Unexpected conservation and global transmission of agrobacterial virulence plasmids
Plasmids are widespread among bacteria and are important because they spread virulence and antibiotic resistance traits, among others. They are horizontally transferred between strains and species, so it is difficult to work out their evolution and epidemiology. Agrobacteria, a diverse grouping of s...
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creator | Weisberg, Alexandra J. Davis, Edward W. Tabima, Javier Belcher, Michael S. Miller, Marilyn Kuo, Chih-Horng Loper, Joyce E. Grünwald, Niklaus J. Putnam, Melodie L. Chang, Jeff H. |
description | Plasmids are widespread among bacteria and are important because they spread virulence and antibiotic resistance traits, among others. They are horizontally transferred between strains and species, so it is difficult to work out their evolution and epidemiology. Agrobacteria, a diverse grouping of species that infect plants, inject oncogenic Ti and Ri plasmids, which cause crown galls and hairy root diseases, respectively. The upside is that these plasmids have become valuable biotechnological tools. Weisberg
et al.
combed through an 80-year-old collection of
Agrobacterium
strains but found a surprisingly low diversity of plasmids. It is puzzling how limited the number of plasmid lineages is despite reported high levels of plasmid recombination, but what is clear is how plant production systems have influenced plasmid spread into various genomic backbones.
Science
, this issue p.
eaba5256
Combined analysis of chromosomal ancestry and horizontally transmitted plasmids offers insights into the spread of bacterial disease.
The accelerated evolution and spread of pathogens are threats to host species. Agrobacteria require an oncogenic Ti or Ri plasmid to transfer genes into plants and cause disease. We developed a strategy to characterize virulence plasmids and applied it to analyze hundreds of strains collected between 1927 and 2017, on six continents and from more than 50 host species. In consideration of prior evidence for prolific recombination, it was surprising that oncogenic plasmids are descended from a few conserved lineages. Characterization of a hierarchy of features that promote or constrain plasticity allowed inference of the evolutionary history across the plasmid lineages. We uncovered epidemiological patterns that highlight the importance of plasmid transmission in pathogen diversification as well as in long-term persistence and the global spread of disease. |
doi_str_mv | 10.1126/science.aba5256 |
format | Article |
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et al.
combed through an 80-year-old collection of
Agrobacterium
strains but found a surprisingly low diversity of plasmids. It is puzzling how limited the number of plasmid lineages is despite reported high levels of plasmid recombination, but what is clear is how plant production systems have influenced plasmid spread into various genomic backbones.
Science
, this issue p.
eaba5256
Combined analysis of chromosomal ancestry and horizontally transmitted plasmids offers insights into the spread of bacterial disease.
The accelerated evolution and spread of pathogens are threats to host species. Agrobacteria require an oncogenic Ti or Ri plasmid to transfer genes into plants and cause disease. We developed a strategy to characterize virulence plasmids and applied it to analyze hundreds of strains collected between 1927 and 2017, on six continents and from more than 50 host species. In consideration of prior evidence for prolific recombination, it was surprising that oncogenic plasmids are descended from a few conserved lineages. Characterization of a hierarchy of features that promote or constrain plasticity allowed inference of the evolutionary history across the plasmid lineages. We uncovered epidemiological patterns that highlight the importance of plasmid transmission in pathogen diversification as well as in long-term persistence and the global spread of disease.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.aba5256</identifier><language>eng</language><publisher>Washington: The American Association for the Advancement of Science</publisher><subject>Agricultural management ; Animal health ; Antibiotic resistance ; Antibiotics ; Bacteria ; Biological evolution ; Biotechnology ; Datasets ; Deoxyribonucleic acid ; Disease ; Disease control ; DNA ; Drug resistance ; Epidemiology ; Eukaryotes ; Evolution ; Evolutionary genetics ; Food safety ; Galls ; Genes ; Genetic engineering ; Genetics ; Hairy root ; Identification methods ; Loci ; Mathematical models ; Modularity ; Pathogenicity ; Pathogens ; Phylogenetics ; Phylogeny ; Plant diseases ; Plant production ; Plasmids ; Recombination ; Replication ; Species ; Strains (organisms) ; Strategy ; Symbiosis ; Virulence</subject><ispartof>Science (American Association for the Advancement of Science), 2020-06, Vol.368 (6495)</ispartof><rights>Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c232t-9951c0fb7e3687b099fd31ed5fb68de86ae34f852504e4e748d13815455ab5a13</citedby><cites>FETCH-LOGICAL-c232t-9951c0fb7e3687b099fd31ed5fb68de86ae34f852504e4e748d13815455ab5a13</cites><orcidid>0000-0002-1833-0695 ; 0000-0002-0045-1368 ; 0000-0002-0399-9556 ; 0000-0003-2352-6817 ; 0000-0003-1656-7602 ; 0000-0003-1229-4272 ; 0000-0002-2857-0529 ; 0000-0002-3603-2691 ; 0000-0003-3501-5969</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,2871,2872,27901,27902</link.rule.ids></links><search><creatorcontrib>Weisberg, Alexandra J.