Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis

Abstract

Peptidoglycans (PGNs) are immunogenic bacterial surface patterns that trigger immune activation in metazoans and plants. It is generally unknown how complex bacterial structures such as PGNs are perceived by plant pattern recognition receptors (PRRs) and whether host hydrolytic activities facilitate decomposition of bacterial matrices and generation of soluble PRR ligands. Here we show that Arabidopsis thaliana, upon bacterial infection or exposure to microbial patterns, produces a metazoan lysozyme-like hydrolase (lysozyme 1, LYS1). LYS1 activity releases soluble PGN fragments from insoluble bacterial cell walls and cleavage products are able to trigger responses typically associated with plant immunity. Importantly, LYS1 mutant genotypes exhibit super-susceptibility to bacterial infections similar to that observed on PGN receptor mutants. We propose that plants employ hydrolytic activities for the decomposition of complex bacterial structures, and that soluble pattern generation might aid PRR-mediated immune activation in cell layers adjacent to infection sites.DOI: http://dx.doi.org/10.7554/eLife.01990.001

Pattern recognition receptors and signaling in plant–microbe interactions

“…Similar constraints are imposed by the host immunity on mutualistic and pathogenic microbes, which include PTI, i.e. elicitor-inactive flg22 alleles in nitrogen-fixing rhizobacteria (Gomez-Gomez et al, 1999) and flg22-induced suppression of their colonization (Lopez-Gomez et al, 2012), and ETS/ETI, i.e. NLR-dependent rhizobacterial resistance (Yang et al, 2010) and bacterial effector-mediated promotion or restriction of symbiosis (Marchetti et al, 2010;Okazaki et al, 2013;Tsukui et al, 2013;Gourion et al, 2015;Yasuda et al, 2016).…”

“…This hypothesis is related to the question of how MAMP ligands integrated inside the microbial cells are presented to PRRs. In A. thaliana, PGN perception requires the host-derived hydrolase LYS1 that releases soluble elicitor-active ligands (Liu et al, 2014). EF-Tu and CSPs are both secreted from the bacterial cytoplasm via an unknown process (Song et al, 2009).…”

From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition

“…PGN fragments are released by plant-derived lysozymes and act as MAMPs to elicit plant immunity (96). Treatment with PGN but not the breakdown molecules from Staphylococcus aureus activates defense responses in Arabidopsis (52).…”

Molecular Patterns of Rhizobacteria Involved in Plant Immunity Elicitation

“…However, no evidence for a role of this polymer as trigger of systemic resistance by beneficial rhizobacteria has been reported so far. Interestingly, a recent study shows that only Bacillus subtilis PGN digests and not the native polymer PGN were able to trigger immune marker gene FRK1 expression in Arabidopsis seedlings as well as medium alkalinization in cultured rice cells (Liu et al, 2014). This work also demonstrates that in planta generation of these immunogenic PGN fragments relies on the activity of a lysozyme-like (LYS1) enzyme which is specifically expressed upon infection.…”

“…Similar PGN perception machinery also involving LysM domain proteins (LYP4 and LYP6) has been reported for rice . Rather than the complex PGN matrix, it is obvious that both plants actually perceive soluble fragments released from PGN by a lysozyme-like enzyme rapidly induced in the plant following infection (Liu et al, 2014).…”