Bacterial rhamnolipids and their 3-hydroxyalkanoate precursors activate Arabidopsis innate 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, mainly 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), which 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, although abolishing sensing by LORE, do not impair their ability to trigger plant defense. Moreover, our results show that the immune response triggered by RLs 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.

Surface Motility Favors Codependent Interaction between Pseudomonas aeruginosa and Burkholderia cenocepacia

“…A mix of purified P. aeruginosa rhamnolipids was obtained from Jeneil Biosurfactant Co. (JBR-599, lot #050629). This mixture containing 51% monorhamnolipids, 45% dirhamnolipids, and 3-hydroxy fatty acids was dissolved in methanol at a concentration of 10 g/L ( 49 ). A 5 μL drop was spotted onto the center of a swarming agar plate prepared as described above, with methanol only used as a mock control.…”

The effect of rhamnolipids on fungal membrane models as described by their interactions with phospholipids and sterols: An in silico study

“…We would like to explore the importance of such interaction in future works to better understand the role of sterols in the plant-defence eliciting property of PLs. Indeed, recent works have reported the key role of sphingolipids in the eliciting action of RLs in plants like A. thaliana ( Schellenberger et al, 2021 ). Not only sphingolipids facilitate the entrance of the RLs in plant membranes (rich on PC in the outer leaflet ( Cordelier et al, 2021 )) but also promote the formation of microdomains ( Yu et al, 2020a ) that would stimulate proteins responsible for the induction of immune response in plants ( Cordelier et al, 2021 ).…”

“…A direct interaction between the RL and the lipids from the plant plasma membranes has been proposed to explain their eliciting properties, in analogy with the mode of action of the lipopeptide surfactin which shares with RLs properties such as amphiphilic structure, small size and eliciting and antimicrobial activities ( Henry et al, 2011 ; Ranf, 2017 ). This has been observed in Arabidopsis thaliana ( Schellenberger et al, 2021 ) as well as in other Brassicaceae of agricultural interest or other plants commonly used in agriculture like grapevines, cherry-tomato fruit, or rapeseed ( Varnier et al, 2009 ; Sanchez et al, 2012 ; Yan et al, 2016 ; Monnier et al, 2018 ).…”

Surface motility favors co-dependent interaction between Pseudomonas aeruginosa and Burkholderia cenocepacia

“…A mix of purified P. aeruginosa rhamnolipids obtained from Jeneil Biosurfactant Co. (JBR-599, lot # 050629). This mixture containing 51 % monorhamnolipids, 45 % dirhamnolipids, and 3-hydroxy fatty acids was dissolved in MeOH at a concentration of 10,000 mg/L (49). A 5 μl drop was spotted onto the center of a swarming agar plate prepared as described above, with MeOH only used as a mock control.…”