Secretome Analysis of the Pine Wood Nematode Bursaphelenchus xylophilus Reveals the Tangled Roots of Parasitism and Its Potential for Molecular Mimicry

PLoS One. 2013 Jun 21;8(6):e67377. doi: 10.1371/journal.pone.0067377. Print 2013.

Abstract

Since it was first introduced into Asia from North America in the early 20(th) century, the pine wood nematode Bursaphelenchus xylophilus has caused the devastating forest disease called pine wilt. The emerging pathogen spread to parts of Europe and has since been found as the causal agent of pine wilt disease in Portugal and Spain. In 2011, the entire genome sequence of B. xylophilus was determined, and it allowed us to perform a more detailed analysis of B. xylophilus parasitism. Here, we identified 1,515 proteins secreted by B. xylophilus using a highly sensitive proteomics method combined with the available genomic sequence. The catalogue of secreted proteins contained proteins involved in nutrient uptake, migration, and evasion from host defenses. A comparative functional analysis of the secretome profiles among parasitic nematodes revealed a marked expansion of secreted peptidases and peptidase inhibitors in B. xylophilus via gene duplication and horizontal gene transfer from fungi and bacteria. Furthermore, we showed that B. xylophilus secreted the potential host mimicry proteins that closely resemble the host pine's proteins. These proteins could have been acquired by host-parasite co-evolution and might mimic the host defense systems in susceptible pine trees during infection. This study contributes to an understanding of their unique parasitism and its tangled roots, and provides new perspectives on the evolution of plant parasitism among nematodes.

MeSH terms

  • Animals
  • Evolution, Molecular*
  • Gene Duplication*
  • Gene Transfer, Horizontal*
  • Helminth Proteins* / genetics
  • Helminth Proteins* / metabolism
  • Molecular Mimicry*
  • Nematoda* / genetics
  • Nematoda* / metabolism
  • Plant Diseases / parasitology

Substances

  • Helminth Proteins

Grant support

This work was supported by a Grant-in-Aid for Scientific Research (KAKENHI 23248024 and 21780147) (http://www.jsps.go.jp/). Ryoji Shinya was supported by JSPS Research Fellowship for Young Scientists (http://www.jsps.go.jp/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.