Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori

Dai, Minli; Yang, Jin; Liu, Xinyi; Gu, Haoyi; Li, Fanchi; Li, Bing; Wei, Jing

doi:10.3390/insects13090792

Cited by 12 publications

(12 citation statements)

References 53 publications

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“…Additionally, scavenger receptors and hemocytins were highlighted after M. manilae parasitization. This result resonated with the findings that wasp parasitism perturbed the expressions of the genes implicated in the host humoral immune response [ 68 , 69 , 70 ]. We randomly selected several immune-related DEGs for qPCR verification, which showed a similar trend in expression patterns with the high throughput sequencing data in response to wasp parasitization.…”

Section: Discussionsupporting

confidence: 77%

Host Transcriptome Analysis of Spodoptera frugiperda Larvae Parasitized by Microplitis manilae

Gulinuer

Xing

Yang

2023

Insects

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It has been extensively found that parasitoids manipulate host physiology to benefit the survival and development of their offspring. However, the underlying regulatory mechanisms have not received much attention. To reveal the effects of parasitization of the larval solitary endoparasitoid Microplitis manilae (Hymenoptera: Braconidae) on host Spodoptera frugiperda (Lepidoptera: Noctuidae), one of the most destructive agricultural pests in China, deep-sequencing-based transcriptome analysis was conducted to compare the host gene expression levels after 2 h, 24 h, and 48 h parasitization. A total of 1861, 962, and 108 differentially expressed genes (DEGs) were obtained from the S. frugiperda larvae at 2 h, 24 h, and 48 h post-parasitization, respectively, compared with unparasitized controls. The changes in host gene expressions were most likely caused by the injection of wasp parasitic factors, including PDVs, that were injected along with the eggs during oviposition. Based on the functional annotations in GO and KEGG databases, we revealed that most DEGs were implicated in host metabolism and immunity. Further analysis of the common DEGs in three comparisons between the unparasitized and parasitized groups identified four genes, including one unknown and three prophenoloxidase (PPO) genes. Moreover, 46 and 7 common DEGs involved in host metabolism and immunity were identified at two or three time points after parasitization, respectively. Among these, most DEGs showed increased expressions at 2 h post-wasp parasitization while exhibiting significantly decreased expression levels at 24 h post-parasitization, demonstrating the expression regulations of M. manilae parasitization on host metabolism and immune-related genes. Further qPCR verification in 20 randomly selected DEGs confirmed the accuracy and reproducibility of the gene expression profiles generated from RNA-seq. This study reveals the molecular regulatory network about how host insects respond to wasp parasitism, laying a solid foundation for revealing the physiological manipulation of wasp parasitization on host insects, which facilitates the development of biological control practices for parasitoids.

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Section: Discussionsupporting

confidence: 77%

Host Transcriptome Analysis of Spodoptera frugiperda Larvae Parasitized by Microplitis manilae

Gulinuer

Xing

Yang

2023

Insects

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“…Drosophila melanogaster can activate humoral immunity and upregulate the expressions of AMPs and stress proteins against parasitoid wasps (Benassi et al, 2000; Yang et al, 2019). Previous studies have shown that when E. japonica parasitizes the silkworm, the AMPs of the silkworm fat body are significantly upregulated (M. Dai et al, 2022; M. L. Dai et al, 2022). This study found that the expressions of AMPs in the midgut of the silkworm were upregulated and then downregulated from the 1st to the 3rd day of parasitism, indicating that the midgut immunity of the silkworm was activated at the initial stage of parasitism, actively resisting the invasion of E. japonica .…”

Section: Discussionmentioning

confidence: 99%

“…The variety of silkworms used in the present study was “Jingsong × Haoyue,” which was kept by our laboratory. The tachinid E. japonica was bred in our laboratory for generations (M. Dai et al, 2022; M. L. Dai et al, 2022). It will parasitize on the 1st day of the fifth instar of the silkworm.…”

Section: Methodsmentioning

confidence: 99%

Tachinid parasitoid Exorista japonica affects the utilization of diet by changing gut microbial composition in the silkworm, Bombyx mori

