The bacterial virulence factors rhamnolipids and their (R)-3-hydroxyalkanoate precursors activateArabidopsisinnate immunity through two independent mechanisms

Abstract

Plant innate immunity is activated upon perception of invasion pattern molecules by plant cell-surface immune receptors. Several bacteria of the genera Pseudomonas and Burkholderia produce rhamnolipids (RLs) from L- rhamnose and (R)-3-hydroxyalkanoate precursors (HAAs). RL and HAA secretion is required to modulate bacterial surface motility, biofilm development, and thus successful colonization of hosts. Here, we show that the lipidic secretome from the opportunistic pathogen Pseudomonas aeruginosa mostly comprising RLs and HAAs stimulates Arabidopsis immunity. We demonstrate that HAAs are sensed by the bulb-type lectin receptor kinase LIPOOLIGOSACCHARIDE-SPECIFIC REDUCED ELICITATION/S-DOMAIN-1-29 (LORE/SD1-29) that also mediates medium-chain 3-hydroxy fatty acid (mc-3-OH-FA) perception in the plant Arabidopsis thaliana. HAA sensing induces canonical immune signaling and local resistance to plant pathogenic Pseudomonas infection. By contrast, RLs trigger an atypical immune response and resistance to Pseudomonas infection independent of LORE. Thus, the glycosyl moieties of RLs, albeit abolishing sensing by LORE, do not impair their ability to trigger plant defense. In addition, our results show that RL-triggered immune response is affected by the sphingolipid composition of the plasma membrane. In conclusion, RLs and their precursors released by bacteria can both be perceived by plants but through distinct mechanisms.SignificanceActivation of plant innate immunity relies on the perception of microorganisms through self and nonself elicitors. Rhamnolipids and their precursor HAAs are exoproducts produced by beneficial and pathogenic bacteria. They are involved in bacterial surface dissemination and biofilm development. As these compounds are released in the extracellular milieu, they have the potential to be perceived by the plant immune system. Our work shows that both compounds independently activate plant immunity. We demonstrate that HAAs are perceived by the receptor protein kinase LORE. By contrast, rhamnolipids are not senses by LORE but activate a non-canonical immune response affected by the sphingolipid composition of the plant plasma membrane. Thus, plants are able to sense bacterial molecules as well as their direct precursors to trigger a distinct immune response.

Modulation of plant plasma membrane structure by exogenous fatty acid hydroperoxide is a potential perception mechanism for their eliciting activity

“…Indeed, many danger signals or invasion patterns are recognized by specific pattern recognition receptors within PPM (Pršić & Ongena, 2020;Schellenberger et al, 2019), and some amphiphilic elicitors, like surfactin from Bacillus and rhamnolipids (RLs) from Pseudomonas, have been strongly suggested to be perceived by the lipid fraction of PPM (Come et al, 2021;Gerbeau-Pissot et al, 2014;Haba et al, 2014;Henry et al, 2011;Herzog et al, 2020;Luzuriaga-Loaiza et al, 2018;Monnier et al, 2018). Very recently, it was also demonstrated that the RL-triggered immune response is independent of the LORE receptor and is affected by the sphingolipid composition of the plasma membrane suggesting a direct interaction of RLs with plant plasma membrane lipids (Schellenberger et al, 2021), similar to what has been shown on membrane models (Luzuriaga-Loaiza et al, 2018).…”