Microbe-associated molecular patterns (MAMPs) are molecular signatures typical of whole classes of microbes, and their recognition plays a key role in innate immunity. Endogenous elicitors are similarly recognized as damage-associated molecular patterns (DAMPs). This review focuses on the diversity of MAMPs/DAMPs and on progress to identify the corresponding pattern recognition receptors (PRRs) in plants. The two best-characterized MAMP/PRR pairs, flagellin/FLS2 and EF-Tu/EFR, are discussed in detail and put into a phylogenetic perspective. Both FLS2 and EFR are leucine-rich repeat receptor kinases (LRR-RKs). Upon treatment with flagellin, FLS2 forms a heteromeric complex with BAK1, an LRR-RK that also acts as coreceptor for the brassinolide receptor BRI1. The importance of MAMP/PRR signaling for plant immunity is highlighted by the finding that plant pathogens use effectors to inhibit PRR complexes or downstream signaling events. Current evidence indicates that MAMPs, DAMPs, and effectors are all perceived as danger signals and induce a stereotypic defense response.

A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors

Elicitor signal transduction leading to production of plant secondary metabolites.

Infection of plants by necrotizing pathogens or colonization of plant roots with certain beneficial microbes causes the induction of a unique physiological state called "priming." The primed state can also be induced by treatment of plants with various natural and synthetic compounds. Primed plants display either faster, stronger, or both activation of the various cellular defense responses that are induced following attack by either pathogens or insects or in response to abiotic stress. Although the phenomenon has been known for decades, most progress in our understanding of priming has been made over the past few years. Here, we summarize the current knowledge of priming in various induced-resistance phenomena in plants.

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Priming: Getting Ready for Battle

Innate immunity constitutes the first line of defense against attempted microbial invasion, and it is a well-described phenomenon in vertebrates and insects. Recent pioneering work has revealed striking similarities between the molecular organization of animal and plant systems for nonself recognition and anti-microbial defense. Like animals, plants have acquired the ability to recognize invariant pathogen-associated molecular patterns (PAMPs) that are characteristic of microbial organisms but which are not found in potential host plants. Such structures, also termed general elicitors of plant defense, are often indispensable for the microbial lifestyle and, upon receptor-mediated perception, inevitably betray the invader to the plant's surveillance system. Remarkable similarities have been uncovered in the molecular mode of PAMP perception in animals and plants, including the discovery of plant receptors resembling mammalian Toll-like receptors or cytoplasmic nucleotide-binding oligomerization domain leucine-rich repeat proteins. Moreover, molecular building blocks of PAMP-induced signaling cascades leading to the transcriptional activation of immune response genes are shared among the two kingdoms. In particular, nitric oxide as well as mitogen-activated protein kinase cascades have been implicated in triggering innate immune responses, part of which is the production of antimicrobial compounds. In addition to PAMP-mediated pathogen defense, disease resistance programs are often initiated upon plant-cultivar-specific recognition of microbial race-specific virulence factors, a recognition specificity that is not known from animals.

Innate immunity in plants and animals: striking similarities and obvious differences

Ca(2+) signals are core transducers and regulators in many adaptation and developmental processes of plants. Ca(2+) signals are represented by stimulus-specific signatures that result from the concerted action of channels, pumps, and carriers that shape temporally and spatially defined Ca(2+) elevations. Cellular Ca(2+) signals are decoded and transmitted by a toolkit of Ca(2+) binding proteins that relay this information into downstream responses. Major transduction routes of Ca(2+) signaling involve Ca(2+)-regulated kinases mediating phosphorylation events that orchestrate downstream responses or comprise regulation of gene expression via Ca(2+)-regulated transcription factors and Ca(2+)-responsive promoter elements. Here, we review some of the remarkable progress that has been made in recent years, especially in identifying critical components functioning in Ca(2+) signal transduction, both at the single-cell and multicellular level. Despite impressive progress in our understanding of the processing of Ca(2+) signals during the past years, the elucidation of the exact mechanistic principles that underlie the specific recognition and conversion of the cellular Ca(2+) currency into defined changes in protein-protein interaction, protein phosphorylation, and gene expression and thereby establish the specificity in stimulus response coupling remain to be explored.

