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Transcriptome dynamics of mutualistic poxvirus infection of tropical fruit fly hosts

ABSTRACT: Parasitoid wasps are one of the most species-rich groups of animals on Earth, due to their ability to successfully develop as parasites of nearly all types of insects. Unlike most known parasitoid wasps that specialize within one or a few host species, Diachasmimorpha longicaudata is a generalist that can survive within multiple genera of tephritid fruit fly hosts, including many globally important pest species. D. longicaudata has therefore been widely released to suppress pest populations as part of biological control efforts in tropical and subtropical agricultural systems. In this study, we investigated the role of a mutualistic poxvirus in shaping the host range of D. longicaudata across three genera of agricultural pest species: two of which are permissive hosts for D. longicaudata parasitism and one that is a nonpermissive host. We found that permissive hosts Ceratitis capitata and Bactrocera dorsalis were highly susceptible to virus infection, displaying rapid virus replication and abundant fly mortality. However, the nonpermissive host Zeugodacus cucurbitae largely overcame virus infection, exhibiting substantially lower mortality and no virus replication. Further investigation of transcriptional dynamics during virus infection demonstrated hindered viral gene expression and limited changes in fly gene expression within the nonpermissive host compared to the permissive species, indicating that the host range of the viral symbiont may dictate the host range of D. longicaudata wasps. These findings also reveal that viral symbiont activity may be a major contributor to the success of D. longicaudata as a generalist parasitoid species and a globally successful biological control agent.

ORGANISM(S): Zeugodacus cucurbitae Ceratitis capitata Bactrocera dorsalis

PROVIDER: GSE228918 | GEO | 2024/03/24

REPOSITORIES: GEO

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Project description:Although host-parasitoid interactions are becoming well characterized at the organismal and cellular levels, much remains to be understood of the molecular bases for the host immune response and the parasitoidsâ ability to defeat this immune response. Leptopilina boulardi and L. heterotoma, two closely related, highly infectious natural parasitoids of Drosophila melanogaster, appear to use very different infection strategies at the cellular level. Here, we further characterize cellular level differences in the infection characteristics of these two wasp species using newly derived, virulent inbred strains, and then use whole genome microarrays to compare the transcriptional response of Drosophila to each. While flies attacked by the melanogaster group specialist Leptopilina boulardi (strain Lb17) up-regulate numerous genes encoding proteolytic enzymes, components of the Toll and JAK/STAT pathways, and the melanization cascade as part of a combined cellular and humoral innate immune response, flies attacked by the generalist L. heterotoma (strain Lh14) do not appear to initiate an immune transcriptional response at the time points post-infection we assayed, perhaps due to the rapid venom-mediated lysis of host hemocytes (blood cells). Thus, the specialist parasitoid appears to invoke a full-blown immune response in the host, but suppresses and/or evades downstream components of this response. Given that activation of the host immune response likely depletes the energetic resources of the host, the specialistâs infection strategy seems relatively disadvantageous. However, we uncover the mechanism for one potentially important fitness tradeoff of the generalistâs highly immune suppressive infection strategy. Experiment Overall Design: The parasitoid wasps L. boulardi and L. heterotoma were allowed to attack late second instar D. melanogaster larvae (72 hrs old at 22ËC) in the following manner. Nine petri dishes containing 60 fly larvae were each exposed to six experienced L. boulardi (strain Lb17) female wasps for 2 hrs, another nine plates were exposed to five L. heterotoma (strain Lh14) females, and nine control plates were left uninfected. For each of three time points post-infection (2-5 hrs, 9-12 hrs, 21-24 hrs), 40 larvae from three replicate plates were removed and frozen at -80ËC for RNA extraction and microarray analysis (3 treatments x 3 time points x 3 replicates = 27 samples total).

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Transcriptome dynamics of mutualistic poxvirus infection of tropical fruit fly hosts

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