Induction of stress‐ and immune‐associated genes in the Indian meal moth Plodia interpunctella against envenomation by the ectoparasitoid Bracon hebetor
Abstract:Envenomation is an important process in parasitism by parasitic wasps; it suppresses the immune and development of host insects. However, the molecular mechanisms of host responses to envenomation are not yet clear. This study aimed to determine the transcription-level responses of the Indian meal moth Plodia interpunctella against envenomation of the ectoparasitoid Bracon hebetor. Quantitative real-time reverse-transcription PCR was used to determine the transcriptional changes of 13 selected genes, which are… Show more
“…For example, Cotesia flavipes influences host metabolism by enhancing the activity of amylase and trehalase in the host Diatraea saccharalis (Rossi et al ., 2014). In contrast, envenomation by the ectoparasitoid Bracon hebetor downregulates the transcription levels of several genes associated with metabolism in the host Plodia interpunctella (Shafeeq et al ., 2017). In a similar investigation into Habrobracon hebetor , researchers measured a significant decline in carbohydrate metabolism in parasitized Pyrrhocoris apterus by monitoring carbon dioxide production (Shaik et al ., 2017).…”
To achieve successful development, female parasitoids, while laying eggs, introduce various virulence factors, mainly venoms, into host insects to manipulate their physiology. Although numerous studies have been conducted to characterize the components of venoms that regulate host immune responses, few systematic investigations have been conducted on the roles of venom proteins in host metabolic regulation. In this investigation, we characterized a novel venom protein in Pachycrepoideus vindemiae called glucose‐6‐phosphate dehydrogenase (PvG6PDH) and showed it has a vital role in regulating host carbohydrate metabolism. PvG6PDH encodes 510 amino acids and features a signal peptide and two conserved “G6PDH” domains. Multiple sequence alignment showed it has high amino acid identity with G6PDH from other pteromalids, and quantitative polymerase chain reaction analysis and immunofluorescent staining demonstrated a significantly higher expression of PvG6PDH in the venom apparatus compared with the carcass. We report that PvG6PDH contributes to parasitism by inhibiting the glucose‐6‐phosphate (G6P) metabolism of host Drosophila melanogaster, as demonstrated by PvG6PDH injection and RNA interference analysis. Further tests revealed that the accumulation of host G6P was caused by the transcriptional inhibition of G6P‐metabolism‐related genes. These findings greatly contribute to our understanding of venom‐mediated host metabolic regulation, further laying the foundation for the development of venom proteins as biological agents for pest control.
“…For example, Cotesia flavipes influences host metabolism by enhancing the activity of amylase and trehalase in the host Diatraea saccharalis (Rossi et al ., 2014). In contrast, envenomation by the ectoparasitoid Bracon hebetor downregulates the transcription levels of several genes associated with metabolism in the host Plodia interpunctella (Shafeeq et al ., 2017). In a similar investigation into Habrobracon hebetor , researchers measured a significant decline in carbohydrate metabolism in parasitized Pyrrhocoris apterus by monitoring carbon dioxide production (Shaik et al ., 2017).…”
To achieve successful development, female parasitoids, while laying eggs, introduce various virulence factors, mainly venoms, into host insects to manipulate their physiology. Although numerous studies have been conducted to characterize the components of venoms that regulate host immune responses, few systematic investigations have been conducted on the roles of venom proteins in host metabolic regulation. In this investigation, we characterized a novel venom protein in Pachycrepoideus vindemiae called glucose‐6‐phosphate dehydrogenase (PvG6PDH) and showed it has a vital role in regulating host carbohydrate metabolism. PvG6PDH encodes 510 amino acids and features a signal peptide and two conserved “G6PDH” domains. Multiple sequence alignment showed it has high amino acid identity with G6PDH from other pteromalids, and quantitative polymerase chain reaction analysis and immunofluorescent staining demonstrated a significantly higher expression of PvG6PDH in the venom apparatus compared with the carcass. We report that PvG6PDH contributes to parasitism by inhibiting the glucose‐6‐phosphate (G6P) metabolism of host Drosophila melanogaster, as demonstrated by PvG6PDH injection and RNA interference analysis. Further tests revealed that the accumulation of host G6P was caused by the transcriptional inhibition of G6P‐metabolism‐related genes. These findings greatly contribute to our understanding of venom‐mediated host metabolic regulation, further laying the foundation for the development of venom proteins as biological agents for pest control.
