{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T15:24:21Z","timestamp":1791386661911,"version":"4.3.3"},"reference-count":85,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,9,30]],"date-time":"2025-09-30T00:00:00Z","timestamp":1759190400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100012331","name":"Flanders Innovation & Entrepreneurship","doi-asserted-by":"crossref","award":["HBC.2020.2306"],"award-info":[{"award-number":["HBC.2020.2306"]}],"id":[{"id":"10.13039\/100012331","id-type":"DOI","asserted-by":"crossref"}]},{"name":"European Union\u2019s Horizon 2020 research and innovation programme","award":["955974"],"award-info":[{"award-number":["955974"]}]}],"content-domain":{"domain":["www.mdpi.com"],"crossmark-restriction":true},"short-container-title":["Viruses"],"abstract":"<jats:p>Plant viruses have detrimental effects on commercial tomato cultivation leading to severe economic consequences. Viral metagenomics studies provide the opportunity to examine in depth the virome composition of a sample set without any pre-existing knowledge of the viral species that are present. In the present study, 101 plant samples were collected from commercial greenhouses in 13 countries in Europe, Africa, Asia, and North America between 2017 and 2024. All samples were processed with the VLP enrichment protocol NetoVIR and the obtained data were analyzed with the ViPER pipeline. Forty-three eukaryotic viral species were identified, with a median identification of 2 species per sample. The most prevalent viral species were pepino mosaic virus (PepMV), tomato brown rugose fruit virus (ToBRFV), and southern tomato virus (STV). The obtained genome sequences were used to study the diversity and phylogeny of these viruses. The three genotypes identified for PepMV showed low diversity within each genotype (96.2\u201399.0% nucleotide identity). Low isolate diversity was also found for ToBRFV and STV. No significant association could be found between STV identification and the presence of symptoms, questioning the pathogenic potential of STV. Three other pathogenic viral species of particular interest due to their effects on tomato cultivation or recent emergence, namely tomato torrado virus (ToTV), tomato fruit blotch virus (ToFBV), and cucumber mosaic virus (CMV), were part of the virome with low prevalence. Our study provided a comprehensive overview of the analyzed samples\u2019 virome, as well as the possibility to inspect the genetic diversity of the identified viral genomes and to look into their potential role in symptom development.<\/jats:p>","DOI":"10.3390\/v17101334","type":"journal-article","created":{"date-parts":[[2025,9,30]],"date-time":"2025-09-30T15:38:55Z","timestamp":1759246735000},"page":"1334","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Metagenomics Study of the Commercial Tomato Virome Focused on Virus Species of Epidemiological Interest"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2016-9930","authenticated-orcid":false,"given":"Zafeiro","family":"Zisi","sequence":"first","affiliation":[{"name":"Laboratory of Viral Metagenomics, KU Leuven, Department of Microbiology, Immunology and Transplantation, REGA Institute, Division of Clinical and Epidemiological Virology, 3000 Leuven, Belgium"},{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabel","family":"Ruiz Movilla","sequence":"additional","affiliation":[{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0791-4369","authenticated-orcid":false,"given":"Nikolas","family":"Basler","sequence":"additional","affiliation":[{"name":"Laboratory of Viral Metagenomics, KU Leuven, Department of Microbiology, Immunology and Transplantation, REGA Institute, Division of Clinical and Epidemiological Virology, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lila","family":"Close","sequence":"additional","affiliation":[{"name":"Laboratory of Viral Metagenomics, KU Leuven, Department of Microbiology, Immunology and Transplantation, REGA Institute, Division of Clinical and Epidemiological Virology, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-7533-0668","authenticated-orcid":false,"given":"Lucas","family":"Ghijselings","sequence":"additional","affiliation":[{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robby","family":"Van der Hoeven","sequence":"additional","affiliation":[{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4262-4498","authenticated-orcid":false,"given":"Maria Ioanna","family":"Papadaki","sequence":"additional","affiliation":[{"name":"Laboratory of Viral Metagenomics, KU Leuven, Department of Microbiology, Immunology and Transplantation, REGA Institute, Division of Clinical and Epidemiological Virology, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ester","family":"Rabbinowitsch","sequence":"additional","affiliation":[{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fiona","family":"Van Reeth","sequence":"additional","affiliation":[{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jill","family":"Swinnen","sequence":"additional","affiliation":[{"name":"Laboratory of Viral Metagenomics, KU Leuven, Department of Microbiology, Immunology and Transplantation, REGA Institute, Division of Clinical and Epidemiological Virology, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-0324-8098","authenticated-orcid":false,"given":"Elise","family":"Vogel","sequence":"additional","affiliation":[{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"},{"name":"DCM NV, 2280 Grobbendonk, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Vos","sequence":"additional","affiliation":[{"name":"Scientia Terrae Research Institute VZW, B-2860 St.