1. The Tomato Virome: Scale and Diversity

Tomato (Solanum lycopersicum) is one of the most important horticultural crops worldwide, with global production reaching approximately 192 million tons in 2023. Despite its economic importance, tomato cultivation is increasingly threatened by viral diseases that reduce yield stability and fruit quality, particularly under intensive greenhouse production systems. Plant viruses are now estimated to cause global economic losses exceeding 30 billion USD annually. However, modern research has fundamentally shifted the conceptual framework of plant virology from single-pathogen diseases to complex viral ecosystems, known as viromes, where multiple viruses coexist and interact within the same host. Recent metagenomic studies have demonstrated that tomato plants routinely harbor multiple viral species simultaneously. A large-scale international survey conducted between 2017 and 2024 analyzed 101 greenhouse tomato samples collected from 13 countries across Europe, Africa, Asia, and North America. Using virus-like particle enrichment combined with bioinformatics analysis (and AI-boosted pipelines), researchers identified 43 eukaryotic viral species(with a median of two viruses per sample), confirming that mixed infections represent the biological norm in commercial production systems. For esample, Three other pathogenic viral species of particular interest because of their effects on tomato cultivation or their recent emergence—namely tomato torrado virus (ToTV, genus Torradovirus), tomato fruit blotch virus (ToFBV, genus Blunervirus), and cucumber mosaic virus (CMV, genus Cucumovirus)—were present in the virome at low prevalence. Among the most prevalent viruses were Pepino mosaic virus (PepMV), Tomato brown rugose fruit virus (ToBRFV), and Southern tomato virus (STV). Genomic analyses revealed low intra-species diversity, suggesting recent global dissemination and strong selective pressures in agricultural environments. Notably, Southern tomato virus did not show a consistent association with visible symptoms, highlighting the need to distinguish between pathogenic, latent, and nonpathogenic viral entities within the tomato virome.

2. Major Emerging and Re-emerging Viruses on Tomato

Within this complex virome landscape, several viruses have emerged as dominant threats due to their rapid spread, adaptability, and ability to overcome resistance mechanisms.Tomato brown rugose fruit virus (ToBRFV) is currently one of the most destructive emerging tomato viruses. Since its identification in 2014, it has spread globally through mechanical transmission and contaminated plant material, including seeds. Its epidemiological success is strongly linked to its ability to overcome the widely deployed Tm-2² resistance gene. Infected crops can experience yield losses ranging from 15 to 55 %, accompanied by severe fruit deformation and quality deterioration. Tomato spotted wilt virus (TSWV), transmitted by the western flower thrips Frankliniella occidentalis, remains a persistent and re-emerging threat. Its epidemiological dynamics are increasingly shaped by resistance-breaking strains and enhanced vector fitness, illustrating the importance of virus–vector co-evolution in disease emergence and spread. Begomoviruses, particularly Tomato yellow leaf curl virus (TYLCV) and Tomato leaf curl New Delhi virus (ToLCNDV), transmitted by the whitefly Bemisia tabaci, continue to expand geographically, especially in tropical and Mediterranean production systems. While TYLCV is now globally established, ToLCNDV continues to spread into new regions, contributing to increasing disease pressure in protected cultivation systems. Pepino mosaic virus (PepMV) remains endemic in greenhouse production systems worldwide. Although generally less destructive than ToBRFV, it continues to cause significant economic losses due to its impact on fruit quality and its persistence in intensive production environments. Its genetic diversity, structured into multiple genotypes (CH2, EU, LP, US1, PES), is particularly important for epidemiology and cross-protection strategies.

