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

Robert Willmann; Heini M. Lajunen; Gitte Erbs; Mari-Anne Newman; Dagmar Kolb; Kenichi Tsuda; Fumiaki Katagiri; Judith Fliegmann; Jean-Jacques Bono; Julie V. Cullimore; Anna K. Jehle; Friedrich Götz; Andreas Kulik; Antonio Molinaro; Volker Lipka; Andrea A. Gust; Thorsten Nürnberger

doi:10.1073/pnas.1112862108

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

Robert Willmann, Heini M. Lajunen, Gitte Erbs, Mari-Anne Newman, Dagmar Kolb, Kenichi Tsuda, Fumiaki Katagiri, Judith Fliegmann, Jean-Jacques Bono, Julie V. Cullimore, Anna K. Jehle, Friedrich Götz, Andreas Kulik, Antonio Molinaro, Volker Lipka, Andrea A. Gust, Thorsten Nürnberger

289 Citations (Scopus)

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.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	108
Issue number	49
Pages (from-to)	19824-19829
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1112862108
Publication status	Published - 6 Dec 2011

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Willmann, R., Lajunen, H. M., Erbs, G., Newman, M-A., Kolb, D., Tsuda, K., Katagiri, F., Fliegmann, J., Bono, J-J., Cullimore, J. V., Jehle, A. K., Götz, F., Kulik, A., Molinaro, A., Lipka, V., Gust, A. A., & Nürnberger, T. (2011). Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proceedings of the National Academy of Sciences of the United States of America, 108(49), 19824-19829. https://doi.org/10.1073/pnas.1112862108

Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. / Willmann, Robert; Lajunen, Heini M.; Erbs, Gitte et al.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 49, 06.12.2011, p. 19824-19829.

Research output: Contribution to journal › Journal article › Research › peer-review

Willmann, R, Lajunen, HM, Erbs, G, Newman, M-A, Kolb, D, Tsuda, K, Katagiri, F, Fliegmann, J, Bono, J-J, Cullimore, JV, Jehle, AK, Götz, F, Kulik, A, Molinaro, A, Lipka, V, Gust, AA & Nürnberger, T 2011, 'Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 49, pp. 19824-19829. https://doi.org/10.1073/pnas.1112862108

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

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.",

author = "Robert Willmann and Lajunen, {Heini M.} and Gitte Erbs and Mari-Anne Newman and Dagmar Kolb and Kenichi Tsuda and Fumiaki Katagiri and Judith Fliegmann and Jean-Jacques Bono and Cullimore, {Julie V.} and Jehle, {Anna K.} and Friedrich G{\"o}tz and Andreas Kulik and Antonio Molinaro and Volker Lipka and Gust, {Andrea A.} and Thorsten N{\"u}rnberger",

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T1 - Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection

AU - Willmann, Robert

AU - Lajunen, Heini M.

AU - Erbs, Gitte

AU - Newman, Mari-Anne

AU - Kolb, Dagmar

AU - Tsuda, Kenichi

AU - Katagiri, Fumiaki

AU - Fliegmann, Judith

AU - Bono, Jean-Jacques

AU - Cullimore, Julie V.

AU - Jehle, Anna K.

AU - Götz, Friedrich

AU - Kulik, Andreas

AU - Molinaro, Antonio

AU - Lipka, Volker

AU - Gust, Andrea A.

AU - Nürnberger, Thorsten

PY - 2011/12/6

Y1 - 2011/12/6

N2 - 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.

AB - 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.

U2 - 10.1073/pnas.1112862108

DO - 10.1073/pnas.1112862108

M3 - Journal article

C2 - 22106285

SN - 0027-8424

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EP - 19829

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 49

ER -

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

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