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      Receptor-mediated exopolysaccharide perception controls bacterial infection.

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          Abstract

          Surface polysaccharides are important for bacterial interactions with multicellular organisms, and some are virulence factors in pathogens. In the legume-rhizobium symbiosis, bacterial exopolysaccharides (EPS) are essential for the development of infected root nodules. We have identified a gene in Lotus japonicus, Epr3, encoding a receptor-like kinase that controls this infection. We show that epr3 mutants are defective in perception of purified EPS, and that EPR3 binds EPS directly and distinguishes compatible and incompatible EPS in bacterial competition studies. Expression of Epr3 in epidermal cells within the susceptible root zone shows that the protein is involved in bacterial entry, while rhizobial and plant mutant studies suggest that Epr3 regulates bacterial passage through the plant's epidermal cell layer. Finally, we show that Epr3 expression is inducible and dependent on host perception of bacterial nodulation (Nod) factors. Plant-bacterial compatibility and bacterial access to legume roots is thus regulated by a two-stage mechanism involving sequential receptor-mediated recognition of Nod factor and EPS signals.

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          Most cited references51

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          Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases.

          Although most higher plants establish a symbiosis with arbuscular mycorrhizal fungi, symbiotic nitrogen fixation with rhizobia is a salient feature of legumes. Despite this host range difference, mycorrhizal and rhizobial invasion shares a common plant-specified genetic programme controlling the early host interaction. One feature distinguishing legumes is their ability to perceive rhizobial-specific signal molecules. We describe here two LysM-type serine/threonine receptor kinase genes, NFR1 and NFR5, enabling the model legume Lotus japonicus to recognize its bacterial microsymbiont Mesorhizobium loti. The extracellular domains of the two transmembrane kinases resemble LysM domains of peptidoglycan- and chitin-binding proteins, suggesting that they may be involved directly in perception of the rhizobial lipochitin-oligosaccharide signal. We show that NFR1 and NFR5 are required for the earliest physiological and cellular responses to this lipochitin-oligosaccharide signal, and demonstrate their role in the mechanism establishing susceptibility of the legume root for bacterial infection.
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            Innate immune recognition of the microbiota promotes host-microbial symbiosis.

            Pattern-recognition receptors (PRRs) are traditionally known to sense microbial molecules during infection to initiate inflammatory responses. However, ligands for PRRs are not exclusive to pathogens and are abundantly produced by the resident microbiota during normal colonization. Mechanism(s) that underlie this paradox have remained unclear. Recent studies reveal that gut bacterial ligands from the microbiota signal through PRRs to promote development of host tissue and the immune system, and protection from disease. Evidence from both invertebrate and vertebrate models reveals that innate immune receptors are required to promote long-term colonization by the microbiota. This emerging perspective challenges current models in immunology and suggests that PRRs may have evolved, in part, to mediate the bidirectional cross-talk between microbial symbionts and their hosts.
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              How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model.

              Nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which the bacteria can enter the plant root. Once the bacteria have been endocytosed within a host-membrane-bound compartment by root cells, the bacteria differentiate into a new form that can convert atmospheric nitrogen into ammonia. Bacterial differentiation and nitrogen fixation are dependent on the microaerobic environment and other support factors provided by the plant. In return, the plant receives nitrogen from the bacteria, which allows it to grow in the absence of an external nitrogen source. Here, we review recent discoveries about the mutual recognition process that allows the model rhizobial symbiont Sinorhizobium meliloti to invade and differentiate inside its host plant alfalfa (Medicago sativa) and the model host plant barrel medic (Medicago truncatula).
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                Author and article information

                Journal
                Nature
                Nature
                1476-4687
                0028-0836
                Jul 16 2015
                : 523
                : 7560
                Affiliations
                [1 ] 1] Centre for Carbohydrate Recognition and Signalling. Aarhus University, Aarhus 8000 C, Denmark [2] Department of Molecular Biology and Genetics, Aarhus University, Aarhus 8000 C, Denmark.
                [2 ] 1] Centre for Carbohydrate Recognition and Signalling. Aarhus University, Aarhus 8000 C, Denmark [2] Department of Molecular Biology and Genetics, Aarhus University, Aarhus 8000 C, Denmark [3] Department of Microbiology and Immunology, University of Otago, Dunedin 9054, New Zealand.
                [3 ] 1] Centre for Carbohydrate Recognition and Signalling. Aarhus University, Aarhus 8000 C, Denmark [2] Department of Chemistry, University of Copenhagen, Frederiksberg 1871 C, Denmark.
                [4 ] Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia 30602, USA.
                [5 ] 1] Centre for Carbohydrate Recognition and Signalling. Aarhus University, Aarhus 8000 C, Denmark [2] Department of Microbiology and Immunology, University of Otago, Dunedin 9054, New Zealand.
                Article
                nature14611
                10.1038/nature14611
                26153863
                2a34a1f2-0287-4114-8532-af3f698b4f30
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