Comparison of even-skipped related gene expression pattern in vertebrates shows an association between expression domain loss and modification of selective constraints on sequences

Authors

  • Fabien Avaron,

    1. Laboratoire de Biologie du Développement, Université de Paris 7, case courrier 7077, 2 place Jussieu, 75251 Paris cedex 5, France
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      Authors contributed equally to this work.

    • 2

      Present address: Ottawa Health Research Institute, 725 Parkdale Avenue, Ottawa, Ontario K1Y 4E9, Canada.

  • Christelle Thaëron-Antono,

    1. Laboratoire de Biologie du Développement, Université de Paris 7, case courrier 7077, 2 place Jussieu, 75251 Paris cedex 5, France
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    • 1

      Authors contributed equally to this work.

  • Caroline W. Beck,

    1. Developmental Biology Programme, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, United Kingdom
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  • Véronique Borday-Birraux,

    1. Laboratoire de Biologie du Développement, Université de Paris 7, case courrier 7077, 2 place Jussieu, 75251 Paris cedex 5, France
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      Present address: Populations, Génétique et Évolution, CNRS, UPR 9034, 1 avenue de la terrasse, 91198 Gif-sur-Yvette cedex, France.

  • Jacqueline Géraudie,

    1. Laboratoire de Biologie du Développement, Université de Paris 7, case courrier 7077, 2 place Jussieu, 75251 Paris cedex 5, France
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      Present address: Laboratoire de Recherche Orthopédique, Faculté de médecine Lariboisière Saint-Louis, 10 avenue de Verdun, 75010 Paris, France.

  • Didier Casane,

    Corresponding author
    1. Laboratoire de Biologie du Développement, “Equipe Phylogénie, Bioinformatique et Génome,” Université de Paris 6, case 24, 75252 Paris cedex 5, France
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      Present address: Populations, Génétique et Évolution, CNRS, UPR 9034, 1 avenue de la terrasse, 91198 Gif-sur-Yvette cedex, France.

  • Patrick Laurenti

    Corresponding author
    1. Laboratoire de Biologie du Développement, Université de Paris 7, case courrier 7077, 2 place Jussieu, 75251 Paris cedex 5, France
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      Present address: Populations, Génétique et Évolution, CNRS, UPR 9034, 1 avenue de la terrasse, 91198 Gif-sur-Yvette cedex, France.


*Authors for correspondence (e-mail Laurenti@ccr.jussieu.fr or didier.casane@snv.jussieu.fr)

Abstract

SUMMARY The even-skipped related genes (evx) encode homeodomain-containing transcription factors that play key roles in body patterning and neurogenesis in a wide array of Eumetazoa species. It is thought that the genome of the last common ancestor of Chordata contained a unique evx gene linked to a unique ancestral Hox complex. During subsequent evolution, two rounds of whole genome duplication followed by individual gene losses gave rise to three paralogs: evx1, evx2, and eve1. Then, eve1 was maintained in Actinopterygii lineage but not in Tetrapoda. To explain this discrepancy, we examined the expression patterns of the evx1 homologue, Xhox3, in Xenopus laevis and that of evx1 and eve1 in Danio rerio. We show here that Xhox3 is expressed in a manner that closely reflects the inferred expression pattern of the evx1 gene in the last common ancestor of Vertebrata (i.e., in gastrula, the central nervous system, the posterior gut, and the tip of the growing tail). Zebrafish evx1 and Xenopus Xhox3 are expressed in homologous cell lineages of the central nervous system and of the posterior gut, but evx1 was undetectable in the gastrula and the tail bud. Strikingly, eve1 is the only evx gene of zebrafish to be expressed in these two latter regions. Thus, the ancestral expression pattern of evx1 in vertebrates appears to have been distributed between evx1 and eve1 in zebrafish. We propose that evx1 and eve1 underwent a complementary loss of expression domain in zebrafish that allowed the maintenance of the two paralogs in accordance with the duplication-degeneration-complementation model. It is important to note that, in zebrafish, Evx1 and Eve1 have lost most of the protein domain upstream of the homeodomain. In addition, Eve1 has accumulated substitutions in positions that are highly conserved in all other Evx proteins. Thus, the reduction of the expression domain of both evx1 and eve1 in zebrafish appears to be associated with the modification of constraints on the protein sequences, allowing the shortening of both genes and an accelerated substitution rate in eve1.

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