Plant-parasitic nematode microRNAs hijack plant AGO1 to induce host-cell reprogramming

Dussutour, A.; Noureddine, Y.; Da Rocha, M.; Yahmi, O.; Mohammed, A. T.; Mulet, K.; Foubert, P.; Seckin, E.; Cheng, A.-P.; Zervudacki, J.; Navarro, L.; Weiber, A.; Quentin, M.; Favery, B.; Jaubert, S.

doi:10.64898/2026.02.13.705329

bioRxiv · 10.64898/2026.02.13.705329

Plant-parasitic nematode microRNAs hijack plant AGO1 to induce host-cell reprogramming

Dussutour, A.·Noureddine, Y.·Da Rocha, M.·Yahmi, O.·Mohammed, A. T.·Mulet, K.·Foubert, P.·Seckin, E.·Cheng, A.-P.·Zervudacki, J.·Navarro, L.·Weiber, A.·Quentin, M.·Favery, B.·Jaubert, S.

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Abstract

Cross-kingdom RNA interference (ckRNAi) is emerging as a mode of inter-organismal gene regulation, yet mechanistic examples in plant-metazoan interactions remain limited. Here, we demonstrate miRNA-driven ckRNAi in the nematode-plant pathosystem. Root-knot nematodes are among the most destructive plant pathogens, reprogramming root tissues to develop into galls containing multinucleated, hypermetabolic giant feeding cells essential for parasitism. AGO1-associated small-RNA immunoprecipitation (AGO1-RIP) from tomato galls revealed the selective in planta loading of 10 M. incognita miRNAs into host AGO1. Integrating degradome profiling, target prediction, and dual-luciferase reporter assays, we validated miRNA-directed silencing of nine tomato transcripts by four secreted nematode miRNAs. These targets map to major pathway classes involved in immune signaling, metabolic regulation, and cellular reprogramming linked to feeding-site establishment. Functional analyses further show that the nematode-secreted miR-2b is enhances giant feeding cell development. Comparative AGO1-RIP in Arabidopsis thaliana identified a conserved subset of AGO1-loaded nematode miRNAs, including miR-2b and miR-100, consistent with shared small-RNA effectors across hosts. Finally, the overlap between AGO1-loaded miRNA families and helminth secreted small-RNA repertoires supports evolutionary convergence on RNA-based virulence strategies. Collectively, our findings establish miRNA-mediated ckRNAi as a mechanistic component of plant-root-knot nematode interactions and provide a framework for leveraging RNA-based vulnerabilities for nematode control.

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Dussutour, A., Noureddine, Y., Da Rocha, M., Yahmi, O., Mohammed, A. T., Mulet, K., Foubert, P., Seckin, E., Cheng, A.-P., Zervudacki, J., Navarro, L., Weiber, A., Quentin, M., Favery, B., Jaubert, S.. 2026-02-16. Plant-parasitic nematode microRNAs hijack plant AGO1 to induce host-cell reprogramming. https://doi.org/10.64898/2026.02.13.705329

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