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Tomato mosaic virus (ToMV) is one of the economically damageable Tobamovirus infecting the tomato in Egypt that has caused significant losses. It is therefore of great interest to trigger systemic resistance to ToMV. In this endeavor, we aimed to explore the capacity of ZnO-NPs (zinc oxide nanoparticles) to trigger tomato plant resistance against ToMV. Effects of ZnO-NPs on tomato (Solanum lycopersicum L.) growth indices and antioxidant defense system activity under ToMV stress were investigated. Noticeably that treatment with ZnO-NPs showed remarkably increased growth indices, photosynthetic attributes, and enzymatic and non-enzymatic antioxidants compared to the challenge control. Interestingly, oxidative damage caused by ToMV was reduced by reducing malondialdehyde, H2O2, and O2 levels. Overall, ZnO-NPs offer a safe and economic antiviral agent against ToMV.

The bumblebee Bombus terrestris is a beneficial pollinator extensively used in tomato production. Our hypothesis was that bumblebee hives collected from a Tomato brown rugose fruit virus (ToBRFV) infected tomato greenhouse, preserve an infectious primary inoculum. Placing a bumblebee hive collected from a ToBRFV contaminated greenhouse, in a glass-/net-house containing only uninfected healthy tomato plants, spread ToBRFV disease. Control uninfected tomato plants grown in a glass-/net-house devoid of any beehive remained uninfected. ToBRFV-contaminated hives carried infectious viral particles as demonstrated in a biological assay on laboratory test plants of virus extracted from hive components. Viral particles isolated from a contaminated hive had a typical tobamovirus morphology observed in transmission electron microscopy. Assembly of ToBRFV genome was achieved by next generation sequencing analysis of RNA adhering to the bumblebee body. Bumblebee dissection showed that ToBRFV was mostly present in the abdomen suggesting viral disease spread via buzz pollination. These results demonstrate that bumblebee hives collected from ToBRFV-contaminated greenhouses carry a primary inoculum that reflects the status of viruses in the growing area. This new mode of ToBRFV spread by pollinators opens an avenue for detection of viruses in a growing area through analysis of the pollinators, as well as emphasizes the need to reevaluate the appropriate disease management protocols.

The tomato Tm-22 gene is a highly effective, and durable resistance gene in agriculture that has protected tomato production against viruses of the Tobamovirus genus, such as tomato mosaic virus (ToMV) and tobacco mosaic virus (TMV) for over 60 years. This dominant R gene, originally sourced from wild tomato species (Solanum peruvianum), acts by recognizing the viral movement protein (MP) and triggering an immune response, often resulting in extreme resistance (ER). However, this durable protection is challenged by a recently emerged new tobamovirus named tomato brown rugose fruit virus (ToBRFV, Tobamovirus fructirugosum). ToBRFV-encoded MP is responsible for ER breakdown. Here, we present evidence that while ToBRFV can evade Tm-22-mediated ER, Nicotiana benthamiana and tomato plants carrying Tm-22 still remain partially resistant to ToBRFV. We show that ToBRFV MP is recognized by and interacts with Tm-22 to trigger an attenuated hypersensitive response. Moreover, we discover that overexpression of Tm-22 can enhance resistance to ToBRFV. These findings demonstrate the practical value of Tm-22 in ongoing resistance breeding programs and open a potential avenue to restore Tm-22 immunity through upregulation of Tm-22 expression.

Tomato mosaic disease, caused by Tomato Mosaic Virus (ToMV), is one of the most destructive diseases which results in serious crop losses. Research investigations dealing with the biocontrol activity of arbuscular mycorrhizal fungi (AMF) against this viral disease are limited. In this study, the biocontrol activity of AMF on tomato plants infected with ToMV was evaluated in the greenhouse. In addition, their impacts on the transcriptional expression levels of thirteen genes controlling the phenylpropanoid, flavonoid and chlorogenic acid biosynthetic pathways were also investigated using quantitative real-time PCR. Transcriptional expressions of the majority of the studied genes were up-regulated by mycorrhizal colonization in the presence of ToMV, particularly PAL1 and HQT , suggesting their pathogen-dependent inducing effect. Under greenhouse conditions, a significant reduction in the disease severity and incidence, as well as the viral accumulation level was observed as a response to the mycorrhizal colonization of the infected plants. Moreover, the evaluated growth parameters, photosynthetic pigments, and flavonoid content were significantly enhanced by AMF colonization. The obtained results demonstrated the protective role of AMF in triggering the plant immunity against ToMV in a pathogen-dependent manner. Beside their protective and growth-promotion activities, AMF are characterized by low-cost and environment-friendly properties which support their possible use for control of tomato mosaic disease.

