Genomic survey of pathogenicity determinants and VNTR markers in the cassava bacterial pathogen Xanthomonas axonopodis pv. Manihotis strain CIO151

Xanthomonas axonopodis pv. manihotis (Xam) is the causal agent of bacterial blight of cassava, which is among the main components of human diet in Africa and South America. Current information about the molecular pathogenicity factors involved in the infection process of this organism is limited. Pr...

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Veröffentlicht in:PloS one 2013-11, Vol.8 (11), p.e79704-e79704
Hauptverfasser: Arrieta-Ortiz, Mario L, Rodríguez-R, Luis M, Pérez-Quintero, Álvaro L, Poulin, Lucie, Díaz, Ana C, Arias Rojas, Nathalia, Trujillo, Cesar, Restrepo Benavides, Mariana, Bart, Rebecca, Boch, Jens, Boureau, Tristan, Darrasse, Armelle, David, Perrine, Dugé de Bernonville, Thomas, Fontanilla, Paula, Gagnevin, Lionel, Guérin, Fabien, Jacques, Marie-Agnès, Lauber, Emmanuelle, Lefeuvre, Pierre, Medina, Cesar, Medina, Edgar, Montenegro, Nathaly, Muñoz Bodnar, Alejandra, Noël, Laurent D, Ortiz Quiñones, Juan F, Osorio, Daniela, Pardo, Carolina, Patil, Prabhu B, Poussier, Stéphane, Pruvost, Olivier, Robène-Soustrade, Isabelle, Ryan, Robert P, Tabima, Javier, Urrego Morales, Oscar G, Vernière, Christian, Carrere, Sébastien, Verdier, Valérie, Szurek, Boris, Restrepo, Silvia, López, Camilo, Koebnik, Ralf, Bernal, Adriana
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container_start_page e79704
container_title PloS one
container_volume 8
creator Arrieta-Ortiz, Mario L
Rodríguez-R, Luis M
Pérez-Quintero, Álvaro L
Poulin, Lucie
Díaz, Ana C
Arias Rojas, Nathalia
Trujillo, Cesar
Restrepo Benavides, Mariana
Bart, Rebecca
Boch, Jens
Boureau, Tristan
Darrasse, Armelle
David, Perrine
Dugé de Bernonville, Thomas
Fontanilla, Paula
Gagnevin, Lionel
Guérin, Fabien
Jacques, Marie-Agnès
Lauber, Emmanuelle
Lefeuvre, Pierre
Medina, Cesar
Medina, Edgar
Montenegro, Nathaly
Muñoz Bodnar, Alejandra
Noël, Laurent D
Ortiz Quiñones, Juan F
Osorio, Daniela
Pardo, Carolina
Patil, Prabhu B
Poussier, Stéphane
Pruvost, Olivier
Robène-Soustrade, Isabelle
Ryan, Robert P
Tabima, Javier
Urrego Morales, Oscar G
Vernière, Christian
Carrere, Sébastien
Verdier, Valérie
Szurek, Boris
Restrepo, Silvia
López, Camilo
Koebnik, Ralf
Bernal, Adriana
description Xanthomonas axonopodis pv. manihotis (Xam) is the causal agent of bacterial blight of cassava, which is among the main components of human diet in Africa and South America. Current information about the molecular pathogenicity factors involved in the infection process of this organism is limited. Previous studies in other bacteria in this genus suggest that advanced draft genome sequences are valuable resources for molecular studies on their interaction with plants and could provide valuable tools for diagnostics and detection. Here we have generated the first manually annotated high-quality draft genome sequence of Xam strain CIO151. Its genomic structure is similar to that of other xanthomonads, especially Xanthomonas euvesicatoria and Xanthomonas citri pv. citri species. Several putative pathogenicity factors were identified, including type III effectors, cell wall-degrading enzymes and clusters encoding protein secretion systems. Specific characteristics in this genome include changes in the xanthomonadin cluster that could explain the lack of typical yellow color in all strains of this pathovar and the presence of 50 regions in the genome with atypical nucleotide composition. The genome sequence was used to predict and evaluate 22 variable number of tandem repeat (VNTR) loci that were subsequently demonstrated as polymorphic in representative Xam strains. Our results demonstrate that Xanthomonas axonopodis pv. manihotis strain CIO151 possesses ten clusters of pathogenicity factors conserved within the genus Xanthomonas. We report 126 genes that are potentially unique to Xam, as well as potential horizontal transfer events in the history of the genome. The relation of these regions with virulence and pathogenicity could explain several aspects of the biology of this pathogen, including its ability to colonize both vascular and non-vascular tissues of cassava plants. A set of 16 robust, polymorphic VNTR loci will be useful to develop a multi-locus VNTR analysis scheme for epidemiological surveillance of this disease.
