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Department of Biological and Medical Sciences
Faculty of Health and Life Sciences
The Sox family of transcription factors regulate many processes during metazoan development, including stem cell maintenance and nervous system specification. Characterising the repertoires and roles of these genes can therefore provide important insights into animal evolution and development. We further characterised the Sox repertoires of several arachnid species with and without an ancestral whole genome duplication (WGD), and compared their expression between the spider Parasteatoda tepidariorum and the harvestman Phalangium opilio. We also found that most Sox families have been retained as ohnologs after WGD and evidence for potential subfunctionalisation and/or neofunctionalization events. Our results also suggest that Sox21b-1 likely regulated segmentation ancestrally in arachnids, playing a similar role to the closely related SoxB gene, Dichaete, in insects. We previously showed that Sox21b-1 is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in P. tepidariorum. We studied the expression and function of Sox21b-1 further in this spider and found that while this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagmata reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures.
Background: The Sox family of transcription factors is an important part of the genetic ‘toolbox’ of all metazoans examined to date and is known to play important developmental roles in vertebrates and insects. However, outside the commonly studied Drosophila model little is known about the repertoire of Sox family transcription factors in other arthropod species. Here we characterise the Sox family in two chelicerate species, the spiders Parasteatoda tepidariorum and Stegodyphus mimosarum, which have experienced a whole genome duplication (WGD) in their evolutionary history.Results: We find that virtually all of the duplicate Sox genes have been retained in these spiders after the WGD. Analysis of the expression of Sox genes in P. tepidariorum embryos suggests that it is likely that some of these genes have neofunctionalised after duplication. Our expression analysis also strengthens the view that an orthologue of vertebrate Group B1 genes, SoxNeuro, is implicated in the earliest events of CNS specification in both vertebrates and invertebrates. In addition, a gene in the Dichaete/Sox21b class is dynamically expressed in the spider segment addition zone, suggestive of an ancient regulatory mechanism controlling arthropod segmentation as recently suggested for flies and beetles. Together with the recent analysis of Sox gene expression in the embryos of other arthropods, our findings support the idea of conserved functions for some of these genes, including potential role for SoxC and SoxD genes in CNS development and SoxF in limb development.Conclusions: Our study provides a new chelicerate perspective to understanding the evolution and function ofSox genes and how the retention of duplicates of such important tool-box genes after WGD has contributed to different aspects of spider embryogenesis. Future characterisation of the function of these genes in spiders will help us to better understand the evolution of the regulation of important developmental processes in arthropods and other metazoans including neurogenesis and segmentation.
Sox genes encode a set of highly conserved transcription factors that regulate many developmental processes. In insects, the SoxB gene Dichaete is the only Sox gene known to be involved in segmentation. To determine if similar mechanisms are used in other arthropods, we investigated the role of Sox genes during segmentation in the spider Parasteatoda tepidariorum. While Dichaete does not appear to be involved in spider segmentation, we found that the closely related Sox21b-1 gene acts as a gap gene during formation of anterior segments and is also part of the segmentation clock for development of the segment addition zone and sequential addition of opisthosomal segments. Thus, we have found that two different mechanisms of segmentation in a non-mandibulate arthropod are regulated by a SoxB gene. Our work provides new insights into the function of an important and conserved gene family, and the evolution of the regulation of segmentation in arthropods.
Wnt signaling regulates many important processes during metazoan development. It has been shown that Wnt ligands represent an ancient and diverse family of proteins that likely function in complex signaling landscapes to induce target cells via receptors including those of the Frizzled (Fz) family. The four subfamilies of Fz receptors also evolved early in metazoan evolution. To date, Fz receptors have been characterised mainly in mammals, the nematode Caenorhabditis elegans and insects such as Drosophila melanogaster. To compare these findings with other metazoans, we explored the repertoire of fz genes in three panarthropod species: Parasteatoda tepidariorum, Glomeris marginata and Euperipatoides kanangrensis, representing the Chelicerata, Myriapoda and Onychophora respectively. We found that these three diverse panarthropods each have four fz genes, with representatives of all four metazoan fz subfamilies found in Glomeris and Euperipatoides, while Parasteatoda does not have a fz3 gene, but has two fz4 paralogues. Furthermore we characterized the expression patterns of all the fz genes among these animals. Our results exemplify the evolutionary diversity of Fz receptors and reveals conserved and divergent aspects of their protein sequences and expression patterns among panarthropods; thus providing new insights into the evolution of Wnt signaling more generally.
Despite considerable differences in morphology and complexity of body plans among animals, a great part of the gene set is shared among Bilateria and their basally branching sister group, the Cnidaria. This suggests that the common ancestor of eumetazoans already had a highly complex gene repertoire. At present it is therefore unclear how morphological diversification is encoded in the genome. Here we address the possibility that differences in gene regulation could contribute to the large morphological divergence between cnidarians and bilaterians. To this end, we generated the first genome-wide map of gene regulatory elements in a nonbilaterian animal, the sea anemone Nematostella vectensis. Using chromatin immunoprecipitation followed by deep sequencing of five chromatin modifications and a transcriptional cofactor, we identified over 5000 enhancers in the Nematostella genome and could validate 75% of the tested enhancers in vivo. We found that in Nematostella, but not in yeast, enhancers are characterized by the same combination of histonemodifications as in bilaterians, and these enhancers preferentially target developmental regulatory genes. Surprisingly, the distribution and abundance of gene regulatory elements relative to these genes are shared between Nematostella and bilaterian model organisms. Our results suggest that complex gene regulation originated at least 600 million yr ago, predating the common ancestor of eumetazoans.