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

Roland Willmann1, Heini M. Lajunen1, Gitte Erbs2, Mari‐Anne Newman2, Dagmar Kolb1, Kenichi Tsuda3, Fumiaki Katagiri3, Judith Fliegmann4,5, Jean‐Jacques Bono6, Julie V. Cullimore6, Anna K. Jehle1, Friedrich Götz7, Andreas Kulik8, Antonio Molinaro9, Volker Lipka10, Andrea A. Gust1, Thorsten Nürnberger1
1Department of Plant Biochemistry, Center for Plant Molecular Biology, University of Tübingen, 72076 Tübingen, Germany;
2Department of Plant Biology and Biotechnology, University of Copenhagen, 1871 Frederiksberg, Denmark
3Center for Microbial and Plant Genomics, Department of Plant Biology, University of Minnesota, St. Paul, MN 55108;
4Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5546, 31326 Castanet-Tolosan, France;
5Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, Unité Mixte de Recherche 5546, 31326 Castanet-Tolosan, France;
6Laboratory of Plant-Microbe Interactions, Institut National de la Recherche Agronomique–Centre National de la Recherche Scientifique, 31326 Castanet-Tolosan, France;
7Department of Microbial Genetics, University of Tübingen, 72076 Tübingen, Germany
8Department of Microbiology/Biotechnology, University of Tübingen, 72076 Tübingen, Germany;
9Dipartimento di Chimica Organica e Biochimica, Università di Napoli Federico II, Napoli 80126, Italy; and
10Department of Plant Cell Biology, Albrecht-von-Haller-Institute of Plant Sciences, Georg-August-University Göttingen, 37073 Göttingen, Germany

Tóm tắt

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.

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