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Open Access Research article

Evolutionary mechanisms driving the evolution of a large polydnavirus gene family coding for protein tyrosine phosphatases

Céline Serbielle1, Stéphane Dupas2, Elfie Perdereau1, François Héricourt134, Catherine Dupuy1, Elisabeth Huguet1 and Jean-Michel Drezen1*

Author affiliations

1 Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 7261, Faculté des Sciences et Techniques, Université F. Rabelais, Parc de Grandmont, 37200, Tours, France

2 IRD, Institut de Recherche pour le Développement, UR 072, Laboratoire Evolution, Génomes et Spéciation, UPR 9034, Centre National de la Recherche Scientifique (CNRS), 91198 Gif sur Yvette Cedex, France et Université Paris-Sud 11, 91405, Orsay Cedex, France

3 Present address: Laboratoire de Biologie des Ligneux et des Grandes Cultures, UPRES EA 1207, Université d'Orléans, 45067, Orléans cedex, France

4 Present address: INRA, USC1328, Arbres et Réponses aux Contraintes Hydriques et Environnementales (ARCHE), BP 6759, 45067, Orléans Cedex 2, France

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Citation and License

BMC Evolutionary Biology 2012, 12:253  doi:10.1186/1471-2148-12-253

Published: 27 December 2012

Abstract

Background

Gene duplications have been proposed to be the main mechanism involved in genome evolution and in acquisition of new functions. Polydnaviruses (PDVs), symbiotic viruses associated with parasitoid wasps, are ideal model systems to study mechanisms of gene duplications given that PDV genomes consist of virulence genes organized into multigene families. In these systems the viral genome is integrated in a wasp chromosome as a provirus and virus particles containing circular double-stranded DNA are injected into the parasitoids’ hosts and are essential for parasitism success. The viral virulence factors, organized in gene families, are required collectively to induce host immune suppression and developmental arrest. The gene family which encodes protein tyrosine phosphatases (PTPs) has undergone spectacular expansion in several PDV genomes with up to 42 genes.

Results

Here, we present strong indications that PTP gene family expansion occurred via classical mechanisms: by duplication of large segments of the chromosomally integrated form of the virus sequences (segmental duplication), by tandem duplications within this form and by dispersed duplications. We also propose a novel duplication mechanism specific to PDVs that involves viral circle reintegration into the wasp genome. The PTP copies produced were shown to undergo conservative evolution along with episodes of adaptive evolution. In particular recently produced copies have undergone positive selection in sites most likely involved in defining substrate selectivity.

Conclusion

The results provide evidence about the dynamic nature of polydnavirus proviral genomes. Classical and PDV-specific duplication mechanisms have been involved in the production of new gene copies. Selection pressures associated with antagonistic interactions with parasitized hosts have shaped these genes used to manipulate lepidopteran physiology with evidence for positive selection involved in adaptation to host targets.

Keywords:
Polydnavirus; Bracovirus; Protein tyrosine phosphatase; Gene duplication; Positive selection