Transcriptomic and metabolomic insights into pine wood nematode resistance mechanisms in Pinus massoniana

Abstract Pine wilt disease (PWD), caused by the pine wood nematode (PWN), is a devastating systemic disease with significantly impacts on pine species, particularly Masson pine (Pinus massoniana) in South China. This study integrated transcriptomic and metabolomic analyses to identify differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) associated with PWN resistance. By comparing the gene expression and metabolic profiles of healthy, mechanically wounded, and PWN-infected Masson pine trees at 28 d post-inoculation, we identified 1,310 DEGs were specifically associated with PWN infection after excluding mechanical damage effects. Notably, combined KEGG analysis of transcriptomic and metabolomic data revealed significant enrichment of the α-linolenic acid metabolism pathway. Within this pathway, genes such as AOS, LCAT3, and DAD1 exhibited differential expression patterns, highlighting its pivotal role in PWN resistance. Metabolomic analysis revealed that key genes involved in jasmonic acid (JA) biosynthesis and plant hormone signaling showing strong regulation. Additionally, qRT-PCR validation of selected DEGs confirmed the expression patterns observed in the transcriptomic data. Physiological assays also validated changes in key hormone levels, such as JA and methyl jasmonate (MeJA), which are upregulated in the early stages of plant infection. These results highlight the importance of JA-mediated defence responses and provide novel insights for breeding strategies to improve P. massoniana’s resistance to PWN infection.