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      The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus

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          Abstract

          Bacterial infection of interior tissues of legume root nodules is controlled at the epidermal cell layer and is closely coordinated with progressing organ development. Using spontaneous nodulating Lotus japonicus plant mutants to uncouple nodule organogenesis from infection, we have determined the role of 16 genes in these two developmental processes. We show that host-encoded mechanisms control three alternative entry processes operating in the epidermis, the root cortex and at the single cell level. Single cell infection did not involve the formation of trans-cellular infection threads and was independent of host Nod-factor receptors and bacterial Nod-factor signals. In contrast, Nod-factor perception was required for epidermal root hair infection threads, whereas primary signal transduction genes preceding the secondary Ca 2+ oscillations have an indirect role. We provide support for the origin of rhizobial infection through direct intercellular epidermal invasion and subsequent evolution of crack entry and root hair invasions observed in most extant legumes.

          Abstract

          Plant and bacteria symbiosis in some species results in the coordinate formation of nitrogen fixing nodules and infection of the plant host. Using mutant Lotus japonicus plants, Madsen and colleagues have determined the role of 16 different genes in these two processes.

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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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            A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals.

            Plants belonging to the legume family develop nitrogen-fixing root nodules in symbiosis with bacteria commonly known as rhizobia. The legume host encodes all of the functions necessary to build the specialized symbiotic organ, the nodule, but the process is elicited by the bacteria. Molecular communication initiates the interaction, and signals, usually flavones, secreted by the legume root induce the bacteria to produce a lipochitin-oligosaccharide signal molecule (Nod-factor), which in turn triggers the plant organogenic process. An important determinant of bacterial host specificity is the structure of the Nod-factor, suggesting that a plant receptor is involved in signal perception and signal transduction initiating the plant developmental response. Here we describe the cloning of a putative Nod-factor receptor kinase gene (NFR5) from Lotus japonicus. NFR5 is essential for Nod-factor perception and encodes an unusual transmembrane serine/threonine receptor-like kinase required for the earliest detectable plant responses to bacteria and Nod-factor. The extracellular domain of the putative receptor has three modules with similarity to LysM domains known from peptidoglycan-binding proteins and chitinases. Together with an atypical kinase domain structure this characterizes an unusual receptor-like kinase.
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              A plant regulator controlling development of symbiotic root nodules.

              Symbiotic nitrogen-fixing root nodules on legumes are founded by root cortical cells that de-differentiate and restart cell division to establish nodule primordia. Bacterial microsymbionts invade these primordia through infection threads laid down by the plant and, after endocytosis, membrane-enclosed bacteroids occupy cells in the nitrogen-fixing tissue of functional nodules. The bacteria excrete lipochitin oligosaccharides, triggering a developmental process that is controlled by the plant and can be suppressed. Nodule inception initially relies on cell competence in a narrow infection zone located just behind the growing root tip. Older nodules then regulate the number of nodules on a root system by suppressing the development of nodule primordia. To identify the regulatory components that act early in nodule induction, we characterized a transposon-tagged Lotus japonicus mutant, nin (for nodule inception), arrested at the stage of bacterial recognition. We show that nin is required for the formation of infection threads and the initiation of primordia. NIN protein has regional similarity to transcription factors, and the predicted DNA-binding/dimerization domain identifies and typifies a consensus motif conserved in plant proteins with a function in nitrogen-controlled development.
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                Author and article information

                Journal
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                12 April 2010
                : 1
                : 1
                : 1-12
                Affiliations
                [1 ]Department of Molecular Biology, Centre for Carbohydrate Recognition and Signalling, Aarhus University , Gustav Wieds Vej 10, Aarhus C DK-8000, Denmark.
                [2 ]Department of Microbiology and Immunology, University of Otago, PO Box 56 , Dunedin 9054, New Zealand.
                [3 ] EPI division, Scottish Crop Research Institute, Invergowrie , Dundee DD2 5DA, UK.
                Author notes
                [†]

                Present address: Génomique, Environnementale et Evolutive Section 3 CNRS UMR8197, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), 46 rue d'Ulm, 75230 Paris Cedex 05, France

                Article
                ncomms1009
                10.1038/ncomms1009
                2892300
                20975672
                95b085cc-a3aa-48e2-8cb0-3ad97f88ff1b
                Copyright © 2010, Nature Publishing Group

                This work is licensed under a Creative Commons Attribution-NonCommercial-Share Alike 3.0 License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/

                History
                : 14 January 2010
                : 05 March 2010
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