Embryonic expression patterns and phylogenetic analysis of panarthropod sox genes: insight into nervous system development, segmentation and gonadogenesis

Abstract

BackgroundSox (Sry-related high-mobility-group box) genes represent important factors in animal development. Relatively little, however, is known about the embryonic expression patterns and thus possible function(s) of Sox genes during ontogenesis in panarthropods (Arthropoda+Tardigrada+Onychophora). To date, studies have been restricted exclusively to higher insects, including the model system Drosophila melanogaster, with no comprehensive data available for any other arthropod group, or any tardigrade or onychophoran.ResultsThis study provides a phylogenetic analysis of panarthropod Sox genes and presents the first comprehensive analysis of embryonic expression patterns in the flour beetle Tribolium castaneum (Hexapoda), the pill millipede Glomeris marginata (Myriapoda), and the velvet worm, Euperipatoides kanangrensis (Onychophora). 24 Sox genes were identified and investigated: 7 in Euperipatoides, 8 in Glomeris, and 9 in Tribolium. Each species possesses at least one ortholog of each of the five expected Sox gene families, B, C, D, E, and F, many of which are differentially expressed during ontogenesis.ConclusionSox gene expression (and potentially function) is highly conserved in arthropods and their closest relatives, the onychophorans. Sox B, C and D class genes appear to be crucial for nervous system development, while the Sox B genes Dichaete (D) and Sox21b likely play an additional conserved role in panarthropod segmentation. The Sox B gene Sox21a likely has a conserved function in foregut and Malpighian tubule development, at least in Hexapoda. The data further suggest that Sox D and E genes are involved in mesoderm differentiation, and that Sox E genes are involved in gonadal development.The new data expand our knowledge about the expression and implied function of Sox genes to Mandibulata (Myriapoda+Pancrustacea) and Panarthropoda (Arthropoda+Onychophora).Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1196-z) contains supplementary material, which is available to authorized users.

Duplication and divergence of Sox genes in spiders

“…In T. castaneum, Sox21b has similar expression to D, early in the SAZ and then in the developing CNS. In E. kanangrensis and G. marginata, there is no early Sox21b expression [45], however in these species, D is expressed during segmentation and then later in the CNS. This suggests that the role of D in segmentation in D. melanogaster and T.…”

“…While SoxD has been reported to be ubiquitously expressed in A. mellifera embryos, it is also expressed in the mushroom bodies of the adult brain [13]. Embryonic brain expression of SoxD orthologues in beetles, myriapods and velvet worms [45], as well as a known role for SoxD genes in aspects of vertebrate neurogenesis [54,57] again suggests conserved roles for SoxD during metazoan evolution.…”

“…However, even with these different modes of neurogenic differentiation, the expression of SoxN orthologues suggests this gene performs the same function. Indeed, the recent study by [45], of T. castaneum, E. kanangrensis and G. marginata also shows that the SoxN orthologues in these species have widespread and early neuroectodermal expression. Taken together these data clearly support the view that throughout the most anterior part of the germ band, which corresponds to the presumptive neuroectoderm in the future head and prosomal segments ( Figure 6C).…”

“…In common with many other gene families in spiders [41], the Sox genes are mostly represented by two or more copies in each group ( Figure 2). In other arthropods examined to date, as well as the onochophoran Euperipatoides kanangrensis [45], there is usually only a single copy of each gene, although [45] recently reported two Group E genes in the millipede G. marginata. In the case of spider Groups D and E, the duplications clearly predate the divergence of the two spider species we analysed since the duplicates group together in the phylogenetic analysis and show extensive homology across the length of the coding sequence ( Figure 1).…”

“…In A. mellifera, late expression of the SoxC gene was observed in the embryonic cephalic lobes and in the mushroom bodies [13]. The expression of SoxC orthologues in the embryonic CNS of other invertebrates [45] suggests that this class of Sox gene may play a conserved role in aspects of neuronal differentiation, which has been lost in D.…”