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

Schellenberger, Romain, Crouzet, Jérôme, Nickzad, Arvin, Shu, Lin-Jie, Kutschera, Alexander, Gerster, Tim, Borie, Nicolas, Dawid, Corinna, Cloutier, Maude, Villaume, Sandra, Dhondt-Cordelier, Sandrine, Hubert, Jane, Cordelier, Sylvain, Mazeyrat-Gourbeyre, Florence, Schmid, Christian, Ongena, Marc, Renault, Jean-Hugues, Haudrechy, Arnaud, Hofmann, Thomas, Baillieul, Fabienne, Clément, Christophe, Zipfel, Cyril, Gauthier, Charles, Déziel, Eric, Ranf, Stefanie and Dorey, Stéphan (2021) Bacterial rhamnolipids and their 3-hydroxyalkanoate precursors activate Arabidopsis innate immunity through two independent mechanisms. Proceedings of the National Academy of Sciences, 118 (39). ISSN 0027-8424

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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.

Item Type: Article
Additional Information: Data Availability: All study data are included in the article and/or supporting information. Acknowledgements: We are thankful to Laetitia Parent and Sylvain Milot for technical support and Ralph Hückelhoven for critical discussion. This work was supported by grants from EliDeRham and Rhamnoprot (Région Grand Est). The project Rhamnoprot is co-funded by the European Union FEDER (Fonds Européens de Développement Régional) program. Financial support from the CNRS, the MESRI (Ministère de l’Enseignement Supérieur, de la Recherche et de l’Innovation), and the Federative Research Structure SFR Condorcet are gratefully acknowledged. Works on rhamnolipids in the E.D. and C.G. laboratories are funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) through Discovery Grants RGPIN-2015-03931 and RGPIN-2020-06771 (to E.D.) and RGPIN-2016-04950 (to C.G.). Work in the S.R. laboratory is supported by the German Research Foundation (SFB924/TP-B10and Emmy Noether programme RA2541/1). M.C. thanks The Natural Sciences and Engineering Research Council of Canada (NSERC) and Fonds de Recherche du Québec–Nature et Technologies (FRQNT) for M.Sc. and Ph.D. scholarships
Uncontrolled Keywords: haa,plant immunity,pseudomonas,rhamnolipids,general ,/dk/atira/pure/subjectarea/asjc/1000
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
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Depositing User: LivePure Connector
Date Deposited: 11 Nov 2021 02:16
Last Modified: 21 Dec 2022 07:31
DOI: 10.1073/pnas.2101366118


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