Timilsina Sujan, Iruegas-Bocardo Fernanda, Jibrin Mustafa O, Sharma Anuj, Subedi Aastha, Kaur Amandeep, Minsavage Gerald V, Huguet-Tapia Jose C, Klein-Gordon Jeannie, Adhikari Pragya, Adhikari Tika B, Cirvilleri Gabriella, de la Barrera Laura Belen Tapia, Bernal Eduardo, Creswell Tom C, Doan Tien Thi Kieu, Coutinho Teresa A, Egel Daniel S, Félix-Gastélum Rubén, Francis David M, Kebede Misrak, Ivey Melanie Lewis, Louws Frank J, Luo Laixin, Maynard Elizabeth T, Miller Sally A, Nguyen Nga Thi Thu, Osdaghi Ebrahim, Quezado-Duval Alice M, Roach Rebecca, Rotondo Francesca, Ruhl Gail E, Shutt Vou M, Thummabenjapone Petcharat, Trueman Cheryl, Roberts Pamela D, Jones Jeffrey B, Vallad Gary E, Goss Erica M
Department of Plant Pathology, University of Florida, Gainesville, Florida, United States of America.
Department of Crop Protection, Ahmadu Bello University, Zaria, Nigeria.
PLoS Pathog. 2025 Apr 9;21(4):e1013036. doi: 10.1371/journal.ppat.1013036. eCollection 2025 Apr.
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.
新出现和再度出现的植物病害继续对全球粮食安全构成多方面威胁。因此，近期人们投入了大量精力来了解病原体出现的本质、传播方式及其进化过程。番茄细菌性斑点病的致病因子之一——穿孔黄单胞菌番茄致病变种（Xep），在世界许多番茄产区迅速出现并取代了其他细菌性斑点病黄单胞菌。在不到三十年的时间里，它已成为全球番茄生产系统中占主导地位的黄单胞菌病原体，为理解新出现的细菌性植物病原体的多样化提供了一个引人注目的例子。尽管自发现以来一直在佛罗里达州对Xep进行持续监测，但在基因组尺度上的全球种群结构和进化尚未得到充分探索。这项工作的目的是确定全球范围内的遗传多样性，以确定不同的番茄产区是否包含基因上不同的Xep种群，研究在东亚番茄种子生产区和其他生产区收集的菌株之间的遗传相关性，并评估III型分泌效应子（关键的致病性和毒力因子）与种群结构的关系中的变异情况。我们使用了来自13个国家的270个菌株的基因组数据进行系统发育分析，并对菌株间的III型效应子基因多样性进行表征。我们的结果显示该病原体具有显著的遗传多样性。我们在包括种子生产区在内的遥远番茄产区发现了基因相似的菌株，以及过去100年中的多样化情况，这与该病原体在杂交番茄生产链中的洲际传播一致。Xep泛基因组的进化，包括III型分泌效应子的获得和丧失，在系统发育谱系内部和之间都很明显。病原体明显的远距离移动，以及可能尚未广泛分布的变体，给番茄生产中出现新变体带来了风险。
