The root-knot nematode effector Mj-MSP18: a Swiss army knife for reprogramming plant immunity

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Abstract

Root-knot nematodes ( Meloidogyne spp.) are obligatory plant root parasites whose effector proteins play a critical role in suppressing plant immunity. However, the effectors direct host targets and underlying molecular mechanisms remain poorly understood. Using TurboID-mediated proximity labeling in tomato ( Solanum lycopersicum ) hairy roots, we identified an interaction between the nematode effector Mj-MSP18 and the tomato BRASSINOSTEROID-SIGNALING KINASE 7 (Sl-BSK7). Yeast two-hybrid (Y2H) assays confirmed that this interaction is conserved in Arabidopsis thaliana and Nicotiana benthamiana . Additionally, yeast three-hybrid and luciferase complementation assays demonstrated that Mj-MSP18 disrupts the interaction between BSK7/8 and FLS2 in both yeast and in planta . Given that the BSK7/8–FLS2 interaction is essential for flg22-induced pattern-triggered immunity (PTI), this disruption likely accounts for the suppression of reactive oxygen species (ROS) production and callose deposition observed upon transient expression of Mj-MSP18 in flg22-treated N. benthamiana leaves. Correspondingly, Arabidopsis and tomato bsk7 mutants exhibited increased susceptibility to root-knot nematode infection.

Furthermore, RNA-seq analysis of tomato hairy roots expressing Mj-MSP18 revealed extensive transcriptional reprogramming, including the downregulation of defence-related genes and hydrogen peroxide response pathways. In addition, Y2H screening identified Sl-MYB and Sl-MYC2 as additional interactors, linking Mj-MSP18 to phytohormone biosynthesis, particularly the brassinosteroid (BR) and salicylic acid (SA) pathways, as validated by targeted metabolite analysis. The conservation of Mj-MSP18 across Meloidogyne species suggests a broadly conserved mechanism for host immune suppression and phytohormone modulation.

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