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

Romain Schellenberger, Jérôme Crouzet, Arvin Nickzad, Lin Jie Shu, Alexander Kutschera, Tim Gerster, Nicolas Borie, Corinna Dawid, Maude Cloutier, Sandra Villaume, Sandrine Dhondt-Cordelier, Jane Hubert, Sylvain Cordelier, Florence Mazeyrat-Gourbeyre, Christian Schmid, Marc Ongena, Jean Hugues Renault, Arnaud Haudrechy, Thomas Hofmann, Fabienne BaillieulChristophe Clément, Cyril Zipfel, Charles Gauthier, Eric Déziel, Stefanie Ranf, Stephan Dorey

Research output: Contribution to journalArticlepeer-review

28 Scopus citations

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 plasmamembrane. In conclusion, RLs and their precursors released by bacteria can both be perceived by plants but through distinct mechanisms.

Original languageEnglish
Article numbere2101366118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number39
DOIs
StatePublished - 28 Sep 2021

Keywords

  • HAA
  • Plant immunity
  • Pseudomonas
  • Rhamnolipids

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