A pioneer nematode effector suppresses plant reactive oxygen species burst by interacting with the class III peroxidase

• Published in: Plant, cell and environment Vol. 47; no. 10; pp. 3813 - 3827
• Main Authors: Rui, Lin, Wen, Tong-Yue, Qiu, Yi-Jun, Yang, Dan, Ye, Jian-Ren, Wu, Xiao-Qin
• Format: Journal Article
• Language: English
• Published: United States 29.05.2024
• Subjects: Bursaphelenchus xylophilus; Pinus thunbergii; immunity
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14939

Bursaphelenchus xylophilus is the pathogen of pine wilt disease, which can devastate the pine forest ecosystem. Usually, plant cells generate reactive oxygen species (ROS) as a defensive substance or signalling molecules to resist the infection of nematodes. However, little is known about how B. xylophilus effectors mediate the plant ROS metabolism. Here, we identified a pioneer B. xylophilus Prx3-interacting effector 1 (BxPIE1) expressed in the dorsal gland cells and the intestine. Silencing of the BxPIE1 gene resulted in reduced nematode reproduction and a delay in disease progression during parasitic stages, with the upregulation of pathogenesis-related (PR) genes PtPR-3 (class Ⅳ chitinase) and PtPR-9 (peroxidase). The protein-protein interaction assays further demonstrated that BxPIE1 interacts with a Pinus thunbergii class III peroxidase (PtPrx3), which produces H O under biotic stress. The expression of BxPIE1 and PtPrx3 was upregulated during the infection stage. Furthermore, BxPIE1 effectively inhibited H O generating from class III peroxidase and ascorbate can recover the virulence of siBxPIE1-treated B. xylophilus by scavenging H O . Taken together, BxPIE1 is an important virulence factor, revealing a novel mechanism utilized by nematodes to suppress plant immunity.