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      Reactive Oxygen Species and Nitric Oxide Control Early Steps of the Legume – Rhizobium Symbiotic Interaction

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          Abstract

          The symbiotic interaction between legumes and nitrogen-fixing rhizobium bacteria leads to the formation of a new organ, the nodule. Early steps of the interaction are characterized by the production of bacterial Nod factors, the reorientation of root-hair tip growth, the formation of an infection thread (IT) in the root hair, and the induction of cell division in inner cortical cells of the root, leading to a nodule primordium formation. Reactive oxygen species (ROS) and nitric oxide (NO) have been detected in early steps of the interaction. ROS/NO are determinant signals to arbitrate the specificity of this mutualistic association and modifications in their content impair the development of the symbiotic association. The decrease of ROS level prevents root hair curling and ITs formation, and that of NO conducts to delayed nodule formation. In root hairs, NADPH oxidases were shown to produce ROS which could be involved in the hair tip growth process. The use of enzyme inhibitors suggests that nitrate reductase and NO synthase-like enzymes are the main route for NO production during the early steps of the interaction. Transcriptomic analyses point to the involvement of ROS and NO in the success of the infection process, the induction of early nodulin gene expression, and the repression of plant defense, thereby favoring the establishment of the symbiosis. The occurrence of an interplay between ROS and NO was further supported by the finding of both S-sulfenylated and S-nitrosylated proteins during early symbiotic interaction, linking ROS/NO production to a redox-based regulation of the symbiotic process.

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          Most cited references 67

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          ROS signaling: the new wave?

          Reactive oxygen species (ROS) play a multitude of signaling roles in different organisms from bacteria to mammalian cells. They were initially thought to be toxic byproducts of aerobic metabolism, but have now been acknowledged as central players in the complex signaling network of cells. In this review, we will attempt to address several key questions related to the use of ROS as signaling molecules in cells, including the dynamics and specificity of ROS signaling, networking of ROS with other signaling pathways, ROS signaling within and across different cells, ROS waves and the evolution of the ROS gene network. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            Coordinating nodule morphogenesis with rhizobial infection in legumes.

            The formation of nitrogen-fixing nodules on legumes requires an integration of infection by rhizobia at the root epidermis and the initiation of cell division in the cortex, several cell layers away from the sites of infection. Several recent developments have added to our understanding of the signaling events in the epidermis associated with the perception of rhizobial nodulation factors and the role of plant hormones in the activation of cell division leading to nodule morphogenesis. This review focuses on the tissue-specific nature of the developmental processes associated with nodulation and the mechanisms by which these processes are coordinated during the formation of a nodule.
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              A burst of plant NADPH oxidases.

              Reactive oxygen species (ROS) are highly reactive molecules able to damage cellular components but they also act as cell signalling elements. ROS are produced by many different enzymatic systems. Plant NADPH oxidases, also known as respiratory burst oxidase homologues (RBOHs), are the most thoroughly studied enzymatic ROS-generating systems and our understanding of their involvement in various plant processes has increased considerably in recent years. In this review we discuss their roles as ROS producers during cell growth, plant development and plant response to abiotic environmental constraints and biotic interactions, both pathogenic and symbiotic. This broad range of functions suggests that RBOHs may serve as important molecular 'hubs' during ROS-mediated signalling in plants. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                08 April 2016
                2016
                : 7
                Affiliations
                Institut Sophia Agrobiotech, UMR INRA Université Nice Sophia Antipolis CNRS Sophia Antipolis, France
                Author notes

                Edited by: Jeremy Astier, Helmholtz Zentrum München, Germany

                Reviewed by: Alberto A. Iglesias, Universidad Nacional del Litoral – Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina; Andreas Niebel, Centre National de la Recherche Scientifique, France

                *Correspondence: Alexandre Boscari, alexandre.boscari@ 123456sophia.inra.fr

                This article was submitted to Plant Biotic Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2016.00454
                4824774
                27092165
                Copyright © 2016 Damiani, Pauly, Puppo, Brouquisse and Boscari.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 71, Pages: 8, Words: 0
                Funding
                Funded by: Institut National de la Recherche Agronomique 10.13039/501100006488
                Funded by: Centre National de la Recherche Scientifique 10.13039/501100004794
                Categories
                Plant Science
                Mini Review

                Plant science & Botany

                symbiosis, legume, nitric oxide, nitrogen fixation, rhizobium

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