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Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection

Author:
Willmann, Roland, Lajunen, Heini M., Erbs, Gitte, Newman, Mari-Anne, Kolb, Dagmar, Tsuda, Kenichi, Katagiri, Fumiaki, Fliegmann, Judith, Bono, Jean-Jacques, Cullimore, Julie V., Jehle, Anna K., Götz, Friedrich, Kulik, Andreas, Molinaro, Antonio, Lipka, Volker, Gust, Andrea A., Nürnberger, Thorsten
Source:
Proceedings of the National Academy of Sciences of the United States of America 2011 v.108 no.49 pp. 19824-19829
ISSN:
0027-8424
Subject:
Animalia, Arabidopsis thaliana, Gram-positive bacteria, Pseudomonas syringae, cell walls, chitin, convergent evolution, eukaryotic cells, fungi, immunity, membrane proteins, mutants, pathovars, peptidoglycans, plasma membrane, receptors, tomatoes, transcriptome
Abstract:
Recognition of microbial patterns by host pattern recognition receptors is a key step in immune activation in multicellular eukaryotes. Peptidoglycans (PGNs) are major components of bacterial cell walls that possess immunity-stimulating activities in metazoans and plants. Here we show that PGN sensing and immunity to bacterial infection in Arabidopsis thaliana requires three lysin-motif (LysM) domain proteins. LYM1 and LYM3 are plasma membrane proteins that physically interact with PGNs and mediate Arabidopsis sensitivity to structurally different PGNs from Gram-negative and Gram-positive bacteria. lym1 and lym3 mutants lack PGN-induced changes in transcriptome activity patterns, but respond to fungus-derived chitin, a pattern structurally related to PGNs, in a wild-type manner. Notably, lym1, lym3, and lym3 lym1 mutant genotypes exhibit supersusceptibility to infection with virulent Pseudomonas syringae pathovar tomato DC3000. Defects in basal immunity in lym3 lym1 double mutants resemble those observed in lym1 and lym3 single mutants, suggesting that both proteins are part of the same recognition system. We further show that deletion of CERK1, a LysM receptor kinase that had previously been implicated in chitin perception and immunity to fungal infection in Arabidopsis, phenocopies defects observed in lym1 and lym3 mutants, such as peptidoglycan insensitivity and enhanced susceptibility to bacterial infection. Altogether, our findings suggest that plants share with metazoans the ability to recognize bacterial PGNs. However, as Arabidopsis LysM domain proteins LYM1, LYM3, and CERK1 form a PGN recognition system that is unrelated to metazoan PGN receptors, we propose that lineage-specific PGN perception systems have arisen through convergent evolution.
Agid:
220865