Vesicular and non-vesicular extracellular small RNAs direct gene silencing in a plant-interacting bacterium

Antinéa Ravet, Jérôme Zervudacki, Meenu Singla-Rastogi, Magali Charvin, Odon Thiebeauld, Alvaro L. Perez-Quintero, Lucas Courgeon, Adrien Candat, Liam Lebeau, Antonio Emidio Fortunato, Venugopal Mendu and Lionel Navarro ()
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Antinéa Ravet: Université PSL, CNRS, INSERM
Jérôme Zervudacki: ImmunRise Technologies (IRT)
Meenu Singla-Rastogi: Université PSL, CNRS, INSERM
Magali Charvin: Université PSL, CNRS, INSERM
Odon Thiebeauld: ImmunRise Technologies (IRT)
Alvaro L. Perez-Quintero: Université PSL, CNRS, INSERM
Lucas Courgeon: Université PSL, CNRS, INSERM
Adrien Candat: Université PSL, CNRS, INSERM
Liam Lebeau: Université PSL, CNRS, INSERM
Antonio Emidio Fortunato: ImmunRise Technologies (IRT)
Venugopal Mendu: Université PSL, CNRS, INSERM
Lionel Navarro: Université PSL, CNRS, INSERM

Nature Communications, 2025, vol. 16, issue 1, 1-22

Abstract: Abstract Extracellular plant small RNAs (sRNAs) and/or double-stranded RNA (dsRNA) precursors act as triggers of RNAi in interacting filamentous pathogens. However, whether any of these extracellular RNA species direct gene silencing in plant-interacting bacteria remains unknown. Here, we show that Arabidopsis transgenic plants expressing sRNAs directed against virulence factors of a Pseudomonas syringae strain, reduce its pathogenesis. This Antibacterial Gene Silencing (AGS) phenomenon is directed by Dicer-Like (DCL)-dependent antibacterial sRNAs, but not cognate dsRNA precursors. Three populations of active extracellular sRNAs were recovered in the apoplast of these transgenic plants. The first one is mainly non-vesicular and associated with proteins, whereas the second one is located inside Extracellular Vesicles (EVs). Intriguingly, the third population is unbound to proteins and in a dsRNA form, unraveling functional extracellular free sRNAs (efsRNAs). Both Arabidopsis transgene- and genome-derived efsRNAs were retrieved inside bacterial cells. Finally, we show that salicylic acid (SA) promotes AGS, and that a substantial set of endogenous efsRNAs exhibits predicted bacterial targets that are down-regulated by SA biogenesis and/or signaling during infection. This study thus unveils an unexpected AGS phenomenon, which may have wider implications in the understanding of how plants regulate microbial transcriptome, microbial community composition and genome evolution of associated bacteria.

Date: 2025
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DOI: 10.1038/s41467-025-57908-1

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