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

Abstract

Since it was first introduced into Asia from North America in the early 20th 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.

Bursaphelenchus xylophilus and B. mucronatus secretomes: a comparative proteomic analysis

“…Additionally, enrichment in peptidase inhibitors were also found in increased proteins of B. xylophilus secretome and previous studies on B. xylophilus secretome20 indicated that the number of secreted peptidase inhibitors in B. xylophilus was significantly greater than in other parasitic nematodes. Peptidases are known to play essential roles against pathogens in plant defence system27 and overexpression of peptidase genes in the host tree is considered one of the most intense reactions in the case B. xylophilus infection28.…”

“…No other quantitative proteomic study involving these two species has been presented before. A comparison of secretome profiles of the plant parasitic nematodes B. xylophilus and Meloidogyne incognita has been previously described and the analysis of GO terms distribution indicated an expansion of peptidases and peptidase inhibitors in B. xylophilus secretome20. The similar comparative functional analysis of B. xylophilus and B. mucronatus secretomes, here presented, also revealed a small expansion in peptidases in B. xylophilus secretome, nevertheless it was the quantitative analysis of B. xylophilus and B. mucronatus secretomes that showed significant differences in protein abundances in both secretomes, pointing out groups of proteins possibly responsible for the main differences between these two species pathogenicity.…”

“…A draft genome sequences of B. xylophilus were also reported in 201119. The availability of all these comprehensive data sets accelerated the postgenomic studies on PWD and a large-scale proteomic study has been conducted to better understand the pathogenicity of B. xylophilus 20. This study presented a complete profile of the B. xylophilus secretome, however, no secretome data for B. mucronatus was yet available.…”

Harnessing the Helminth Secretome for Therapeutic Immunomodulators

“…Following the death of the plant cells, the nematode feeds on fungal growth [79]. Due to this special feeding habit, ES products of the parasite include cell-wall-degrading enzymes like cellulases, pectate lyase, expansin-like, and venom allergen-like proteins.…”

Phytopathogenic Nematodes

“…The stylet is a protrusible, hollow puncturing device, that is used to penetrate plant cell walls. Figure courtesy of Shinya et al (2013) within a lineage. Most, but not all, economically high impact plant parasites such a root knot, cyst and lesion nematodes belong to the most distal nematode clade (Clade 12; Holterman et al Mol Biol Evol 23:1792-1800.…”