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Open Access Highly Accessed Research article

Insights into the evolution of the snail superfamily from metazoan wide molecular phylogenies and expression data in annelids

Pierre Kerner123, Johanne Hung2, Julien Béhague12, Martine Le Gouar2, Guillaume Balavoine12 and Michel Vervoort123*

Author Affiliations

1 Programme Development and Neurobiology, Institut Jacques Monod, UMR 7592 CNRS/Université Paris Diderot – Paris 7, 15 rue Hélène Brion, 75205 Paris Cedex 13, France

2 Evolution et Développement des Métazoaires, Centre de Génétique Moléculaire- FRE 3144 CNRS, 1, av. de la terrasse, 91198 Gif-sur-Yvette, France

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

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BMC Evolutionary Biology 2009, 9:94  doi:10.1186/1471-2148-9-94

Published: 9 May 2009

Abstract

Background

An important issue concerning the evolution of duplicated genes is to understand why paralogous genes are retained in a genome even though the most likely fate for a redundant duplicated gene is nonfunctionalization and thereby its elimination. Here we study a complex superfamily generated by gene duplications, the snail related genes that play key roles during animal development. We investigate the evolutionary history of these genes by genomic, phylogenetic, and expression data studies.

Results

We systematically retrieved the full complement of snail related genes in several sequenced genomes. Through phylogenetic analysis, we found that the snail superfamily is composed of three ancestral families, snail, scratchA and scratchB. Analyses of the organization of the encoded proteins point out specific molecular signatures, indicative of functional specificities for Snail, ScratchA and ScratchB proteins. We also report the presence of two snail genes in the annelid Platynereis dumerilii, which have distinct expression patterns in the developing mesoderm, nervous system, and foregut. The combined expression of these two genes is identical to that of two independently duplicated snail genes in another annelid, Capitella spI, but different aspects of the expression patterns are differentially shared among paralogs of Platynereis and Capitella.

Conclusion

Our study indicates that the snail and scratchB families have expanded through multiple independent gene duplications in the different bilaterian lineages, and highlights potential functional diversifications of Snail and ScratchB proteins following duplications, as, in several instances, paralogous proteins in a given species show different domain organizations. Comparisons of the expression pattern domains of the two Platynereis and Capitella snail paralogs provide evidence for independent subfunctionalization events which have occurred in these two species. We propose that the snail related genes may be especially prone to subfunctionalization, and this would explain why the snail superfamily underwent so many independent duplications leading to maintenance of functional paralogs.