3. The Historic and Still Problematic Case of Tobamoviruses

Tobamoviruses are highly resilient, ancient plant RNA viruses with extraordinary environmental stability and global agricultural relevance, particularly in solanaceous crops such as tomato. Among them, Tomato brown rugose fruit virus (ToBRFV) has emerged as a major global threat due to its ability to overcome traditional resistance genes and spread rapidly through mechanical and seed-based transmission. These viruses cause severe yield and quality losses and are difficult to control due to their persistence in the environment and the lack of fully resistant cultivars. Plants respond through multilayered immune systems involving hormonal signaling, RNA silencing, and immune receptors, yet tobamoviruses have evolved efficient countermeasures to evade these defenses. Recent research highlights significant advances in understanding virus–host interactions, viral evolution, and novel control strategies, including plant-derived antiviral compounds and computer-aided drug discovery. However, current management remains largely reliant on hygiene and exclusion practices. The emergence of ToBRFV underscores the urgent need for integrated approaches combining plant breeding, molecular biology, and innovative antiviral technologies to ensure sustainable tomato production globally.

4. Recent Advances in Tomato Metagenomics and HTS-Based Surveillance

Traditional diagnostic tools such as PCR, ELISA, and LAMP remain essential for routine virus detection, but they are inherently limited by their dependence on prior sequence knowledge. In contrast, high-throughput sequencing (HTS) has become the reference standard for modern plant virology, enabling unbiased detection of both known and novel viruses. Metagenomic approaches now include virus-like particle enrichment, double-stranded RNA sequencing, and small RNA profiling, each providing complementary but methodologically biased perspectives on viral diversity. These approaches have significantly improved the ability to detect cryptic infections and characterize complex viromes in agricultural systems. Bioinformatics pipelines enable computational analysis and genome reconstruction, taxonomic classification, and diversity analysis of viral populations. However, the lack of full methodological standardization remains a limitation for cross-study comparability and global surveillance harmonization.

5. Artificial Intelligence and AI-based Predictive Virology on Tomato

Artificial intelligence is rapidly transforming plant virology from descriptive science into a predictive and mechanistic discipline. AI-based epidemiological models integrate genomic, environmental, and vector-related data to forecast disease emergence, transmission dynamics, and outbreak risk under changing climatic conditions. At the molecular level, structural prediction systems (such as AlphaFold Multimer) enable the modeling of protein–protein interactions between plant hosts and pathogens. This provides unprecedented insight into viral infection strategies, particularly the mechanisms by which pathogens suppress plant immune responses. A key conceptual framework supported by these advances is the evolutionary arms race between plant defense proteins and pathogen effectors. Molecular interaction systems in tomato and other crops demonstrate how small structural changes can determine susceptibility or resistance, providing a rational basis for engineering durable resistance traits.

6. Integrated Management Implications for Tomato Industry

Effective management of emerging tomato viruses requires a multi-layered and integrated strategy combining biosecurity, vector control, host resistance, and surveillance. Biosecurity remains the first line of defense, particularly against mechanically transmitted viruses such as Tomato brown rugose fruit virus, where strict hygiene and control of plant material movement are essential. Vector management is equally critical, especially for viruses transmitted by Bemisia tabaci and Frankliniella occidentalis, where ecological and integrated pest management strategies must be applied. Host resistance continues to be a cornerstone of disease control, although its long-term effectiveness is increasingly challenged by the emergence of resistance-breaking viral strains. Cross-protection strategies remain effective in specific systems, particularly for Pepino mosaic virus, when carefully managed. The integration of high-throughput diagnostics and continuous surveillance is essential for early detection and rapid response. Together, these approaches form the foundation of modern virus management in intensive tomato production systems.

7. Conclusions and Future Perspectives

Tomato virology is undergoing a profound transformation driven by advances in metagenomics, systems biology, and artificial intelligence. The traditional concept of single-virus diseases is being replaced by a more accurate understanding of virome-driven disease ecology, where multiple interacting viruses shape disease outcomes. Future progress will depend on the integration of global surveillance networks, standardized analytical frameworks, predictive AI-based epidemiology, and the development of durable multi-virus resistance strategies. Strengthening the connection between molecular virology, field epidemiology, and decision-support systems will be essential for sustainable tomato production. Ultimately, the future of tomato health management will rely on a predictive, systems-based approach in which viral evolution, vector ecology, and artificial intelligence converge to anticipate and mitigate disease outbreaks before they become economically damaging epidemics.