Cargando…

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

SIMPLE SUMMARY: The dipteran parasitoid Tachinidae are important biocontrol agents and some of them are pests in sericulture. We previously have demonstrated that tachinid parasitoid Exorista japonica parasitism causes pupation defects in Bombyx mori. However, the underlying mechanism is not fully u...

Descripción completa

Detalles Bibliográficos
Autores principales: Dai, Minli, Yang, Jin, Liu, Xinyi, Gu, Haoyi, Li, Fanchi, Li, Bing, Wei, Jing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9506100/
https://www.ncbi.nlm.nih.gov/pubmed/36135493
http://dx.doi.org/10.3390/insects13090792
_version_ 1784796638732091392
author Dai, Minli
Yang, Jin
Liu, Xinyi
Gu, Haoyi
Li, Fanchi
Li, Bing
Wei, Jing
author_facet Dai, Minli
Yang, Jin
Liu, Xinyi
Gu, Haoyi
Li, Fanchi
Li, Bing
Wei, Jing
author_sort Dai, Minli
collection PubMed
description SIMPLE SUMMARY: The dipteran parasitoid Tachinidae are important biocontrol agents and some of them are pests in sericulture. We previously have demonstrated that tachinid parasitoid Exorista japonica parasitism causes pupation defects in Bombyx mori. However, the underlying mechanism is not fully understood. In this study, we performed transcriptome analysis of the fat body of B. mori parasitized by E. japonica. We found that the host basal metabolism was inhibited whereas the immune response was activated. These results indicate that the tachinid parasitoid perturbs the basal metabolism and activates the energetically costly immunity of the host, leading to the development arrest of the host. This study provides insights into how tachinid parasitoids modify host basal metabolism and immune response for the benefit of developing parasitoid larvae. ABSTRACT: The dipteran tachinid parasitoids are important biocontrol agents, and they must survive the harsh environment and rely on the resources of the host insect to complete their larval stage. We have previously demonstrated that the parasitism by the tachinid parasitoid Exorista japonica, a pest of the silkworm, causes pupation defects in Bombyx mori. However, the underlying mechanism is not fully understood. Here, we performed transcriptome analysis of the fat body of B. mori parasitized by E. japonica. We identified 1361 differentially expressed genes, with 394 genes up-regulated and 967 genes down-regulated. The up-regulated genes were mainly associated with immune response, endocrine system and signal transduction, whereas the genes related to basal metabolism, including energy metabolism, transport and catabolism, lipid metabolism, amino acid metabolism and carbohydrate metabolism were down-regulated, indicating that the host appeared to be in poor nutritional status but active in immune response. Moreover, by time-course gene expression analysis we found that genes related to amino acid synthesis, protein degradation and lipid metabolism in B. mori at later parasitization stages were inhibited. Antimicrobial peptides including Cecropin A, Gloverin and Moricin, and an immulectin, CTL11, were induced. These results indicate that the tachinid parasitoid perturbs the basal metabolism and induces the energetically costly immunity of the host, and thus leading to incomplete larval–pupal ecdysis of the host. This study provided insights into how tachinid parasitoids modify host basal metabolism and immune response for the benefit of developing parasitoid larvae.
format Online
Article
Text
id pubmed-9506100
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-95061002022-09-24 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 Insects Article SIMPLE SUMMARY: The dipteran parasitoid Tachinidae are important biocontrol agents and some of them are pests in sericulture. We previously have demonstrated that tachinid parasitoid Exorista japonica parasitism causes pupation defects in Bombyx mori. However, the underlying mechanism is not fully understood. In this study, we performed transcriptome analysis of the fat body of B. mori parasitized by E. japonica. We found that the host basal metabolism was inhibited whereas the immune response was activated. These results indicate that the tachinid parasitoid perturbs the basal metabolism and activates the energetically costly immunity of the host, leading to the development arrest of the host. This study provides insights into how tachinid parasitoids modify host basal metabolism and immune response for the benefit of developing parasitoid larvae. ABSTRACT: The dipteran tachinid parasitoids are important biocontrol agents, and they must survive the harsh environment and rely on the resources of the host insect to complete their larval stage. We have previously demonstrated that the parasitism by the tachinid parasitoid Exorista japonica, a pest of the silkworm, causes pupation defects in Bombyx mori. However, the underlying mechanism is not fully understood. Here, we performed transcriptome analysis of the fat body of B. mori parasitized by E. japonica. We identified 1361 differentially expressed genes, with 394 genes up-regulated and 967 genes down-regulated. The up-regulated genes were mainly associated with immune response, endocrine system and signal transduction, whereas the genes related to basal metabolism, including energy metabolism, transport and catabolism, lipid metabolism, amino acid metabolism and carbohydrate metabolism were down-regulated, indicating that the host appeared to be in poor nutritional status but active in immune response. Moreover, by time-course gene expression analysis we found that genes related to amino acid synthesis, protein degradation and lipid metabolism in B. mori at later parasitization stages were inhibited. Antimicrobial peptides including Cecropin A, Gloverin and Moricin, and an immulectin, CTL11, were induced. These results indicate that the tachinid parasitoid perturbs the basal metabolism and induces the energetically costly immunity of the host, and thus leading to incomplete larval–pupal ecdysis of the host. This study provided insights into how tachinid parasitoids modify host basal metabolism and immune response for the benefit of developing parasitoid larvae. MDPI 2022-08-31 /pmc/articles/PMC9506100/ /pubmed/36135493 http://dx.doi.org/10.3390/insects13090792 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Dai, Minli
Yang, Jin
Liu, Xinyi
Gu, Haoyi
Li, Fanchi
Li, Bing
Wei, Jing
Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori
title Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori
title_full Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori
title_fullStr Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori
title_full_unstemmed Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori
title_short Parasitism by the Tachinid Parasitoid Exorista japonica Leads to Suppression of Basal Metabolism and Activation of Immune Response in the Host Bombyx mori
title_sort parasitism by the tachinid parasitoid exorista japonica leads to suppression of basal metabolism and activation of immune response in the host bombyx mori
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9506100/
https://www.ncbi.nlm.nih.gov/pubmed/36135493
http://dx.doi.org/10.3390/insects13090792
work_keys_str_mv AT daiminli parasitismbythetachinidparasitoidexoristajaponicaleadstosuppressionofbasalmetabolismandactivationofimmuneresponseinthehostbombyxmori
AT yangjin parasitismbythetachinidparasitoidexoristajaponicaleadstosuppressionofbasalmetabolismandactivationofimmuneresponseinthehostbombyxmori
AT liuxinyi parasitismbythetachinidparasitoidexoristajaponicaleadstosuppressionofbasalmetabolismandactivationofimmuneresponseinthehostbombyxmori
AT guhaoyi parasitismbythetachinidparasitoidexoristajaponicaleadstosuppressionofbasalmetabolismandactivationofimmuneresponseinthehostbombyxmori
AT lifanchi parasitismbythetachinidparasitoidexoristajaponicaleadstosuppressionofbasalmetabolismandactivationofimmuneresponseinthehostbombyxmori
AT libing parasitismbythetachinidparasitoidexoristajaponicaleadstosuppressionofbasalmetabolismandactivationofimmuneresponseinthehostbombyxmori
AT weijing parasitismbythetachinidparasitoidexoristajaponicaleadstosuppressionofbasalmetabolismandactivationofimmuneresponseinthehostbombyxmori