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Parasites alter host energy homeostasis for their own development, but the mechanisms underlying this phenomenon remain largely unknown. Here, we show that Cotesia vestalis, an endoparasitic wasp of Plutella xylostella larvae, stimulates a reduction of host lipid levels. This process requires excess secretion of P. xylostella tachykinin (PxTK) peptides from enteroendocrine cells (EEs) in the midgut of the parasitized host larvae. We found that parasitization upregulates PxTK signaling to suppress lipogenesis in midgut enterocytes (ECs) in a non-cell-autonomous manner, and the reduced host lipid level benefits the development of wasp offspring and their subsequent parasitic ability. We further found that a C. vestalis bracovirus (CvBV) gene, CvBV 9–2, is responsible for PxTK induction, which in turn reduces the systemic lipid level of the host. Taken together, these findings illustrate a novel mechanism for parasite manipulation of host energy homeostasis by a symbiotic bracovirus gene to promote the development and increase the parasitic efficiency of an agriculturally important wasp species., Author summary Parasitic wasps are ubiquitous on earth and diverse. They lay eggs in or on the bodies of their hosts, and they have evolved adaptive strategies to regulate the energy metabolism of their hosts to match their own specific nutrition requirements. Here, we found that Cotesia vestalis, a solitary endoparasitoid of Plutella xylostella, uses symbiotic bracovirus as a weapon to manipulate host systemic lipid levels. Specifically, a C. vestalis bracovirus (CvBV) gene, CvBV 9–2, is responsible for the induction of PxTK, which in turn suppresses lipogenesis in the midgut of the parasitized host, leading to a nutritional lipid level suitable for the development and subsequent parasitic efficiency of C. vestalis wasps. Our study provides innovative insights into the mechanisms by which parasitic wasps manipulate host lipid homeostasis and may help to expand our knowledge of other parasitic systems.

Some DNA viruses infect host animals usually by integrating their DNAs into the host genome. However, the mechanisms for integration remain largely unknown. Here, we find that Cotesia vestalis bracovirus (CvBV), a polydnavirus of the parasitic wasp C. vestalis (Haliday), integrates its DNA circles into host Plutella xylostella (L.) genome by two distinct strategies, conservatively and randomly, through high-throughput sequencing analysis. We confirmed that the conservatively integrating circles contain an essential “8+5” nucleotides motif which is required for integration. Then we find CvBV circles are integrated into the caterpillar’s genome in three temporal patterns, the early, mid and late stage-integration. We further identify that three CvBV-encoded integrases are responsible for some, but not all of the virus circle integrations, indeed they mainly participate in the processes of early stage-integration. Strikingly, we find two P. xylostella retroviral integrases (PxIN1 and PxIN2) are highly induced upon wasp parasitism, and PxIN1 is crucial for integration of some other early-integrated CvBV circles, such as CvBV_04, CvBV_12 and CvBV_24, while PxIN2 is important for integration of a late-integrated CvBV circle, CvBV_21. Our data uncover a novel mechanism in which CvBV integrates into the infected host genome, not only by utilizing its own integrases, but also by recruiting host enzymes. These findings will strongly deepen our understanding of how bracoviruses regulate and integrate into their hosts., Author summary Parasitoid wasps are a very large group of animals that live in or on the other arthropods. Polydnaviruses (PDVs) are a special kind of DNA virus associated parasitic wasps (primary hosts), which do not replicate in their infected caterpillar hosts (secondary hosts). During parasitoid oviposition, PDVs enter infected hosts and integrate their DNA into the genome of infected hosts, then their virulence genes begin to express and manipulate multiple biological process of hosts to fulfill all the requirements of parasitoids offspring. However, the mechanisms for integration remain largely unknown. Our research found the integration of PDVs is not only by utilizing its own integrases, but also by recruiting host enzymes. Here, we provide a new concept that host intergrases are involved in the integration of PDVs into host genome, and it greatly enhance our understanding of how PDVs regulate and integrate into their hosts, and may also inspire studies on how some DNA viruses may integrate their DNAs into human genome.

Venoms secreted by the venom gland (VG) of parasitoid wasp help ensure successful parasitism by host immune suppression and developmental regulation. Cotesia vestalis, a larval endoparasitoid, and Diadromus collaris, a pupal endoparasitoid, parasitize the diamondback moth (DBM), Plutella xylostella. To explore and compare the venom components of two endoparasitoids, we sequenced transcriptomes of the VGs and wasp bodies without VGs (BWVGs) of the two endoparasitoids. Statistically enriched GO terms and KEGG pathways of the two VGs compared to respective whole-body background were similar and reflected active protein biosynthesis activities in the two VGs. 1,595 VG specific genes of the D. collaris VG and 1,461 VG specific genes of the C. vestalis VG were identified by comparative transcript profiling. A total of 444 and 513 genes encoding potential secretory proteins were identified and defined as putative venom genes in D. collaris VG and C. vestalis VG, respectively. The putative venom genes of the two wasps showed no significant similarity or convergence. More venom genes were predicted in D. collaris VG than C. vestalis VG, especially hydrolase-coding genes. Differences in the types and quantities of putative venom genes shed light on different venom functions.

