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

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 t...

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Autores principales: Li, Yongxia, Feng, Yuqian, Wang, Xuan, Cui, Jing, Deng, Xun, Zhang, Xingyao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7358211/
https://www.ncbi.nlm.nih.gov/pubmed/32660425
http://dx.doi.org/10.1186/s12864-020-06876-5
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author Li, Yongxia
Feng, Yuqian
Wang, Xuan
Cui, Jing
Deng, Xun
Zhang, Xingyao
author_facet Li, Yongxia
Feng, Yuqian
Wang, Xuan
Cui, Jing
Deng, Xun
Zhang, Xingyao
author_sort Li, Yongxia
collection PubMed
description 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.
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spelling pubmed-73582112020-07-17 Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress Li, Yongxia Feng, Yuqian Wang, Xuan Cui, Jing Deng, Xun Zhang, Xingyao BMC Genomics Research Article 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. BioMed Central 2020-07-13 /pmc/articles/PMC7358211/ /pubmed/32660425 http://dx.doi.org/10.1186/s12864-020-06876-5 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Li, Yongxia
Feng, Yuqian
Wang, Xuan
Cui, Jing
Deng, Xun
Zhang, Xingyao
Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
title 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_short Adaptation of pine wood nematode Bursaphelenchus xylophilus to β-pinene stress
title_sort adaptation of pine wood nematode bursaphelenchus xylophilus to β-pinene stress
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7358211/
https://www.ncbi.nlm.nih.gov/pubmed/32660425
http://dx.doi.org/10.1186/s12864-020-06876-5
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