</creatorcontrib><creatorcontrib>Davis, Edward W.</creatorcontrib><creatorcontrib>Tabima, Javier</creatorcontrib><creatorcontrib>Belcher, Michael S.</creatorcontrib><creatorcontrib>Miller, Marilyn</creatorcontrib><creatorcontrib>Kuo, Chih-Horng</creatorcontrib><creatorcontrib>Loper, Joyce E.</creatorcontrib><creatorcontrib>Grünwald, Niklaus J.</creatorcontrib><creatorcontrib>Putnam, Melodie L.</creatorcontrib><creatorcontrib>Chang, Jeff H.</creatorcontrib><title>Unexpected conservation and global transmission of agrobacterial virulence plasmids</title><title>Science (American Association for the Advancement of Science)</title><description>Plasmids are widespread among bacteria and are important because they spread virulence and antibiotic resistance traits, among others. They are horizontally transferred between strains and species, so it is difficult to work out their evolution and epidemiology. Agrobacteria, a diverse grouping of species that infect plants, inject oncogenic Ti and Ri plasmids, which cause crown galls and hairy root diseases, respectively. The upside is that these plasmids have become valuable biotechnological tools. Weisberg
et al.
combed through an 80-year-old collection of
Agrobacterium
strains but found a surprisingly low diversity of plasmids. It is puzzling how limited the number of plasmid lineages is despite reported high levels of plasmid recombination, but what is clear is how plant production systems have influenced plasmid spread into various genomic backbones.
Science
, this issue p.
eaba5256
Combined analysis of chromosomal ancestry and horizontally transmitted plasmids offers insights into the spread of bacterial disease.
The accelerated evolution and spread of pathogens are threats to host species. Agrobacteria require an oncogenic Ti or Ri plasmid to transfer genes into plants and cause disease. We developed a strategy to characterize virulence plasmids and applied it to analyze hundreds of strains collected between 1927 and 2017, on six continents and from more than 50 host species. In consideration of prior evidence for prolific recombination, it was surprising that oncogenic plasmids are descended from a few conserved lineages. Characterization of a hierarchy of features that promote or constrain plasticity allowed inference of the evolutionary history across the plasmid lineages. We uncovered epidemiological patterns that highlight the importance of plasmid transmission in pathogen diversification as well as in long-term persistence and the global spread of disease.</description><subject>Agricultural management</subject><subject>Animal health</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Biological evolution</subject><subject>Biotechnology</subject><subject>Datasets</subject><subject>Deoxyribonucleic acid</subject><subject>Disease</subject><subject>Disease control</subject><subject>DNA</subject><subject>Drug resistance</subject><subject>Epidemiology</subject><subject>Eukaryotes</subject><subject>Evolution</subject><subject>Evolutionary genetics</subject><subject>Food safety</subject><subject>Galls</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genetics</subject><subject>Hairy root</subject><subject>Identification methods</subject><subject>Loci</subject><subject>Mathematical models</subject><subject>Modularity</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Plant diseases</subject><subject>Plant production</subject><subject>Plasmids</subject><subject>Recombination</subject><subject>Replication</subject><subject>Species</subject><subject>Strains (organisms)</subject><subject>Strategy</subject><subject>Symbiosis</subject><subject>Virulence</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNpdkL1PwzAQxS0EEqUws0ZiYUl7tuPEHlHFl1SJATpHjnOpUqV2sJMK_nscNRPTSe9-d_fuEXJPYUUpy9fBtGgNrnSlBRP5BVlQUCJVDPglWQDwPJVQiGtyE8IBIPYUX5DPncWfHs2AdWKcDehPemidTbStk33nKt0lg9c2HNsQJt01id77qMcR38buqfVjN11O-k5HrA635KrRXcC7uS7J7uX5a_OWbj9e3zdP29QwzoZUKUENNFWBPJdFBUo1NadYi6bKZY0y18izRsZnIMMMi0zWlEsqMiF0JTTlS_J43tt79z1iGMpo0mDXaYtuDCXLKHAhASb04R96cKO30V2kQBUsF4WK1PpMGe9C8NiUvW-P2v-WFMop5HIOuZxD5n_A1HLM</recordid><startdate>20200605</startdate><enddate>20200605</enddate><creator>Weisberg, Alexandra J.</creator><creator>Davis, Edward W.</creator><creator>Tabima, Javier</creator><creator>Belcher, Michael S.