Abstract
BackgroundGenomic approaches provide unique opportunities to study interactions of insects with their pathogens. We developed a cDNA microarray to analyze the gene transcription profile of the lepidopteran pest Spodoptera frugiperda in response to injection of the polydnavirus HdIV associated with the ichneumonid wasp Hyposoter didymator. Polydnaviruses are associated with parasitic ichneumonoid wasps and are required for their development within the lepidopteran host, in which they act as potent immunosuppressive pathogens. In this study, we analyzed transcriptional variations in the two main effectors of the insect immune response, the hemocytes and the fat body, after injection of filter-purified HdIV.ResultsResults show that 24 hours post-injection, about 4% of the 1750 arrayed host genes display changes in their transcript levels with a large proportion (76%) showing a decrease. As a comparison, in S. frugiperda fat body, after injection of the pathogenic JcDNV densovirus, 8 genes display significant changes in their transcript level. They differ from the 7 affected by HdIV and, as opposed to HdIV injection, are all up-regulated. Interestingly, several of the genes that are modulated by HdIV injection have been shown to be involved in lepidopteran innate immunity. Levels of transcripts related to calreticulin, prophenoloxidase-activating enzyme, immulectin-2 and a novel lepidopteran scavenger receptor are decreased in hemocytes of HdIV-injected caterpillars. This was confirmed by quantitative RT-PCR analysis but not observed after injection of heat-inactivated HdIV. Conversely, an increased level of transcripts was found for a galactose-binding lectin and, surprisingly, for the prophenoloxidase subunits. The results obtained suggest that HdIV injection affects transcript levels of genes encoding different components of the host immune response (non-self recognition, humoral and cellular responses).ConclusionThis analysis of the host-polydnavirus interactions by a microarray approach indicates that the presence of HdIV induces, directly or indirectly, variations in transcript levels of specific host genes, changes that could be responsible in part for the alterations observed in the parasitized host physiology. Development of such global approaches will allow a better understanding of the strategies employed by parasites to manipulate their host physiology, and will permit the identification of potential targets of the immunosuppressive polydnaviruses.
Highlights
Genomic approaches provide unique opportunities to study interactions of insects with their pathogens
The transcriptomic analysis of S.frugiperda genes conducted here shows that injection of filterpurified Hyposoter didymator ichnovirus (HdIV) results in modifications of transcript levels for several host genes
Results obtained for the genes studied after injection of heat-inactivated HdIV suggest that HdIV transcription is required for the changes observed
Summary
Genomic approaches provide unique opportunities to study interactions of insects with their pathogens. We analyzed transcriptional variations in the two main effectors of the insect immune response, the hemocytes and the fat body, after injection of filter-purified HdIV. Signal transduction pathways leading to their transcription are probably similar to those of Drosophila, since regulatory motifs such as the kappaBlike and GATA sequences have been identified [11,12,13] and transcriptional induction by immune challenge has been reported [14]. Pattern recognition proteins such as hemolin, peptidoglycan recognition protein, beta-1,3glucan recognition proteins and immulectins have been described in lepidopteran insects [15]. The subsequently recruited hemocytes adhere to the one already spread on the bead in successive layers (Figure 1A, b and 1c) and the capsule, with abundant desmosomelike structures, is complete around most of the beads 8 hours after injection (Figure 1A, d and 1d')
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