-Katelijne-Waver, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Inge","family":"Hanssen","sequence":"additional","affiliation":[{"name":"DCM NV, 2280 Grobbendonk, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1188-9733","authenticated-orcid":false,"given":"Jelle","family":"Matthijnssens","sequence":"additional","affiliation":[{"name":"Laboratory of Viral Metagenomics, KU Leuven, Department of Microbiology, Immunology and Transplantation, REGA Institute, Division of Clinical and Epidemiological Virology, 3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,9,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Rivarez, M.P.S., Vu\u010durovi\u0107, A., Mehle, N., Ravnikar, M., and Kutnjak, D. (2021). Global Advances in Tomato Virome Research: Current Status and the Impact of High-Throughput Sequencing. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.671925"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Jones, R.A.C. (2021). Global Plant Virus Disease Pandemics and Epidemics. Plants, 10.","DOI":"10.3390\/plants10020233"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.coviro.2015.01.005","article-title":"Ecosystem Simplification, Biodiversity Loss and Plant Virus Emergence","volume":"10","author":"Roossinck","year":"2015","journal-title":"Curr. Opin. Virol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Dombrovsky, A., and Smith, E. (2017). Seed Transmission of Tobamoviruses: Aspects of Global Disease Distribution. Advances in Seed Biology, IntechOpen Limited.","DOI":"10.5772\/intechopen.70244"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/bs.aivir.2016.02.004","article-title":"Future Scenarios for Plant Virus Pathogens as Climate Change Progresses","volume":"95","author":"Jones","year":"2016","journal-title":"Adv. Virus Res."},{"key":"ref_6","unstructured":"FAOSTAT (Food and Agriculture Organization of the United Nations) (2024, December 04). Crops and Livestock Products. Available online: https:\/\/www.fao.org\/faostat\/en\/#data\/QCL."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1094\/MPMI-23-5-0539","article-title":"Emerging Viral Diseases of Tomato Crops","volume":"23","author":"Hanssen","year":"2010","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1007\/s11816-020-00638-1","article-title":"Molecular Genetic Approaches for Enhancing Stress Tolerance and Fruit Quality of Tomato","volume":"14","author":"Wai","year":"2020","journal-title":"Plant Biotechnol. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Shahriari, Z., Su, X., Zheng, K., and Zhang, Z. (2023). Advances and Prospects of Virus-Resistant Breeding in Tomatoes. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms242015448"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1111\/j.1364-3703.2009.00600.x","article-title":"Pepino Mosaic Virus: A Successful Pathogen That Rapidly Evolved from Emerging to Endemic in Tomato Crops","volume":"11","author":"Hanssen","year":"2010","journal-title":"Mol. Plant Pathol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1094\/PDIS.2000.84.1.103C","article-title":"First Report of Pepino Mosaic Virus on Tomato","volume":"84","author":"Stijger","year":"2000","journal-title":"Plant Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3359","DOI":"10.1128\/JVI.02980-13","article-title":"Ecological and Genetic Determinants of Pepino Mosaic Virus Emergence","volume":"88","author":"Fraile","year":"2014","journal-title":"J. Virol."},{"key":"ref_13","unstructured":"(2024, December 04). EPPO Global Database. Available online: https:\/\/gd.eppo.int\/taxon\/PEPMV0\/distribution."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1111\/j.1365-3059.2006.01406.x","article-title":"Effect of Pepino Mosaic Virus on the Yield and Quality of Glasshouse-Grown Tomatoes in the UK","volume":"55","author":"Spence","year":"2006","journal-title":"Plant Pathol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Luria, N., Smith, E., Reingold, V., Bekelman, I., Lapidot, M., Levin, I., Elad, N., Tam, Y., Sela, N., and Abu-Ras, A. (2017). A New Israeli Tobamovirus Isolate Infects Tomato Plants Harboring Tm-22 Resistance Genes. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0170429"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"89","DOI":"10.17660\/ActaHortic.2021.1316.13","article-title":"Tomato Genetic Resistance to Tobamoviruses Is Compromised","volume":"1316","author":"Avni","year":"2021","journal-title":"Acta Hortic."