The evolution of engrailed genes after duplication and speciation events

Abstract

Members of the engrailed class encode transcription factors involved in major steps of metazoan development. Few developmental regulatory genes have been studied in such a wide range of animals. Furthermore duplications of an ancestral engrailed gene independently generated multiple engrailed paralogues in several organisms. This offers the opportunity to reconstruct the evolution of the engrailed family and to study the processes involved in the functional diversification following speciation or duplication events. The ancestral function of engrailedis very likely involved in neurogenesis. Recent studies in Drosophila and mice have shown its crucial role in neuronal connectivity and neuromuscular targeting. engrailed was probably recruited very early for a role in segmentation through intercalary evolution. Several new functions were acquired later on in specific phyla. Some duplication events have been followed by the loss of one paralogue, whereas others have led to the functional diversification of the paralogues. The Duplication-Degenerescence-Complementation model recently proposed by Force et al. seems to be the main process involved in functional diversification after duplication events. This does not exclude acquisition of new functions for one or both paralogues after duplication. The acquisition of such new functions principally involves the evolution of cis-regulatory sequences, but evolution of the coding sequence has also been revealed. However, in all engrailed duplications studied, even in ancient chromosomal duplications, the paralogues have kept redundant functions. In fact, selection seems to maintain a certain redundancy between engrailed paralogues.

ceh-16/engrailedpatterns the embryonic epidermis ofCaenorhabditis elegans

“…In Drosophila and vertebrates engrailed-like genes have been duplicated during evolution (Gibert, 2002), whereas in the nematode Caenorhabditis elegans only one engrailed-like gene exists (this work). Phenotypic analysis of mutants and mosaic animals revealed that ceh-16/engrailed is required embryonically for the differentiation of the seam cells.…”

“…1 in the supplementary material). Besides the homeodomain referred to as Engrailed Homology domain 4 (EH4), CEH-16 possesses at least EH1, EH2 and EH3 [of the five known EH domains (Gibert, 2002)]. EH1 is constituted by the engrailed repressor domain, which binds to Groucho in Drosophila.…”

“…This segregation mechanism might be controlled in part by regulation of cell adhesion molecules (Dahmann and Basler, 1999). It has been suggested that the ancestral function of engrailed may be neuronal targeting, because it regulates the connectivity through the transcriptional regulation of cell adhesion molecules in the central nervous system in arthropods and vertebrates (Gibert, 2002;Vincent, 1998). Moreover, engrailed has been proposed to play a general role in segmentation of protostomes (Prud'homme et al, 2003).…”

A Maximum Likelihood Method for Detecting Functional Divergence at Individual Codon Sites, with Application to Gene Family Evolution

“…It provides a mechanism for evolution of divergent protein functions (Piatigorsky and Wistow 1991;Ohta 1993;Hughes 1994), novel gene expression patterns (Force et al 1999;Lynch and Force 2000), or both (Gibert 2002;Hughes 2002). For example, a single gene that is expressed in different tissues might experience conflicting selective pressures, the result being a compromise between optimal adaptations for any one tissue.…”

“…For example, a single gene that is expressed in different tissues might experience conflicting selective pressures, the result being a compromise between optimal adaptations for any one tissue. Duplication of such a locus can lead to specialized patterns of expression among gene copies (Force et al 1999), providing natural selection the freedom to promote tissue-specific functional divergence (e.g., Gibert 2002). The tremendous diversity of extant gene families, taken together with the observation that there is often an acceleration of amino acid substitution rates following gene duplication (Li 1985;Lynch and Conery 2000), suggests that gene duplication has been an important mechanism for functional divergence of genetic systems.…”