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Title: The repABC plasmids with quorum-regulated transfer systems in members of the Rhizobiales divide into two structurally and separately evolving groups

Journal Article · · Genome Biology and Evolution
DOI: https://doi.org/10.1093/gbe/evv227 · OSTI ID:1288452
 [1];  [2];  [3];  [3]
  1. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States). Dept. of Microbiology; Univ. of Illinois at Urbana-Champaign, Urbana, ILL (United States). Dept. of Microbiology
  2. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States). Dept. of Microbiology and Carl R. Woese Inst. for Genomic Biology
  3. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States). Dept. of Microbiology
+ Show Author Affiliations

The large repABC plasmids of the order Rhizobiales with Class I quorum-regulated conjugative transfer systems often define the nature of the bacterium that harbors them. These otherwise diverse plasmids contain a core of highly conserved genes for replication and conjugation raising the question of their evolutionary relationships. In an analysis of 18 such plasmids these elements fall into two organizational classes, Group I and Group II, based on the sites at which cargo DNA is located. Cladograms constructed from proteins of the transfer and quorum-sensing components indicated that those of the Group I plasmids, while coevolving, have diverged from those coevolving proteins of the Group II plasmids. Moreover, within these groups the phylogenies of the proteins usually occupy similar, if not identical, tree topologies. Remarkably, such relationships were not seen among proteins of the replication system; although RepA and RepB coevolve, RepC does not. Nor do the replication proteins coevolve with the proteins of the transfer and quorum-sensing systems. Functional analysis was mostly consistent with phylogenies. TraR activated promoters from plasmids within its group, but not between groups and dimerized with TraR proteins from within but not between groups. However, oriT sequences, which are highly conserved, were processed by the transfer system of plasmids regardless of group. Here, we conclude that these plasmids diverged into two classes based on the locations at which cargo DNA is inserted, that the quorum-sensing and transfer functions are coevolving within but not between the two groups, and that this divergent evolution extends to function.

Research Organization:
Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
SC0006642; AC02-06CH11357
OSTI ID:
1288452
Journal Information:
Genome Biology and Evolution, Journal Name: Genome Biology and Evolution Journal Issue: 12 Vol. 7; ISSN 1759-6653
Publisher:
Society for Molecular Biology and EvolutionCopyright Statement
Country of Publication:
United States
Language:
English

