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Plant viruses have been traditionally considered pathogens restricted to plant hosts. However, recent studies have shown that some plant viruses can infect and replicate in filamentous fungi and oomycetes, suggesting that their host range is broader than previously thought, and that their ecological interactions are more complex. In this study, we investigated the ability of the well-characterized positive-sense RNA plant virus Tobacco mosaic virus (TMV) to replicate in four major phytopathogenic fungi from different taxonomic groups: Botrytis cinerea, Fusarium oxysporum f. sp. lycopersici, Verticillium dahliae, and Monilinia fructicola. Using a recombinant TMV-based vector expressing a green fluorescent protein (TMV-GFP-1056) as reporter, we demonstrated that TMV can enter, replicate, and persist within the mycelia of B. cinerea and V. dahliae—at least through the first subculture. However, it cannot replicate in F. oxysporum f. sp. lycopersici and M. fructicola. RNA interference (RNAi) is a conserved eukaryotic epigenetic mechanism that provides an efficient defence against viruses. We explored the role of RNAi in the interaction between TMV and the mycelia of V. dahliae and B. cinerea. Our results revealed a strong induction of the Dicer-like 1 and Argonaute 1 genes, which are key compounds of the RNA silencing pathway. This RNAi-based response impaired TMV-GFP replication in both fungi. Notably, despite viral replication and RNAi activation, the virulence of V. dahliae and B. cinerea on their respective host plants remained unaffected. These findings reinforce the emerging recognition of cross-kingdom virus transmission and interactions, which likely play a crucial role in pathogen ecology and viral evolution. Understanding these virus–fungus interactions not only sheds light on RNAi interference silencing mechanisms but also suggests that plant viruses like TMV could serve as simple and effective tools for functional genomic studies in fungi, such as in V. dahliae and B. cinerea.

The increasing demand for sustainable agriculture has accelerated research into eco-friendly plant health management, particularly through natural substances rich in bioactive compounds. In this study, various substances, including essential oils, extracts from Aloe vera, artichoke and ornamental plants, by-products from beer and coffee processing, and selected commercial formulations including biostimulants and a plant strengthener, were evaluated for their antimicrobial properties and ability to trigger plant defenses. Notably, Agapanthus spp. exhibited strong antifungal activity against the fungus Botrytis cinerea (Bc), while thyme, tea tree, and lavender essential oils were effective against both Bc and the bacterium Pseudomonas syringae pv. tomato (Pst). Greenhouse trials on tomato plants demonstrated the protective effects of A. vera gel and ornamental plant extracts against Bc and Potato virus Y (PVY), while coffee and artichoke extracts were effective against Pst. An alginate-based formulation containing thyme oil showed enhanced in planta efficacy against the three pathogens. Gene expression analyses revealed early upregulation of PR-1 and PR-4, especially with alginate treatments and A. vera gel at 12 h post-treatment (hpt) while coffee extract triggered the strongest late response at 72 hpt. These findings highlight the potential of plant-derived substances in promoting sustainable plant disease management through both direct antimicrobial action and immune system activation.