Plant viruses drive widespread crop epidemics, yet the host plant responses across different cell types, particularly how these responses are influenced by cultivars with varying genetic backgrounds, including the presence of resistance (R) genes, remain poorly understood. Using tomato brown rugose fruit virus (ToBRFV) and two tomato cultivars, ‘Jinpeng No. 1’ (JP) and ‘Rutgers’ (RG), with different genetic backgrounds, this study used single‐cell RNA sequencing to explore infection dynamics and responses at the cellular level. Results showed that ToBRFV accumulated to different levels in the two cultivars, likely due to differences in their genetic backgrounds, particularly the distinct genotypes of the Tm‐22 and tm‐2 alleles. Following infection, the composition of cell types in tomato leaves also varied between the two cultivars. While the entry or movement of ToBRFV in the JP cultivar was not fully prevented early on, the viral accumulation in certain cell types of this cultivar was restricted. ToBRFV alters signalling pathways based on cell type and cultivars. Pseudotime analysis revealed that, in JP plants, ToBRFV reverses expression of brassinosteroid (BR) positive regulators during mesophyll cell development. Silencing positive BR regulators increased infection in JP plants, while suppressing it in RG plants, linking BR signalling to JP‐dependent resistance. Exogenous BR suppressed ToBRFV in JP but enhanced it in RG plants. This study reveals the differential involvement of BR signalling during viral infection in the two cultivars, offering a framework for future studies of plant‐virus interactions.

The vast majority of known viruses belong to the positive-sense single-stranded RNA (+ssRNA) class. Tobamoviruses are among the most destructive plant viruses and threaten global food security. It is generally accepted that +ssRNA viruses including tobamoviruses encode proteins solely on their positive strand (+RNA). Here, we identified additional open-reading frames (ORFs) in the negative strand of tobamoviruses, named reverse ORFs (rORFs). Using cucumber green mottle mosaic virus (CGMMV) as a model, we detected the corresponding peptides of rORFs by mass spectrometry analysis and confirmed the translation of rORFs by ribosome profiling. Furthermore, we demonstrated that these rORFs may be translated from an internal ribosome entry site. Mutation of rORF1 and rORF2 significantly reduced the virulence of CGMMV, whereas ectopic expression of rORF1 and rORF2 could rescue the pathogenicity of the mutants. While the rORF2 protein localizes at the cell membrane and in the nucleolus, rORF1 colocalizes with peroxisomes, where it interacts with the viral 126-kD replication protein. Additionally, we screened peroxisomal rORF1-interacting proteins using artificial intelligence tools and found that PEX3 mediated rORF1 targeting to peroxisomes. This study reveals that the tobamoviral proteome is larger than previously thought, and sheds light on peroxisomes as novel virulence targets important for virus infectivity.

Tomato brown rugose fruit virus (ToBRFV) is a new damaging plant virus of great interest from both an economical and research point of view. ToBRFV is transmitted by contact, remains infective for months, and to-date, no resistant cultivars have been developed. Due to the relevance of this virus, new effective, sustainable, and operator-safe antiviral agents are needed. Thus, 4-hydroxybenzoic acid was identified as the main product of the alkaline autoxidation at high temperature of the methanolic extract of the leaves of C. micranthum, known for antiviral activity. The autoxidized extract and 4-hydroxybenzoic acid were assayed in in vitro experiments, in combination with a mechanical inoculation test of tomato plants. Catechinic acid, a common product of rearrangement of catechins in hot alkaline solution, was also tested. Degradation of the viral particles, evidenced by the absence of detectable ToBRFV RNA and the loss of virus infectivity, as a possible consequence of disassembly of the virus coat protein (CP), were shown. Homology modeling was then applied to prepare the protein model of ToBRFV CP, and its structure was optimized. Molecular docking simulation showed the interactions of the two compounds, with the amino acid residues responsible for CP-CP interactions. Catechinic acid showed the best binding energy value in comparison with ribavirin, an anti-tobamovirus agent.