Zhu

Dai

et al. 2023

Arch Insect Biochem Physiol

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Changes in both intake and digestion of feed have been demonstrated in the host following parasitization. However, its regulatory mechanism has not been clarified. In this study, silkworms and Exorista japonica were used as research objects to analyze the effect of parasitism on the midgut immune system of the silkworm. After being parasitized, the expressions of antimicrobial peptide (AMP) genes of silkworms showed a fluctuating trend of first upregulation and then downregulation, while phenoloxidase and lysozyme activities were inhibited. To study the possible impact of the downregulation of AMP genes on intestinal microorganisms, the characteristics of the intestinal microbial population of silkworms on the third day of parasitism were analyzed. The relative abundance of Firmicutes, Proteobacteria, and Bacteroidota decreased, while that of Actinobacteriota increased. The increased abundance of conditionally pathogenic bacteria Serratia and Staphylococcus might lead to a decrease in the amount of silkworm ingestion. Meanwhile, the abundance of Acinetobacter, Bacillus, Pseudomonas, and Enterobacter promotes an increase in the digestion of nutrients. This study indicated that the imbalance of intestinal microbial homeostasis caused by parasitism may affect the absorption and digestion of nutrients by the host. Collectively, our findings provided a new clue for further exploring the mechanism of nutrient transport among the host, parasitoid, and intestinal microorganisms.

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“…The tachinid parasitoids Exorista japonica (Diptera: Tachinidae), E. sorbillans and Blepharipa zebina (Diptera: Tachinidae) are major larval endoparasites of B. mori and Antheraea pernyi (Lepidoptera: Saturniidae) , causing severe damage to sericulture industry (Dindo & Nakamura, 2018;Jayaram et al, 2014;Rath & Sinha, 2005). We have previously demonstrated that the larval development of B. mori is accelerated, and the expression of NOS in B. mori is up-regulated by E. japonica parasitism (Dai, Yang, et al, 2022;Dai, Ye, et al, 2022), suggesting that NO might be involved in host development, which provides us a good system to study the role of NO in the host under the parasitoid stress. In this study, the effects of E. sorbillans parasitism on host NO production and the role of host NO in E. sorbillans development were investigated.…”

Section: Introductionmentioning

confidence: 99%

A parasitoid regulates 20E synthesis and antibacterial activity of the host for development by inducing host nitric oxide production

Dai,

Jiang,

et al. 2024

Insect Molecular Biology

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Parasitoids are important components of the natural enemy guild in the biological control of insect pests. They depend on host resources to complete the development of a specific stage or whole life cycle and thus have evolved towards optimal host exploitation strategies. In the present study, we report a specific survival strategy of a fly parasitoid Exorista sorbillans (Diptera: Tachinidae), which is a potential biological control agent for agricultural pests and a pest in sericulture. We found that the expression levels of nitric oxide synthase (NOS) and nitric oxide (NO) production in host Bombyx mori (Lepidoptera: Bombycidae) were increased after E. sorbillans infection. Reducing NOS expression and NO production with an NOS inhibitor (NG‐nitro‐L‐arginine methyl ester hydrochloride) in infected B. mori significantly impeded the growth of E. sorbillans larvae. Moreover, the biosynthesis of 20‐hydroxyecdysone (20E) in infected hosts was elevated with increasing NO production, and inhibiting NOS expression lowered 20E biosynthesis. More importantly, induced NO synthesis was required to eliminate intracellular bacterial pathogens that presumably competed for shared host resources. Inhibiting NOS expression down‐regulated the transcription of antimicrobial peptide genes and increased the number of bacteria in parasitized hosts. Collectively, this study revealed a new perspective on the role of NO in host–parasitoid interactions and a novel mechanism for parasitoid regulation of host physiology to support its development.

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Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori

Cited by 12 publications

References 53 publications

Host Transcriptome Analysis of Spodoptera frugiperda Larvae Parasitized by Microplitis manilae

Host Transcriptome Analysis of Spodoptera frugiperda Larvae Parasitized by Microplitis manilae

Tachinid parasitoid Exorista japonica affects the utilization of diet by changing gut microbial composition in the silkworm, Bombyx mori

A parasitoid regulates 20E synthesis and antibacterial activity of the host for development by inducing host nitric oxide production

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