THE ROOT-KNOT NEMATODE EFFECTOR MJ-MSP18: A SWISS ARMY KNIFE FOR REPROGRAMMING PLANT IMMUNITY

Chen, Y.; Maulana, M. I.; Oklestkova, J.; Siroka, J.; Jonckheere, V.; De Gernier, H.; Bauters, L.; Zhang, N.; Strnad, M.; Van Damme, P.; Goossens, A.; Gheysen, G.; Stojilkovic, B.

doi:10.1101/2025.08.28.672664

bioRxiv · 10.1101/2025.08.28.672664

THE ROOT-KNOT NEMATODE EFFECTOR MJ-MSP18: A SWISS ARMY KNIFE FOR REPROGRAMMING PLANT IMMUNITY

Chen, Y.·Maulana, M. I.·Oklestkova, J.·Siroka, J.·Jonckheere, V.·De Gernier, H.·Bauters, L.·Zhang, N.·Strnad, M.·Van Damme, P.·Goossens, A.·Gheysen, G.·Stojilkovic, B.

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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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Chen, Y., Maulana, M. I., Oklestkova, J., Siroka, J., Jonckheere, V., De Gernier, H., Bauters, L., Zhang, N., Strnad, M., Van Damme, P., Goossens, A., Gheysen, G., Stojilkovic, B.. 2025-08-29. THE ROOT-KNOT NEMATODE EFFECTOR MJ-MSP18: A SWISS ARMY KNIFE FOR REPROGRAMMING PLANT IMMUNITY. https://doi.org/10.1101/2025.08.28.672664

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