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. 2011 May 31;12:278.
doi: 10.1186/1471-2164-12-278.

BMP Signaling Components in Embryonic Transcriptomes of the Hover Fly Episyrphus Balteatus (Syrphidae)

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BMP Signaling Components in Embryonic Transcriptomes of the Hover Fly Episyrphus Balteatus (Syrphidae)

Steffen Lemke et al. BMC Genomics. .
Free PMC article

Abstract

Background: In animals, signaling of Bone Morphogenetic Proteins (BMPs) is essential for dorsoventral (DV) patterning of the embryo, but how BMP signaling evolved with changes in embryonic DV differentiation is largely unclear. Based on the extensive knowledge of BMP signaling in Drosophila melanogaster, the morphological diversity of extraembryonic tissues in different fly species provides a comparative system to address this question. The closest relatives of D. melanogaster with clearly distinct DV differentiation are hover flies (Diptera: Syrphidae). The syrphid Episyrphus balteatus is a commercial bio-agent against aphids and has been established as a model organism for developmental studies and chemical ecology. The dorsal blastoderm of E. balteatus gives rise to two extraembryonic tissues (serosa and amnion), whereas in D. melanogaster, the dorsal blastoderm differentiates into a single extraembryonic epithelium (amnioserosa). Recent studies indicate that several BMP signaling components of D. melanogaster, including the BMP ligand Screw (Scw) and other extracellular regulators, evolved in the dipteran lineage through gene duplication and functional divergence. These findings raise the question of whether the complement of BMP signaling components changed with the origin of the amnioserosa.

Results: To search for BMP signaling components in E. balteatus, we generated and analyzed transcriptomes of freshly laid eggs (0-30 minutes) and late blastoderm to early germband extension stages (3-6 hours) using Roche/454 sequencing. We identified putative E. balteatus orthologues of 43% of all annotated D. melanogaster genes, including the genes of all BMP ligands and other BMP signaling components.

Conclusion: The diversification of several BMP signaling components in the dipteran linage of D. melanogaster preceded the origin of the amnioserosa.[Transcriptome sequence data from this study have been deposited at the NCBI Sequence Read Archive (SRP005289); individually assembled sequences have been deposited at GenBank (JN006969-JN006986).].

