Expression of immune-response genes in lepidopteran host is suppressed by venom from an endoparasitoid, Pteromalus puparum

Abstract

BackgroundThe relationships between parasitoids and their insect hosts have attracted attention at two levels. First, the basic biology of host-parasitoid interactions is of fundamental interest. Second, parasitoids are widely used as biological control agents in sustainable agricultural programs. Females of the gregarious endoparasitoid Pteromalus puparum (Hymenoptera: Pteromalidae) inject venom along with eggs into their hosts. P. puparum does not inject polydnaviruses during oviposition. For this reason, P. puparum and its pupal host, the small white butterfly Pieris rapae (Lepidoptera: Pieridae), comprise an excellent model system for studying the influence of an endoparasitoid venom on the biology of the pupal host. P. puparum venom suppresses the immunity of its host, although the suppressive mechanisms are not fully understood. In this study, we tested our hypothesis that P. puparum venom influences host gene expression in the two main immunity-conferring tissues, hemocytes and fat body.ResultsAt 1 h post-venom injection, we recorded significant decreases in transcript levels of 217 EST clones (revealing 113 genes identified in silico, including 62 unknown contigs) derived from forward subtractive libraries of host hemocytes and in transcript levels of 288 EST clones (221 genes identified in silico, including 123 unknown contigs) from libraries of host fat body. These genes are related to insect immune response, cytoskeleton, cell cycle and apoptosis, metabolism, transport, stress response and transcriptional and translational regulation. We verified the reliability of the suppression subtractive hybridization (SSH) data with semi-quantitative RT-PCR analysis of a set of randomly selected genes. This analysis showed that most of the selected genes were down-regulated after venom injection.ConclusionsOur findings support our hypothesis that P. puparum venom influences gene expression in host hemocytes and fat body. Specifically, the venom treatments led to reductions in expression of a large number of genes. Many of the down-regulated genes act in immunity, although others act in non-immune areas of host biology. We conclude that the actions of venom on host gene expression influence immunity as well as other aspects of host biology in ways that benefit the development and emergence of the next generation of parasitoids.

Venom of Parasitoid, Pteromalus puparum, Suppresses Host, Pieris rapae, Immune Promotion by Decreasing Host C-Type Lectin Gene Expression

“…rapae pupae has been described previously [32]. The full length cDNA of the Pr-CTL gene (GenBank accession number: JN133501) was obtained by rapid amplification of cDNA ends (RACE).…”

“…Beads were prepared for injection as previously described [32]. At 4 h post immune induction, the total RNA sample was isolated using Trizol Reagent (Invitrogen, California, USA) from the pupa.…”

Effect of Plant Based Essential Oil on Immune Response of Silkworm, Antheraea assama Westwood (Lepidoptera: Saturniidae)

“…Activation of PO activity confers resistance against invading nonself material, but it may not always adequately reflect overall resistance against all insults (Schwarzenbach and Ward, 2007). Although consistent measurement of phenoloxidase activity and haemocyte count have been successfully used in immunity studies in insects (Schwarzenbach and Ward, 2007;Lourenco et al, 2005;Schmid et al, 2008), study of immune related gene expression in haemolymph and fat bodies responsible for conferring immunity are required to understand the complex mechanism of immune response occurring in response to oil treatment (Fang et al, 2010).…”

An Efficient Innate Immune Response ofDanaus genutia(Lepidoptera: Nymphalidae) Larvae is Independent of Hemocyte Concentration AgainstE. coli

“…Both these outcomes signify high efficiency of the larval immune system against E. coli. The hemocytes consist of several components which are essential for defense against various pathogens (Clark et al, 1997;Fang et al, 2010). The humoral immunity of the insect is equipped with antimicrobial peptides and the enzyme phenoloxidase, which critically eliminates the microbial infection from the insect system.…”