doi_str_mv 10.1371/journal.pone.0079704
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Manihotis strain CIO151</title><source>Public Library of Science (PLoS) Journals Open Access</source><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><source>Free Full-Text Journals in Chemistry</source><creator>Arrieta-Ortiz, Mario L ; Rodríguez-R, Luis M ; Pérez-Quintero, Álvaro L ; Poulin, Lucie ; Díaz, Ana C ; Arias Rojas, Nathalia ; Trujillo, Cesar ; Restrepo Benavides, Mariana ; Bart, Rebecca ; Boch, Jens ; Boureau, Tristan ; Darrasse, Armelle ; David, Perrine ; Dugé de Bernonville, Thomas ; Fontanilla, Paula ; Gagnevin, Lionel ; Guérin, Fabien ; Jacques, Marie-Agnès ; Lauber, Emmanuelle ; Lefeuvre, Pierre ; Medina, Cesar ; Medina, Edgar ; Montenegro, Nathaly ; Muñoz Bodnar, Alejandra ; Noël, Laurent D ; Ortiz Quiñones, Juan F ; Osorio, Daniela ; Pardo, Carolina ; Patil, Prabhu B ; Poussier, Stéphane ; Pruvost, Olivier ; Robène-Soustrade, Isabelle ; Ryan, Robert P ; Tabima, Javier ; Urrego Morales, Oscar G ; Vernière, Christian ; Carrere, Sébastien ; Verdier, Valérie ; Szurek, Boris ; Restrepo, Silvia ; López, Camilo ; Koebnik, Ralf ; Bernal, Adriana</creator><creatorcontrib>Arrieta-Ortiz, Mario L ; Rodríguez-R, Luis M ; Pérez-Quintero, Álvaro L ; Poulin, Lucie ; Díaz, Ana C ; Arias Rojas, Nathalia ; Trujillo, Cesar ; Restrepo Benavides, Mariana ; Bart, Rebecca ; Boch, Jens ; Boureau, Tristan ; Darrasse, Armelle ; David, Perrine ; Dugé de Bernonville, Thomas ; Fontanilla, Paula ; Gagnevin, Lionel ; Guérin, Fabien ; Jacques, Marie-Agnès ; Lauber, Emmanuelle ; Lefeuvre, Pierre ; Medina, Cesar ; Medina, Edgar ; Montenegro, Nathaly ; Muñoz Bodnar, Alejandra ; Noël, Laurent D ; Ortiz Quiñones, Juan F ; Osorio, Daniela ; Pardo, Carolina ; Patil, Prabhu B ; Poussier, Stéphane ; Pruvost, Olivier ; Robène-Soustrade, Isabelle ; Ryan, Robert P ; Tabima, Javier ; Urrego Morales, Oscar G ; Vernière, Christian ; Carrere, Sébastien ; Verdier, Valérie ; Szurek, Boris ; Restrepo, Silvia ; López, Camilo ; Koebnik, Ralf ; Bernal, Adriana</creatorcontrib><description>Xanthomonas axonopodis pv. manihotis (Xam) is the causal agent of bacterial blight of cassava, which is among the main components of human diet in Africa and South America. Current information about the molecular pathogenicity factors involved in the infection process of this organism is limited. Previous studies in other bacteria in this genus suggest that advanced draft genome sequences are valuable resources for molecular studies on their interaction with plants and could provide valuable tools for diagnostics and detection. Here we have generated the first manually annotated high-quality draft genome sequence of Xam strain CIO151. Its genomic structure is similar to that of other xanthomonads, especially Xanthomonas euvesicatoria and Xanthomonas citri pv. citri species. Several putative pathogenicity factors were identified, including type III effectors, cell wall-degrading enzymes and clusters encoding protein secretion systems. Specific characteristics in this genome include changes in the xanthomonadin cluster that could explain the lack of typical yellow color in all strains of this pathovar and the presence of 50 regions in the genome with atypical nucleotide composition. The genome sequence was used to predict and evaluate 22 variable number of tandem repeat (VNTR) loci that were subsequently demonstrated as polymorphic in representative Xam strains. Our results demonstrate that Xanthomonas axonopodis pv. manihotis strain CIO151 possesses ten clusters of pathogenicity factors conserved within the genus Xanthomonas. We report 126 genes that are potentially unique to Xam, as well as potential horizontal transfer events in the history of the genome. The relation of these regions with virulence and pathogenicity could explain several aspects of the biology of this pathogen, including its ability to colonize both vascular and non-vascular tissues of cassava plants. A set of 16 robust, polymorphic VNTR loci will be useful to develop a multi-locus VNTR analysis scheme for epidemiological surveillance of this disease.