| Summary: | <i>Stenotrophomonas maltophilia</i> influences the reproduction, pathogenicity, and gene expression of aseptic <i>Bursaphelenchus xylophilus</i> after inoculation of aseptic <i>Pinus massoniana</i>. Pine wilt disease is a destructive pine forest disease caused by <i>B. xylophilus</i>, and its pathogenesis is unclear. The role of bacteria associated with <i>B. xylophilus</i> in pine wilt disease has attracted widespread attention. <i>S. maltophilia</i> is one of the most dominant bacteria in <i>B. xylophilus</i>, and its effect is ambiguous. This study aims to explore the role of <i>S. maltophilia</i> in pine wilt disease. The reproduction and virulence of aseptic <i>B. xylophilus</i> and <i>B. xylophilus</i> containing <i>S. maltophilia</i> were examined by inoculating aseptic <i>P. massoniana</i> seedlings. The gene expressions of two nematode treatments were identified by transcriptome sequencing. The reproduction and virulence of <i>B. xylophilus</i> containing <i>S. maltophilia</i> were stronger than that of aseptic nematodes. There were 4240 differentially expressed genes between aseptic <i>B. xylophilus</i> and <i>B. xylophilus</i> containing <i>S. maltophilia</i> after inoculation of aseptic <i>P. massoniana</i>, including 1147 upregulated genes and 2763 downregulated genes. These differentially expressed genes were significantly enriched in some immune-related gene ontology (GO) categories, such as membrane, transporter activity, metabolic processes, and many immune-related pathways, such as the wnt, rap1, PI3K-Akt, cAMP, cGMP-PKG, MAPK, ECM-receptor interaction, and calcium signaling pathways. The polyubiquitin-rich gene, leucine-rich repeat serine/threonine-protein kinase gene, glyceraldehyde-3-phosphate dehydrogenase (GAPDH) gene, acetyl-CoA carboxylase gene, and heat shock protein genes were the key genes associated with immune resistance. Moreover, there were four cell wall hydrolase genes, thirty-six detoxification- and pathogenesis-related protein genes, one effector gene and ten cathepsin L-like cysteine proteinase genes that were differentially expressed. After inoculation of the host pine, <i>S. maltophilia</i> could affect the virulence and reproduction of <i>B. xylophilus</i> by regulating the expression of parasitic, immune, and pathogenicity genes of <i>B. xylophilus</i>.
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