Phylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneri
The emergence of plant pathogens is often associated with waves of unique evolutionary and epidemiological events. Xanthomonas hortorum pv. gardneri is one of the major pathogens causing bacterial spot disease of tomatoes. After its first report in the 1950s, there were no formal reports on this pat...
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The American Phytopathological Society
2024-10-01
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| Series: | Molecular Plant-Microbe Interactions |
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| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-04-24-0035-R |
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| author | Mustafa O. Jibrin Anuj Sharma Carla N. Mavian Sujan Timilsina Amandeep Kaur Fernanda Iruegas-Bocardo Neha Potnis Gerald V. Minsavage Teresa A. Coutinho Tom C. Creswell Daniel S. Egel David M. Francis Misrak Kebede Sally A. Miller María J. Montelongo Ekaterina Nikolaeva María J. Pianzzola Olivier Pruvost Alice M. Quezado-Duval Gail E. Ruhl Vou M. Shutt Elizabeth Maynard Diego C. Maeso María I. Siri Cheryl L. Trueman Marco Salemi Gary E. Vallad Pamela D. Roberts Jeffrey B. Jones Erica M. Goss |
| author_facet | Mustafa O. Jibrin Anuj Sharma Carla N. Mavian Sujan Timilsina Amandeep Kaur Fernanda Iruegas-Bocardo Neha Potnis Gerald V. Minsavage Teresa A. Coutinho Tom C. Creswell Daniel S. Egel David M. Francis Misrak Kebede Sally A. Miller María J. Montelongo Ekaterina Nikolaeva María J. Pianzzola Olivier Pruvost Alice M. Quezado-Duval Gail E. Ruhl Vou M. Shutt Elizabeth Maynard Diego C. Maeso María I. Siri Cheryl L. Trueman Marco Salemi Gary E. Vallad Pamela D. Roberts Jeffrey B. Jones Erica M. Goss |
| author_sort | Mustafa O. Jibrin |
| collection | DOAJ |
| description | The emergence of plant pathogens is often associated with waves of unique evolutionary and epidemiological events. Xanthomonas hortorum pv. gardneri is one of the major pathogens causing bacterial spot disease of tomatoes. After its first report in the 1950s, there were no formal reports on this pathogen until the 1990s, despite active global research on the pathogens that cause tomato and pepper bacterial spot disease. Given the recently documented global distribution of X. hortorum pv. gardneri, our objective was to examine genomic diversification associated with its emergence. We sequenced the genomes of X. hortorum pv. gardneri strains collected in eight countries to examine global population structure and pathways of emergence using phylodynamic analysis. We found that strains isolated post-1990 group by region of collection and show minimal impact of recombination on genetic variation. A period of rapid geographic expansion in X. hortorum pv. gardneri is associated with acquisition of a large plasmid conferring copper tolerance by horizontal transfer and coincides with the burgeoning hybrid tomato seed industry through the 1980s. The ancestry of X. hortorum pv. gardneri is consistent with introduction to hybrid tomato seed production and dissemination during the rapid increase in trade of hybrid seeds. [Figure: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| format | Article |
| id | doaj-art-c6d6c8a18c2548049fe9384b82849e53 |
| institution | OA Journals |
| issn | 0894-0282 1943-7706 |
| language | English |
| publishDate | 2024-10-01 |
| publisher | The American Phytopathological Society |
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| series | Molecular Plant-Microbe Interactions |
| spelling | doaj-art-c6d6c8a18c2548049fe9384b82849e532025-08-20T01:47:19ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062024-10-01371071272010.1094/MPMI-04-24-0035-RPhylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneriMustafa O. Jibrin0Anuj Sharma1Carla N. Mavian2Sujan Timilsina3Amandeep Kaur4Fernanda Iruegas-Bocardo5Neha Potnis6Gerald V. Minsavage7Teresa A. Coutinho8Tom C. Creswell9Daniel S. Egel10David M. Francis11Misrak Kebede12Sally A. Miller13María J. Montelongo14Ekaterina Nikolaeva15María J. Pianzzola16Olivier Pruvost17Alice M. Quezado-Duval18Gail E. Ruhl19Vou M. Shutt20Elizabeth Maynard21Diego C. Maeso22María I. Siri23Cheryl L. Trueman24Marco Salemi25Gary E. Vallad26Pamela D. Roberts27Jeffrey B. Jones28Erica M. Goss29Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.Department of Pathology, Immunology, and Laboratory Medicine, University of Florida, Gainesville, FL 32610, U.S.A.Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.Department of Entomology and Plant Pathology, Auburn University, Auburn, AL 36849, U.S.A.Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.Department of Microbiology and Plant Pathology, Centre for Microbial Ecology and Genomics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South AfricaBotany and Plant Pathology Department, Purdue University, West Lafayette, IN 47907, U.S.A.Botany and Plant Pathology Department, Purdue University, West Lafayette, IN 47907, U.S.A.Department of Horticulture and Crop Science, The Ohio State University, Wooster, OH 44691, U.S.A.Plant Pathology Department, School of Plant Science, Haramaya University, Dire Dawa, EthiopiaDepartment of Plant Pathology, The Ohio State University, Wooster, OH 44691, U.S.A.Molecular Microbiology Laboratory, Biosciences Department, School of Chemistry, Universidad de la República, Montevideo, CP1800, UruguayBureau of Plant Industry, Pennsylvania Department of Agriculture, Harrisburg, PA 17110, U.S.A.Molecular Microbiology Laboratory, Biosciences Department, School of Chemistry, Universidad de la República, Montevideo, CP1800, UruguayUMR PVBMT, CIRAD, St.-Pierre, Réunion, FranceEmbrapa Hortalicas, Laboratorio de Fitopatologia, Brasília-DF, C.P. 218, BrazilBotany and Plant Pathology Department, Purdue University, West Lafayette, IN 47907, U.S.A.Department of Microbiology and Plant Pathology, Centre for Microbial Ecology and Genomics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South AfricaDepartment of Horticulture and Landscape Architecture, Purdue University, IN 46383, U.S.A.Instituto Nacional de Investigacion Agropecuaria, INIA Las Brujas, Las Brujas, Canelones, UruguayMolecular Microbiology Laboratory, Biosciences Department, School of Chemistry, Universidad de la República, Montevideo, CP1800, UruguayDepartment of Plant Agriculture, Ridgetown Campus, University of Guelph, Ridgetown, ON N0P 2C0, CanadaDepartment of Pathology, Immunology, and Laboratory Medicine, University of Florida, Gainesville, FL 32610, U.S.A.Gulf Coast Research and Education Center, University of Florida, Wimauma, FL 33598, U.S.A.Southwest Florida Research and Education Center, University of Florida, Immokalee, FL 34142, U.S.A.Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.The emergence of plant pathogens is often associated with waves of unique evolutionary and epidemiological events. Xanthomonas hortorum pv. gardneri is one of the major pathogens causing bacterial spot disease of tomatoes. After its first report in the 1950s, there were no formal reports on this pathogen until the 1990s, despite active global research on the pathogens that cause tomato and pepper bacterial spot disease. Given the recently documented global distribution of X. hortorum pv. gardneri, our objective was to examine genomic diversification associated with its emergence. We sequenced the genomes of X. hortorum pv. gardneri strains collected in eight countries to examine global population structure and pathways of emergence using phylodynamic analysis. We found that strains isolated post-1990 group by region of collection and show minimal impact of recombination on genetic variation. A period of rapid geographic expansion in X. hortorum pv. gardneri is associated with acquisition of a large plasmid conferring copper tolerance by horizontal transfer and coincides with the burgeoning hybrid tomato seed industry through the 1980s. The ancestry of X. hortorum pv. gardneri is consistent with introduction to hybrid tomato seed production and dissemination during the rapid increase in trade of hybrid seeds. [Figure: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-04-24-0035-Rbacterial plant pathogengenome evolutionphylodynamics |
| spellingShingle | Mustafa O. Jibrin Anuj Sharma Carla N. Mavian Sujan Timilsina Amandeep Kaur Fernanda Iruegas-Bocardo Neha Potnis Gerald V. Minsavage Teresa A. Coutinho Tom C. Creswell Daniel S. Egel David M. Francis Misrak Kebede Sally A. Miller María J. Montelongo Ekaterina Nikolaeva María J. Pianzzola Olivier Pruvost Alice M. Quezado-Duval Gail E. Ruhl Vou M. Shutt Elizabeth Maynard Diego C. Maeso María I. Siri Cheryl L. Trueman Marco Salemi Gary E. Vallad Pamela D. Roberts Jeffrey B. Jones Erica M. Goss Phylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneri Molecular Plant-Microbe Interactions bacterial plant pathogen genome evolution phylodynamics |
| title | Phylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneri |
| title_full | Phylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneri |
| title_fullStr | Phylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneri |
| title_full_unstemmed | Phylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneri |
| title_short | Phylodynamic Insights into Global Emergence and Diversification of the Tomato Pathogen Xanthomonas hortorum pv. gardneri |
| title_sort | phylodynamic insights into global emergence and diversification of the tomato pathogen xanthomonas hortorum pv gardneri |
| topic | bacterial plant pathogen genome evolution phylodynamics |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-04-24-0035-R |
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