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0079704</identifier><identifier>PMID: 24278159</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bacteria ; Bacteriology ; Bioinformatics ; Blight ; Cassava ; Cattle ; Cell walls ; Clusters ; Deoxyribonucleic acid ; DNA ; Epidemiology ; Gene sequencing ; Genes ; Genome, Bacterial - genetics ; Genomes ; Genomics ; Health aspects ; Horizontal transfer ; Horticulture ; Infection ; Life Sciences ; Loci ; Manihot ; Microbiology and Parasitology ; Minisatellite Repeats - genetics ; Nucleotide sequence ; Pathogenicity ; Pathogens ; Phylogenetics ; Phytopathology and phytopharmacy ; Plant tissues ; Plants (botany) ; Secretion ; Strains (organisms) ; Surveys ; Transfer RNA ; Vegetal Biology ; Virulence ; Virulence - genetics ; Xanthomonas axonopodis - genetics ; Xanthomonas axonopodis - pathogenicity</subject><ispartof>PloS one, 2013-11, Vol.8 (11), p.e79704-e79704</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Arrieta-Ortiz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/3.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Manihotis strain CIO151</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Xanthomonas axonopodis pv. manihotis (Xam) is the causal agent of bacterial blight of cassava, which is among the main components of human diet in Africa and South America. Current information about the molecular pathogenicity factors involved in the infection process of this organism is limited. Previous studies in other bacteria in this genus suggest that advanced draft genome sequences are valuable resources for molecular studies on their interaction with plants and could provide valuable tools for diagnostics and detection. Here we have generated the first manually annotated high-quality draft genome sequence of Xam strain CIO151. Its genomic structure is similar to that of other xanthomonads, especially Xanthomonas euvesicatoria and Xanthomonas citri pv. citri species. Several putative pathogenicity factors were identified, including type III effectors, cell wall-degrading enzymes and clusters encoding protein secretion systems. Specific characteristics in this genome include changes in the xanthomonadin cluster that could explain the lack of typical yellow color in all strains of this pathovar and the presence of 50 regions in the genome with atypical nucleotide composition. The genome sequence was used to predict and evaluate 22 variable number of tandem repeat (VNTR) loci that were subsequently demonstrated as polymorphic in representative Xam strains. Our results demonstrate that Xanthomonas axonopodis pv. manihotis strain CIO151 possesses ten clusters of pathogenicity factors conserved within the genus Xanthomonas. We report 126 genes that are potentially unique to Xam, as well as potential horizontal transfer events in the history of the genome. The relation of these regions with virulence and pathogenicity could explain several aspects of the biology of this pathogen, including its ability to colonize both vascular and non-vascular tissues of cassava plants. A set of 16 robust, polymorphic VNTR loci will be useful to develop a multi-locus VNTR analysis scheme for epidemiological surveillance of this disease.</description><subject>Bacteria</subject><subject>Bacteriology</subject><subject>Bioinformatics</subject><subject>Blight</subject><subject>Cassava</subject><subject>Cattle</subject><subject>Cell walls</subject><subject>Clusters</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Epidemiology</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genome, Bacterial - genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Horizontal transfer</subject><subject>Horticulture</subject><subject>Infection</subject><subject>Life Sciences</subject><subject>Loci</subject><subject>Manihot</subject><subject>Microbiology and Parasitology</subject><subject>Minisatellite Repeats - genetics</subject><subject>Nucleotide sequence</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Phylogenetics</subject><subject>Phytopathology and phytopharmacy</subject><subject>Plant tissues</subject><subject>Plants (botany)</subject><subject>Secretion</subject><subject>Strains (organisms)</subject><subject>Surveys</subject><subject>Transfer RNA</subject><subject>Vegetal