RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infection

The brown planthopper (BPH), Nilaparvata lugens, is the most devastating insect pest of rice. Biological control with fungal entomopathogens is an attractive alternative to chemical pesticides for controlling BPH. However, the efficacy of fungal bioagents is often limited by the immune defense respo...

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Main Authors: Zhu-Long Shao, Chen-Ping Lan, Xiao-Ping Yu, Zheng-Liang Wang
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Biological Control
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Online Access:http://www.sciencedirect.com/science/article/pii/S1049964425000817
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author Zhu-Long Shao
Chen-Ping Lan
Xiao-Ping Yu
Zheng-Liang Wang
author_facet Zhu-Long Shao
Chen-Ping Lan
Xiao-Ping Yu
Zheng-Liang Wang
author_sort Zhu-Long Shao
collection DOAJ
description The brown planthopper (BPH), Nilaparvata lugens, is the most devastating insect pest of rice. Biological control with fungal entomopathogens is an attractive alternative to chemical pesticides for controlling BPH. However, the efficacy of fungal bioagents is often limited by the immune defense responses of host insects. Toll-like receptors (TLRs) are a family of crucial pattern recognition proteins that are responsible for the immunologic recognition of invading pathogen in insects. Here, we demonstrated that the suppression of a key TLR-encoding gene NlToll1 in BPH through RNA interference (RNAi) could significantly improve the insecticidal efficacy of an entomopathogenic fungus Metarhizium anisopliae. The open reading frame (ORF) of NlToll1 was 3351 bp in length encoding a 126.7 kDa protein with a typical intracellular Toll/interleukin-1 receptor (TIR) domain, two transmembrane domains and 14 extracellular leucine-rich repeats (LRRs). The qRT-PCR results showed that the expression of NlToll1 had obvious spatiotemporal preferences and strongly induced by topical infection with M. anisopliae. Silencing of NlToll1 using RNAi led to a significantly reduced survival rate and an increased susceptibility of BPH fifth-instar nymphs to fungal infection, which might be partially owing to the immunosuppressive effects by repressing expression of antimicrobial peptide genes and the dysbiosis of gut bacterial community caused by NlToll1 silencing. Our results manifested that the combination use of RNAi and fungal entomopathogens would be an effective avenue for exploiting pesticide-free BPH management strategies.
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spelling doaj-art-f799bb3c88e64fc6bade89bb09c1a10b2025-08-20T03:48:47ZengElsevierBiological Control1049-96442025-06-0120510577110.1016/j.biocontrol.2025.105771RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infectionZhu-Long Shao0Chen-Ping Lan1Xiao-Ping Yu2Zheng-Liang Wang3Zhejiang Provincial Key Laboratory of Biometrology and Inspection and Quarantine, College of Life Sciences, China Jiliang University, Hangzhou 310018, China; Key Laboratory of Microbiological Metrology, Measurement and Bio-product Quality Security (State Administration for Market Regulation), China Jiliang University, Hangzhou 310018, ChinaZhejiang Provincial Key Laboratory of Biometrology and Inspection and Quarantine, College of Life Sciences, China Jiliang University, Hangzhou 310018, China; Key Laboratory of Microbiological Metrology, Measurement and Bio-product Quality Security (State Administration for Market Regulation), China Jiliang University, Hangzhou 310018, ChinaZhejiang Provincial Key Laboratory of Biometrology and Inspection and Quarantine, College of Life Sciences, China Jiliang University, Hangzhou 310018, China; Key Laboratory of Microbiological Metrology, Measurement and Bio-product Quality Security (State Administration for Market Regulation), China Jiliang University, Hangzhou 310018, ChinaZhejiang Provincial Key Laboratory of Biometrology and Inspection and Quarantine, College of Life Sciences, China Jiliang University, Hangzhou 310018, China; Key Laboratory of Microbiological Metrology, Measurement and Bio-product Quality Security (State Administration for Market Regulation), China Jiliang University, Hangzhou 310018, China; Corresponding author at: Zhejiang Provincial Key Laboratory of Biometrology and Inspection and Quarantine, College of Life Sciences, China Jiliang University, Hangzhou 310018, China.The brown planthopper (BPH), Nilaparvata lugens, is the most devastating insect pest of rice. Biological control with fungal entomopathogens is an attractive alternative to chemical pesticides for controlling BPH. However, the efficacy of fungal bioagents is often limited by the immune defense responses of host insects. Toll-like receptors (TLRs) are a family of crucial pattern recognition proteins that are responsible for the immunologic recognition of invading pathogen in insects. Here, we demonstrated that the suppression of a key TLR-encoding gene NlToll1 in BPH through RNA interference (RNAi) could significantly improve the insecticidal efficacy of an entomopathogenic fungus Metarhizium anisopliae. The open reading frame (ORF) of NlToll1 was 3351 bp in length encoding a 126.7 kDa protein with a typical intracellular Toll/interleukin-1 receptor (TIR) domain, two transmembrane domains and 14 extracellular leucine-rich repeats (LRRs). The qRT-PCR results showed that the expression of NlToll1 had obvious spatiotemporal preferences and strongly induced by topical infection with M. anisopliae. Silencing of NlToll1 using RNAi led to a significantly reduced survival rate and an increased susceptibility of BPH fifth-instar nymphs to fungal infection, which might be partially owing to the immunosuppressive effects by repressing expression of antimicrobial peptide genes and the dysbiosis of gut bacterial community caused by NlToll1 silencing. Our results manifested that the combination use of RNAi and fungal entomopathogens would be an effective avenue for exploiting pesticide-free BPH management strategies.http://www.sciencedirect.com/science/article/pii/S1049964425000817Brown planthopperEntomopathogenic fungiToll-like receptorRNA interference
spellingShingle Zhu-Long Shao
Chen-Ping Lan
Xiao-Ping Yu
Zheng-Liang Wang
RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infection
Biological Control
Brown planthopper
Entomopathogenic fungi
Toll-like receptor
RNA interference
title RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infection
title_full RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infection
title_fullStr RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infection
title_full_unstemmed RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infection
title_short RNAi-mediated suppression of toll-like receptor NlToll1 enhances Nilaparvata lugens susceptibility to entomopathogenic fungal infection
title_sort rnai mediated suppression of toll like receptor nltoll1 enhances nilaparvata lugens susceptibility to entomopathogenic fungal infection
topic Brown planthopper
Entomopathogenic fungi
Toll-like receptor
RNA interference
url http://www.sciencedirect.com/science/article/pii/S1049964425000817
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