[en] Induced systemic resistance (ISR) triggered by beneficial bacteria represents a promising approach in sustainable agriculture, as it provides long-lasting and broad-spectrum protection to plants. Among the candidate compounds that could implement ISR as a strategy are cyclic lipopeptides and particularly surfactin (SRF) produced by biocontrol bacilli, which has a strong elicitor potential on various host species. However, the success of ISR elicitors, thus SRF as well, is so far rather limited due to a range of factors including our global lack of knowledge about the molecular mechanisms underpinning their plant immunization activity. To shed a light on this intriguing phenomenon we elucidated activation of immune responses by SRF in the model plant Arabidopsis thaliana, on which SRF also has eliciting activity.
Our data showed that SRF bypasses perception by pattern-recognition receptors involved in the recognition of molecular patterns harboured by pathogenic microbes. Moreover, SRF activates early immune events and ISR independently of the NADPH oxidase (RBOHD) and the receptor-like cytoplasmic kinase (BIK1), almost invariably associated with pathogen induced plant immune response. Given the amphiphilic nature of the molecule we postulated that SRF would preferably interact with the lipid fraction of plant cell plasma membranes (PM) to trigger signaling events. To get further insight into the mechanistics of this interaction, we used different approaches combining functional bioassays with in silico modeling and experimental biophysics. Our results pointed out that SRF preferentially interacts with glucosylceramides (GluCer), a specific class of sphingolipids primarily located in the PM outer leaflet, where they are assembling with sterols to form microdomains. By docking into GluCer-enriched domains, surfactin causes changes in PM structural and rheological properties that could be perceived by plant cell as a mechanical stress and thus trigger early immune responses such as production of ROS and influx of calcium.
Altogether these data demonstrate that SRF perception is independent of pathways plants are using for pathogen recognition and relies mechanistically on a unique lipid-mediated process. Also, they open a possibility for optimization of application of SRF as biostimulant, by using sphingolipidome profile as criteria for rational choice of plant species on which it can be applied.