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The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization journal February 2001
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Structural Elements Required for Replication and Incompatibility of the Rhizobium etli Symbiotic Plasmid journal June 2000
The Bases of Crown Gall Tumorigenesis journal July 2000
Quorum Sensing but Not Autoinduction of Ti Plasmid Conjugal Transfer Requires Control by the Opine Regulon and the Antiactivator TraM journal February 2000
TraG from RP4 and TraG and VirD4 from Ti Plasmids Confer Relaxosome Specificity to the Conjugal Transfer System of pTiC58 journal March 2000
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Two Opines Control Conjugal Transfer of an Agrobacterium Plasmid by Regulating Expression of Separate Copies of the Quorum-Sensing Activator Gene traR journal February 2002
Quorum Sensing in Rhizobium sp. Strain NGR234 Regulates Conjugal Transfer (tra) Gene Expression and Influences Growth Rate journal February 2003
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Horizontal gene transfer and diverse functional constrains within a common replication-partitioning system in Alphaproteobacteria: the repABC operon journal January 2009
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Incompatibility Properties of Tartrate Utilization Plasmids Derived fromAgrobacterium vitisStrains journal January 1998
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Characteristics of the nopaline catabolic plasmid in Agrobacterium strains K84 and K1026 used for biological control of crown gall disease journal March 1990
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On plasmid incompatibility journal September 1978
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Characteristics of the nopaline catabolic plasmid in Agrobacterium strains K84 and K1026 used for biological control of crown gall disease journal March 1990
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The repABC plasmid family journal July 2008
Genetic and functional characterization of a yet-unclassified rhizobial Dtr (DNA-transfer-and-replication) region from a ubiquitous plasmid conjugal system present in Sinorhizobium meliloti, in Sinorhizobium medicae, and in other nonrhizobial Gram-negative bacteria journal May 2012
RepA and RepB exert plasmid incompatibility repressing the transcription of the repABC operon journal November 2013
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Rhizobium etli CFN42 contains at least three plasmids of the repABC family: a structural and evolutionary analysis journal September 2002
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The partitioned Rhizobium etli genome: Genetic and metabolic redundancy in seven interacting replicons journal February 2006
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products journal May 2000
Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. journal January 1992
TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. journal May 1994
A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii journal June 1998
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Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells journal April 1999
The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization journal February 2001
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Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm journal October 2000
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Broad Host Range and Promoter Selection Vectors for Bacteria that Interact with Plants journal January 1992
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Broad Host Range and Promoter Selection Vectors for Bacteria that Interact with Plants journal January 1992
Further Evidence that the Vitopine-type pTi's of Agrobacterium vitis Represent a Novel Group of Ti Plasmids journal January 1996
Construction of a Derivative of Agrobacterium tumefaciens C58 That Does Not Mutate to Tetracycline Resistance journal January 2001
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The Composite Genome of the Legume Symbiont Sinorhizobium meliloti journal July 2001
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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
Plasmids with a Chromosome-Like Role in Rhizobia journal January 2011
Quorum-Dependent Mannopine-Inducible Conjugative Transfer of an Agrobacterium Opine-Catabolic Plasmid journal December 2013
Transsexuality in the Rhizosphere: Quorum Sensing Reversibly Converts Agrobacterium tumefaciens from Phenotypically Female to Male journal March 2009
The tRNA arg Gene and engA Are Essential Genes on the 1.7-Mb pSymB Megaplasmid of Sinorhizobium meliloti and Were Translocated Together from the Chromosome in an Ancestral Strain journal November 2012
Multiple genes coding for octopine-degrading enzymes in Agrobacterium. journal January 1978
Interactions between octopine and nopaline plasmids in Agrobacterium tumefaciens. journal January 1980
Relationship of plasmids responsible for hairy root and crown gall tumorigenicity. journal January 1980
Genetic and Sequence Analysis of the pTiC58 trb Locus, Encoding a Mating-Pair Formation System Related to Members of the Type IV Secretion Family journal December 1998
Essential Components of the Ti Plasmidtrb System, a Type IV Macromolecular Transporter journal August 1999
