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The brain regulatory program predates central nervous system evolution

ABSTRACT: Understanding how brains evolved is critical to determine the origin(s) of centralized nervous systems. Brains are patterned along their anteroposterior axis by stripes of gene expression that appear to be conserved, suggesting brains are homologous. However, the striped expression is also part of the deeply conserved anteroposterior axial program. An emerging hypothesis is that similarities in brain patterning are convergent, arising through the repeated co-option of axial programs. To resolve whether shared brain neurogenic programs likely reflect convergence or homology, we investigated the evolution of axial programs in neurogenesis. We show that the bilaterian anteroposterior program patterns the nerve net of the cnidarian Nematostella along the oral-aboral axis arguing that anteroposterior programs regionalized developing nervous systems in the cnidarian-bilaterian common ancestor prior to the emergence of brains. This finding rejects shared patterning as sufficient evidence to support brain homology and provides functional support for the plausibility that axial programs could be co-opted if nervous systems centralized in multiple lineages

ORGANISM(S): Nematostella vectensis

PROVIDER: GSE218419 | GEO | 2022/11/22

REPOSITORIES: GEO

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Project description:The process of calcium carbonate biomineralization has arisen multiple times during metazoan evolution. In the phylum Cnidaria, biomineralization has mostly been studied in the subclass Hexacorallia (i.e. stony corals) in comparison to the subclass Octocorallia (i.e. red corals); the two diverged approximately 600 million years ago. The precious Mediterranean red coral, Corallium rubrum, is an octocorallian species, which produces two distinct high-magnesium calcite biominerals, the axial skeleton and the sclerites. In order to gain insight into the red coral biomineralization process and cnidarian biomineralization evolution, we studied the protein repertoire forming the organic matrix (OM) of its two biominerals. We combined High-Resolution Mass Spectrometry and transcriptome analysis to study the OM composition of the axial skeleton and the sclerites. We identified a total of 102 OM proteins, 52 are shared between the two red coral biominerals with scleritin being the most abundant protein in each fraction. Contrary to reef building corals, the red coral is collagen-rich (10 collagen-like proteins). Agrin-like glycoproteins and proteins with sugar-binding domains are also predominant. Twenty-seven and 23 proteins were uniquely assigned to the axial skeleton and the sclerites, respectively. Their inferred regulatory function suggests that the difference between the two biominerals rather relies on the modeling of the matrix network than on specific structural components. At least one OM component appears to have been horizontally transferred from prokaryotes early during Octocorallia evolution. Our results support the view that calcification of the red coral axial skeleton likely represents a secondary calcification of an ancestral gorgonian horny axis. In addition, the comparison with stony coral skeletomes highlighted the low proportion of similar proteins between the biomineral OMs of hexacorallian and octocorallian corals, suggesting an independent acquisition of calcification in anthozoans.

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The brain regulatory program predates central nervous system evolution

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