Abstract
Ichnoviruses are large dsDNA viruses that belong to the Polydnaviridae family. They are specifically associated with endoparasitic wasps of the family Ichneumonidae and essential for host parasitization by these wasps. We sequenced the Hyposoter didymator Ichnovirus (HdIV) encapsidated genome for further analysis of the transcription pattern of the entire set of HdIV genes following the parasitization of four different lepidopteran host species. The HdIV genome was found to consist of at least 50 circular dsDNA molecules, carrying 135 genes, 98 of which formed 18 gene families. The HdIV genome had general features typical of Ichnovirus (IV) genomes and closely resembled that of the IV carried by Hyposoter fugitivus. Subsequent transcriptomic analysis with Illumina technology during the course of Spodoptera frugiperda parasitization led to the identification of a small subset of less than 30 genes with high RPKM values in permissive hosts, consisting with these genes encoding crucial virulence proteins. Comparisons of HdIV expression profiles between host species revealed differences in transcript levels for given HdIV genes between two permissive hosts, S. frugiperda and Pseudoplusia includens. However, we found no evident intrafamily gene-specific transcription pattern consistent with the presence of multigenic families within IV genomes reflecting an ability of the wasps concerned to exploit different host species. Interestingly, in two non-permissive hosts, Mamestra brassiccae and Anticarsia gemmatalis (most of the parasitoid eggs were eliminated by the host cellular immune response), HdIV genes were generally less strongly transcribed than in permissive hosts. This suggests that successful parasitism is dependent on the expression of given HdIV genes exceeding a particular threshold value. These results raise questions about the mecanisms involved in regulating IV gene expression according to the nature of the lepidopteran host species encountered.
Highlights
Polydnaviruses (PDV) are large circular dsDNA viruses carried by thousands of endoparasitic wasp species
General features of the Hyposoter didymator Ichnovirus (HdIV) encapsidated genome The main characteristics of the sequenced HdIV encapsidated genome, presented in Table 1, are very similar to those reported for other IV genomes: 50 circular molecules ranging in size from 36 kb to 2.5 kb, a genome size of 263 kb, a GC content of 43%, and 134 putative open reading frames (ORF), corresponding to 31% of the genome (Figure 1; Table S2)
We found that 65 of the total of 135 predicted HdIV genes could be grouped into the six multigene families classically found in Campopleginae IV genomes [13,17]: the ‘‘Cysteine motif proteins’’ (Cys), ‘‘Repeat element’’ (Rep), ‘‘Viral innexins’’ (Vinx), ‘‘Viral ankyrins’’ (Vank), ‘‘Polar-Residue-Rich Proteins’’ (PRRP) and ‘‘N-genes’’ families (Table 1)
Summary
Polydnaviruses (PDV) are large circular dsDNA viruses carried by thousands of endoparasitic wasp species. Their genome is segmented into tens of molecules of various sizes. PDV particles are produced from the proviral template exclusively in a specific tissue of the ovaries in the female, the calyx. They are stored within the lumen of the oviducts and are injected into the insect host during oviposition [1,2,3]. PDV particles rapidly infect most of the host cells, in which the genes encoded by the encapsidated viral genome are expressed. PDVs do not replicate in the parasitized insect, as the genes required for replication are present in the wasp genome and are not packaged into the virus particles [11,12]
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