Abstract
BackgroundInsect hosts have evolved immunity against invasion by parasitoids, and in co-evolutionary response parasitoids have also developed strategies to overcome host immune systems. The mechanisms through which parasitoid venoms disrupt the promotion of host immunity are still unclear. We report here a new mechanism evolved by parasitoid Pteromalus puparum, whose venom inhibited the promotion of immunity in its host Pieris rapae (cabbage white butterfly).Methodology/Principal FindingsA full-length cDNA encoding a C-type lectin (Pr-CTL) was isolated from P. rapae. Quantitative PCR and immunoblotting showed that injection of bacterial and inert beads induced expression of Pr-CTL, with peaks of mRNA and Pr-CTL protein levels at 4 and 8 h post beads challenge, respectively. In contrast, parasitoid venom suppressed Pr-CTL expression when co-injected with beads, in a time and dose-dependent manner. Immunolocalization and immunoblotting results showed that Pr-CTL was first detectable in vesicles present in cytoplasm of granulocytes in host hemolymph, and was then secreted from cells into circulatory fluid. Finally, the secreted Pr-CTL bound to cellular membranes of both granulocytes and plasmatocytes. Injection of double-stranded RNA specific for target gene decreased expression of Pr-CTL, and a few other host immune-related genes. Suppression of Pr-CTL expression also down-regulated antimicrobial and phenoloxidase activities, and reducing phagocytotic and encapsulation rates in host. The inhibitory effect of parasitoid venom on host encapsulation is consistent with its effect in suppressing Pr-CTL expression. Binding assay results showed that recombinant Pr-CTL directly attached to the surface of P. puparum egges. We infer that Pr-CTL may serve as an immune signalling co-effector, first binding to parasitoid eggs, regulating expression of a set of immune-related genes and promoting host immunity.Conclusions/Significance P. puparum venom inhibits promotion of host immune responses by silencing expression of host C-type lectin gene Pr-CTL, whose expression affected transcription of other host immune-related genes.
Highlights
Insects are subject to infection by a broad range of foreign invaders at different developmental stages [1,2]
Molecular cloning and structural features of Pr-C-type lectins (CTLs) gene The cloning of a 39-end fragment of a cDNA encoding C-type lectin, Pr-CTL, from a subtractive cDNA library prepared from hemocytes of P. rapae pupae has been described previously [32]
The predicted sequence of Pr-CTL was analysed using the Pfam database, which showed the presence of two tandem carbohydrate recognition domains (CRDs; PF00059)
Summary
Insects are subject to infection by a broad range of foreign invaders at different developmental stages [1,2]. The eggs and larvae of endoparasitoids develop in their host bodies, where they are subject to attack by host immune responses, including cellular and humoral responses, like encapsulation and melanization [12]. As a result of long-term co-evolution with their hosts, some hymenopteran parasitoids possess both maternal and embryonic active factors to positively suppress defences in their hosts [13,14]. These factors include polydnaviruses (PDVs), viruslike particles contained in the ovary calyx fluid, proteins secreted from venom gland or ovaries, as well as teratocytes and their secreted proteins [13,15]. We report here a new mechanism evolved by parasitoid Pteromalus puparum, whose venom inhibited the promotion of immunity in its host Pieris rapae (cabbage white butterfly)
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