</creator><creator>Miller, Marilyn</creator><creator>Kuo, Chih-Horng</creator><creator>Loper, Joyce 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resistance</topic><topic>Epidemiology</topic><topic>Eukaryotes</topic><topic>Evolution</topic><topic>Evolutionary genetics</topic><topic>Food safety</topic><topic>Galls</topic><topic>Genes</topic><topic>Genetic engineering</topic><topic>Genetics</topic><topic>Hairy root</topic><topic>Identification methods</topic><topic>Loci</topic><topic>Mathematical models</topic><topic>Modularity</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Plant diseases</topic><topic>Plant production</topic><topic>Plasmids</topic><topic>Recombination</topic><topic>Replication</topic><topic>Species</topic><topic>Strains (organisms)</topic><topic>Strategy</topic><topic>Symbiosis</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Weisberg, Alexandra J.</creatorcontrib><creatorcontrib>Davis, Edward W.</creatorcontrib><creatorcontrib>Tabima, Javier</creatorcontrib><creatorcontrib>Belcher, Michael S.</creatorcontrib><creatorcontrib>Miller, Marilyn</creatorcontrib><creatorcontrib>Kuo, Chih-Horng</creatorcontrib><creatorcontrib>Loper, Joyce E.</creatorcontrib><creatorcontrib>Grünwald, Niklaus J.</creatorcontrib><creatorcontrib>Putnam, Melodie L.</creatorcontrib><creatorcontrib>Chang, Jeff H.</creatorcontrib><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials 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Chih-Horng</au><au>Loper, Joyce E.</au><au>Grünwald, Niklaus J.</au><au>Putnam, Melodie L.</au><au>Chang, Jeff H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Unexpected conservation and global transmission of agrobacterial virulence plasmids</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><date>2020-06-05</date><risdate>2020</risdate><volume>368</volume><issue>6495</issue><issn>0036-8075</issn><eissn>1095-9203</eissn><abstract>Plasmids are widespread among bacteria and are important because they spread virulence and antibiotic resistance traits, among others. They are horizontally transferred between strains and species, so it is difficult to work out their evolution and epidemiology. Agrobacteria, a diverse grouping of species that infect plants, inject oncogenic Ti and Ri plasmids, which cause crown galls and hairy root diseases, respectively. The upside is that these plasmids have become valuable biotechnological tools. Weisberg
et al.
combed through an 80-year-old collection of
Agrobacterium
strains but found a surprisingly low diversity of plasmids. It is puzzling how limited the number of plasmid lineages is despite reported high levels of plasmid recombination, but what is clear is how plant production systems have influenced plasmid spread into various genomic backbones.
Science
, this issue p.
eaba5256
Combined analysis of chromosomal ancestry and horizontally transmitted plasmids offers insights into the spread of bacterial disease.
The accelerated evolution and spread of pathogens are threats to host species. Agrobacteria require an oncogenic Ti or Ri plasmid to transfer genes into plants and cause disease. We developed a strategy to characterize virulence plasmids and applied it to analyze hundreds of strains collected between 1927 and 2017, on six continents and from more than 50 host species. In consideration of prior evidence for prolific recombination, it was surprising that oncogenic plasmids are descended from a few conserved lineages. Characterization of a hierarchy of features that promote or constrain plasticity allowed inference of the evolutionary history across the plasmid lineages. We uncovered epidemiological patterns that highlight the importance of plasmid transmission in pathogen diversification as well as in long-term persistence and the global spread of disease.</abstract><cop>Washington</cop><pub>The American Association for the Advancement of Science</pub><doi>10.1126/science.aba5256</doi><orcidid>https://orcid.org/0000-0002-1833-0695</orcidid><orcidid>https://orcid.org/0000-0002-0045-1368</orcidid><orcidid>https://orcid.org/0000-0002-0399-9556</orcidid><orcidid>https://orcid.org/0000-0003-2352-6817</orcidid><orcidid>https://orcid.org/0000-0003-1656-7602</orcidid><orcidid>https://orcid.org/0000-0003-1229-4272</orcidid><orcidid>https://orcid.org/0000-0002-2857-0529</orcidid><orcidid>https://orcid.org/0000-0002-3603-2691</orcidid><orcidid>https://orcid.org/0000-0003-3501-5969</orcidid></addata></record> |
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subjects | Agricultural management Animal health Antibiotic resistance Antibiotics Bacteria Biological evolution Biotechnology Datasets Deoxyribonucleic acid Disease Disease control DNA Drug resistance Epidemiology Eukaryotes Evolution Evolutionary genetics Food safety Galls Genes Genetic engineering Genetics Hairy root Identification methods Loci Mathematical models Modularity Pathogenicity Pathogens Phylogenetics Phylogeny Plant diseases Plant production Plasmids Recombination Replication Species Strains (organisms) Strategy Symbiosis Virulence |
title | Unexpected conservation and global transmission of agrobacterial virulence plasmids |
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