Bacteria-derived Peptidoglycans Constitute Pathogen-associated Molecular Patterns Triggering Innate Immunity in Arabidopsis

Abstract

The innate immune system is a host defense mechanism that is evolutionarily conserved from insects to human and is mainly involved in the recognition and control of the early stage of infection in all animals (1). Over the last decade, it has become increasingly evident that also plants have acquired the ability to recognize "non self" via sensitive perception systems for components of microorganisms called pathogen-associated molecular patterns (PAMPs) 2 (2-4). As classically defined, PAMPs are highly characteristic of potentially infectious microbes, but are not present in the host. In addition, such patterns are often vital for microbial survival and are therefore not subject to mutational variation. PAMPs that trigger innate immune responses in various vertebrate and non-vertebrate organisms include lipopolysaccharides (LPS) from Gram-negative bacteria, eubacterial flagellin, viral, and bacterial nucleic acids, fungal cell wall-derived glucans, chitins, mannans, or proteins and peptidoglycans (PGN) from Gram-positive bacteria (5-8). Peptidoglycan (PGN) is an essential and unique component of the bacterial envelope that provides rigidity and structure to the bacterial cell. Virtually all bacteria contain a layer of PGN, but the amount, location, and specific composition vary. PGN is a polymer of alternating N-acetylglucosamine (GlcNAc) and N-acetyl-muramic acid (MurNAc) residues in ␤-1-4 linkage which are cross-linked by short peptides (9, 10). The glycan chains display little variation among different bacterial species while the peptide subunit and the interpeptide bridge reveal species specific differences. PGN from Staphylococcus aureus belongs to the L-lysine (Lys)-type, which is primarily found in Gram-positive bacteria whereas meso-diaminopimelate (Dap)-type PGN is typical for many Gram-negative bacteria.As PGNs are located on most bacterial surfaces they constitute excellent targets for recognition by the innate immune system. Indeed, PGN is known for a long time to promote an innate immune response in vertebrates and insects (11-13), and a breakdown product of PGN, muramyl dipeptide (MurNAc-L-Ala-D-Glu; MDP) was found to be the minimal chemical structure required for PAMP activity in mammals (14). PGN is perceived in animals via various pattern recognition receptors (PRRs), including scavenger receptors, nucleotide-binding oligomerization domain-containing proteins (NODs), a family of peptidoglycan recognition proteins (PGRPs), PGN-lytic enzymes and Toll-like receptor TLR2 (15-19).Remarkable similarities have been uncovered in the molecular mode of PAMP perception in animals and plants (2,20,21). Perception of flagellin in Arabidopsis was shown to be depend-* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis

“…15 PGN is an essential structural component of the bacterial cell wall and acts as a PAMP on Arabidopsis. 16,17 It is therefore plausible that PGN constitutes a ligand for any of the three LysM motifs of CERK1. To test this hypothesis, we purified Pto DC3000 PGN as described by Erbs et al 16 Both chitin and PGN induced ROS generation on Col-0 plants as expected (Fig.…”

VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression

“…MPK3 in the response to a diversity of stresses, e.g., treatment with the plant pathogen Pseudomonas syringae, various pathogen-associated molecular patterns, wounding, and oxidative stress (18,(25)(26)(27). The 1,000-bp promoter region of Trxh8 harbors six VRE copies (Fig.…”

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

“…Polymeric PGNs from Gram-positive and Gram-negative bacteria or a mixture of oligomeric muropeptides derived thereof act as PAMPs in the model plant Arabidopsis thaliana (18,19). Our previous experiments suggested that the carbohydrate backbone of PGN is important for its immunogenic activity and that PGN is recognized in a receptor-mediated manner in Arabidopsis (19).…”

“…Our previous experiments suggested that the carbohydrate backbone of PGN is important for its immunogenic activity and that PGN is recognized in a receptor-mediated manner in Arabidopsis (19). Plant lysin-motif (LysM) domain proteins have been widely implicated in the recognition of GlcNAc-containing glycans.…”