Diversification of an emerging bacterial plant pathogen; insights into the global spread of Xanthomonas euvesicatoria pv. perforans

Emerging and re-emerging plant diseases continue to present multifarious threats to global food security. Considerable recent efforts are therefore being channeled towards understanding the nature of pathogen emergence, their spread and evolution. Xanthomonas euvesicatoria pv. perforans (Xep), one of the causal agents of bacterial spot of tomato, rapidly emerged and displaced other bacterial spot xanthomonads in many tomato production regions around the world. In less than three decades, it has become a dominant xanthomonad pathogen in tomato production systems across the world and presents a compelling example for understanding diversification of recently emerged bacterial plant pathogens. Although Xep has been continuously monitored in Florida since its discovery, the global population structure and evolution at the genome-scale is yet to be fully explored. The objectives of this work were to determine genetic diversity globally to ascertain if different tomato production regions contain genetically distinct Xep populations, to examine genetic relatedness of strains collected in tomato seed production areas in East Asia and other production regions, and to evaluate variation in type III secretion effectors, which are critical pathogenicity and virulence factors, in relationship to population structure. We used genome data from 270 strains from 13 countries for phylogenetic analysis and characterization of type III effector gene diversity among strains. Our results showed notable genetic diversity in the pathogen. We found genetically similar strains in distant tomato production regions, including seed production regions, and diversification over the past 100 years, which is consistent with intercontinental dissemination of the pathogen in hybrid tomato production chains. Evolution of the Xep pangenome, including the acquisition and loss of type III secreted effectors, is apparent within and among phylogenetic lineages. The apparent long-distance movement of the pathogen, together with variants that may not yet be widely distributed, poses risks of emergence of new variants in tomato production.

Authors

Institutions

Publication Details

Journal
PLoS Pathogens
Published
2025-04-09
DOI
https://doi.org/10.1371/journal.ppat.1013036
Citations
4
Primary Topic
Plant Pathogenic Bacteria Studies
Type
article
Field-Weighted Citation Impact
5.25

Funders

Controls
|||
ALL TIME
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
article

Diversification of an emerging bacterial plant pathogen; insights into the global spread of Xanthomonas euvesicatoria pv. perforans

Ebrahim Osdaghi, Francesca Rotondo, Eduardo Bernal, Jeffrey B. Jones et al.
4 citations
PLoS Pathogens
Plant Pathogenic Bacteria Studies
5.25
article

Diversification of an emerging bacterial plant pathogen; insights into the global spread of Xanthomonas euvesicatoria pv. perforans

Ebrahim Osdaghi, Francesca Rotondo, Eduardo Bernal, Jeffrey B. Jones, Mustafa O. Jibrin, Sally A. Miller, Teresa A. Coutinho, David M. Francis, A. M. Quezado‐Duval, Pragya Adhikari, Nguyễn Thị Thu Ngà, Jeannie M. Klein-Gordon, Rubén Felix-Gástelum, Daniel S. Egel, Anuj Sharma, Thuy Doan, Cheryl L. Trueman, Rebecca Roach, Frank J. Louws, Melanie L. Lewis Ivey, Aastha Subedi, Gerald V. Minsavage, Petcharat Thummabenjapone, Tom Creswell, Erica M. Goss, Laixin Luo, Gabriella Cirvilleri, José C. Huguet‐Tapia, Gail E. Ruhl, Sujan Timilsina, Fernanda Iruegas-Bocardo, Gary E. Vallad, Tika B. Adhikari, Pamela D. Roberts, Amandeep Kaur, Laura Belen Tapia de la Barrera, Elizabeth Maynard, Vou Moses Shutt, Misrak Kebede
article en
4 citations

Abstract

Emerging and re-emerging plant diseases continue to present multifarious threats to global food security. Considerable recent efforts are therefore being channeled towards understanding the nature of pathogen emergence, their spread and evolution. Xanthomonas euvesicatoria pv. perforans (Xep), one of the causal agents of bacterial spot of tomato, rapidly emerged and displaced other bacterial spot xanthomonads in many tomato production regions around the world. In less than three decades, it has become a dominant xanthomonad pathogen in tomato production systems across the world and presents a compelling example for understanding diversification of recently emerged bacterial plant pathogens. Although Xep has been continuously monitored in Florida since its discovery, the global population structure and evolution at the genome-scale is yet to be fully explored. The objectives of this work were to determine genetic diversity globally to ascertain if different tomato production regions contain genetically distinct Xep populations, to examine genetic relatedness of strains collected in tomato seed production areas in East Asia and other production regions, and to evaluate variation in type III secretion effectors, which are critical pathogenicity and virulence factors, in relationship to population structure. We used genome data from 270 strains from 13 countries for phylogenetic analysis and characterization of type III effector gene diversity among strains. Our results showed notable genetic diversity in the pathogen. We found genetically similar strains in distant tomato production regions, including seed production regions, and diversification over the past 100 years, which is consistent with intercontinental dissemination of the pathogen in hybrid tomato production chains. Evolution of the Xep pangenome, including the acquisition and loss of type III secreted effectors, is apparent within and among phylogenetic lineages. The apparent long-distance movement of the pathogen, together with variants that may not yet be widely distributed, poses risks of emergence of new variants in tomato production.

PLoS PathogensVol. 21(4)
Ahmadu Bello University (NG), North Carolina State University (US), University of Jos (NG), Can Tho University (VN), Khon Kaen University (TH), Brazilian Agricultural Research Corporation (BR), Purdue University West Lafayette (US), University of Tehran (IR), University of Florida (US), Universidad Autónoma de Occidente (MX), Centro de Investigación en Alimentación y Desarrollo (MX), Ambiente Italia (Italy) (IT), Southwest Florida Research (US), Addis Ababa Science and Technology University (ET), Department of Primary Industries (AU), China Agricultural University (CN), The Ohio State University (US), University of Pretoria (ZA), University of Guelph (CA), University of West Florida (US)
U.S. Department of Agriculture, Ontario Agri-Food Innovation Alliance, National Institute of Food and Agriculture
Zero hunger
Openalex Percentile: Top 6%
Plant Pathogenic Bacteria Studies
5.25
DOIOpen Access PDFOpenAlex
AI Navigator

Ask Laika to Summarize, Analyze, and Connect papers live on the map.

Summarize Papers & Methodologies

Extract key findings, datasets, and comparative methods across publications.

Benchmark Rankings & Visual Analytics

Rank top research institutions, authors, funders, topics, and journals by Field-Weighted Citation Impact (FWCI) and paper volume with instant charts.

Connect Distant Disciplines

Bridge topological clusters on the map to find hidden collaborative intersections.