Genetic diversity, genotyping and evolutionary history of the global population of Orthotospovirus tomatomaculae genomic segments

Tomato spotted wilt virus (Orthotospovirus tomatomaculae; TSWV) is a destructive pathogen that affects over 1000 plant species worldwide. To elucidate its evolutionary mechanisms, genetic diversity and emergence timeline, we examined around 100 TSWV isolates with complete genome sequences available in GenBank. This study also included the complete genome of a TSWV isolate, IRP4, which has recently been implicated in an outbreak affecting greenhouse-grown bell peppers in Iran. Pairwise genetic divergence analysis revealed varying levels of genetic differences among TSWV RNA segments. Phylogenetic and sequence analysis determined that the global TSWV population consists of three major groups based on each of the three RNA segments (L, M, and S). Results suggested multiple introductions of the virus into different regions, indicating that the geographical origin of the isolates is not the sole factor determining their phylogenetic grouping. The large incongruences observed in the phylogeny of the TSWV segments and the analysis of genetic diversity patterns highlight extensive reassortment events in TSWV. As a result, 11 genotypes were identified within the TSWV population. The Iranian IRP4 isolate, along with nine other isolates from Europe, Asia, and South America shared a common genotype designated L3-M1-S1. This suggests that this potentially reassortant genotype has undergone long-distance intercontinental movement. Similar to IRP4, the majority of TSWV isolates with the L3-M1-S1 genotype were also obtained from pepper, suggesting a potential role of the host plant in the evolution of this genotype. Furthermore, temporal analysis suggests that the existing population of TSWV, circulating between 1996 and 2023, originated from a common ancestor that existed 107–284 years ago. The population size of TSWV experienced a significant expansion for 10–15 years since 1980 and then remained constant until recently.