Adaptation of pine wood nematode Bursaphelenchus xylophilus to \u03b2-pinene stress

Yongxia Li,Xuan Wang,Yuqian Feng,Xingyao Zhang,Xun Deng,Jing Cui

doi:10.1186/s12864-020-06876-5

Abstract

BackgroundThe 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.ResultsA 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.ConclusionIn 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.

Highlights

The pine wood nematode (PWN; Bursaphelenchus xylophilus) is the most damaging biological pest in pine forest ecosystems in China
The results indicate that β-pinene inhibited the propagation of B. xylophilus, and the effect was concentrationdependent (Fig. 2)
When nematodes were treated with β-pinene for a short time (48 h), the propagation ratio was highest at a β-pinene concentration of 25.74 mg/mL

Summary

Introduction

The pine wood nematode (PWN; Bursaphelenchus xylophilus) is the most damaging biological pest in pine forest ecosystems in China. The major terpenes produced by pine trees are α-pinene and βpinene, and both can enhance the resistance of pine trees to external biological stress from fungi, bacteria, insects, and nematodes [8,9,10,11]. These molecules exert strong poisoning and repelling effects against non-pine pests and pathogenic fungi [12,13,14,15,16,17,18]. Low concentrations of β-pinene can inhibit the reproduction rate of PWN, while high concentrations can promote reproduction, suggesting that PWN may utilize high concentrations of β-pinene to promote reproduction and overcome resistance of host trees [10, 21, 24, 25]

Methods

Results

Discussion

Conclusion