Global analysis of dorsoventral patterning in the wasp Nasonia reveals extensive incorporation of novelty in a regulatory network

Abstract

BackgroundGene regulatory networks (GRNs) underlie developmental patterning and morphogenetic processes, and changes in the interactions within the underlying GRNs are a major driver of evolutionary processes. In order to make meaningful comparisons that can provide significant insights into the evolution of regulatory networks, homologous networks from multiple taxa must be deeply characterized. One of the most thoroughly characterized GRNs is the dorsoventral (DV) patterning system of the Drosophila melanogaster embryo. We have developed the wasp Nasonia as a comparative DV patterning model because it has shown the convergent evolution of a mode of early embryonic patterning very similar to that of the fly, and it is of interest to know whether the similarity at the gross level also extends to the molecular level.ResultsWe used RNAi to dorsalize and ventralize Nasonia embryos, RNAseq to quantify transcriptome-wide expression levels, and differential expression analysis to identify genes whose expression levels change in either RNAi case. This led to the identification of >100 genes differentially expressed and regulated along the DV axis. Only a handful of these genes are shared DV components in both fly and wasp. Many of those unique to Nasonia are cytoskeletal and adhesion molecules, which may be related to the divergent cell and tissue behavior observed at gastrulation. In addition, many transcription factors and signaling components are only DV regulated in Nasonia, likely reflecting the divergent upstream patterning mechanisms involved in producing the conserved pattern of cell fates observed at gastrulation. Finally, several genes that lack Drosophila orthologs show robust and distinct expression patterns. These include genes with vertebrate homologs that have been lost in the fly lineage, genes that are found only among Hymenoptera, and several genes that entered the Nasonia genome through lateral transfer from endosymbiotic bacteria.ConclusionsAltogether, our results provide insights into how GRNs respond to new functional demands and how they can incorporate novel components.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0285-y) contains supplementary material, which is available to authorized users.

Ploidy has little effect on timing early embryonic events in the haplo‐diploid wasp Nasonia

“…The conspicuous absence of Nv‐tribbles in this region is interesting, as Drosophila tribbles is upregulated in the mesoderm, and plays an important role in delaying mitosis in the mesoderm during gastrulation which is crucial for its proper morphogenesis (Großhans & Wieschaus, ). This observation fits an emerging pattern, where several genes required for Drosophila mesoderm morphogenesis are restricted to the ventral neuroectoderm in Nasonia (Pers et al, ). Knockdown of Nv‐tribbles was only effective against the maternal contributions (Supporting Information Figure ), while zygotic levels increased to be close to normal (not shown).…”

Ankyrin domain encoding genes resulting from an ancient horizontal transfer are functionally integrated into developmental gene regulatory networks in the waspNasonia

“…In fact, there is evidence that these genes entered the genome of the ancestor of Nasonia through at least one horizontal gene transfer (HGT) event, followed by several waves of duplication and divergence. We have previously shown that these ankyrin domain encoding genes are expressed in specific patterns along the DV axis [15], and here we demonstrate that they also are functionally incorporated into the DV patterning GRN, and their loss leads to variable disruptions to patterning. Through examination of another wasp, Melittobia digitata, we also show that some of the functional incorporation is ancient within the Superfamily, while there is also strong evidence of recent gains and/or losses of function in the Nasonia and Melittobia lineages.…”

“…Having split from Drosophila melanogaster over 300 MYA [11], the two have converged on a similar mode of embryogenesis [12], and share a nearly identical expression of tissue-specific marker genes just prior to gastrulation [13]. We have previously shown that most genes differentially expressed along the DV axis of the Nasonia embryo are not conserved components of the Drosophila DV GRN, making the comparison between the fly and wasp DV GRNs an ideal system for understanding how GRNs evolve while producing similar patterning results [14, 15].…”

Transcriptomic and functional analysis of the oosome, a unique form of germ plasm in the waspNasonia vitripennis

“…At the blastoderm stage, Nv-tdrd7 is moderately enriched in the pole cells and is zygotically expressed in a ventral-posterior patch (Fig. 3B2), which was detected in our earlier analysis of dorsal-ventral patterning [48]. After gastrulation, Nv-tdrd7 is strongly upregulated in a group of cells that are near to where the germ cells migrate, but it is not clear if they are germ cells (Fig.…”