Background Parasitic insects are well-known biological control agents for arthropod pests worldwide. They are capable of regulating their host’s physiology, development and behaviour. However, many of the molecular mechanisms involved in host-parasitoid interaction remain unknown. Results We sequenced the genomes of two parasitic wasps (Cotesia vestalis, and Diadromus collaris) that parasitize the diamondback moth Plutella xylostella using Illumina and Pacbio sequencing platforms. Genome assembly using SOAPdenovo produced a 178 Mb draft genome for C. vestalis and a 399 Mb draft genome for D. collaris. A total set that contained 11,278 and 15,328 protein-coding genes for C. vestalis and D. collaris, respectively, were predicted using evidence (homology-based and transcriptome-based) and de novo prediction methodology. Phylogenetic analysis showed that the braconid C. vestalis and the ichneumonid D. collaris diverged approximately 124 million years ago. These two wasps exhibit gene gains and losses that in some cases reflect their shared life history as parasitic wasps and in other cases are unique to particular species. Gene families with functions in development, nutrient acquisition from hosts, and metabolism have expanded in each wasp species, while genes required for biosynthesis of some amino acids and steroids have been lost, since these nutrients can be directly obtained from the host. Both wasp species encode a relative higher number of neprilysins (NEPs) thus far reported in arthropod genomes while several genes encoding immune-related proteins and detoxification enzymes were lost in both wasp genomes. Conclusions We present the annotated genome sequence of two parasitic wasps C. vestalis and D. collaris, which parasitize a common host, the diamondback moth, P. xylostella. These data will provide a fundamental source for studying the mechanism of host control and will be used in parasitoid comparative genomics to study the origin and diversification of the parasitic lifestyle.

Polydnaviruses (PDVs) are obligatory symbionts with parasitoid wasps. The PDV virions are produced solely in wasp (the primary host) calyx cells. They are injected into caterpillar hosts (the secondary host) during parasitoid oviposition, where they express irreplaceable actions to ensure survival and development of wasp larvae. Some of PDV gene products suppress host immune responses while others alter host growth, metabolism or endocrine system. Here, we treat new findings on PDV gene products and their action on immunity within secondary hosts.

Defensins are a class of small and diverse cysteine-rich proteins which have broad-spectrum antimicrobial activities. We identified and characterized a full-length cDNA encoding a putative defensin-like peptide from the whitefly Bemisia tabaci by RACE and quantitative real-time (qRT)-PCR. The full-length cDNA, named Btdef, was 388 bp long and contained an open reading frame of 228 bp. The putative mature Btdef had 46 amino acids with a molecular weight of 5.06 kDa. The deduced amino acid sequence showed significant homology with insect defensins from Heliothis virescens (76%) and Galleria mellonella (75%). The predicted mature form of Btdef was expressed as a recombinant peptide in Escherichia coli. Antimicrobial assays of the purified product indicated that Btdef was most active against fungi. qRT-PCR analyses indicated that Btdef mRNA was constitutively expressed in different tissues of B. tabaci, including fat body, midgut, ovaries and salivary gland, and was induced by fungal infection. Btdef mRNA expression was also significantly altered after feeding on different host plants, indicating that diet affects immune defences in B. tabaci. These results describe for the first time the basic properties of a defensin-like peptide from B. tabaci that probably plays an important role in the immune response against pathogens.

Here we completed the whole genome sequence of Cotesia vestalis bracovirus (CvBV) by deep sequencing and compared the genome features of CvBV to those of other polydnaviruses (PDVs). The genome is 540,215 base pairs divided into 35 genomic segments that range from 2.6 to 39.2 kb. Comparison of CvBV with other PDVs shows that more segments are found, including new segments that have no corresponding segments in other phylogenetically related PDVs, which suggests that there might be still more segments not being sequenced in the present known PDVs. We identified eight gene families and five genes in CvBV, including new genes which were first found in PDVs. Strikingly, we identified a putative helicase protein displaying similarity to human Pif1 helicase, which has never been reported for other PDVs. This finding will bring new insights in research of these special viruses.