b, b′, d, d′). Lateral (a, b, c, d) and ventral (a′, b′, c′, d′) views are shown. Anterior is to the left. See text for a detailed description of expression patterns