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Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta

SIMPLE SUMMARY: The red imported fire ant (Solenopsis invicta) is a highly invasive pest that causes significant damage to human health, agriculture, and biodiversity. Microbial insecticides have been identified as effective and promising alternatives for pest control. However, their efficacy is lim...

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Autores principales: Wu, Hongxin, Xu, Yating, Zafar, Junaid, Mandal, Surajit De, Lin, Liangjie, Lu, Yongyue, Jin, Fengliang, Pang, Rui, Xu, Xiaoxia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10455567/
https://www.ncbi.nlm.nih.gov/pubmed/37623411
http://dx.doi.org/10.3390/insects14080701
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author Wu, Hongxin
Xu, Yating
Zafar, Junaid
Mandal, Surajit De
Lin, Liangjie
Lu, Yongyue
Jin, Fengliang
Pang, Rui
Xu, Xiaoxia
author_facet Wu, Hongxin
Xu, Yating
Zafar, Junaid
Mandal, Surajit De
Lin, Liangjie
Lu, Yongyue
Jin, Fengliang
Pang, Rui
Xu, Xiaoxia
author_sort Wu, Hongxin
collection PubMed
description SIMPLE SUMMARY: The red imported fire ant (Solenopsis invicta) is a highly invasive pest that causes significant damage to human health, agriculture, and biodiversity. Microbial insecticides have been identified as effective and promising alternatives for pest control. However, their efficacy is limited by the host’s immune system. In this study, we utilized RNA sequencing technology and bioinformatics methods to investigate gene expression changes in S. invicta infected with Metarhizium anisopliae at different time points (0, 6, 24, and 48 h). We identified 33 differentially expressed immune-related genes and constructed illustrative Toll and Imd signaling pathways diagrams. Our findings revealed that M. anisopliae suppresses the immune gene expression of S. invicta during the early stages of infection while inducing upregulation in the later stages. This suggests the potential of M. anisopliae as a potent biopesticide for controlling S. invicta populations. Overall, these findings provide a foundation for further understanding the immune mechanisms of S. invicta and its molecular response to M. anisopliae. ABSTRACT: The red imported fire ant (Solenopsis invicta Buren, 1972) is a globally significant invasive species, causing extensive agricultural, human health, and biodiversity damage amounting to billions of dollars worldwide. The pathogenic fungus Metarhizium anisopliae (Metchnikoff) Sorokin (1883), widely distributed in natural environments, has been used to control S. invicta populations. However, the interaction between M. anisopliae and the immune system of the social insect S. invicta remains poorly understood. In this study, we employed RNA-seq to investigate the effects of M. anisopliae on the immune systems of S. invicta at different time points (0, 6, 24, and 48 h). A total of 1313 differentially expressed genes (DEGs) were identified and classified into 12 expression profiles using short time-series expression miner (STEM) for analysis. Weighted gene co-expression network analysis (WGCNA) was employed to partition all genes into 21 gene modules. Upon analyzing the statistically significant WGCNA model and conducting Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis on the modules, we identified key immune pathways, including the Toll and Imd signaling pathways, lysosomes, autophagy, and phagosomes, which may collectively contribute to S. invicta defense against M. anisopliae infection. Subsequently, we conducted a comprehensive scan of all differentially expressed genes and identified 33 immune-related genes, encompassing various aspects such as recognition, signal transduction, and effector gene expression. Furthermore, by integrating the significant gene modules derived from the WGCNA analysis, we constructed illustrative pathway diagrams depicting the Toll and Imd signaling pathways. Overall, our research findings demonstrated that M. anisopliae suppressed the immune response of S. invicta during the early stages while stimulating its immune response at later stages, making it a potential biopesticide for controlling S. invicta populations. These discoveries lay the foundation for further understanding the immune mechanisms of S. invicta and the molecular mechanisms underlying its response to M. anisopliae.
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spelling pubmed-104555672023-08-26 Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta Wu, Hongxin Xu, Yating Zafar, Junaid Mandal, Surajit De Lin, Liangjie Lu, Yongyue Jin, Fengliang Pang, Rui Xu, Xiaoxia Insects Article SIMPLE SUMMARY: The red imported fire ant (Solenopsis invicta) is a highly invasive pest that causes significant damage to human health, agriculture, and biodiversity. Microbial insecticides have been identified as effective and promising alternatives for pest control. However, their efficacy is limited by the host’s immune system. In this study, we utilized RNA sequencing technology and bioinformatics methods to investigate gene expression changes in S. invicta infected with Metarhizium anisopliae at different time points (0, 6, 24, and 48 h). We identified 33 differentially expressed immune-related genes and constructed illustrative Toll and Imd signaling pathways diagrams. Our findings revealed that M. anisopliae suppresses the immune gene expression of S. invicta during the early stages of infection while inducing upregulation in the later stages. This suggests the potential of M. anisopliae as a potent biopesticide for controlling S. invicta populations. Overall, these findings provide a foundation for further understanding the immune mechanisms of S. invicta and its molecular response to M. anisopliae. ABSTRACT: The red imported fire ant (Solenopsis invicta Buren, 1972) is a globally significant invasive species, causing extensive agricultural, human health, and biodiversity damage amounting to billions of dollars worldwide. The pathogenic fungus Metarhizium anisopliae (Metchnikoff) Sorokin (1883), widely distributed in natural environments, has been used to control S. invicta populations. However, the interaction between M. anisopliae and the immune system of the social insect S. invicta remains poorly understood. In this study, we employed RNA-seq to investigate the effects of M. anisopliae on the immune systems of S. invicta at different time points (0, 6, 24, and 48 h). A total of 1313 differentially expressed genes (DEGs) were identified and classified into 12 expression profiles using short time-series expression miner (STEM) for analysis. Weighted gene co-expression network analysis (WGCNA) was employed to partition all genes into 21 gene modules. Upon analyzing the statistically significant WGCNA model and conducting Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis on the modules, we identified key immune pathways, including the Toll and Imd signaling pathways, lysosomes, autophagy, and phagosomes, which may collectively contribute to S. invicta defense against M. anisopliae infection. Subsequently, we conducted a comprehensive scan of all differentially expressed genes and identified 33 immune-related genes, encompassing various aspects such as recognition, signal transduction, and effector gene expression. Furthermore, by integrating the significant gene modules derived from the WGCNA analysis, we constructed illustrative pathway diagrams depicting the Toll and Imd signaling pathways. Overall, our research findings demonstrated that M. anisopliae suppressed the immune response of S. invicta during the early stages while stimulating its immune response at later stages, making it a potential biopesticide for controlling S. invicta populations. These discoveries lay the foundation for further understanding the immune mechanisms of S. invicta and the molecular mechanisms underlying its response to M. anisopliae. MDPI 2023-08-11 /pmc/articles/PMC10455567/ /pubmed/37623411 http://dx.doi.org/10.3390/insects14080701 Text en © 2023 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
Wu, Hongxin
Xu, Yating
Zafar, Junaid
Mandal, Surajit De
Lin, Liangjie
Lu, Yongyue
Jin, Fengliang
Pang, Rui
Xu, Xiaoxia
Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta
title Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta
title_full Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta
title_fullStr Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta
title_full_unstemmed Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta
title_short Transcriptomic Analysis Reveals the Impact of the Biopesticide Metarhizium anisopliae on the Immune System of Major Workers in Solenopsis invicta
title_sort transcriptomic analysis reveals the impact of the biopesticide metarhizium anisopliae on the immune system of major workers in solenopsis invicta
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10455567/
https://www.ncbi.nlm.nih.gov/pubmed/37623411
http://dx.doi.org/10.3390/insects14080701
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