Parasitization by Cotesia chilonis Influences Gene Expression in Fatbody and Hemocytes of Chilo suppressalis

BACKGROUND: During oviposition many parasitoid wasps inject various factors, such as polydnaviruses (PDVs), along with eggs that manipulate the physiology and development of their hosts. These manipulations are thought to benefit the parasites. However, the detailed mechanisms of insect host-parasitoid interactions are not fully understood at the molecular level. Based on recent findings that some parasitoids influence gene expression in their hosts, we posed the hypothesis that parasitization by a braconid wasp, Cotesia chilonis, influences the expression of genes responsible for development, metabolism and immune functions in the fatbody and hemocytes of its host, Chilo suppressalis. METHODOLOGY/PRINCIPAL FINDINGS: We obtained 39,344,452 reads, which were assembled into 146,770 scaffolds, and 76,016 unigenes. Parasitization impacted gene expression in fatbody and hemocytes. Of these, 8096 fatbody or 5743 hemocyte unigenes were down-regulated, and 2572 fatbody or 1452 hemocyte unigenes were up-regulated. Gene ontology data showed that the majority of the differentially expressed genes are involved in enzyme-regulated activity, binding, transcription regulator activity and catalytic activity. qPCR results show that most anti-microbial peptide transcription levels were up-regulated after parasitization. Expression of bracovirus genes was detected in parasitized larvae with 19 unique sequences identified from six PDV gene families including ankyrin, CrV1 protein, cystatin, early-expressed (EP) proteins, lectin, and protein tyrosine phosphatase. CONCLUSIONS: The current study supports our hypothesis that parasitization influences the expression of fatbody and hemocyte genes in the host, C. suppressalis. The general view is that manipulation of host metabolism and immunity benefits the development and emergence of the parasitoid offsprings. The accepted beneficial mechanisms include the direct impact of parasitoid-associated virulence factors such as venom and polydnavirus on host tissues (such as cell damage) and, more deeply, the ability of these factors to influence gene expression. We infer that insect parasitoids generally manipulate their environments, the internal milieu of their hosts.