Dataset Information

Comparative transcriptomic analysis of candidate effectors to explore the infection and survival strategy of Bursaphelenchus xylophilus during different interaction stages with pine trees.

ABSTRACT:

Background

The pine wood nematode (PWN), Bursaphelenchus xylophilus, is a devastating pathogen of many Pinus species in China. The aim of this study was to understand the interactive molecular mechanism of PWN and its host by comparing differentially expressed genes and candidate effectors from three transcriptomes of B. xylophilus at different infection stages.

Results

In total, 62, 69 and 46 candidate effectors were identified in three transcriptomes (2.5 h postinfection, 6, 12 and 24 h postinoculation and 6 and 15 d postinfection, respectively). In addition to uncharacterized pioneers, other candidate effectors were involved in the degradation of host tissues, suppression of host defenses, targeting plant signaling pathways, feeding and detoxification, which helped B. xylophilus survive successfully in the host. Seven candidate effectors were identified in both our study and the B. xylophilus transcriptome at 2.5 h postinfection, and one candidate effector was identified in all three transcriptomes. These common candidate effectors were upregulated at infection stages, and one of them suppressed pathogen-associated molecular pattern (PAMP) PsXEG1-triggered cell death in Nicotiana benthamiana.

Conclusions

The results indicated that B. xylophilus secreted various candidate effectors, and some of them continued to function throughout all infection stages. These various candidate effectors were important to B. xylophilus infection and survival, and they functioned in different ways (such as breaking down host cell walls, suppressing host defenses, promoting feeding efficiency, promoting detoxification and playing virulence functions). The present results provide valuable resources for in-depth research on the pathogenesis of B. xylophilus from the perspective of effectors.

SUBMITTER: Hu LJ

PROVIDER: S-EPMC8132355 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.