Genomic Dissection Explains Temporal Dynamics of Xanthomonas euvesicatoria pv. perforans

Bacterial spot of tomato caused by four taxonomically diverse Xanthomonas pathogens is one of the main seed-borne constraints of the tomato industry worldwide. Among the four bacterial spot xanthomonads, Xanthomonas euvesicatoria pv. perforans has a particular importance in terms of competitive aggressiveness and global distribution. Bacterial spot of tomato was observed for the first time in Iran in 2015, where X. euvesicatoria pv. perforans was identified as the causal agent. While occurrence of this disease appeared to have subsided in the following years, a resurgence of the disease in the main tomato-growing areas of Iran has raised serious concerns since 2023. In this study, we assessed the range of new bacterial spot outbreaks in the country during 2023-2024. Our data showed that the disease is currently present in five Iranian provinces, including the two provinces where it had originally been reported in 2015. Whole genome sequence-based phylogenomic investigations suggested that the causal agent of tomato bacterial spot in Iran is still X. euvesicatoria pv. perforans, while genetic diversity was observed in the recently emerging population of the pathogen compared to the old population. The bacterial strains isolated in 2023-2024 surveys were phylogenetically distinct from those isolated in 2014-2016 surveys. Furthermore, type III effector repertoires varied significantly among the strains isolated in this study, regardless of their geographic origin. We provide novel insights into the ever-changing nature of tomato bacterial spot pathogens, highlighting the impact of seed-borne lineages of X. euvesicatoria pv. perforans in the population dynamics of the bacterium.