4.8 Article

Bacterial rhamnolipids and their 3-hydroxyalkanoate precursors activate Arabidopsis innate immunity two independent mechanisms

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2101366118

Keywords

plant immunity; rhamnolipids; HAA; Pseudomonas

Funding

  1. European Union FEDER (Fonds Europeens de Developpement Regional) program
  2. CNRS
  3. MESRI (Ministere de l'Enseignement Superieur, de la Recherche et de l'Innovation)
  4. Natural Sciences and Engineering Research Council of Canada (NSERC) [RGPIN-2015-03931, RGPIN-2020-06771, RGPIN-2016-04950]
  5. German Research Foundation [SFB924/TP-B10, RA2541/1]
  6. Natural Sciences and Engineering Research Council of Canada (NSERC)
  7. Fonds de Recherche du Quebec - Nature et Technologies (FRQNT)
  8. EliDeRham and Rhamnoprot (Region Grand Est)
  9. Federative Research Structure SFR Condorcet

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Plant innate immunity is activated by lipidic secretome from opportunistic pathogen Pseudomonas aeruginosa, including rhamnolipids and hydroxy fatty acids, through distinct mechanisms. While hydroxy fatty acids are sensed by a specific receptor kinase in plants, rhamnolipids trigger an atypical immune response independently of this receptor. The immune response triggered by rhamnolipids is influenced by the sphingolipid composition of the plasma membrane.
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.

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