Tomato brown rugose fruit virus (ToBRFV) is a rapidly spreading pathogen that poses a significant threat to tomato production worldwide. We previously identified a locus on tomato chromosome 11 controlling tolerance to the virus. We further established that combining this locus with one that maps to the Tm-1 region on chromosome 2 confers resistance to the virus. Here we sought to determine whether, and how, the Tm-1 gene itself is involved in ToBRFV resistance. Overexpression of Tm-1 in a tolerant genotype significantly reduced viral accumulation, conferring resistance to ToBRFV. On the other hand, overexpression of Tm-1 in a susceptible genotype only delayed symptom appearance. Moreover, effective RNAi-silencing of Tm-1 in the resistant genotype yielded susceptible plants. These findings show that the Tm-1 gene interacts genetically with the locus controlling tolerance on chromosome 11 and that this interaction is critical for achieving effective resistance to ToBRFV. In addition, the symptomatic plants obtained following silencing of Tm-1 in the resistant genotype indicate that tolerance is also dependent on normal expression levels of the recessive tm-1 allele.

Summary The tobamovirus tomato brown rugose fruit virus (ToBRFV) has recently emerged, causing significant damage to the tomato industry in various regions worldwide, including the US. ToBRFV evades the widely used Tm‐22 resistance gene, which encodes a nucleotide‐binding leucine‐rich repeat (NLR) class immune receptor with an N‐terminal coiled‐coil (CC) domain that confers resistance to the tomato mosaic virus (ToMV). In this study, we tested a transgenic tomato line (tomatoNN) expressing the Nicotiana glutinosa N gene, which encodes an NLR with a Toll‐Interleukin 1 homology domain (TIR) at the N‐terminus, for resistance to ToBRFV. Our results demonstrate that tomatoNN is resistant to ToBRFV, evidenced by the necrotic local lesions observed on the inoculated leaves and the absence of symptoms on systemic leaves. This correlates with very low to non‐detectable virus levels in double antibody sandwich enzyme‐linked immunosorbent (DAS‐ELISA) and quantitative reverse transcription‐polymerase chain reaction (RT‐qPCR) assays. Furthermore, our findings reveal that tomatoNN is resistant to ToBRFV at 22 °C, but not at 30 °C, showing that the temperature‐sensitive nature of N‐mediated resistance also extends to ToBRFV resistance in tomato. These results highlight the significant potential of using tomatoNN to breed tomato cultivars resistant to ToBRFV, offering a new approach to managing the global pandemic caused by this emerging virus.

The tobamovirus tomato brown rugose fruit virus (ToBRFV), a major threat to tomato production worldwide, has recently been documented in mixed infections with the potexvirus pepino mosaic virus (PepMV) CH2 strain in traded tomatoes in Israel. A study of greenhouse tomato plants in Israel revealed severe new viral disease symptoms including open unripe fruits and yellow patched leaves. PepMV was only detected in mixed infections with ToBRFV in all 104 tested sites, using serological and molecular analyses. Six PepMV isolates were identified, all had predicted amino acids characteristic of CH2 mild strains excluding an isoleucine at amino acid position 995 of the replicase. High-throughput sequencing of viral RNA extracted from four selected symptomatic plants showed solely the ToBRFV and PepMV, with total aligned read ratios of 40.61% and 11.73%, respectively, indicating prevalence of the viruses. Analyses of interactions between the co-infecting viruses by sequential and mixed viral inoculations of tomato plants, at various temperatures, showed a prominent increase in PepMV titers in ToBRFV pre-inoculated plants and in mixed-infected plants at 18–25 °C, compared to PepMV-single inoculations, as analyzed by Western blot and quantitative RT-PCR tests. These results suggest that Israeli mild PepMV isolate infections, preceded by ToBRFV, could induce symptoms characteristic of PepMV aggressive strains.