Comparative genomics and adaptive evolution of tomato-infecting viruses

Tomato ( Solanum lycopersicum L.) is one of the most economically important vegetable crops worldwide and hosts an exceptionally diverse virome comprising more than 300 viruses, viroids, and satellite agents. The rapid expansion of high-throughput sequencing (HTS) has generated extensive viral genomic datasets, providing new opportunities to investigate the diversity, evolution, and global dissemination of tomato-infecting viruses. However, the increasing availability of viral genome sequences has also highlighted a fundamental limitation of sequence-based inference: the amount of genomic variation within a viral population does not directly indicate its adaptive or epidemiological significance. Recent advances in the comparative and population genomics of tomato viruses are critically evaluated here, with particular emphasis on the relationships among genomic variation, resistance-breaking phenotypes, virome composition, and population-level spread. Major tomato viruses, including Tomato brown rugose fruit virus, Tobamovirus fructirugosum (ToBRFV), Tomato yellow leaf curl virus, Begomovirus coheni (TYLCV), and Tomato spotted wilt virus, Orthotospovirus tomatomaculae (TSWV), illustrate how mutation, recombination, mixed infection, host-associated selection, and transmission contribute differently to viral diversification and adaptation. Comparative evidence indicates that epidemiological success can occur under markedly different population-genomic patterns and that only a subset of genomic changes remains compatible with viral replication, movement, resistance breaking, transmission, and population persistence. Virome studies further demonstrate that detection of viral diversity does not itself establish productive host infection, pathogenicity, or epidemiological significance, whereas current phylodynamic approaches remain substantially more effective for reconstructing the dissemination of established viral lineages than for predicting their future adaptive or epidemiological expansion. A major unresolved challenge is therefore to determine which genomic variants identified by comparative and population analyses have functional consequences and subsequently increase in frequency and geographic distribution. Addressing this problem requires integration of genome-resolved population data with experimental genotype–phenotype validation, transmission biology, longitudinal sampling, and epidemiological metadata. Such integration can strengthen genomic surveillance and provide a more rigorous basis for evaluating resistance-breaking variants, emerging viral lineages, and the durability of resistance in tomato production systems.