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      Bacterial LuxR solos have evolved to respond to different molecules including signals from plants

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          Abstract

          A future challenge will be understanding the extensive communication that most likely takes place in bacterial interspecies and interkingdom signaling between plants and bacteria. A major bacterial inter-cellular signaling system in Gram-negative bacteria is LuxI/R quorum sensing (QS) based on the production (via the LuxI-family proteins) and detection (via the LuxR-family proteins) of N-acyl homoserine lactones (AHLs) signaling molecules. LuxR proteins which have the same modular structure of QS LuxRs but are devoid of a cognate LuxI AHL synthase are called solos. LuxR solos have been shown to be responsible to respond to exogenous AHLs produced by neighboring cells as well endogenously produced AHLs. It is now also evident that some LuxR proteins have evolved from the ability to binding AHLs and respond to other molecules/signals. For example, recent research has shown that a sub-family of LuxR solos responds to small molecules produced by plants. This indicates the presence of a uni-directional interkingdom signaling system occurring from plants to bacteria. In addition LuxR solos have now been also implicated to respond to endogenously produced signals which are not AHLs. In this Mini Review article we will discuss current trends and implications of the role of LuxR solos in bacterial responses to other signals using proteins related to AHL QS systems.

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          Most cited references 49

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          Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing.

          Quorum sensing is an example of community behavior prevalent among diverse bacterial species. The term "quorum sensing" describes the ability of a microorganism to perceive and respond to microbial population density, usually relying on the production and subsequent response to diffusible signal molecules. A significant number of gram-negative bacteria produce acylated homoserine lactones (acyl-HSLs) as signal molecules that function in quorum sensing. Bacteria that produce acyl-HSLs can respond to the local concentration of the signaling molecules, and high population densities foster the accumulation of inducing levels of acyl-HSLs. Depending upon the bacterial species, the physiological processes regulated by quorum sensing are extremely diverse, ranging from bioluminescence to swarming motility. Acyl-HSL quorum sensing has become a paradigm for intercellular signaling mechanisms. A flurry of research over the past decade has led to significant understanding of many aspects of quorum sensing including the synthesis of acyl-HSLs, the receptors that recognize the acyl-HSL signal and transduce this information to the level of gene expression, and the interaction of these receptors with the transcriptional machinery. Recent studies have begun to integrate acyl-HSL quorum sensing into global regulatory networks and establish its role in developing and maintaining the structure of bacterial communities.
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            Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators.

            The importance of accurate demographic information is reflected in the United States Constitution, Article 1, which provides for a decennial census of this country's human population. Bacteria also conduct a census of their population and do so more frequently, more efficiently, and as far we know, with little if any of the political contentiousness caused by human demographers. Many examples have been found of particular bacterial genes, operons, or regulons that are expressed preferentially at high cell densities. Many of these are regulated by proteins related to the LuxR and LuxI proteins of Vibrio fischeri, and by a diffusible pheromone called an autoinducer. LuxR and LuxI and their cognate autoinducer (3-oxohexanoyl homoserine lactone, designated VAI-1) provide an important model to describe the functions of this family of proteins. LuxR is a VAI-1 receptor and a VAI-1-dependent transcriptional activator, and LuxI directs the synthesis of VAI-1. VAI-1 diffuses across the bacterial envelope, and intracellular concentrations of it are therefore strongly increased by nearby VAI-1-producing bacteria. Similar systems regulate pathogenesis factors in Pseudomonas aeruginosa and Erwinia spp., as well as T1 plasmid conjugal transfer in Agrobacterium tumefaciens, and many other genes in numerous genera of gram-negative bacteria. Genetic analyses of these systems have revealed a high degree of functional conservation, while also uncovering features that are unique to each.
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              Biofilm formation by plant-associated bacteria.

              Plants support a diverse array of bacteria, including parasites, mutualists, and commensals on and around their roots, in the vasculature, and on aerial tissues. These microbes have a profound influence on plant health and productivity. Bacteria physically interact with surfaces to form complex multicellular and often multispecies assemblies, including biofilms and smaller aggregates. There is growing appreciation that the intensity, duration, and outcome of plant-microbe interactions are significantly influenced by the conformation of adherent microbial populations. Biofilms on different tissues have unique properties, reflecting the prevailing conditions at those sites. Attachment is required for biofilm formation, and bacteria interact with plant tissues through adhesins including polysaccharides and surface proteins, with initial contact often mediated by active motility. Recognition between lectins and their cognate carbohydrates is a common means of specificity. Biofilm development and the resulting intimate interactions with plants often require cell-cell communication between colonizing bacteria.
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                Author and article information

                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                12 November 2013
                2013
                : 4
                Affiliations
                International Centre for Genetic Engineering and Biotechnology Trieste, Italy
                Author notes

                Edited by: Anton Dr. Hartmann, Helmholtz Zentrum München, German Research Center for Environmental Health, Germany

                Reviewed by: Choong-Min Ryu, Korea Research Institute of Bioscience and Biotechnology, South Korea; Andrea Genre, University of Turin, Italy

                *Correspondence: Vittorio Venturi, International Centre for Genetic Engineering and Biotechnology, Padriciano 99, 34149 Trieste, Italy e-mail: venturi@ 123456icgeb.org

                Present address: Zulma R. Suárez-Moreno, Biocultivos S. A. Instituto de Biotecnología, Universidad Nacional de Colombia, Ciudad Universitaria, Cra. 30 Np. 45-03, Bogotá DC, Colombia; Juan F. González, Department of Microbial Infection and Immunity, The Ohio State University, Columbus OH, USA

                This article was submitted to Plant-Microbe Interaction, a section of the journal Frontiers in Plant Science.

                Article
                10.3389/fpls.2013.00447
                3824090
                Copyright © 2013 Patel, Suárez-Moreno, Degrassi, Subramoni, González and Venturi.

                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: 1, Tables: 0, Equations: 0, References: 48, Pages: 5, Words: 0
                Categories
                Plant Science
                Mini Review Article

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