Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and Metabolomics

In this study, we selected <i>Sitona callosus</i>, one of the primary insect pests of alfalfa, as the experimental insect and infected it with <i>Beauveria bassiana</i>. Transcriptomic and metabolomic analyses were conducted to explore alterations in gene expression and metab...

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Main Authors: Nan Li, Xin Gu, Ming Xin, Xinpu Wang
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Insects
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Online Access:https://www.mdpi.com/2075-4450/15/12/940
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author Nan Li
Xin Gu
Ming Xin
Xinpu Wang
author_facet Nan Li
Xin Gu
Ming Xin
Xinpu Wang
author_sort Nan Li
collection DOAJ
description In this study, we selected <i>Sitona callosus</i>, one of the primary insect pests of alfalfa, as the experimental insect and infected it with <i>Beauveria bassiana</i>. Transcriptomic and metabolomic analyses were conducted to explore alterations in gene expression and metabolic processes in <i>S. callosus</i> at 48, 96, and 144 h post infection with <i>B. bassiana</i>. The transcriptomic analysis unveiled that <i>B. bassiana</i> infection boosted immune responses in tubercula, affecting carbohydrate metabolism, cytochrome P450 activity, lysosome function, apoptosis regulation, phagosome formation, glutathione metabolism, amino acid metabolism, and pathogen response pathways. Subsequent metabolomics analysis confirmed that glycerophospholipids, carboxylic acids and derivatives, organooxygen compounds, keto acids and derivatives, and azane immune metabolites were significantly upregulated in response to <i>B. bassiana</i> infection. Additionally, we utilized the Pearson correlation coefficient method to examine the relationships between differentially expressed immune-related genes and metabolites, revealing notably strong correlations between these two sets of variables. By leveraging the WGCNA method to analyze immune metabolite data for immune-related genes, we identified hub genes crucial at various stages of immune activation. These central genes predominantly included C-type lectin receptors for pattern recognition, cytochrome P450 enzymes linked to detoxification processes, and cathepsin proteases. By combining transcriptome and metabolome analyses, it was determined that autophagy and arachidonic acid metabolism play significant roles in the response of <i>S. callosus</i> to infection by <i>B. bassiana</i>. This research will facilitate the understanding of the immune response to <i>B. bassiana</i> infection in adult <i>S. callosus</i>, laying a theoretical groundwork for future biological control strategies targeting <i>S. callosus</i>.
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spelling doaj-art-15fc1df067fa4bd3b7810ce12f71b63c2025-08-20T02:00:38ZengMDPI AGInsects2075-44502024-11-01151294010.3390/insects15120940Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and MetabolomicsNan Li0Xin Gu1Ming Xin2Xinpu Wang3School of Forestry and Prataculture, Ningxia University, Yinchuan 750021, ChinaSchool of Agriculture, Ningxia University, Yinchuan 750021, ChinaSchool of Agriculture, Ningxia University, Yinchuan 750021, ChinaSchool of Agriculture, Ningxia University, Yinchuan 750021, ChinaIn this study, we selected <i>Sitona callosus</i>, one of the primary insect pests of alfalfa, as the experimental insect and infected it with <i>Beauveria bassiana</i>. Transcriptomic and metabolomic analyses were conducted to explore alterations in gene expression and metabolic processes in <i>S. callosus</i> at 48, 96, and 144 h post infection with <i>B. bassiana</i>. The transcriptomic analysis unveiled that <i>B. bassiana</i> infection boosted immune responses in tubercula, affecting carbohydrate metabolism, cytochrome P450 activity, lysosome function, apoptosis regulation, phagosome formation, glutathione metabolism, amino acid metabolism, and pathogen response pathways. Subsequent metabolomics analysis confirmed that glycerophospholipids, carboxylic acids and derivatives, organooxygen compounds, keto acids and derivatives, and azane immune metabolites were significantly upregulated in response to <i>B. bassiana</i> infection. Additionally, we utilized the Pearson correlation coefficient method to examine the relationships between differentially expressed immune-related genes and metabolites, revealing notably strong correlations between these two sets of variables. By leveraging the WGCNA method to analyze immune metabolite data for immune-related genes, we identified hub genes crucial at various stages of immune activation. These central genes predominantly included C-type lectin receptors for pattern recognition, cytochrome P450 enzymes linked to detoxification processes, and cathepsin proteases. By combining transcriptome and metabolome analyses, it was determined that autophagy and arachidonic acid metabolism play significant roles in the response of <i>S. callosus</i> to infection by <i>B. bassiana</i>. This research will facilitate the understanding of the immune response to <i>B. bassiana</i> infection in adult <i>S. callosus</i>, laying a theoretical groundwork for future biological control strategies targeting <i>S. callosus</i>.https://www.mdpi.com/2075-4450/15/12/940<i>Beauveria bassiana</i><i>Sitona callosus</i>RNA-Seqmetabolomicsimmune response
spellingShingle Nan Li
Xin Gu
Ming Xin
Xinpu Wang
Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and Metabolomics
Insects
<i>Beauveria bassiana</i>
<i>Sitona callosus</i>
RNA-Seq
metabolomics
immune response
title Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and Metabolomics
title_full Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and Metabolomics
title_fullStr Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and Metabolomics
title_full_unstemmed Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and Metabolomics
title_short Revealing the Immune Response of <i>Sitona callosus</i> Gyllenhal to Entomopathogenic Fungi <i>Beauveria bassiana</i> Infection Through Integrative Analyses of Transcriptomics and Metabolomics
title_sort revealing the immune response of i sitona callosus i gyllenhal to entomopathogenic fungi i beauveria bassiana i infection through integrative analyses of transcriptomics and metabolomics
topic <i>Beauveria bassiana</i>
<i>Sitona callosus</i>
RNA-Seq
metabolomics
immune response
url https://www.mdpi.com/2075-4450/15/12/940
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