Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress

Abstract Background The pine wood nematode (PWN; Bursaphelenchus xylophilus) is the most damaging biological pest in pine forest ecosystems in China. However, the pathogenic mechanism remains unclear. Tracheid cavitation induced by excess metabolism of volatile terpenes is a typical characteristic o...

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Main Authors: Yongxia Li, Yuqian Feng, Xuan Wang, Jing Cui, Xun Deng, Xingyao Zhang
Format: Article
Language:English
Published: BMC 2020-07-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-06876-5
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spelling doaj-c2b991b8788c4818ae87611c8063e8392020-11-25T03:07:20ZengBMCBMC Genomics1471-21642020-07-0121111610.1186/s12864-020-06876-5Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stressYongxia Li0Yuqian Feng1Xuan Wang2Jing Cui3Xun Deng4Xingyao Zhang5Lab. of Forest Pathogen Integrated Biology, Research institute of Forestry New Technology, Chinese Academy of ForestryLab. of Forest Pathogen Integrated Biology, Research institute of Forestry New Technology, Chinese Academy of ForestryLab. of Forest Pathogen Integrated Biology, Research institute of Forestry New Technology, Chinese Academy of ForestryLab. of Forest Pathogen Integrated Biology, Research institute of Forestry New Technology, Chinese Academy of ForestryLab. of Forest Pathogen Integrated Biology, Research institute of Forestry New Technology, Chinese Academy of ForestryLab. of Forest Pathogen Integrated Biology, Research institute of Forestry New Technology, Chinese Academy of ForestryAbstract Background The pine wood nematode (PWN; Bursaphelenchus xylophilus) is the most damaging biological pest in pine forest ecosystems in China. However, the pathogenic mechanism remains unclear. Tracheid cavitation induced by excess metabolism of volatile terpenes is a typical characteristic of pine trees infected by B. xylophilus. β-pinene, one of the main volatile terpenes, influences PWN colonization and reproduction, stimulating pathogenicity during the early stages of infection. To elucidate the response mechanism of PWN to β-pinene, pathogenesis, mortality, and reproduction rate were investigated under different concentrations of β-pinene using a transcriptomics approach. Results A low concentration of β-pinene (BL, C < 25.74 mg/ml) inhibited PWN reproduction, whereas a high concentration (BH, C > 128.7 mg/ml) promoted reproduction. Comparison of PWN expression profiles under low (BL, 21.66 mg/ml) and high (BH, 214.5 mg/ml) β-pinene concentrations at 48 h identified 659 and 418 differentially expressed genes (DEGs), respectively, compared with controls. Some key DEGs are potential regulators of β-pinene via detoxification metabolism (cytochrome P450, UDP-glucuronosyltransferases and short-chain dehydrogenases), ion channel/transporter activity (unc and ATP-binding cassette families), and nuclear receptor -related genes. Gene Ontology enrichment analysis of DEGs revealed metabolic processes as the most significant biological processes, and catalytic activity as the most significant molecular function for both BL and BH samples. Kyoto Encyclopedia of Genes and Genomes (KEGG) Orthology (KO) analysis showed that xenobiotics biodegradation and metabolism, carbohydrate metabolism, lipid metabolism, amino acid metabolism, metabolism of cofactors and vitamins, and transport and catabolism were the dominant terms in metabolism categories. Conclusion In addition to detoxification via reduction/oxidation (redox) activity, PWN responds to β-pinene through amino acid metabolism, carbohydrate metabolism, and other pathways including growth regulation and epidermal protein changes to overcome β-pinene stress. This study lays a foundation for further exploring the pathogenic mechanism of PWN.http://link.springer.com/article/10.1186/s12864-020-06876-5Pine wood nematodeβ-PineneReproduction rateMortalityTranscriptome
collection DOAJ
language English
format Article
sources DOAJ
author Yongxia Li
Yuqian Feng
Xuan Wang
Jing Cui
Xun Deng
Xingyao Zhang
spellingShingle Yongxia Li
Yuqian Feng
Xuan Wang
Jing Cui
Xun Deng
Xingyao Zhang
Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
BMC Genomics
Pine wood nematode
β-Pinene
Reproduction rate
Mortality
Transcriptome
author_facet Yongxia Li
Yuqian Feng
Xuan Wang
Jing Cui
Xun Deng
Xingyao Zhang
author_sort Yongxia Li
title Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
title_short Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
title_full Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
title_fullStr Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
title_full_unstemmed Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
title_sort adaptation of pine wood nematode bursaphelenchus xylophilus to β-pinene stress
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2020-07-01
description Abstract Background The pine wood nematode (PWN; Bursaphelenchus xylophilus) is the most damaging biological pest in pine forest ecosystems in China. However, the pathogenic mechanism remains unclear. Tracheid cavitation induced by excess metabolism of volatile terpenes is a typical characteristic of pine trees infected by B. xylophilus. β-pinene, one of the main volatile terpenes, influences PWN colonization and reproduction, stimulating pathogenicity during the early stages of infection. To elucidate the response mechanism of PWN to β-pinene, pathogenesis, mortality, and reproduction rate were investigated under different concentrations of β-pinene using a transcriptomics approach. Results A low concentration of β-pinene (BL, C < 25.74 mg/ml) inhibited PWN reproduction, whereas a high concentration (BH, C > 128.7 mg/ml) promoted reproduction. Comparison of PWN expression profiles under low (BL, 21.66 mg/ml) and high (BH, 214.5 mg/ml) β-pinene concentrations at 48 h identified 659 and 418 differentially expressed genes (DEGs), respectively, compared with controls. Some key DEGs are potential regulators of β-pinene via detoxification metabolism (cytochrome P450, UDP-glucuronosyltransferases and short-chain dehydrogenases), ion channel/transporter activity (unc and ATP-binding cassette families), and nuclear receptor -related genes. Gene Ontology enrichment analysis of DEGs revealed metabolic processes as the most significant biological processes, and catalytic activity as the most significant molecular function for both BL and BH samples. Kyoto Encyclopedia of Genes and Genomes (KEGG) Orthology (KO) analysis showed that xenobiotics biodegradation and metabolism, carbohydrate metabolism, lipid metabolism, amino acid metabolism, metabolism of cofactors and vitamins, and transport and catabolism were the dominant terms in metabolism categories. Conclusion In addition to detoxification via reduction/oxidation (redox) activity, PWN responds to β-pinene through amino acid metabolism, carbohydrate metabolism, and other pathways including growth regulation and epidermal protein changes to overcome β-pinene stress. This study lays a foundation for further exploring the pathogenic mechanism of PWN.
topic Pine wood nematode
β-Pinene
Reproduction rate
Mortality
Transcriptome
url http://link.springer.com/article/10.1186/s12864-020-06876-5
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