Background: Recently, pine wood nematode (PWN, Bursaphelenchus xylophilus) has been found in the extreme cold area of northeast China. The third-stage dispersal juvenile (DJ3) of PWN, which is a long-lived stress-resistant stage, plays an important role in the process of PWN spreading to low-temperature areas, as this stage can survive under unfavorable conditions. Results: Weighted correlation network analysis (WGCNA) was used to analyze the expression patterns of 15,889 genes included in 21 RNA-Seq results of PWN at DJ3 and the other 6 different stages, and a total of 12 coexpression modules were obtained. Among them, the magenta module has the highest correlation with DJ3, which included a total of 652 genes. KEGG enrichment analysis showed that most of the genes in the magenta module were involved in metabolic processes, which were related to autophagy and longevity regulation. These pathways included starch and sucrose metabolism, which contains trehalose metabolism. To explore the function of trehalose in DJ3 formation and survival under − 20 °C, a trehalose-6-phosphate synthase encoding gene (Bx-tps), a trehalose-6-phosphate phosphatase encoding gene (Bx-tpp) and 7 trehalase encoding genes (Bx-tres) were identified and investigated. The expression of these 9 genes was related to the formation of DJ3. A treatment under − 20 °C induced the accumulation of trehalose. The survival rate of DJ3 at -20 °C reduced after silencing of any of these trehalose metabolism genes. Further analysis suggested that two trehalose synthesis genes were highly correlated with DJ3 and might be involved in autophagy by regulating with energy conversion related genes. Conclusions: The above results indicated that trehalose metabolism promotes DJ3 formation and helps DJ3 survive at -20 °C. Although trehalose accumulation is favorable for DJ3 to cope with low-temperature stress, multiple trehalose metabolism genes need to work together. There may be a multi-path regulated physiological process involving trehalose synthesis genes under low-temperature stress resistance. This physiological process may regulate the formation and maintenance of DJ3 through autophagy and energy conversion.

Transcription factors (TFs) have been shown to play important roles in determining poplar susceptibility. In this study, the transcript profiles of five resistance-related TF groups at different time points were investigated to study the roles of TFs in the compatible interaction between ‘Robusta’ (Populus nigra × P. deltoides) and the virulent E4 race of Melampsora larici-populina. The susceptibility test indicated that the parasitic process of E4 could be divided into two representative time periods: the infection phase and the production phase. Bioinformatics analysis showed that in these two phases, E4 infection induced a network of TFs in ‘Robusta’. Although some TFs responded rapidly and positively, most TFs did not respond to E4, especially during the infection phase. The ethylene, jasmonic acid, and auxin pathways were downregulated, while a calcium-binding protein was upregulated. No other significantly changed phytohormone-related genes were found, which was consistent with the pathological process in the absence of an immune response, suggesting that the lack of response of most TFs during the infection phase of E4 is related to the susceptibility of ‘Robusta’.

Following the invasion by the pine wood nematode (PWN) into north‐east China, a notable disparity in susceptibility was observed among Pinaceae species. Larix olgensis exhibited marked resilience and suffered minimal fatalities, while Pinus koraiensis experienced significant mortality due to PWN infection. Our research demonstrated that the PWNs in L . olgensis showed a 13.43% reduction in lipid content compared to P . koraiensis ( p < 0.05), which was attributable to the accumulation of caffeic acid in L . olgensis . This reduction in lipid content was correlated with a decreased overwintering survival of PWNs. The diminished lipid reserves were associated with substantial stunting in PWNs, including reduced body length and maximum body width. The result suggests that lower lipid content is a major factor contributing to the lower overwintering survival rate of PWNs in L . olgensis induced by caffeic acid. Through verification tests, we concluded that the minimal fatalities observed in L . olgensis could be attributed to the reduced overwintering survival of PWNs, a consequence of caffeic acid‐induced stunting. This study provides valuable insights into PWN–host interactions and suggests that targeting caffeic acid biosynthesis pathways could be a potential strategy for managing PWN in forest ecosystems.

In diseased Korean pine trees (Pinus koraiensis), Cronartium ribicola develops aecia only in the bole, where sugar is initially sufficient. However, the molecular mechanisms underlying sugar depletion in diseased Korean pine trees remain unelucidated, hindering sugar-targeted control strategies. Focusing on host responses, this study integrated metabolomics, transcriptomics, and targeted glycomics based on spatial partitioning to investigate sugar metabolic reprogramming in the bole of diseased pines. Multi-omics revealed severe sugar depletion in the blister area, which was significantly correlated with relative C. ribicola DNA level. However, the transcription of sugar synthesis genes was upregulated, while sugar degradation genes were downregulated, indicating decoupling between sugar metabolism and transcription. Concurrently, T6P–Tre-centered reprogramming was identified: Pktppd and Pktpp4, encoding enzymes that convert T6P into Tre, were downregulated, leading to elevated T6P and reduced Tre levels. This T6P–Tre shift likely acts as a signal to activate genes related to sugar accumulation in response to sugar depletion, thereby explaining the observed transcriptional-metabolic decoupling. Targeting the T6P–Tre module to modulate host sugar allocation and restrict sugar availability to the pathogen may offer a novel strategy for the targeted control of Korean pine blister rust (KPBR).