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Title: Identification of a diguanylate cyclase expressed in the presence of plants and its application for discovering candidate gene products involved in plant colonization by Pantoea sp. YR343

Journal Article · · PLoS ONE

Microbial colonization of plant roots is a highly complex process that requires the coordination and regulation of many gene networks, yet the identities and functions of many of these gene products have yet to be discovered. Pantoea sp. YR343, a gamma-proteobacterium isolated from the rhizosphere of Populus deltoides , forms robust biofilms along the root surfaces of Populus and possesses plant growth-promoting characteristics. In this work, we identified three diguanylate cyclases in the plant-associated microbe Pantoea sp. YR343 that are expressed in the presence of plant roots. One of these diguanylate cyclases, DGC2884, localizes to discrete sites in the cells and its overexpression results in reduced motility and increased EPS production and biofilm formation. We performed a genetic screen by expressing this diguanylate cyclase from an inducible promoter in order to identify candidate gene products that may be involved in root colonization by Pantoea sp. YR343. Further, we demonstrate the importance of other domains in DGC2884 to its activity, which in combination with the genes identified by transposon mutagenesis, may yield insights into the mechanisms of plant association as well as the activity and regulation of homologous enzymes in medically and agriculturally relevant microbes.

Sponsoring Organization:
USDOE
OSTI ID:
1808919
Alternate ID(s):
OSTI ID: 1813277
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 7 Vol. 16; ISSN 1932-6203
Publisher:
Public Library of Science (PLoS)Copyright Statement
Country of Publication:
United States
Language:
English

References (56)

