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      PRRs and NB-LRRs: From Signal Perception to Activation of Plant Innate Immunity

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          Abstract

          To ward off pathogens and pests, plants use a sophisticated immune system. They use pattern-recognition receptors (PRRs), as well as nucleotide-binding and leucine-rich repeat (NB-LRR) domains, for detecting nonindigenous molecular signatures from pathogens. Plant PRRs induce local and systemic immunity. Plasma-membrane-localized PRRs are the main components of multiprotein complexes having additional transmembrane and cytosolic kinases. Topical research involving proteins and their interactive partners, along with transcriptional and posttranscriptional regulation, has extended our understanding of R-gene-mediated plant immunity. The unique LRR domain conformation helps in the best utilization of a surface area and essentially mediates protein–protein interactions. Genome-wide analyses of inter- and intraspecies PRRs and NB-LRRs offer innovative information about their working and evolution. We reviewed plant immune responses with relevance to PRRs and NB-LRRs. This article focuses on the significant functional diversity, pathogen-recognition mechanisms, and subcellular compartmentalization of plant PRRs and NB-LRRs. We highlight the potential biotechnological application of PRRs and NB-LRRs to enhance broad-spectrum disease resistance in crops.

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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.
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              CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis.

              Ayako Miya, Premkumar Albert, Tomonori Shinya … (2007)
              Chitin is a major component of fungal cell walls and serves as a microbe-associated molecular pattern (MAMP) for the detection of various potential pathogens in innate immune systems of both plants and animals. We recently showed that chitin elicitor-binding protein (CEBiP), plasma membrane glycoprotein with LysM motifs, functions as a cell surface receptor for chitin elicitor in rice. The predicted structure of CEBiP does not contain any intracellular domains, suggesting that an additional component(s) is required for signaling through the plasma membrane into the cytoplasm. Here, we identified a receptor-like kinase, designated CERK1, which is essential for chitin elicitor signaling in Arabidopsis. The KO mutants for CERK1 completely lost the ability to respond to the chitin elicitor, including MAPK activation, reactive oxygen species generation, and gene expression. Disease resistance of the KO mutant against an incompatible fungus, Alternaria brassicicola, was partly impaired. Complementation with the WT CERK1 gene showed cerk1 mutations were responsible for the mutant phenotypes. CERK1 is a plasma membrane protein containing three LysM motifs in the extracellular domain and an intracellular Ser/Thr kinase domain with autophosphorylation/myelin basic protein kinase activity, suggesting that CERK1 plays a critical role in fungal MAMP perception in plants.
              Article 0 comments Cited 394 times – based on 0 reviews     Review now
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                Author and article information

                Journal
                Journal ID (nlm-ta): Int J Mol Sci
                Journal ID (iso-abbrev): Int J Mol Sci
                Journal ID (publisher-id): ijms
                Title: International Journal of Molecular Sciences
                Publisher: MDPI
                ISSN (Electronic): 1422-0067
                Publication date (Electronic): 16 April 2019
                Publication date Collection: April 2019
                Volume: 20
                Issue: 8
                Electronic Location Identifier: 1882
                Affiliations
                [1 ]Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310027, China
                [2 ]Department of Botany, Government College University, Faisalabad 38000, Pakistan
                [3 ]State Key Laboratory of Grassland Agro-ecosystems, School of Life Science, Lanzhou University, Lanzhou 730000, China; aqeelbutt99@ 123456gmail.com
                Author notes
                [* ]Correspondence: alinoman@ 123456gcuf.edu.pk (A.N.); yglou@ 123456zju.edu.cn (Y.L.); Tel.: +86-571-889-8622 (Y.L.)
                Author information
                https://orcid.org/0000-0002-4159-199X
                https://orcid.org/0000-0003-0690-4783
                https://orcid.org/000-0002-3262-6134
                Article
                Publisher ID: ijms-20-01882
                DOI: 10.3390/ijms20081882
                PMC ID: 6514886
                PubMed ID: 30995767
                SO-VID: 8315bcdb-cc5b-4623-90aa-148305231fbd
                Copyright © © 2019 by the authors.
                License:

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 18 February 2019
                Date accepted : 10 April 2019
                Categories
                Subject: Review

                ScienceOpen disciplines: Molecular biology
                Keywords: defense,plants,pamps,pathogenesis,transcriptional activity
                Data availability:
                ScienceOpen disciplines: Molecular biology
                Keywords: defense, plants, pamps, pathogenesis, transcriptional activity

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