Biology</subject><subject>Virulence</subject><subject>Virulence - genetics</subject><subject>Xanthomonas axonopodis - genetics</subject><subject>Xanthomonas axonopodis - 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survey of pathogenicity determinants and VNTR markers in the cassava bacterial pathogen Xanthomonas axonopodis pv. Manihotis strain CIO151</title><author>Arrieta-Ortiz, Mario L ; Rodríguez-R, Luis M ; Pérez-Quintero, Álvaro L ; Poulin, Lucie ; Díaz, Ana C ; Arias Rojas, Nathalia ; Trujillo, Cesar ; Restrepo Benavides, Mariana ; Bart, Rebecca ; Boch, Jens ; Boureau, Tristan ; Darrasse, Armelle ; David, Perrine ; Dugé de Bernonville, Thomas ; Fontanilla, Paula ; Gagnevin, Lionel ; Guérin, Fabien ; Jacques, Marie-Agnès ; Lauber, Emmanuelle ; Lefeuvre, Pierre ; Medina, Cesar ; Medina, Edgar ; Montenegro, Nathaly ; Muñoz Bodnar, Alejandra ; Noël, Laurent D ; Ortiz Quiñones, Juan F ; Osorio, Daniela ; Pardo, Carolina ; Patil, Prabhu B ; Poussier, Stéphane ; Pruvost, Olivier ; Robène-Soustrade, Isabelle ; Ryan, Robert P ; Tabima, Javier ; Urrego Morales, Oscar G ; Vernière, Christian ; Carrere, Sébastien ; Verdier, Valérie ; Szurek, Boris ; Restrepo, Silvia ; López, Camilo ; Koebnik, Ralf ; Bernal, Adriana</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-673740c002d6a5a20802d0301cfe55ce654321b5d923eb2c99bae7d604cc87a53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Bacteria</topic><topic>Bacteriology</topic><topic>Bioinformatics</topic><topic>Blight</topic><topic>Cassava</topic><topic>Cattle</topic><topic>Cell walls</topic><topic>Clusters</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Epidemiology</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Genome, Bacterial - genetics</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Health aspects</topic><topic>Horizontal transfer</topic><topic>Horticulture</topic><topic>Infection</topic><topic>Life Sciences</topic><topic>Loci</topic><topic>Manihot</topic><topic>Microbiology and Parasitology</topic><topic>Minisatellite Repeats - genetics</topic><topic>Nucleotide sequence</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Phylogenetics</topic><topic>Phytopathology and phytopharmacy</topic><topic>Plant tissues</topic><topic>Plants (botany)</topic><topic>Secretion</topic><topic>Strains (organisms)</topic><topic>Surveys</topic><topic>Transfer RNA</topic><topic>Vegetal Biology</topic><topic>Virulence</topic><topic>Virulence - genetics</topic><topic>Xanthomonas axonopodis - genetics</topic><topic>Xanthomonas axonopodis - pathogenicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Arrieta-Ortiz, Mario L</creatorcontrib><creatorcontrib>Rodríguez-R, Luis M</creatorcontrib><creatorcontrib>Pérez-Quintero, Álvaro L</creatorcontrib><creatorcontrib>Poulin, Lucie</creatorcontrib><creatorcontrib>Díaz, Ana C</creatorcontrib><creatorcontrib>Arias Rojas, Nathalia</creatorcontrib><creatorcontrib>Trujillo, Cesar</creatorcontrib><creatorcontrib>Restrepo Benavides, 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M</au><au>Pérez-Quintero, Álvaro L</au><au>Poulin, Lucie</au><au>Díaz, Ana C</au><au>Arias Rojas, Nathalia</au><au>Trujillo, Cesar</au><au>Restrepo Benavides, Mariana</au><au>Bart, Rebecca</au><au>Boch, Jens</au><au>Boureau, Tristan</au><au>Darrasse, Armelle</au><au>David, Perrine</au><au>Dugé de Bernonville, Thomas</au><au>Fontanilla, Paula</au><au>Gagnevin, Lionel</au><au>Guérin, Fabien</au><au>Jacques, Marie-Agnès</au><au>Lauber, Emmanuelle</au><au>Lefeuvre, Pierre</au><au>Medina, Cesar</au><au>Medina, Edgar</au><au>Montenegro, Nathaly</au><au>Muñoz Bodnar, Alejandra</au><au>Noël, Laurent D</au><au>Ortiz Quiñones, Juan F</au><au>Osorio, Daniela</au><au>Pardo, Carolina</au><au>Patil, Prabhu B</au><au>Poussier, Stéphane</au><au>Pruvost, Olivier</au><au>Robène-Soustrade, Isabelle</au><au>Ryan, Robert P</au><au>Tabima, Javier</au><au>Urrego Morales, Oscar G</au><au>Vernière, Christian</au><au>Carrere, Sébastien</au><au>Verdier, Valérie</au><au>Szurek, Boris</au><au>Restrepo, Silvia</au><au>López, Camilo</au><au>Koebnik, Ralf</au><au>Bernal, Adriana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic survey of pathogenicity determinants and VNTR markers in the cassava