Decoding the Pine Wood Nematode’s survival mystery: Gene family expansion drives adaptation revealed by dual-omics

TL;DR

This study reveals how the pine wood nematode adapts to harsh environments and causes disease through the expansion of three key gene families.

Contribution

The study identifies three gene families responsible for the nematode's environmental adaptability and pathogenicity through dual-omics and functional validation.

Findings

BolA-like genes help the nematode survive harsh conditions by acting as a cellular repair system.

DGAT genes support survival during starvation and cold by enhancing lipid storage.

PLCP genes are critical for the nematode's ability to infect host pine trees.

Abstract

The pine wood nematode (PWN) Bursaphelenchus xylophilus is a highly destructive invasive pest that has spread from North America to Eurasia, demonstrating remarkable adaptability across environments. However, the molecular mechanisms underlying environmental adaptation of B. xylophilus remain poorly understood. In this study, we integrated genomic and transcriptomic analyses of B. xylophilus and its native sibling species B. mucronatus, which is native in China. Functional validation of key genes was conducted using RNA interference, BAX, and inoculation assays. Our research focused on three rapidly expanding gene families in B. xylophilus, including the BolA-like superfamily, diacylglycerol acyltransferase (DGAT), and papain-like cysteine peptidase (PLCP). Key genes were functionally validated to elucidate their roles in environmental adaptability. The BolA-like genes were identified as critical stress-response elements, enabling B. xylophilus to survive under harsh conditions. The DGAT genes are essential for lipid biosynthesis and play pivotal roles in resisting starvation and cold. Regarding pathogenicity, the PLCP gene family has been identified as a critical virulence determinant facilitating B. xylophilus infection on host pine trees. These expanded gene families collectively enhance stress tolerance and virulence in B. xylophilus. The findings of this study not only reveal the genetic basis of PWN’s invasive success, but also provide a foundation for managing climate-driven disease spread.

The PWN is an invasive species that causes pine wilt disease (PWD). As a major globally recognized forest pest, it is listed as an A1 quarantine pest by the European and Mediterranean Plant Protection Organization. PWN has adapted to environments across North America, Asia, and Europe, leading to severe infestations worldwide. However, the mechanisms underlying its environmental adaptability remain unclear. Our study reveals that the genetic advantage contributing to PWN’s destructiveness stems from the expansion of three gene families, which together enable survival under environmental stress and drive PWD. First, BolA-like genes act as a universal cellular repair system, allowing the nematode to withstand abiotic stresses. Second, DGAT genes enhance lipid storage, generating energy reserves that support survival during starvation and cold exposure. Third, the PLCP gene family has been identified as a critical virulence determinant facilitating B. xylophilus infection on host pine trees. Collectively, these findings indicate that the invasive success of PWN arises from the co-expansion and functional integration of the BolA-like, DGAT, and PLCP gene families. Their coordinated activity forms an integrated system that enhances both environmental adaptability and pathogenicity, thereby driving global population expansion.

Figures