Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>

<i>Bursaphelenchus xylophilus</i> causes pine wilt disease, which poses a serious threat to forestry ecology around the world. Microorganisms are environmentally friendly alternatives to the use of chemical nematicides to control <i>B. xylophilus</i> in a sustainable way. In...

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Main Authors: Xin Hao, Jie Chen, Yongxia Li, Xuefeng Liu, Yang Li, Bowen Wang, Jingxin Cao, Yaru Gu, Wei Ma, Ling Ma
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/12/4/543
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author Xin Hao
Jie Chen
Yongxia Li
Xuefeng Liu
Yang Li
Bowen Wang
Jingxin Cao
Yaru Gu
Wei Ma
Ling Ma
author_facet Xin Hao
Jie Chen
Yongxia Li
Xuefeng Liu
Yang Li
Bowen Wang
Jingxin Cao
Yaru Gu
Wei Ma
Ling Ma
author_sort Xin Hao
collection DOAJ
description <i>Bursaphelenchus xylophilus</i> causes pine wilt disease, which poses a serious threat to forestry ecology around the world. Microorganisms are environmentally friendly alternatives to the use of chemical nematicides to control <i>B. xylophilus</i> in a sustainable way. In this study, we isolated a nematophagous fungus—<i>Arthrobotrys robusta</i>—from the xylem of diseased <i>Pinus massoniana.</i> The nematophagous activity of <i>A. robusta</i> against the PWNs was observed after just 6 h. We found that <i>B. xylophilus</i> entered the trap of <i>A. robusta</i> at 24 h, and the nervous system and immunological response of <i>B. xylophilus</i> were stimulated by metabolites that <i>A. robusta</i> produced. At 30 h of exposure to <i>A. robusta</i>, <i>B. xylophilus</i> exhibited significant constriction, and we were able to identify xenobiotics. <i>Bursaphelenchus xylophilus</i> activated xenobiotic metabolism, which expelled the xenobiotics from their bodies, by providing energy through lipid metabolism. When PWNs were exposed to <i>A. robusta</i> for 36 h, lysosomal and autophagy-related genes were activated, and the bodies of the nematodes underwent disintegration. Moreover, a gene co-expression pattern network was constructed by WGCNA and Cytoscape. The gene co-expression pattern network suggested that metabolic processes, developmental processes, detoxification, biological regulation, and signaling were influential when the <i>B. xylophilus</i> specimens were exposed to <i>A. robusta</i>. Additionally, bZIP transcription factors, ankyrin, ATPases, innexin, major facilitator, and cytochrome P450 played critical roles in the network. This study proposes a model in which mobility improved whenever <i>B. xylophilus</i> entered the traps of <i>A. robusta</i>. The model will provide a solid foundation with which to understand the molecular and evolutionary mechanisms underlying interactions between nematodes and nematophagous fungi. Taken together, these findings contribute in several ways to our understanding of <i>B. xylophilus</i> exposed to microorganisms and provide a basis for establishing an environmentally friendly prevention and control strategy.
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spelling doaj.art-7492502808d141fdafe3df6e178a5fd12023-11-16T19:43:48ZengMDPI AGCells2073-44092023-02-0112454310.3390/cells12040543Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>Xin Hao0Jie Chen1Yongxia Li2Xuefeng Liu3Yang Li4Bowen Wang5Jingxin Cao6Yaru Gu7Wei Ma8Ling Ma9School of Forestry, Northeast Forestry University, Harbin 150040, ChinaSchool of Forestry, Northeast Forestry University, Harbin 150040, ChinaKey Laboratory of Forest Protection, National Forestry and Grassland Administration, Ecology and Nature Conservation Institute, Chinese Academy of Forestry, Beijing 100091, ChinaSchool of Forestry, Northeast Forestry University, Harbin 150040, ChinaSchool of Forestry, Northeast Forestry University, Harbin 150040, ChinaSchool of Art and Archaeology, Zhejiang University, Hangzhou 310028, ChinaSchool of Forestry, Northeast Forestry University, Harbin 150040, ChinaSchool of Forestry, Northeast Forestry University, Harbin 150040, ChinaCollege of Pharmaceutical Sciences, Heilongjiang University of Chinese Medicine, Harbin 150040, ChinaSchool of Forestry, Northeast Forestry University, Harbin 150040, China<i>Bursaphelenchus xylophilus</i> causes pine wilt disease, which poses a serious threat to forestry ecology around the world. Microorganisms are environmentally friendly alternatives to the use of chemical nematicides to control <i>B. xylophilus</i> in a sustainable way. In this study, we isolated a nematophagous fungus—<i>Arthrobotrys robusta</i>—from the xylem of diseased <i>Pinus massoniana.</i> The nematophagous activity of <i>A. robusta</i> against the PWNs was observed after just 6 h. We found that <i>B. xylophilus</i> entered the trap of <i>A. robusta</i> at 24 h, and the nervous system and immunological response of <i>B. xylophilus</i> were stimulated by metabolites that <i>A. robusta</i> produced. At 30 h of exposure to <i>A. robusta</i>, <i>B. xylophilus</i> exhibited significant constriction, and we were able to identify xenobiotics. <i>Bursaphelenchus xylophilus</i> activated xenobiotic metabolism, which expelled the xenobiotics from their bodies, by providing energy through lipid metabolism. When PWNs were exposed to <i>A. robusta</i> for 36 h, lysosomal and autophagy-related genes were activated, and the bodies of the nematodes underwent disintegration. Moreover, a gene co-expression pattern network was constructed by WGCNA and Cytoscape. The gene co-expression pattern network suggested that metabolic processes, developmental processes, detoxification, biological regulation, and signaling were influential when the <i>B. xylophilus</i> specimens were exposed to <i>A. robusta</i>. Additionally, bZIP transcription factors, ankyrin, ATPases, innexin, major facilitator, and cytochrome P450 played critical roles in the network. This study proposes a model in which mobility improved whenever <i>B. xylophilus</i> entered the traps of <i>A. robusta</i>. The model will provide a solid foundation with which to understand the molecular and evolutionary mechanisms underlying interactions between nematodes and nematophagous fungi. Taken together, these findings contribute in several ways to our understanding of <i>B. xylophilus</i> exposed to microorganisms and provide a basis for establishing an environmentally friendly prevention and control strategy.https://www.mdpi.com/2073-4409/12/4/543<i>Bursaphelenchus xylophilus</i>pine wilt diseasenematophagous fungitranscriptomic analysis<i>Arthrobotrys robusta</i>
spellingShingle Xin Hao
Jie Chen
Yongxia Li
Xuefeng Liu
Yang Li
Bowen Wang
Jingxin Cao
Yaru Gu
Wei Ma
Ling Ma
Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>
Cells
<i>Bursaphelenchus xylophilus</i>
pine wilt disease
nematophagous fungi
transcriptomic analysis
<i>Arthrobotrys robusta</i>
title Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>
title_full Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>
title_fullStr Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>
title_full_unstemmed Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>
title_short Molecular Defense Response of <i>Bursaphelenchus xylophilus</i> to the Nematophagous Fungus <i>Arthrobotrys robusta</i>
title_sort molecular defense response of i bursaphelenchus xylophilus i to the nematophagous fungus i arthrobotrys robusta i
topic <i>Bursaphelenchus xylophilus</i>
pine wilt disease
nematophagous fungi
transcriptomic analysis
<i>Arthrobotrys robusta</i>
url https://www.mdpi.com/2073-4409/12/4/543
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