Abstract
BackgroundAn 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.ResultsWe 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.ConclusionOur 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.
Highlights
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
Carboxy-terminal Binding Protein (CtBP) domains contain the PXD/LSX motif required for the recruitment of the co-repressor CtBP by Snail proteins, an important event for the function of these proteins as transcriptional repressors (Figure 3B) [48,49]. We found this domain to be present only in Snail proteins, but neither in ScratchA nor ScratchB proteins (Figure 1). In both vertebrates and arthropods, we often found a CtBP domain in the N-terminal part of the protein close to the SNAG domain and we suggest that this may represent the ancestral situation for bilaterian Snail proteins
We suggest that the different expressions of the paralogs in both Platynereis and Capitella are due to subfunctionalization, a process by which ancestral genetic functions are shared out between paralogs, following gene duplication, and which is believed to be important for the maintenance of paralogs over long evolutionary times (e.g. [52,53])
Summary
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. System (CNS and PNS) in which snail acts in both neural precursors, such as Neuroblasts (NBs) and Ganglion Mother Cells (GMCs), and postmitotic neurons [26,32,33] In several of these tissues, snail has redundant roles with its paralogs, for example with escargot in the wing and haltere discs [31] and with both escargot and worniu in the CNS and PNS [26,32,33]. In agreement with their involvement in the formation of very diverse structures, Drosophila snail/escargot/worniu genes function in several cellular processes, such as the control of cell shape changes, cell movements, asymmetric cell divisions, cell fate specification and cell differentiation In agreement with their involvement in the formation of very diverse structures, Drosophila snail/escargot/worniu genes function in several cellular processes, such as the control of cell shape changes, cell movements, asymmetric cell divisions, cell fate specification and cell differentiation (e.g. [29,31,32,34,35,36]). scratch is mainly expressed in the developing nervous system formation and has been shown to promote neuronal development in the CNS [28]
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