Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilus

Bursaphelenchus xylophilus is a pathogenic nematode responsible for pine wilt disease, which can cause the demise of pine trees and discoloration of trunks. As rotenone is an important botanical pesticide, its impact on B. xylophilus was investigated through RNA-seq to understand the response mechan...

Full description

Saved in:
Bibliographic Details
Main Authors: Buyong Wang, Rongrong Wen, Xuenan Mao, Jie Chen, Xin Hao
Format: Article
Language:English
Published: Elsevier 2024-11-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324013691
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846161708864765952
author Buyong Wang
Rongrong Wen
Xuenan Mao
Jie Chen
Xin Hao
author_facet Buyong Wang
Rongrong Wen
Xuenan Mao
Jie Chen
Xin Hao
author_sort Buyong Wang
collection DOAJ
description Bursaphelenchus xylophilus is a pathogenic nematode responsible for pine wilt disease, which can cause the demise of pine trees and discoloration of trunks. As rotenone is an important botanical pesticide, its impact on B. xylophilus was investigated through RNA-seq to understand the response mechanism of nematode. The bioassay results yielded the 12-h LC30 (1.35 mg L−1) and LC50 (2.60 mg L−1) values for rotenone. Differential gene expression analysis identified 172 and 614 differentially expressed genes (DEGs) in B. xylophilus exposed to two different concentrations of rotenone (1.35 and 2.60 mg L−1). To validate these findings, the expression patterns of 10 DEGs were confirmed through RT-qPCR. Additionally, all DEGs were categorized into eight gene expression profiles using STEM. Notably, the gene ontology (GO) processes of ''single-organism process,'' ''metabolic process,'' and ''catalytic activity'' were prominently enriched in rotenone-treated samples, suggesting a role for metabolic and catalytic pathways in the nematode's response to rotenone stress. KEGG pathways related to ''carbon metabolism,'' ''drug metabolism-cytochrome P450,'' and ''metabolism of xenobiotics by cytochrome P450'' were similarly enriched, indicating potential mechanisms for detoxification resistance and oxidative stress resistance. The analysis pointed to the pivotal roles of detoxification- and oxidoreduction-related genes, as well as signal transduction-related genes, in enabling B. xylophilus to adapt to rotenone exposure. These insights could markedly enhance our understanding of nematode resistance mechanisms and potentially inform the development of more effective rotenone-based strategies for controlling B. xylophilus.
format Article
id doaj-art-cdf77ebaa513406caef29a9936203c75
institution Kabale University
issn 0147-6513
language English
publishDate 2024-11-01
publisher Elsevier
record_format Article
series Ecotoxicology and Environmental Safety
spelling doaj-art-cdf77ebaa513406caef29a9936203c752024-11-21T06:02:06ZengElsevierEcotoxicology and Environmental Safety0147-65132024-11-01287117293Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilusBuyong Wang0Rongrong Wen1Xuenan Mao2Jie Chen3Xin Hao4College of Agricultural and Biological Engineering, Heze University, Heze 274015, ChinaCollege of Agricultural and Biological Engineering, Heze University, Heze 274015, ChinaWageningen University & Research, Wageningen 6700 HB, the NetherlandsYunnan Provincial Key Laboratory for Conservation and Utilization of In-forest Resource, College of Forestry, Southwest Forestry University, Kunming 650224, China; Corresponding authors.Yunnan Provincial Key Laboratory for Conservation and Utilization of In-forest Resource, College of Forestry, Southwest Forestry University, Kunming 650224, China; Corresponding authors.Bursaphelenchus xylophilus is a pathogenic nematode responsible for pine wilt disease, which can cause the demise of pine trees and discoloration of trunks. As rotenone is an important botanical pesticide, its impact on B. xylophilus was investigated through RNA-seq to understand the response mechanism of nematode. The bioassay results yielded the 12-h LC30 (1.35 mg L−1) and LC50 (2.60 mg L−1) values for rotenone. Differential gene expression analysis identified 172 and 614 differentially expressed genes (DEGs) in B. xylophilus exposed to two different concentrations of rotenone (1.35 and 2.60 mg L−1). To validate these findings, the expression patterns of 10 DEGs were confirmed through RT-qPCR. Additionally, all DEGs were categorized into eight gene expression profiles using STEM. Notably, the gene ontology (GO) processes of ''single-organism process,'' ''metabolic process,'' and ''catalytic activity'' were prominently enriched in rotenone-treated samples, suggesting a role for metabolic and catalytic pathways in the nematode's response to rotenone stress. KEGG pathways related to ''carbon metabolism,'' ''drug metabolism-cytochrome P450,'' and ''metabolism of xenobiotics by cytochrome P450'' were similarly enriched, indicating potential mechanisms for detoxification resistance and oxidative stress resistance. The analysis pointed to the pivotal roles of detoxification- and oxidoreduction-related genes, as well as signal transduction-related genes, in enabling B. xylophilus to adapt to rotenone exposure. These insights could markedly enhance our understanding of nematode resistance mechanisms and potentially inform the development of more effective rotenone-based strategies for controlling B. xylophilus.http://www.sciencedirect.com/science/article/pii/S0147651324013691Bursaphelenchus xylophilusRNA-seqRotenoneResistanceCo-expression network
spellingShingle Buyong Wang
Rongrong Wen
Xuenan Mao
Jie Chen
Xin Hao
Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilus
Ecotoxicology and Environmental Safety
Bursaphelenchus xylophilus
RNA-seq
Rotenone
Resistance
Co-expression network
title Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilus
title_full Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilus
title_fullStr Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilus
title_full_unstemmed Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilus
title_short Unveiling the co-expression network and molecular targets behind rotenone resistance in the Bursaphelenchus xylophilus
title_sort unveiling the co expression network and molecular targets behind rotenone resistance in the bursaphelenchus xylophilus
topic Bursaphelenchus xylophilus
RNA-seq
Rotenone
Resistance
Co-expression network
url http://www.sciencedirect.com/science/article/pii/S0147651324013691
work_keys_str_mv AT buyongwang unveilingthecoexpressionnetworkandmoleculartargetsbehindrotenoneresistanceinthebursaphelenchusxylophilus
AT rongrongwen unveilingthecoexpressionnetworkandmoleculartargetsbehindrotenoneresistanceinthebursaphelenchusxylophilus
AT xuenanmao unveilingthecoexpressionnetworkandmoleculartargetsbehindrotenoneresistanceinthebursaphelenchusxylophilus
AT jiechen unveilingthecoexpressionnetworkandmoleculartargetsbehindrotenoneresistanceinthebursaphelenchusxylophilus
AT xinhao unveilingthecoexpressionnetworkandmoleculartargetsbehindrotenoneresistanceinthebursaphelenchusxylophilus