Second Messenger-Mediated Adjustment of Bacterial Swimming Velocity journal April 2010
MASE1 and MASE2: Two Novel Integral Membrane Sensory Domains
  • Nikolskaya, Anastasia N.; Mulkidjanian, Armen Y.; Beech, Iwona B.
  • Journal of Molecular Microbiology and Biotechnology, Vol. 5, Issue 1 https://doi.org/10.1159/000068720
journal January 2003
Quorum Sensing Controls Biofilm Formation in Vibrio cholerae through Modulation of Cyclic Di-GMP Levels and Repression of vpsT journal April 2008
Common Extracellular Sensory Domains in Transmembrane Receptors for Diverse Signal Transduction Pathways in Bacteria and Archaea journal January 2003
The c-di-GMP Binding Protein YcgR Controls Flagellar Motor Direction and Speed to Affect Chemotaxis by a “Backstop Brake” Mechanism journal April 2010
Plant-Growth-Promoting Rhizobacteria journal October 2009
Contribution of Erwinia amylovora Exopolysaccharides Amylovoran and Levan to Biofilm Formation: Implications in Pathogenicity journal November 2009
Riboswitches in Eubacteria Sense the Second Messenger Cyclic Di-GMP journal July 2008
Type VI secretion systems in plant-associated bacteria: T6SS in phytobacteria journal November 2017
Western blot: Technique, theory, and trouble shooting journal January 2012
Cyclic di-GMP as a second messenger journal April 2006
Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria journal September 2002
Pantoea stewartii subsp. stewartii: lessons learned from a xylem-dwelling pathogen of sweet corn: Pantoea stewartii subsp. stewartii journal February 2011
Improved gfp and inaZ Broad-Host-Range Promoter-Probe Vectors journal November 2000
Chp8, a Diguanylate Cyclase from Pseudomonas syringae pv. Tomato DC3000, Suppresses the Pathogen-Associated Molecular Pattern Flagellin, Increases Extracellular Polysaccharides, and Promotes Plant Immune Evasion journal July 2014
Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth: The Streptomyces BldD regulon journal September 2010
Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae journal June 2015
The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors journal October 2001
The structure and inhibition of a GGDEF diguanylate cyclase complexed with (c-di-GMP) 2 at the active site journal November 2011
The EMBL-EBI search and sequence analysis tools APIs in 2019 journal April 2019
Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger journal March 2013
The Pfam protein families database in 2019 journal October 2018
Expression Patterns, Genomic Conservation and Input Into Developmental Regulation of the GGDEF/EAL/HD-GYP Domain Proteins in Streptomyces journal October 2018
Broad-Host-Range Expression Vectors with Tightly Regulated Promoters and Their Use To Examine the Influence of TraR and TraM Expression on Ti Plasmid Quorum Sensing journal July 2008
You’ve come a long way: c-di-GMP signaling journal April 2012
Dynamics of Aspen Roots Colonization by Pseudomonads Reveals Strain-Specific and Mycorrhizal-Specific Patterns of Biofilm Formation journal May 2018
New insights on molecular regulation of biofilm formation in plant-associated bacteria: Molecular regulation of biofilm formation journal November 2015
Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii journal April 2006
Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms journal May 2013
PAS Domains: Internal Sensors of Oxygen, Redox Potential, and Light journal June 1999
YfiBNR Mediates Cyclic di-GMP Dependent Small Colony Variant Formation and Persistence in Pseudomonas aeruginosa journal March 2010
PilZ domain is part of the bacterial c-di-GMP binding protein journal October 2005
Identification of Erwinia amylovora, the Fireblight Pathogen, by Colony Hybridization with DNA from Plasmid pEA29 journal November 1988
Nucleotide, c-di-GMP, c-di-AMP, cGMP, cAMP, (p)ppGpp signaling in bacteria and implications in pathogenesis journal January 2013
Biofilm Formation by Plant-Associated Bacteria journal October 2007
The structure–function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain journal April 2007
Get the Message Out: Cyclic-Di-GMP Regulates Multiple Levels of Flagellum-Based Motility journal January 2008
RNA-Based Fluorescent Biosensors for Live Cell Imaging of Second Messengers Cyclic di-GMP and Cyclic AMP-GMP journal March 2013
Biofilm formation in plant–microbe associations journal December 2004
Cyclic Diguanylate Inversely Regulates Motility and Aggregation in Clostridium difficile journal July 2012
The plant immune system journal November 2006
A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization journal April 2016
GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria: GIL, a new c-di-GMP-binding domain journal July 2014
The PilZ Domain Is a Receptor for the Second Messenger c-di-GMP journal August 2006
The YfiBNR Signal Transduction Mechanism Reveals Novel Targets for the Evolution of Persistent Pseudomonas aeruginosa in Cystic Fibrosis Airways journal June 2012
Mechanisms of Cyclic-di-GMP Signaling in Bacteria journal December 2006
High levels of cyclic-di-GMP in plant-associated P seudomonas correlate with evasion of plant immunity: Pseudomonas cyclic-di-GMP and plant immune evasion journal October 2015
Computationally Guided Discovery and Experimental Validation of Indole-3-acetic Acid Synthesis Pathways journal November 2019
Identification of psl, a Locus Encoding a Potential Exopolysaccharide That Is Essential for Pseudomonas aeruginosa PAO1 Biofilm Formation journal July 2004
Principles of c-di-GMP signalling in bacteria journal April 2009
Investigating the Allosteric Regulation of YfiN from Pseudomonas aeruginosa: Clues from the Structure of the Catalytic Domain journal November 2013
Gateway-Based Destination Vectors for Functional Analyses of Bacterial ORFeomes: Application to the Min System in Brucella abortus journal December 2006
Vibrio cholerae VpsT Regulates Matrix Production and Motility by Directly Sensing Cyclic di-GMP journal February 2010
Biofilms and Cyclic di-GMP (c-di-GMP) Signaling: Lessons from Pseudomonas aeruginosa and Other Bacteria journal April 2016
A gene cluster for amylovoran synthesis in Erwinia amylovora: characterization and relationship to cps genes in Erwinia stewartii journal May 1993
Allosteric Control of Cyclic di-GMP Signaling journal October 2006