Abstract
Parasitoids are insects that use other insects as hosts. They sabotage host cellular and humoral defences to promote the survival of their offspring by injecting viruses and venoms along with their eggs. Many pathogens and parasites disrupt host epigenetic mechanisms to overcome immune system defences, and we hypothesized that parasitoids may use the same strategy. We used the ichneumon wasp Pimpla turionellae as a model idiobiont parasitoid to test this hypothesis, with pupae of the greater wax moth Galleria mellonella as the host. We found that parasitoid infestation involves the suppression of host immunity-related effector genes and the modulation of host genes involved in developmental hormone signalling. The transcriptional reprogramming of host genes following the injection of parasitoid eggs was associated with changes in host epigenetic mechanisms. The introduction of parasitoids resulted in a transient decrease in host global DNA methylation and the modulation of acetylation ratios for specific histones. Genes encoding regulators of histone acetylation and deacetylation were mostly downregulated in the parasitized pupae, suggesting that parasitoids can suppress host transcription. We also detected a strong parasitoid-specific effect on host microRNAs regulating gene expression at the post-transcriptional level. Our data therefore support the hypothesis that parasitoids may favour the survival of their offspring by interfering with host epigenetic mechanisms to suppress the immune system and disrupt development.
Highlights
Parasitic wasps are a polyphyletic group of insects within the order Hymenoptera that have evolved to use other insects as hosts for their offspring
The coevolution of parasitoids and their hosts has led to counterstrategies in parasitoid wasps to circumvent such host defence reactions
P. turionellae arrests the development of G. mellonella pupae but can suppress the host immune system [8,9,10]
Summary
Parasitic wasps are a polyphyletic group of insects within the order Hymenoptera that have evolved to use other insects as hosts for their offspring. The impact of parasitoids on host DNA methylation was determined by comparing the amount of 5methylcytidine monophosphate (5 m-dCMP) released from the genomic DNA of infested pupae and controls at different time points following the injection of wasp eggs. We measured the expression of microRNAs (miRNAs), which regulate target genes at the posttranscriptional level [26] These short, noncoding RNAs, 18–24 nucleotides in length, inhibit the translation of specific mRNAs by base-pairing with the untranslated regions or occasionally the coding region, and they play a role in insect antiviral responses [27]. The expression profiles of conserved miRNAs in parasitized G. mellonella pupae and controls were monitored by microarray analysis. To determine changes in miRNA expression profiles during parasitization, total RNA was isolated from parasitized G. mellonella pupae and controls 4 h after egg deposition as described above. For the analysis of miRNAs, log values were assessed with significance threshold of p < 0.01
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