Development of RNAi in a Drosophila endoparasitoid wasp and demonstration of its efficiency in impairing venom protein production

Colinet, Dominique; Kremmer, Laurent; Lemauf, Séverine; Rebuf, Christian; Gatti, Jean‐Luc; Poirié, Marylène

doi:10.1016/j.jinsphys.2014.02.011

Cited by 32 publications

(36 citation statements)

References 29 publications

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“…Deciphering the role of major venom proteins in Psyttalia parasitism success, especially those with no predicted function, is a key challenge. This will require further exploration using techniques such as RNAi, demonstrated as an efficient approach for impairing the production of parasitoid venom proteins42.…”

Section: Discussionmentioning

confidence: 99%

Comparative venomics of Psyttalia lounsburyi and P. concolor, two olive fruit fly parasitoids: a hypothetical role for a GH1 β-glucosidase

Mathe‐Hubert

Colinet

Deleury

et al. 2016

Sci Rep

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Venom composition of parasitoid wasps attracts increasing interest – notably molecules ensuring parasitism success on arthropod pests – but its variation within and among taxa is not yet understood. We have identified here the main venom proteins of two braconid wasps, Psyttalia lounsburyi (two strains from South Africa and Kenya) and P. concolor, olive fruit fly parasitoids that differ in host range. Among the shared abundant proteins, we found a GH1 β-glucosidase and a family of leucine-rich repeat (LRR) proteins. Olive is extremely rich in glycoside compounds that are hydrolyzed by β-glucosidases into defensive toxic products in response to phytophagous insect attacks. Assuming that Psyttalia host larvae sequester ingested glycosides, the injected venom GH1 β-glucosidase could induce the release of toxic compounds, thus participating in parasitism success by weakening the host. Venom LRR proteins are similar to truncated Toll-like receptors and may possibly scavenge the host immunity. The abundance of one of these LRR proteins in the venom of only one of the two P. lounsburyi strains evidences intraspecific variation in venom composition. Altogether, venom intra- and inter-specific variation in Psyttalia spp. were much lower than previously reported in the Leptopilina genus (Figitidae), suggesting it might depend upon the parasitoid taxa.

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Section: Discussionmentioning

confidence: 99%

Comparative venomics of Psyttalia lounsburyi and P. concolor, two olive fruit fly parasitoids: a hypothetical role for a GH1 β-glucosidase

Mathe‐Hubert

Colinet

Deleury

et al. 2016

Sci Rep

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“…This might be performed using the RNAi technique, as RNAi-mediated complete extinction of a venom protein was recently evidenced in an endoparasitoid wasp [54]. Results will open the way to a better understanding on aphid-parasitoid immune and nutritional parasitoid interactions.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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BackgroundEndoparasitoid 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.ResultsA 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-342) contains supplementary material, which is available to authorized users.

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“…; Keebaugh and Schlenke ; Mortimer ; Colinet et al. ). The canonical antiwasp immune response of some, but not all, drosophilids involves melanotic encapsulation, and concomitant death, of the wasp embryo (Kacsoh et al.…”

Section: Discussionmentioning

confidence: 99%

“…), and the promising recent developments in wasp RNAi (e.g., Colinet et al. ), will enable the integration of powerful omics and genetic manipulation approaches to identify genes and pathways relevant to the Spiroplasma protective mechanism and uncover their evolutionary patterns.…”

Section: Discussionmentioning

confidence: 99%

“…The strategies employed by parasitoids to suppress Drosophila immune response are extremely diverse and rely on substances injected by the wasp during oviposition (reviewed in Heavner et al 2013;Keebaugh and Schlenke 2013;Mortimer 2013;Colinet et al 2014). The canonical antiwasp immune response of some, but not all, drosophilids involves melanotic encapsulation, and concomitant death, of the wasp embryo (Kacsoh et al 2014).…”

Section: Discussionmentioning

confidence: 99%

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Independent origins of resistance or susceptibility of parasitic wasps to a defensive symbiont

Mateos

Winter

et al. 2016

Ecology and Evolution

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Insect microbe associations are diverse, widespread, and influential. Among the fitness effects of microbes on their hosts, defense against natural enemies is increasingly recognized as ubiquitous, particularly among those associations involving heritable, yet facultative, bacteria. Protective mutualisms generate complex ecological and coevolutionary dynamics that are only beginning to be elucidated. These depend in part on the degree to which symbiont‐mediated protection exhibits specificity to one or more members of the natural enemy community. Recent findings in a well‐studied defensive mutualism system (i.e., aphids, bacteria, parasitoid wasps) reveal repeated instances of evolution of susceptibility or resistance to defensive bacteria by parasitoids. This study searched for similar patterns in an emerging model system for defensive mutualisms: the interaction of Drosophila, bacteria in the genus Spiroplasma, and wasps that parasitize larval stages of Drosophila. Previous work indicated that three divergent species of parasitic wasps are strongly inhibited by the presence of Spiroplasma in three divergent species of Drosophila, including D. melanogaster. The results of this study uncovered two additional wasp species that are susceptible to Spiroplasma and two that are unaffected by Spiroplasma, implying at least two instances of loss or gain of susceptibility to Spiroplasma among larval parasitoids of Drosophila.

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Development of RNAi in a Drosophila endoparasitoid wasp and demonstration of its efficiency in impairing venom protein production

Cited by 32 publications

References 29 publications

Comparative venomics of Psyttalia lounsburyi and P. concolor, two olive fruit fly parasitoids: a hypothetical role for a GH1 β-glucosidase

Comparative venomics of Psyttalia lounsburyi and P. concolor, two olive fruit fly parasitoids: a hypothetical role for a GH1 β-glucosidase

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

Independent origins of resistance or susceptibility of parasitic wasps to a defensive symbiont

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