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Evodevo
2018 Jan 22;9:5. doi: 10.1186/s13227-018-0094-1.
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SoxB2 in sea urchin development: implications in neurogenesis, ciliogenesis and skeletal patterning.
Anishchenko E
,
Arnone MI
,
D'Aniello S
.
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Background: Current studies in evolutionary developmental biology are focused on the reconstruction of gene regulatory networks in target animal species. From decades, the scientific interest on genetic mechanisms orchestrating embryos development has been increasing in consequence to the fact that common features shared by evolutionarily distant phyla are being clarified. In 2011, a study across eumetazoan species showed for the first time the existence of a highly conserved non-coding element controlling the SoxB2 gene, which is involved in the early specification of the nervous system. This discovery raised several questions about SoxB2 function and regulation in deuterostomes from an evolutionary point of view.
Results: Due to the relevant phylogenetic position within deuterostomes, the sea urchin Strongylocentrotus purpuratus represents an advantageous animal model in the field of evolutionary developmental biology. Herein, we show a comprehensive study of SoxB2 functions in sea urchins, in particular its expression pattern in a wide range of developmental stages, and its co-localization with other neurogenic markers, as SoxB1, SoxC and Elav. Moreover, this work provides a detailed description of the phenotype of sea urchin SoxB2 knocked-down embryos, confirming its key function in neurogenesis and revealing, for the first time, its additional roles in oral and aboral ectoderm cilia and skeletal rod morphology.
Conclusions: We concluded that SoxB2 in sea urchins has a neurogenic function; however, this gene could have multiple roles in sea urchin embryogenesis, expanding its expression in non-neurogenic cells. We showed that SoxB2 is functionally conserved among deuterostomes and suggested that in S. purpuratus this gene acquired additional functions, being involved in ciliogenesis and skeletal patterning.
Fig. 1. SoxB1 and SoxB2 genes expression in S. purpuratus during first week of development. Colorimetric (a–a′, b–b′, c–c′, d–d′, e–e′, f–f′, g–g′, h–h′, i–i′) and double fluorescent (a″, b″, c″, d″, e″, f″, g″, h″) SoxB1 and SoxB2 in situ hybridizations in embryos at 24–144 hpf. Fluorescent in situ hybridizations: SoxB1 is green and SoxB2 is red. The nuclear marker DAPI is shown in blue
Fig. 2. SoxC, Elav and SoxB2 genes expression in S. purpuratus at 48 hpf. FISH in sea urchin embryos: SoxC is represented in green and SoxB2 in red. Embryos are shown from lateral (a) and apical (b) views. Regions of co-expression are shown in yellow. c FISH in sea urchin embryos; Elav is green and SoxB2 is red. Embryos are shown from the oral view. d FISH in sea urchin embryos; Elav is green and SoxC is red. Embryos are shown from lateral view. DAPI is shown in blue
Fig. 3. SoxB2 MO-1 and MO-2 injection effect on skeleton formation in 48 and 72 hpf S. purpuratus embryos. Oral (a, b, c, d, e, f), lateral (a′, b′, c′, d′, e′, f′) and vegetal (a″, b″, c″, d″, e″, f″) view of embryos at 48 hpf (a–c″) and 72 hpf (d–f″). Uninjected control embryos (a–a″ and d–d″) were compared with morphants, injected with SoxB2 MO-1 (b–b″, e–e″) and SoxB2 MO-2 (c–c″, f–f″)
Fig. 4. SoxB2 MO-1 injection effect on nervous system formation and ciliogenesis in 72 hpf S. purpuratus embryos. Oral (a, b, c, d), lateral (a′, b′, c′, d′) and vegetal (a″, b″, c″, d″) views of embryos at 72 hpf. Uninjected control embryos (a–a″ and c–c″) were compared with morphants, injected with SoxB2 MO-1 (b–b″, d–d″). Serotonin is shown in red, DAPI in blue, Synaptotagmin B (1e11) in a–b″ and AcTubulin in c–d″ are shown in green
Fig. 5. Expression levels of developmental genes in S. purpuratus SoxB2 morphants. Ratio of gene expression levels comparing SoxB2 morphants and uninjected control embryos at 72 hpf (a) and 48 hpf (d) by qPCR. Significant alterations in gene expression are below and above the gray bar (value ± 0.5). The histograms are represented in a Log10 scale for the y-axis. Decreasing levels of SoxB1 (green) and Onecut (red) expression in SoxB2 morphants was shown using FISH (c). Morphants were compared with uninjected control sea urchin embryos at 48 hpf, the images were taken from the apical view (b)
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