A neprilysin effector from the pinewood nematode <scp> <i>Bursaphelenchus xylophilus</i> </scp> targets pine caffeic acid <scp> <i>O</i> </scp> ‐methyltransferase and inhibits lignin biosynthesis

BACKGROUND: Pine wilt disease caused by Bursaphelenchus xylophilus can devastate the pine forest ecosystem. Lignification is a vital strategy to help hosts resist pathogens, but how B. xylophilus effectors regulate the lignin biosynthesis of pine trees are unknown. RESULTS: In this study, we identified a B. xylophilus neprilysin effector BxNEP1, which rose in the three B. xylophilus transcriptomes of different infection stages. We demonstrated that BxNEP1 is required for B. xylophilus reproduction and virulence during parasitic stages. Silencing of the BxNEP1 gene resulted in the upregulation of pathogenesis-related (PR) genes PtPR-2, PtPR-5, PtPR-6 and PtLOX-5, as well as increased endogenous jasmonic acid levels in Pinus thunbergii. Protein-protein interaction assays further confirmed that BxNEP1 interacts with a P. thunbergii caffeic acid O-methyltransferase (PtCOMT), which is a major enzyme in lignin biosynthesis. Gene expression pattern indicated that BxNEP1 overcame PtCOMT quickly in the interaction between B. xylophilus and P. thunbergii at early infection stage. Furthermore, BxNEP1 effectively inhibited lignin biosynthesis by directly suppressing the gene expression of PtCOMT or indirectly downregulating PtCOMT expression through reducing JA production. CONCLUSION: In conclusion, when B. xylophilus secretes BxNEP1 into pines, BxNEP1 inhibits lignin biosynthesis in pine trees through two distinct regulatory mechanisms to promote nematode parasitism. This study unveils a novel mechanism exploited by nematodes to suppress plant immunity, which can lead to the development of new strategies for B. xylophilus control in pines. © 2026 Society of Chemical Industry.