The Replicator of the Nopaline-Type Ti Plasmid pTiC58 Is a Member of the repABC Family and Is Influenced by the TraR-Dependent Quorum-Sensing Regulatory System journal January 2000
Structural Elements Required for Replication and Incompatibility of the Rhizobium etli Symbiotic Plasmid journal June 2000
The Bases of Crown Gall Tumorigenesis journal July 2000
Quorum Sensing but Not Autoinduction of Ti Plasmid Conjugal Transfer Requires Control by the Opine Regulon and the Antiactivator TraM journal February 2000
TraG from RP4 and TraG and VirD4 from Ti Plasmids Confer Relaxosome Specificity to the Conjugal Transfer System of pTiC58 journal March 2000
Identification of the Partitioning Site within therepABC-Type Replicon of the Composite Paracoccus versutus Plasmid pTAV1 journal November 2001
Dynamics of Genome Architecture in Rhizobium sp. Strain NGR234 journal January 2002
A New Type IV Secretion System Promotes Conjugal Transfer in Agrobacterium tumefaciens journal September 2002
Quorum Sensing in Rhizobium sp. Strain NGR234 Regulates Conjugal Transfer (tra) Gene Expression and Influences Growth Rate journal February 2003
Uniform nomenclature for bacterial plasmids: a proposal. journal January 1976
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
Plasmids with a Chromosome-Like Role in Rhizobia journal January 2011
Quorum-Dependent Mannopine-Inducible Conjugative Transfer of an Agrobacterium Opine-Catabolic Plasmid journal December 2013
Transsexuality in the Rhizosphere: Quorum Sensing Reversibly Converts Agrobacterium tumefaciens from Phenotypically Female to Male journal March 2009
The tRNA arg Gene and engA Are Essential Genes on the 1.7-Mb pSymB Megaplasmid of Sinorhizobium meliloti and Were Translocated Together from the Chromosome in an Ancestral Strain journal November 2012
The oriT region of the Agrobacterium tumefaciens Ti plasmid pTiC58 shares DNA sequence identity with the transfer origins of RSF1010 and RK2/RP4 and with T-region borders. journal October 1992
A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. journal May 1994
A new regulatory element modulates homoserine lactone-mediated autoinduction of Ti plasmid conjugal transfer. journal January 1995
Activity of the Agrobacterium Ti plasmid conjugal transfer regulator TraR is inhibited by the product of the traM gene. journal January 1995
The tra region of the nopaline-type Ti plasmid is a chimera with elements related to the transfer systems of RSF1010, RP4, and F. journal July 1996
Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. journal January 1996
The Replicator of the Nopaline-Type Ti Plasmid pTiC58 Is a Member of the repABC Family and Is Influenced by the TraR-Dependent Quorum-Sensing Regulatory System journal January 2000
Structural Elements Required for Replication and Incompatibility of the Rhizobium etli Symbiotic Plasmid journal June 2000
The Bases of Crown Gall Tumorigenesis journal July 2000
Quorum Sensing but Not Autoinduction of Ti Plasmid Conjugal Transfer Requires Control by the Opine Regulon and the Antiactivator TraM journal February 2000
TraG from RP4 and TraG and VirD4 from Ti Plasmids Confer Relaxosome Specificity to the Conjugal Transfer System of pTiC58 journal March 2000
Identification of the Partitioning Site within therepABC-Type Replicon of the Composite Paracoccus versutus Plasmid pTAV1 journal November 2001
Dynamics of Genome Architecture in Rhizobium sp. Strain NGR234 journal January 2002
A New Type IV Secretion System Promotes Conjugal Transfer in Agrobacterium tumefaciens journal September 2002
Two Opines Control Conjugal Transfer of an Agrobacterium Plasmid by Regulating Expression of Separate Copies of the Quorum-Sensing Activator Gene traR journal February 2002
Quorum Sensing in Rhizobium sp. Strain NGR234 Regulates Conjugal Transfer (tra) Gene Expression and Influences Growth Rate journal February 2003
Plasmid transfer systems in the rhizobia journal August 2009
Plasmid transfer systems in the rhizobia journal August 2009
MUSCLE: a multiple sequence alignment method with reduced time and space complexity journal August 2004
Horizontal gene transfer and diverse functional constrains within a common replication-partitioning system in Alphaproteobacteria: the repABC operon journal January 2009
The replication origin of a repABC plasmid journal January 2011
Confidence Limits on Phylogenies: An Approach Using the Bootstrap journal July 1985

Cited By (4)

Evolutionary Relatedness and Classification of Tumor-Inducing and Opine-Catabolic Plasmids in Three Rhizobium rhizogenes Strains Isolated from the Same Crown Gall Tumor journal April 2019
Symbiosis genes show a unique pattern of introgression and selection within a Rhizobium leguminosarum species complex posted_content November 2019
Quorum-dependent transfer of the opine-catabolic plasmid pAoF64/95 is regulated by a novel mechanism involving inhibition of the TraR antiactivator TraM journal April 2018
Symbiosis genes show a unique pattern of introgression and selection within a Rhizobium leguminosarum species complex posted_content November 2019

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Alphaproteobacteria
RepABC
agrobacterium-tumefaciens
broad-host-range
complete nucleotide-sequence
conjugal transfer
conjugative transfer genes
etli symbiotic plasmid
horizontal transfer
multiple sequence alignment
plasmid evolution
quorum-sensing
sp strain ngr234
trar-like protein
tumefaciens ti plasmid
tumor-inducing ti