“…We suppressed the CmHem expression by RNAi, and the mature larvae could not pupate normally. Further, Plodia interpunctella hemolin is expressed only in epidermis, suggesting its functional association with metamorphosis ( Aye et al, 2008 ; Shafeeq, Ulabdin & Lee, 2017 ). The proteomic analysis of hemolymph proteins during larva-to-pupal metamorphosis of B. mori further supports the functional role of hemolin in the metamorphosis process, as many immune-associated proteins, including hemolin, were found to be related to metamorphosis ( Hou et al, 2010 ).…”
Background
As a member of the immunoglobulin superfamily, hemolins play a vital role in insect development and defense against pathogens. However, the innate immune response of hemolin to baculovirus infection varies among different insects.
Methods and results
In this study, the hemolin-like gene from a Crambidae insect, Cnaphalocrocis medinalis, CmHem was cloned, and its role in insect development and baculovirus infection was analyzed. A 1,528 bp contig as potential hemolin-like gene of C. medinalis was reassembled from the transcriptome. Further, the complete hemolin sequence of C. medinalis (CmHem) was cloned and sequenced. The cDNA of CmHem was 1,515 bp in length and encoded 408 amino acids. The deduced amino acid of CmHem has relatively low identities (41.9–62.3%) to various insect hemolins. However, it contains four Ig domains similarity to other insect hemolins. The expression level of CmHem was the highest in eggs, followed by pupae and adults, and maintained a low expression level at larval stage. The synthesized siRNAs were injected into mature larvae, and the CmHem transcription decreased by 51.7%. Moreover, the abdominal somites of larvae became straightened, could not pupate normally, and then died. Infection with a baculovirus, C. medinalis granulovirus (CnmeGV), the expression levels of CmHem in the midgut and fat body of C. medinalis significantly increased at 12 and 24 h, respectively, and then soon returned to normal levels.
Conclusions
Our results suggested that hemolin may be related to the metamorphosis of C. medinalis. Exposure to baculovirus induced the phased expression of hemolin gene in the midgut and fat body of C. medinalis, indicated that hemolin involved in the immune recognition of Crambidae insects to baculovirus.
“…Venom of H. hebetor , or its envenomation, has been shown to play a crucial role in manipulating the physiological processes of paralyzed host larvae. This includes actions such as blocking neuromuscular transmission [ 27 , 28 , 29 ]; changing the level of adipokinetic hormone [ 30 , 31 ]; inducing the expression of stress- and immune-associated genes [ 32 , 33 ]; inhibiting eicosanoid biosynthesis, leading to increased oxidative stress [ 34 ]; altering the midgut bacterial community [ 35 ]; and suppressing immunity through the inhibition of phenoloxidase activity, as well as a reduction in hemocyte encapsulation [ 36 ]. In addition, venom of H. hebetor has been found to exhibit anti-inflammatory properties by inhibiting nitric oxide production and reducing the levels of proinflammatory mediators and cytokines through modulation of the nuclear factor kappa B and mitogen-activated protein kinase pathways [ 37 ].…”
The ectoparasitoid Habrobracon hebetor (Hymenoptera: Braconidae) exhibits a broad parasitic capability towards various lepidopteran pests, with venom serving as a crucial virulent factor ensuring successful parasitization and subsequent host mortality. Analyzing the constituents of its venom is essential for elucidating the mechanisms underlying efficient host killing by this parasitoid and for exploring potentially functional venom proteins. Through a transcriptomic analysis, a total of 34 venom proteins were identified within the venom of H. hebetor, encompassing known components such as serine protease, metalloproteinase, esterase, and serine protease inhibitors commonly present in parasitoid venoms. Unique components like paralytic protein and ion transport peptide-like were identified, possibly specific to certain parasitoids, along with novel proteins with uncharacterized functions. Spatial gene expression profiling of the identified venom proteins using transcriptomic data, corroborated by quantitative PCR validation for 13 randomly selected proteins, revealed abundant expression levels in the venom apparatus, affirming them as genuine venom components. Notably, the paralytic protein exhibited prominent expression, with the highest FPKM (fragments per kilobase of transcript per million fragments mapped) value of 24,704.87 in the venom apparatus, indicative of its significant role in successful parasitism by H. hebetor. The identification of these venom proteins establishes a foundation for the further exploration of bioactive agents for pest management strategies.
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