The pine wood nematode (PWN) Bursaphelenchus xylophilus is one of the most widespread plant-parasitic nematodes (PPNs) and is responsible for massive losses of Pinus species in the world. Pine wilt disease (PWD) is caused by B. xylophilus, which has been destroying conifer forests (Liu et al., 2021). Fundamentally, B. xylophilus is known as a migratory endoparasitic nematode associated with the vascular system. PWNs are transmitted to the vascular system and resin canals of healthy trees by mature Monochamus alternatus (Japanese sawyer beetle), feeding on living parenchyma and epithelial cells, especially in East Asia. Under this condition, plant tissue disorders
Background Bursaphelenchus xylophilus is the causal agent of pine wilt disease (PWD) that has caused enormous ecological and economic losses in China. The mechanism in the interaction between nematodes and pine remains unclear. Plant parasitic nematodes (PPNs) secrete effectors into host plant tissues. However, it is poorly studied that role of effector in the infection of pine wood nematode (PWN). Results We cloned, characterized and functionally validated the B. xylophilus effector BxML1, containing an MD-2-related lipid-recognition (ML) domain. This protein inhibits immune responses triggered by the molecular pattern BxCDP1 of B. xylophilus. An insitu hybridization assay demonstrated that BxML1 was expressed mainly in the dorsal glands and intestine of B. xylophilus. Subcellular localization analysis showed the presence of BxML1 in the cytoplasm and nucleus. Furthermore, number of B. xylophilus and morbidity of pine were significantly reduced in Pinus thunbergii infected with B. xylophilus when BxML was silenced. Using yeast two-hybrid (Y2H) and coimmunoprecipitation (CoIP) assays, we found that the BxML1 interacts with cyclophilin protein PtCyP1 in P. thunbergii. Conclusions This study illustrated that BxML1 plays a critical role in the B. xylophilus–plant interaction and virulence of B. xylophilus.
Lipase is involved in lipid hydrolysis, which is related to nematodes' energy reserves and stress resistance. However, the role of lipases in Bursaphelenchus xylophilus, a notorious plant‐parasitic nematode responsible for severe damage to pine forest ecosystems, remains largely obscure. Here, we characterized a class III lipase as a candidate effector and named it BxLip‐3. It was transcriptionally up‐regulated in the parasitic stages of B. xylophilus and specifically expressed in the oesophageal gland cells and the intestine. In addition, BxLip‐3 suppressed cell death triggered by the pathogen‐associated molecular patterns PsXEG1 and BxCDP1 in Nicotiana benthamiana, and its Lipase‐3 domain is essential for immunosuppression. Silencing of the BxLip‐3 gene resulted in a delay in disease onset and increased the activity of antioxidant enzymes and the expression of pathogenesis‐related (PR) genes. Plant chitinases are thought to be PR proteins involved in the defence system against pathogen attack. Using yeast two‐hybrid and co‐immunoprecipitation assays, we identified two class I chitinases in Pinus thunbergii, PtChia1‐3 and PtChia1‐4, as targets of BxLip‐3. The expression of these two chitinases was up‐regulated during B. xylophilus inoculation and inhibited by BxLip‐3. Overall, this study illustrated that BxLip‐3 is a crucial virulence factor that plays a critical role in the interaction between B. xylophilus and host pine.
Bursaphelenchus xylophilus is the most economically important species of migratory plant-parasitic nematodes (PPNs) and causes severe damage to forestry in China. The successful infection of B. xylophilus relies on the secretion of a repertoire of effector proteins. The effectors, which suppress the host pine immune response, are key to the facilitation of B. xylophilus parasitism. An exhaustive list of candidate effectors of B. xylophilus was predicted, but not all have been identified and characterized. Here, an effector, named BxSCD3, has been implicated in the suppression of host immunity. BxSCD3 could suppress pathogen-associated molecular patterns (PAMPs) PsXEG1- and INF1-triggered cell death when it was secreted into the intracellular space in Nicotiana benthamiana. BxSCD3 was highly up-regulated in the early infection stages of B. xylophilus. BxSCD3 does not affect B. xylophilus reproduction, either at the mycophagous stage or the phytophagous stage, but it contributes to the virulence of B. xylophilus. Moreover, BxSCD3 significantly influenced the relative expression levels of defense-related (PR) genes PtPR-3 and PtPR-6 in Pinus thunbergii in the early infection stage. These results suggest that BxSCD3 is an important toxic factor and plays a key role in the interaction between B. xylophilus and host pine.
Pine wilt disease (PWD) (caused by the nematode Bursaphelenchus xylophilus) is extremely harmful to pine forests in East Asia. As a low-resistance pine species, Pinus thunbergii is more vulnerable to pine wood nematode (PWN) than Pinus densiflora and Pinus massoniana. Field inoculation experiments were conducted on PWN-resistant and susceptible P. thunbergii, and the difference in transcription profiles 24 hours after inoculation was analyzed. We identified 2,603 differentially expressed genes (DEGs) in PWN-susceptible P. thunbergii, while 2,559 DEGs were identified in PWN-resistant P. thunbergii. Before inoculation, DEGs between PWN-resistant and PWN-susceptible P. thunbergii were enriched in the REDOX activity pathway (152 DEGs), followed by the oxidoreductase activity pathway (106 DEGs); After inoculation with PWN, however, the opposite was observed, DEGs were enriched in the oxidoreductase activity pathway (119 DEGs), followed by the REDOX activity pathway (84 DEGs). Before inoculation, according to the metabolic pathway analysis results, we found more genes upregulated in phenylpropanoid metabolic pathways and enriched in lignin synthesis pathways; cinnamoyl-CoA reductase (CCR)-coding genes related to lignin synthesis were upregulated in PWN-resistant P. thunbergii and downregulated in PWN-susceptible P. thunbergii, and the lignin content was always higher in resistant than in susceptible P. thunbergii. These results reveal distinctive strategies of resistant and susceptible P. thunbergii in dealing with PWN infections.
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