bacterial pathogen Xanthomonas axonopodis pv. Manihotis strain CIO151</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-11-22</date><risdate>2013</risdate><volume>8</volume><issue>11</issue><spage>e79704</spage><epage>e79704</epage><pages>e79704-e79704</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Xanthomonas axonopodis pv. manihotis (Xam) is the causal agent of bacterial blight of cassava, which is among the main components of human diet in Africa and South America. Current information about the molecular pathogenicity factors involved in the infection process of this organism is limited. Previous studies in other bacteria in this genus suggest that advanced draft genome sequences are valuable resources for molecular studies on their interaction with plants and could provide valuable tools for diagnostics and detection. Here we have generated the first manually annotated high-quality draft genome sequence of Xam strain CIO151. Its genomic structure is similar to that of other xanthomonads, especially Xanthomonas euvesicatoria and Xanthomonas citri pv. citri species. Several putative pathogenicity factors were identified, including type III effectors, cell wall-degrading enzymes and clusters encoding protein secretion systems. Specific characteristics in this genome include changes in the xanthomonadin cluster that could explain the lack of typical yellow color in all strains of this pathovar and the presence of 50 regions in the genome with atypical nucleotide composition. The genome sequence was used to predict and evaluate 22 variable number of tandem repeat (VNTR) loci that were subsequently demonstrated as polymorphic in representative Xam strains. Our results demonstrate that Xanthomonas axonopodis pv. manihotis strain CIO151 possesses ten clusters of pathogenicity factors conserved within the genus Xanthomonas. We report 126 genes that are potentially unique to Xam, as well as potential horizontal transfer events in the history of the genome. The relation of these regions with virulence and pathogenicity could explain several aspects of the biology of this pathogen, including its ability to colonize both vascular and non-vascular tissues of cassava plants. A set of 16 robust, polymorphic VNTR loci will be useful to develop a multi-locus VNTR analysis scheme for epidemiological surveillance of this disease.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24278159</pmid><doi>10.1371/journal.pone.0079704</doi><tpages>e79704</tpages><orcidid>https://orcid.org/0000-0003-2645-8098</orcidid><orcidid>https://orcid.org/0000-0002-0110-1423</orcidid><orcidid>https://orcid.org/0000-0002-2348-0778</orcidid><orcidid>https://orcid.org/0000-0002-2312-2073</orcidid><orcidid>https://orcid.org/0000-0002-2205-2886</orcidid><orcidid>https://orcid.org/0000-0002-4419-0542</orcidid><orcidid>https://orcid.org/0000-0002-9334-5862</orcidid><orcidid>https://orcid.org/0000-0001-5933-4476</orcidid><orcidid>https://orcid.org/0000-0002-1808-7082</orcidid><orcidid>https://orcid.org/0000-0001-5425-9454</orcidid><orcidid>https://orcid.org/0000-0002-1442-917X</orcidid><orcidid>https://orcid.org/0000-0002-3557-697X</orcidid><orcidid>https://orcid.org/0000-0003-3530-8251</orcidid><orcidid>https://orcid.org/0000-0002-2830-9830</orcidid><oa>free_for_read</oa></addata></record>
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subjects Bacteria
Bacteriology
Bioinformatics
Blight
Cassava
Cattle
Cell walls
Clusters
Deoxyribonucleic acid
DNA
Epidemiology
Gene sequencing
Genes
Genome, Bacterial - genetics
Genomes
Genomics
Health aspects
Horizontal transfer
Horticulture
Infection
Life Sciences
Loci
Manihot
Microbiology and Parasitology
Minisatellite Repeats - genetics
Nucleotide sequence
Pathogenicity
Pathogens
Phylogenetics
Phytopathology and phytopharmacy
Plant tissues
Plants (botany)
Secretion
Strains (organisms)
Surveys
Transfer RNA
Vegetal Biology
Virulence
Virulence - genetics
Xanthomonas axonopodis - genetics
Xanthomonas axonopodis - pathogenicity
title Genomic survey of pathogenicity determinants and VNTR markers in the cassava bacterial pathogen Xanthomonas axonopodis pv. Manihotis strain CIO151
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