Gene expression profiling of Spodoptera frugiperda hemocytes and fat body using cDNA microarray reveals polydnavirus-associated variations in lepidopteran host genes transcript levels

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.

Transcriptomic Immune Response of Tenebrio molitor Pupae to Parasitization by Scleroderma guani

“…Microarray experiments showed that two PGRPs of Drosophila were significantly upregulated after parasitoid attack [49]. Hyposoter didymator polydnavirus infection can down-regulate a Spodoptera frugiperda gene with high similarity with the Manduca sexta immulectin-2 [50]. Especially, it was reported that the gene lectin - 24A was massively up-regulated in parasitized Drosophila larvae after parasitization at the time when the capsule was formed [51].…”

Recent findings in evolution and function of insect innexins

“…The Vinnexins initially were hypothesized to disrupt hemocytic encapsulation, the primary anti-parasitoid immune response of caterpillars, presumably by inhibiting gap junctional intercellular communication [78,79]. Like many IV genes, vinnexin transcripts are broadly detected in host caterpillar tissues [31,97]. However, an antibody against the C. sonorensis IV (CsIV) VinnexinQ2 (Cs-VnxQ2) only identified the protein in CsIV-infected hemocytes of the caterpillar Heliothis virescens, where the protein localized to cellular membranes [31].…”

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

“…Transcriptomic analyses of these particular host-parasitoid interactions have so far focused on host genes (26,27) or on specific virulence genes or multigenic families and have rarely given a global vision of PDV transcription during these interactions (3,5,28). Recently, an extensive BV transcriptome profile was reported, which concerned Microplitis demolitor BV (MdBV) expression in Pseudoplusia includens, where the spatial and temporal expressions of most predicted open reading frames (ORFs) of this BV were analyzed by reverse transcription-PCR (RT-PCR) (29).…”