Pattern recognition receptors and signaling in plant-microbe interactions

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Abstract

Plants solely rely on innate immunity of each individual cell to deal with a diversity of microbes in the environment. Extracellular recognition of microbe- and host damage-associated molecular patterns leads to the first layer of inducible defenses, termed pattern-triggered immunity (PTI). In plants, pattern recognition receptors (PRRs) described to date are all membrane-associated receptor-like kinases or receptor-like proteins, reflecting the prevalence of apoplastic colonization of plant-infecting microbes. An increasing inventory of elicitor-active patterns and PRRs indicates that a large number of them are limited to a certain range of plant groups/species, pointing to dynamic and convergent evolution of pattern recognition specificities. In addition to common molecular principles of PRR signaling, recent studies have revealed substantial diversification between PRRs in their functions and regulatory mechanisms. This serves to confer robustness and plasticity to the whole PTI system in natural infections, wherein different PRRs are simultaneously engaged and faced with microbial assaults. We review the functional significance and molecular basis of PRR-mediated pathogen recognition and disease resistance, and also an emerging role for PRRs in homeostatic association with beneficial or commensal microbes.

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The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota.

June Round, S Lee, Jennifer Li … (2011)

Mucosal surfaces constantly encounter microbes. Toll-like receptors (TLRs) mediate recognition of microbial patterns to eliminate pathogens. By contrast, we demonstrate that the prominent gut commensal Bacteroides fragilis activates the TLR pathway to establish host-microbial symbiosis. TLR2 on CD4(+) T cells is required for B. fragilis colonization of a unique mucosal niche in mice during homeostasis. A symbiosis factor (PSA, polysaccharide A) of B. fragilis signals through TLR2 directly on Foxp3(+) regulatory T cells to promote immunologic tolerance. B. fragilis lacking PSA is unable to restrain T helper 17 cell responses and is defective in niche-specific mucosal colonization. Therefore, commensal bacteria exploit the TLR pathway to actively suppress immunity. We propose that the immune system can discriminate between pathogens and the microbiota through recognition of symbiotic bacterial molecules in a process that engenders commensal colonization.

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Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.

Cyril Zipfel, Gernot Kunze, Delphine Chinchilla … (2006)

Higher eukaryotes sense microbes through the perception of pathogen-associated molecular patterns (PAMPs). Arabidopsis plants detect a variety of PAMPs including conserved domains of bacterial flagellin and of bacterial EF-Tu. Here, we show that flagellin and EF-Tu activate a common set of signaling events and defense responses but without clear synergistic effects. Treatment with either PAMP results in increased binding sites for both PAMPs. We used this finding in a targeted reverse-genetic approach to identify a receptor kinase essential for EF-Tu perception, which we called EFR. Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires EF-Tu binding sites and responsiveness upon transient expression of EFR. Arabidopsis efr mutants show enhanced susceptibility to the bacterium Agrobacterium tumefaciens, as revealed by a higher efficiency of T-DNA transformation. These results demonstrate that EFR is the EF-Tu receptor and that plant defense responses induced by PAMPs such as EF-Tu reduce transformation by Agrobacterium.

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A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence.

Delphine Chinchilla, Cyril Zipfel, Silke Robatzek … (2007)

Plants sense potential microbial invaders by using pattern-recognition receptors to recognize pathogen-associated molecular patterns (PAMPs). In Arabidopsis thaliana, the leucine-rich repeat receptor kinases flagellin-sensitive 2 (FLS2) (ref. 2) and elongation factor Tu receptor (EFR) (ref. 3) act as pattern-recognition receptors for the bacterial PAMPs flagellin and elongation factor Tu (EF-Tu) (ref. 5) and contribute to resistance against bacterial pathogens. Little is known about the molecular mechanisms that link receptor activation to intracellular signal transduction. Here we show that BAK1 (BRI1-associated receptor kinase 1), a leucine-rich repeat receptor-like kinase that has been reported to regulate the brassinosteroid receptor BRI1 (refs 6,7), is involved in signalling by FLS2 and EFR. Plants carrying bak1 mutations show normal flagellin binding but abnormal early and late flagellin-triggered responses, indicating that BAK1 acts as a positive regulator in signalling. The bak1-mutant plants also show a reduction in early, but not late, EF-Tu-triggered responses. The decrease in responses to PAMPs is not due to reduced sensitivity to brassinosteroids. We provide evidence that FLS2 and BAK1 form a complex in vivo, in a specific ligand-dependent manner, within the first minutes of stimulation with flagellin. Thus, BAK1 is not only associated with developmental regulation through the plant hormone receptor BRI1 (refs 6,7), but also has a functional role in PRR-dependent signalling, which initiates innate immunity.