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Open Access Research article

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

Qi Fang1, Lei Wang1, Jiaying Zhu1, Yanmin Li1, Qisheng Song2, David W Stanley3, Zunnu-raen Akhtar1 and Gongyin Ye1*

Author Affiliations

1 State Key Laboratory of Rice Biology & Key Laboratory of Molecular Biology of Crop Pathogens and Insects of Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou 310029, China

2 Division of Plant Sciences, University of Missouri, Columbia, MO 65211, USA

3 USDA/Agricultural Research Service, Biological Control of Insects Research Laboratory, Columbia, MO 65203, USA

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BMC Genomics 2010, 11:484  doi:10.1186/1471-2164-11-484

Published: 2 September 2010

Abstract

Background

The 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.

Results

At 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.

Conclusions

Our 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.