BackgroundMolecular and genetic analyses conducted in model organisms such as Drosophila and vertebrates, have provided a wealth of information about how networks of transcription factors control the proper development of these species. Much less is known, however, about the evolutionary origin of these elaborated networks and their large-scale evolution. Here we report the first evolutionary analysis of a whole superfamily of transcription factors, the basic helix-loop-helix (bHLH) proteins, at the scale of the whole metazoan kingdom.ResultsWe identified in silico the putative full complement of bHLH genes in the sequenced genomes of 12 different species representative of the main metazoan lineages, including three non-bilaterian metazoans, the cnidarians Nematostella vectensis and Hydra magnipapillata and the demosponge Amphimedon queenslandica. We have performed extensive phylogenetic analyses of the 695 identified bHLHs, which has allowed us to allocate most of these bHLHs to defined evolutionary conserved groups of orthology.ConclusionThree main features in the history of the bHLH gene superfamily can be inferred from these analyses: (i) an initial diversification of the bHLHs has occurred in the pre-Cambrian, prior to metazoan cladogenesis; (ii) a second expansion of the bHLH superfamily occurred early in metazoan evolution before bilaterians and cnidarians diverged; and (iii) the bHLH complement during the evolution of the bilaterians has been remarkably stable. We suggest that these features may be extended to other developmental gene families and reflect a general trend in the evolution of the developmental gene repertoires of metazoans.
The nerve cell is a eumetazoan (cnidarians and bilaterians) synapomorphy [1]; this cell type is absent in sponges, a more ancient phyletic lineage. Here, we demonstrate that despite lacking neurons, the sponge Amphimedon queenslandica expresses the Notch-Delta signaling system and a proneural basic helix loop helix (bHLH) gene in a manner that resembles the conserved molecular mechanisms of primary neurogenesis in bilaterians. During Amphimedon development, a field of subepithelial cells expresses the Notch receptor, its ligand Delta, and a sponge bHLH gene, AmqbHLH1. Cells that migrate out of this field express AmqDelta1 and give rise to putative sensory cells that populate the larval epithelium. Phylogenetic analysis suggests that AmqbHLH1 is descendent from a single ancestral bHLH gene that later duplicated to produce the atonal/neurogenin-related bHLH gene families, which include most bilaterian proneural genes [2]. By way of functional studies in Xenopus and Drosophila, we demonstrate that AmqbHLH1 has a strong proneural activity in both species with properties displayed by both neurogenin and atonal genes. From these results, we infer that the bilaterian neurogenic circuit, comprising proneural atonal-related bHLH genes coupled with Notch-Delta signaling, was functional in the very first metazoans and was used to generate an ancient sensory cell type.
BackgroundFunctional studies in model organisms, such as vertebrates and Drosophila, have shown that basic Helix-loop-Helix (bHLH) proteins have important roles in different steps of neurogenesis, from the acquisition of neural fate to the differentiation into specific neural cell types. However, these studies highlighted many differences in the expression and function of orthologous bHLH proteins during neural development between vertebrates and Drosophila. To understand how the functions of neural bHLH genes have evolved among bilaterians, we have performed a detailed study of bHLH genes during nervous system development in the polychaete annelid, Platynereis dumerilii, an organism which is evolutionary distant from both Drosophila and vertebrates.ResultsWe have studied Platynereis orthologs of the most important vertebrate neural bHLH genes, i.e. achaete-scute, neurogenin, atonal, olig, and NeuroD genes, the latter two being genes absent of the Drosophila genome. We observed that all these genes have specific expression patterns during nervous system formation in Platynereis. Our data suggest that in Platynereis, like in vertebrates but unlike Drosophila, (i) neurogenin is the main proneural gene for the formation of the trunk central nervous system, (ii) achaete-scute and olig genes are involved in neural subtype specification in the central nervous system, in particular in the specification of the serotonergic phenotype. In addition, we found that the Platynereis NeuroD gene has a broad and early neuroectodermal expression, which is completely different from the neuronal expression of vertebrate NeuroD genes.ConclusionOur analysis suggests that the Platynereis bHLH genes have both proneural and neuronal specification functions, in a way more akin to the vertebrate situation than to that of Drosophila. We conclude that these features are ancestral to bilaterians and have been conserved in the vertebrates and annelids lineages, but have diverged in the evolutionary lineage leading to Drosophila.
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