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Evolution of the insect Sox genes.

ABSTRACT: BACKGROUND: The Sox gene family of transcriptional regulators have essential roles during development and have been extensively studied in vertebrates. The mouse, human and fugu genomes contain at least 20 Sox genes, which are subdivided into groups based on sequence similarity of the highly conserved HMG domain. In the well-studied insect Drosophila melanogaster, eight Sox genes have been identified and are involved in processes such as neurogenesis, dorsal-ventral patterning and segmentation. RESULTS: We examined the available genome sequences of Apis mellifera, Nasonia vitripennis, Tribolium castaneum, Anopheles gambiae and identified Sox family members which were classified by phylogenetics using the HMG domains. Using in situ hybridisation we determined the expression patterns of eight honeybee Sox genes in honeybee embryo, adult brain and queen ovary. AmSoxB group genes were expressed in the nervous system, brain and Malphigian tubules. The restricted localization of AmSox21b and AmSoxB1 mRNAs within the oocyte, suggested a role in, or that they are regulated by, dorsal-ventral patterning. AmSoxC, D and F were expressed ubiquitously in late embryos and in the follicle cells of the queen ovary. Expression of AmSoxF and two AmSoxE genes was detected in the drone testis. CONCLUSION: Insect genomes contain between eight and nine Sox genes, with at least four members belonging to Sox group B and other Sox subgroups each being represented by a single Sox gene. Hymenopteran insects have an additional SoxE gene, which may have arisen by gene duplication. Expression analyses of honeybee SoxB genes implies that this group of genes may be able to rapidly evolve new functions and expression domains, while the combined expression pattern of all the SoxB genes is maintained.

SUBMITTER: Wilson MJ

PROVIDER: S-EPMC2386450 | biostudies-other | 2008

REPOSITORIES: biostudies-other

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Evolution of the insect Sox genes.

Wilson Megan J MJ Dearden Peter K PK

BMC evolutionary biology 20080426

<h4>Background</h4>The Sox gene family of transcriptional regulators have essential roles during development and have been extensively studied in vertebrates. The mouse, human and fugu genomes contain at least 20 Sox genes, which are subdivided into groups based on sequence similarity of the highly conserved HMG domain. In the well-studied insect Drosophila melanogaster, eight Sox genes have been identified and are involved in processes such as neurogenesis, dorsal-ventral patterning and segment ...[more]

PMID: 18439299

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Project description: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 a 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 of Sox 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.

Project description:BACKGROUND: Sox domain containing genes are important metazoan transcriptional regulators implicated in a wide rage of developmental processes. The vertebrate B subgroup contains the Sox1, Sox2 and Sox3 genes that have early functions in neural development. Previous studies show that Drosophila Group B genes have been functionally conserved since they play essential roles in early neural specification and mutations in the Drosophila Dichaete and SoxN genes can be rescued with mammalian Sox genes. Despite their importance, the extent and organisation of the Group B family in Drosophila has not been fully characterised, an important step in using Drosophila to examine conserved aspects of Group B Sox gene function. RESULTS: We have used the directed cDNA sequencing along with the output from the publicly-available genome sequencing projects to examine the structure of Group B Sox domain genes in Drosophila melanogaster, Drosophila pseudoobscura, Anopheles gambiae and Apis mellifora. All of the insect genomes contain four genes encoding Group B proteins, two of which are intronless, as is the case with vertebrate group B genes. As has been previously reported and unusually for Group B genes, two of the insect group B genes, Sox21a and Sox21b, contain introns within their DNA-binding domains. We find that the highly unusual multi-exon structure of the Sox21b gene is common to the insects. In addition, we find that three of the group B Sox genes are organised in a linked cluster in the insect genomes. By in situ hybridisation we show that the pattern of expression of each of the four group B genes during embryogenesis is conserved between D. melanogaster and D. pseudoobscura. CONCLUSION: The DNA-binding domain sequences and genomic organisation of the group B genes have been conserved over 300 My of evolution since the last common ancestor of the Hymenoptera and the Diptera. Our analysis suggests insects have two Group B1 genes, SoxN and Dichaete, and two Group B2 genes. The genomic organisation of Dichaete and another two Group B genes in a cluster, suggests they may be under concerted regulatory control. Our analysis suggests a simple model for the evolution of group B Sox genes in insects that differs from the proposed evolution of vertebrate Group B genes.

Project description:Cephalopods provide an unprecedented opportunity for comparative studies of the developmental genetics of organ systems that are convergent with analogous vertebrate structures. The Sox-family of transcription factors is an important class of DNA-binding proteins that are known to be involved in many aspects of differentiation, but have been largely unstudied in lophotrochozoan systems. Using a degenerate primer strategy we have isolated coding sequence for three members of the Sox family of transcription factors from a cephalopod mollusk, the European cuttlefish Sepia officinalis: Sof-SoxE, Sof-SoxB1, and Sof-SoxB2. Analyses of their expression patterns during organogenesis reveals distinct spatial and temporal expression domains. Sof-SoxB1 shows early ectodermal expression throughout the developing epithelium, which is gradually restricted to presumptive sensory epithelia. Expression within the nervous system appears by mid-embryogenesis. Sof-SoxB2 expression is similar to Sof-SoxB1 within the developing epithelia in early embryogenesis, however appears in largely non-overlapping expression domains within the central nervous system and is not expressed in the maturing sensory epithelium. In contrast, Sof-SoxE is expressed throughout the presumptive mesodermal territories at the onset of organogenesis. As development proceeds, Sof-SoxE expression is elevated throughout the developing peripheral circulatory system. This expression disappears as the circulatory system matures, but expression is maintained within undifferentiated connective tissues throughout the animal, and appears within the nervous system near the end of embryogenesis. SoxB proteins are widely known for their role in neural specification in numerous phylogenetic lineages. Our data suggests that Sof-SoxB genes play similar roles in cephalopods. In contrast, Sof-SoxE appears to be involved in the early stages of vasculogenesis of the cephalopod closed circulatory system, a novel role for a member of this gene family.

Dataset Information

Evolution of the insect Sox genes.

Publications

Evolution of the insect Sox genes.

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