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

Abstract

BackgroundDuring 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 FindingsWe 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.ConclusionsThe 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.

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

“…To date, only two other high-throughput transcriptomic approaches have been conducted on similar host-parasitoid systems involving DsIV and CchBV; in each case, the expressions of only 19 viral genes from 5 and 6 gene families, respectively, were detected (30,31). Even if the reference genomes are not available for these viruses, the expression of a larger number of genes might have been expected, considering the number of genes predicted in related viruses (19,23).…”

“…In addition, deep sequencing approaches at the transcriptome level concerned the expression of the Diadegma semiclausum ichnovirus (DsIV) in Plutella xylostella larvae and the expression of Cotesia chilonis bracovirus (CchBV) in the Chilo suppressalis host. In these de novo transcriptomic approaches applied to new model species, the relative contributions of IV and BV gene expression could not be evaluated because the genomes of these PDVs have not yet been sequenced (30,31).…”

Molecular characterization and expression profiles of nicotinic acetylcholine receptors in the rice striped stem borer, Chilo suppressalis (Lepidoptera: Crambidae)

“…The tissues included the brain, subesophageal ganglion, thoracic ganglion, abdominal ganglion, hemocytes, fat body, foregut, midgut, hindgut and Malpighian tubules. For hemocyte collection, the fifth-instar larvae were surface-sterilized with 75% ethanol and total hemolymph was collected with a 20 μL sterilized pipette by cutting the proleg, followed by centrifugation at 200× g for 10 min at 4°C to collect the hemocyte precipitate (Wu et al, 2013b). Other tissues were dissected on ice from the fifth-instar larvae.…”

THE ENDOPARASITOID Pteromalus puparum INFLUENCES HOST GENE EXPRESSION WITHIN FIRST HOUR OF PARASITIZATION

“…In the Plutella xyl ostella/ Diadegma semiclausum (Hymenoptera: Ichneumonidae; a larval endoparasitoid with PDV and venom) system, 53 immune‐related host genes were differentially transcribed from 6 to 48 h PP (Etebari et al., ). Similarly, in the Chilo suppresalis / Cotesia chilonis (Hymenoptera: Braconidae; a larval endoparasitoid with venom and PDV) system, 59 immune‐related transcripts in host larval fat body were differentially expressioned from 6 to 48 h PP (Wu et al., ). A larger number of genes were influenced in the Octodonta nipae / Tetrastichus brontispae (Hymenoptera: Eulophidae; a pupal endoparasitoid) system, with 87 immune‐related genes differentially expressed from 6 to 120 h PP (Tang et al., ).…”

“…The expression of all PGRP and GRP unigenes as well as three CTL unigenes in T. molitor pupae wase increased after parasitization, and those of two CTL unigenes were suppressed (Zhu et al., ). PGRP and SR in fat body as well as SR in hemocytes were downregulated in C. suppressalis larvae parasitized by C. chilonis , and GRP and CTL both in fat body and hemocytes were upregulated in parasitized larvae (Wu et al., ). Our interpretation is PRRs are important for host immune response to parasitization.…”