https://www.jstor.org/stable/info/25680077

Calcium signals: the lead currency of plant information processing

Nitric oxide (NO) has recently emerged as an important cellular mediator in plant defense responses. However, elucidation of the biochemical mechanisms by which NO participates in this signaling pathway is still in its infancy. We previously demonstrated that cryptogein, an elicitor of tobacco defense responses, triggers a NO burst within minutes in epidermal sections from tobacco leaves (Nicotiana tabacum cv Xanthi). Here, we investigate the signaling events that mediate NO production, and analyze NO signaling activities in the cryptogein transduction pathway. Using flow cytometry and spectrofluorometry, we observed that cryptogein-induced NO production in tobacco cell suspensions is sensitive to nitric oxide synthase inhibitors and may be catalyzed by variant P, a recently identified pathogen-inducible plant nitric oxide synthase. NO synthesis is tightly regulated by a signaling cascade involving Ca2+ influx and phosphorylation events. Using tobacco cells constitutively expressing the Ca2+ reporter apoaequorin in the cytosol, we have shown that NO participates in the cryptogein-mediated elevation of cytosolic free Ca2+ through the mobilization of Ca2+ from intracellular stores. The NO donor diethylamine NONOate promoted an increase in cytosolic free Ca2+ concentration, which was sensitive to intracellular Ca2+ channel inhibitors. Moreover, NO appears to be involved in the pathway(s) leading to the accumulation of transcripts encoding the heat shock protein TLHS-1, the ethylene-forming enzyme cEFE-26, and cell death. In contrast, NO does not act upstream of the elicitor-induced activation of mitogen-activated protein kinase, the opening of anion channels, nor expression of GST, LOX-1, PAL, and PR-3 genes. Collectively, our data indicate that NO is intimately involved in the signal transduction processes leading to cryptogein-induced defense responses.

http://www.plantphysiol.org/content/plantphysiol/135/1/516.full.pdf

Analysis of Nitric Oxide Signaling Functions in Tobacco Cells Challenged by the Elicitor Cryptogein

Characterization of the Cryptogein Binding Sites on Plant Plasma Membranes

We previously reported that the signal transduction of cryptogein, an elicitor of defense reactions in Nicotiana tabacum cells, involves upstream protein phosphorylation. In the present study, induction of these early physiological events was further investigated with inhibitors of protein phosphatase (PP), okadaic acid, and calyculin A. Calyculin A mimicked the effects of cryptogein, inducing an influx of calcium, an extracellular alkalinization, and the production of active oxygen species (AOS), suggesting that during cryptogein signal transduction the balance between specific protein kinase (PK) and PP activities was modified. To identify the phosphorylated proteins that could be involved early in the elicitor signaling pathway, we analyzed by 2-D electrophoresis the in vivo phosphorylation status of proteins after cryptogein, staurosporine, and calyculin A treatments of tobacco cells (5 min). Of about 100 phospho-labeled polypeptides, 19 showed increased 32P incorporation after 5 min of cryptogein treatment. Phosphorylation of 12 of the 19 polypeptides depended upon calcium influx. Staurosporine inhibited the phosphorylations induced by cryptogein whereas calyculin A activated the phosphorylation of 18 of these polypeptides. This study highlighted the role of PKs and/or constitutive active PPs whose activation and inhibition, respectively, resulted in an increased phosphorylation of proteins that may be involved in cryptogein signal transduction. Identification of the phosphoproteins is in progress and will increase our knowledge of signal transduction pathways implicated in plant defense responses.

https://apsjournals.apsnet.org/doi/pdfplus/10.1094/MPMI.2000.13.8.821

Phosphoproteins involved in the signal transduction of cryptogein, an elicitor of defense reactions in tobacco.

Elicitins are a family of small proteins secreted by Phytophthora species that have a high degree of homology and elicit defense reactions in tobacco (Nicotiana tabacum). They display acidic or basic characteristics, the acidic elicitins being less efficient in inducing plant necrosis. In this study we compared the binding properties of four elicitins (two basic and two acidic) and early-induced signal transduction events (Ca2+ influx, extracellular medium alkalinization, and active oxygen species production). The affinity for tobacco plasma membrane-binding sites and the number of binding sites were similar for all four elicitins. Furthermore, elicitins compete with one another for binding sites, suggesting that they interact with the same receptor. The four elicitins induced Ca2+ influx, extracellular medium alkalinization, and the production of active oxygen species in tobacco cell suspensions, but the intensity and kinetics of these effects were different from one elicitin to another. As a general observation the concentrations that induce similar levels of biological activities were lower for basic elicitins (with the exception of cinnamomin-induced Ca2+ uptake). The qualitative similarity of early events induced by elicitins indicates a common transduction scheme, whereas fine signal transduction tuning is different in each elicitin.

Angela Lebrun-Garcia

Papers

Analysis of Nitric Oxide Signaling Functions in Tobacco Cells Challenged by the Elicitor Cryptogein

Characterization of the Cryptogein Binding Sites on Plant Plasma Membranes

Phosphoproteins involved in the signal transduction of cryptogein, an elicitor of defense reactions in tobacco.

Comparison of Binding Properties and Early Biological Effects of Elicitins in Tobacco Cells