Research article

atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes

Elena Simionato¹ , Pierre Kerner¹ , Nicolas Dray¹ , Martine Le Gouar¹ , Valérie Ledent² , Detlev Arendt³ and Michel Vervoort^1,4

¹Evolution et Développement des métazoaires, Centre de Génétique Moléculaire-UPR 2167 CNRS, 1, av. de la terrasse, 91198 Gif-sur-Yvette, France

²Belgian EMBnet Node – Laboratoire de Bioinformatique, Université Libre de Bruxelles, Institut de Biologie et de Médecine Moléculaires, Rue des Professeurs Jeener et Brachet 12, B-6041 Gosselies, Belgium

³Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany

⁴UFR Sciences du Vivant, Université Paris Diderot – Paris 7, 5, rue Marie-Andrée Lagroua Weill-Hallé, 75205 Paris Cedex 13, France

author email corresponding author email

BMC Evolutionary Biology 2008, 8:170doi:10.1186/1471-2148-8-170

Published:	9 June 2008

Abstract

Background

Functional 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.

Results

We 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.

Conclusion

Our 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.