Section: Genomics
Topic: Evolution, Genetics/genomics

Convergent origin and accelerated evolution of vesicle-associated RhoGAP proteins in two unrelated parasitoid wasps

10.24072/pcjournal.406 - Peer Community Journal, Volume 4 (2024), article no. e36.

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Animal venoms and other protein-based secretions that perform a variety of functions, from predation to defense, are highly complex cocktails of bioactive compounds. Gene duplication, accompanied by modification of the expression and/or function of one of the duplicates under the action of positive selection, followed by further duplication to produce multigene families of toxins is a well-documented process in venomous animals. This evolutionary model has been less described in parasitoid wasps, which use maternal fluids, including venom, to protect their eggs from encapsulation by the host immune system. Here, we evidence the convergent recruitment and accelerated evolution of two multigene families of RhoGAPs presumably involved in virulence in two unrelated parasitoid wasp species, Leptopilina boulardi (Figitidae) and Venturia canescens (Icheumonidae). In both species, these RhoGAPs are associated with vesicles that act as transport systems to deliver virulence factors, but are produced in different tissues: the venom gland in Leptopilina sp. and the ovarian calyx in V. canescens. We show that the gene encoding the cellular RacGAP1 is at the origin of the virulent RhoGAP families found in Leptopilina sp. and V. canescens. We also show that both RhoGAP families have undergone evolution under positive selection and that almost all of these RhoGAPs lost their GAP activity and GTPase binding ability due to substitutions in key amino acids. These results suggest an accelerated evolution and functional diversification of these vesicle-associated RhoGAPs in the two phylogenetically distant parasitoid species. The potential new function(s) and the exact mechanism of action of these proteins in host cells remain to be elucidated.

Published online:
DOI: 10.24072/pcjournal.406
Type: Research article
Colinet, Dominique 1; Cavigliasso, Fanny 1; Leobold, Matthieu 2; Pichon, Apolline 3; Urbach, Serge 3; Cazes, Dominique 1; Poullet, Marine 1; Belghazi, Maya 4; Volkoff, Anne-Nathalie 3; Drezen, Jean-Michel 2; Gatti, Jean-Luc 1; Poirié, Marylène 1

1 Université Côte d’Azur, INRAE, CNRS, ISA, Sophia Antipolis, France
2 Institut de Recherche sur la Biologie de l'Insecte (IRBI), UMR 7261, CNRS - Université de Tours, Tours, France
3 DGIMI, Univ Montpellier, INRAE, Montpellier, France
4 Aix Marseille Université, CNRS, Plateforme Protéomique, IMM FR3479, Marseille Protéomique (MaP), Marseille, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Colinet, Dominique and Cavigliasso, Fanny and Leobold, Matthieu and Pichon, Apolline and Urbach, Serge and Cazes, Dominique and Poullet, Marine and Belghazi, Maya and Volkoff, Anne-Nathalie and Drezen, Jean-Michel and Gatti, Jean-Luc and Poiri\'e, Maryl\`ene},
     title = {Convergent origin and accelerated evolution of vesicle-associated {RhoGAP} proteins in two unrelated parasitoid wasps},
     journal = {Peer Community Journal},
     eid = {e36},
     publisher = {Peer Community In},
     volume = {4},
     year = {2024},
     doi = {10.24072/pcjournal.406},
     language = {en},
     url = {}
AU  - Colinet, Dominique
AU  - Cavigliasso, Fanny
AU  - Leobold, Matthieu
AU  - Pichon, Apolline
AU  - Urbach, Serge
AU  - Cazes, Dominique
AU  - Poullet, Marine
AU  - Belghazi, Maya
AU  - Volkoff, Anne-Nathalie
AU  - Drezen, Jean-Michel
AU  - Gatti, Jean-Luc
AU  - Poirié, Marylène
TI  - Convergent origin and accelerated evolution of vesicle-associated RhoGAP proteins in two unrelated parasitoid wasps
JO  - Peer Community Journal
PY  - 2024
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%A Colinet, Dominique
%A Cavigliasso, Fanny
%A Leobold, Matthieu
%A Pichon, Apolline
%A Urbach, Serge
%A Cazes, Dominique
%A Poullet, Marine
%A Belghazi, Maya
%A Volkoff, Anne-Nathalie
%A Drezen, Jean-Michel
%A Gatti, Jean-Luc
%A Poirié, Marylène
%T Convergent origin and accelerated evolution of vesicle-associated RhoGAP proteins in two unrelated parasitoid wasps
%J Peer Community Journal
%D 2024
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%I Peer Community In
%R 10.24072/pcjournal.406
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%F 10_24072_pcjournal_406
Colinet, Dominique; Cavigliasso, Fanny; Leobold, Matthieu; Pichon, Apolline; Urbach, Serge; Cazes, Dominique; Poullet, Marine; Belghazi, Maya; Volkoff, Anne-Nathalie; Drezen, Jean-Michel; Gatti, Jean-Luc; Poirié, Marylène. Convergent origin and accelerated evolution of vesicle-associated RhoGAP proteins in two unrelated parasitoid wasps. Peer Community Journal, Volume 4 (2024), article  no. e36. doi : 10.24072/pcjournal.406.

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100248

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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