Figures

Figure 1
Figure 1
Overview of E. balteatus transcriptome assembly and annotation. (A) Number of sequences per 200-nucleotide-bin (y-axis) is shown as function of assembled sequence lengths (x-axis). Numbers of assembled contigs (dark grey) and singletons (light grey) are shown on a logarithmic scale (left scale), and the proportion of annotated E. balteatus sequences (red graph) are shown in percent (right scale). Note that sequences below 100 nt were not used for further analyses and were excluded from bin 0-200. (B) Gene ontology assignments of annotated E. balteatus genes, red bars indicate the proportion of annotated E. balteatus sequences in percent.
Figure 2
Figure 2
Coverage of previously identified E. balteatus developmental genes. (A) Eba-bcd (GenBank accession: HM044914), (B) Eba-cad (FJ387230), (C) Eba-nos (FJ387226), (D) Eba-tor (HM044920), (E) Eba-otd (FJ387225), (F) Eba-hb (FJ387229), (G) Eba-Kr (HM044918), (H) Eba-kni (HM044916), (I) Eba-gt (HM044915), (J) Eba-h (AY645032), (K) Eba-eve (AY645031), (L) Eba-zen (DQ323932), (M) Eba-kkb (HM067828), and (N) Eba-tll (HM044919). Coverage (i.e., number of reads) is shown as function of nucleotide position in cDNA (x-axis; ORF in grey). Coverage in the maternal cDNA pool (0-0.5 hrs) is labeled in red, coverage in the zygotic cDNA pool (3-6 hrs) is labeled in blue. Average coverage is indicated by dotted horizontal lines. Fold-changes in coverage levels from maternal to zygotic pool are given in green (increase) or red (decrease) numbers. A listing of coverage values detailing ORF and UTR is given in Additional file 2. Scale bars (top right of panel) are 500 nt.
Figure 3
Figure 3
Orthologies of BMP signaling components based on maximum likelihood gene trees using predicted amino acid sequences. (A) TGFß ligands (substitution model DCMut+i+g+g); (B) TGFβ type I and type II receptors (substitution model WAG+i+g+f); (C) SMAD family (substitution model LG+g+f); (D) Metalloproteases related to Tld and Tok (substitution model Dayhoff+g+f); (E) Kekkon family (substitution model LG+i+g+f); (F) Crossveinless family (substitution model Dayhoff+i+g+f); (G) DAN family (substitution model Dayhoff+i+g+f); scale bars indicate estimated changes/position. BeetleBase (T. castaneum) and GenBank accession numbers (all others): (A) Act (Activin-β; NM_143685), Tca Act (TC015806), Tca BMP10 (TC006506), Daw (dawdle; NM_078737), Tca Daw (TC04297), Dpp (decapentaplegic; NM_057963), Eba Dpp (JN006972), Tca Dpp (TC008466), Gbb (glass bottom boat; NM_057992), Eba Gbb (JN006973), Tca Gbb1 (TC014017), Tca Gbb2 (TC014018), Mav (maverick; NM_079887.2), Tca Mav (TC004299), Myo (myoglianin; NM_166786) Tca Myo (TC015805), Scw (screw; NM_080124.4), Eba Scw (JN006978); (B) Babo (baboon; NM_057652), Eba Babo (JN006969), Tca Babo (TC003240), Put (punt; NM_169591), Eba Put (JN006976), Tca Put (TC011357), Sax (saxophone; NM_078928), Eba Sax (JN006977), Tca Sax (TC015984), Tkv (thickveins; NM_175975), Eba Tkv (JN006980), Tca Tkv (TC006474), Wit (wishful thinking; NM_079953), Eba Wit (JN006986), Tca Wit (TC009314); (C) Mad (mothers against dpp; NM_057669), Eba Mad (JN006974), Tca Mad (TC014924), Med (Medea; NM_079871), Eba Med (JN006975), Tca Med (TC010848), Smox (smad on X; NM_078524), Eba Smox (JN006979), Tca Smox (TC010162); (D) Tld (tolloid; NM_079763), Eba Tld (JN006985), Tok (tolkin; NM_057531), Tca Tok (TC011197); (E) Kek1 (kekkon-1; NM_078835), Kek2 (NM_078827), Tca Kek2 (TC007053), Tca Kek2' (TC008448), Eba Kek2 (JN006983), Kek3 (NM_078851), Tca Kek3 (TC007226), Kek4 (NM_135771), Tca Kek4 (TC007110), Tca Kek4' (TC008070), Kek5 (NM_133154), Eba Kek5 (JN006984); (F) Cv (crossveinless; NM_080525), Eba Cv (JN006982), Eba Cv-like (JN006970), Srw (shrew; NM_139629), Tsg (twisted gastrulation; NM_078580), Eba Tsg (JN006981), Tca Tsg (TC003620); (G) Mmu Cerberus (Mus musculus; NM_009887), Mmu Dante (NM_201227), Mmu Gremlin (NM_011824), Tca Gremlin (TC007044), Eba DAN (JN006971), Mmu DAN (NM_008675.2), Tca DAN (TC014861).
Figure 4
Figure 4
Coverage of maternal E. balteatus genes in comparison with transcriptome data from 0-2 hours old D. melanogaster embryos. (A) Scatter plot of orthologous genes for which we determined expression levels in E. balteatus (using 454 data from 0-0.5 hrs old embryos) and D. melanogaster (using RNAseq data from 0-2 hrs old embryos) on a log2 scale. The 14 previously identified E. balteatus genes are circled in red (if their D. melanogaster orthologues are known to have a maternal effect) or in blue (if their D. melanogaster orthologues are thought to lack a maternal effect). Asterisks demark genes that have been manually annotated. Genes not detected at the indicated developmental stage in one of the two species are plotted outside the scale (grey area). (B,C) Same as in (A) but limited to 15 identified genes encoding BMP signaling components (B) or 89 genes of gene specific transcription factors (C, list of genes based on flyTF, see Material and Methods). Genes that might lack significant maternal expression in one of the two species are indicated. Our analysis suggests that the zygotic D. melanogaster genes crossveinless-2, kekkon-5, doublesex, abdominal-A, vrille and Optix are expressed maternally in E. balteatus, while the maternal D. melanogaster transcription factor BEAF-32 may lack significant maternal expression in E. balteatus.
Figure 5
Figure 5
Evolution of BMP signaling components and amnioserosa origin.

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