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Open Access Research article

Identification of the main venom protein components of Aphidius ervi, a parasitoid wasp of the aphid model Acyrthosiphon pisum

Dominique Colinet123, Caroline Anselme1237, Emeline Deleury123, Donato Mancini4, Julie Poulain5, Carole Azéma-Dossat5, Maya Belghazi6, Sophie Tares123, Francesco Pennacchio4, Marylène Poirié123 and Jean-Luc Gatti1238*

Author Affiliations

1 INRA, ISA, UMR 1355, Evolution et Spécificité des Interactions Multitrophiques (ESIM), Sophia Antipolis, 06903, France

2 Université Nice Sophia Antipolis, ISA, Sophia Antipolis 06903, France

3 CNRS, ISA, UMR 7254, Sophia Antipolis 06903, France

4 Dipartimento di Agraria, Laboratorio di Entomologia “E. Tremblay”, Università degli Studi di Napoli “Federico II”, Portici, Napoli, Italy

5 Commissariat à l'Energie Atomique (CEA), Institut de Génomique (IG), Génoscope, Evry, France

6 CNRS, Aix-Marseille Université, UMR 7286, CRN2M, Centre d'Analyses Protéomiques de Marseille (CAPM), Faculté de Médecine - Secteur Nord, 51, bd Dramard, Marseille, France

7 Current address: Université de Picardie Jules Verne (UPJV), CNRS FRE 3498 EDYSAN, Bio-écologie des Insectes Phytophages et Entomophages (BIPE), Amiens, France

8 Evolution and Specificity of Multitrophic Interactions (ESIM), UMR 1355 "Sophia Agrobiotech Institute" (ISA), Institut National de la Recherche Agronomique, INRA PACA, 400 route des Chappes, Sophia Antipolis 06903, France

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BMC Genomics 2014, 15:342  doi:10.1186/1471-2164-15-342

Published: 6 May 2014

Abstract

Background

Endoparasitoid wasps are important natural enemies of the widely distributed aphid pests and are mainly used as biological control agents. However, despite the increased interest on aphid interaction networks, only sparse information is available on the factors used by parasitoids to modulate the aphid physiology. Our aim was here to identify the major protein components of the venom injected at oviposition by Aphidius ervi to ensure successful development in its aphid host, Acyrthosiphon pisum.

Results

A combined large-scale transcriptomic and proteomic approach allowed us to identify 16 putative venom proteins among which three γ-glutamyl transpeptidases (γ-GTs) were by far the most abundant. Two of the γ-GTs most likely correspond to alleles of the same gene, with one of these alleles previously described as involved in host castration. The third γ-GT was only distantly related to the others and may not be functional owing to the presence of mutations in the active site. Among the other abundant proteins in the venom, several were unique to A. ervi such as the molecular chaperone endoplasmin possibly involved in protecting proteins during their secretion and transport in the host. Abundant transcripts encoding three secreted cystein-rich toxin-like peptides whose function remains to be explored were also identified.

Conclusions

Our data further support the role of γ-GTs as key players in A. ervi success on aphid hosts. However, they also evidence that this wasp venom is a complex fluid that contains diverse, more or less specific, protein components. Their characterization will undoubtedly help deciphering parasitoid-aphid and parasitoid-aphid-symbiont interactions. Finally, this study also shed light on the quick evolution of venom components through processes such as duplication and convergent recruitment of virulence factors between unrelated organisms.

Keywords:
Parasitoid wasp; Aphid; Acyrthosiphon pisum; Aphidius ervi; Venom proteins; Virulence; γ-glutamyl transpeptidase; Cystein-rich peptides