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

Lin Rui, Tong‐Yue Wen, Yi‐Jun Qiu, Dan Yang, Jianren Ye, Xiao‐Qin Wu

2024Plant Cell & Environment14 citationsDOI

Abstract

Abstract 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 2 O 2 under biotic stress. The expression of BxPIE1 and PtPrx3 was upregulated during the infection stage. Furthermore, BxPIE1 effectively inhibited H 2 O 2 generating from class III peroxidase and ascorbate can recover the virulence of siBxPIE1 ‐treated B. xylophilus by scavenging H 2 O 2 . Taken together, BxPIE1 is an important virulence factor, revealing a novel mechanism utilized by nematodes to suppress plant immunity.

Topics & Concepts

Bursaphelenchus xylophilusEffectorPeroxidaseReactive oxygen speciesBiologyVirulencePinus thunbergiiWilt diseaseNematodeCell biologyMicrobiologyDownregulation and upregulationBotanyBiochemistryGeneEcologyEnzymeNematode management and characterization studiesLegume Nitrogen Fixing SymbiosisPlant-Microbe Interactions and Immunity
A pioneer nematode effector suppresses plant reactive oxygen species burst by interacting with the class III peroxidase | Litcius