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1016\/j.tplants.2020.03.015","article-title":"Tomato Yellow Leaf Curl Virus: Impact, Challenges, and Management","volume":"25","author":"Prasad","year":"2020","journal-title":"Trends Plant Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1111\/mpp.12481","article-title":"Tomato Leaf Curl New Delhi Virus: A Widespread Bipartite Begomovirus in the Territory of Monopartite Begomoviruses","volume":"18","author":"Zaidi","year":"2017","journal-title":"Mol. Plant Pathol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Qi, S., Zhang, S., Islam, M.M., El-Sappah, A.H., Zhang, F., and Liang, Y. (2021). Natural Resources Resistance to Tomato Spotted Wilt Virus (TSWV) in Tomato (Solanum lycopersicum). Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222010978"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Kanapiya, A., Amanbayeva, U., Tulegenova, Z., Abash, A., Zhangazin, S., Dyussembayev, K., and Mukiyanova, G. (2024). Recent Advances and Challenges in Plant Viral Diagnostics. Front. Plant Sci., 15.","DOI":"10.3389\/fpls.2024.1451790"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Gonz\u00e1lez-P\u00e9rez, E., Chiquito-Almanza, E., Villalobos-Reyes, S., Canul-Ku, J., and Anaya-L\u00f3pez, J.L. (2024). Diagnosis and Characterization of Plant Viruses Using HTS to Support Virus Management and Tomato Breeding. Viruses, 16.","DOI":"10.20944\/preprints202404.1813.v1"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1094\/PHYTO-12-14-0356-RVW","article-title":"Plant Virus Metagenomics: Advances in Virus Discovery","volume":"105","author":"Roossinck","year":"2015","journal-title":"Phytopathology"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Bassi, C., Guerriero, P., Pierantoni, M., Callegari, E., and Sabbioni, S. (2022). Novel Virus Identification through Metagenomics: A Systematic Review. Life, 12.","DOI":"10.3390\/life12122048"},{"key":"ref_24","unstructured":"Wang, A., and Zhou, X. (2016). Diagnosis of Plant Viruses Using Next-Generation Sequencing and Metagenomic Analysis. Current Research Topics in Plant Virology, Springer International Publishing."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Concei\u00e7\u00e3o-Neto, N., Zeller, M., Lefr\u00e8re, H., De Bruyn, P., Beller, L., Deboutte, W., Yinda, C.K., Lavigne, R., Maes, P., and Ranst, M.V. (2015). Modular Approach to Customise Sample Preparation Procedures for Viral Metagenomics: A Reproducible Protocol for Virome Analysis. Sci. Rep., 5.","DOI":"10.1038\/srep16532"},{"key":"ref_26","unstructured":"De Coninck, L. ViPER. Zenodo., 2021."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.jviromet.2009.07.008","article-title":"Real-Time Quantitative PCR Based Sensitive Detection and Genotype Discrimination of Pepino Mosaic Virus","volume":"162","author":"Mehle","year":"2009","journal-title":"J. Virol. Methods"},{"key":"ref_28","unstructured":"ISF-ISHI-Veg (2020). Detection of Infectious Tomato Brown Rugose Fruit Virus (ToBRFV) in Tomato and Pepper Seeds, International Seed Federation."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Elvira Gonz\u00e1lez, L., Peir\u00f3, R., Rubio, L., and Galipienso, L. (2021). Persistent Southern Tomato Virus (STV) Interacts with Cucumber Mosaic and\/or Pepino Mosaic Virus in Mixed- Infections Modifying Plant Symptoms, Viral Titer and Small RNA Accumulation. Microorganisms, 9.","DOI":"10.3390\/microorganisms9040689"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.jviromet.2015.04.029","article-title":"Detection and Absolute Quantitation of Tomato Torrado Virus (ToTV) by Real Time RT-PCR","volume":"221","author":"Rubio","year":"2015","journal-title":"J. Virol. Methods"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Maachi, A., Torre, C., Sempere, R.N., Hernando, Y., Aranda, M.A., and Donaire, L. (2021). Use of High-Throughput Sequencing and Two RNA Input Methods to Identify Viruses Infecting Tomato Crops. Microorganisms, 9.","DOI":"10.3390\/microorganisms9051043"},{"key":"ref_32","first-page":"286","article-title":"Multiplex Nested Reverse Transcription-Polymerase Chain Reaction in a Single Tube for Sensitive and Simultaneous Detection of Four RNA Viruses and Pseudomonas savastanoi pv","volume":"93","author":"Bertolini","year":"2003","journal-title":"savastanoi in Olive Trees. Phytopathology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1111\/j.1745-7270.2006.00216.x","article-title":"Quantitative Determination of Cucumber Mosaic Virus Genome RNAs in Virions by Real-Time Reverse Transcription-Polymerase Chain Reaction","volume":"38","author":"Feng","year":"2006","journal-title":"Acta Biochim. Biophys. Sin."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1007\/s10658-007-9255-0","article-title":"Genetic Characterization of Pepino Mosaic Virus Isolates from Belgian Greenhouse Tomatoes Reveals Genetic Recombination","volume":"121","author":"Hanssen","year":"2008","journal-title":"Eur. J. Plant Pathol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2488","DOI":"10.1038\/s41564-024-01796-6","article-title":"Diverse RNA Viruses of Parasitic Nematodes Can Elicit Antibody Responses in Vertebrate Hosts","volume":"9","author":"Quek","year":"2024","journal-title":"Nat. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Mbigha Donfack, K.C., De Coninck, L., Ghogomu, S.M., and Matthijnssens, J. (2024). Aedes Mosquito Virome in Southwestern Cameroon: Lack of Core Virome, But a Very Rich and Diverse Virome in Ae. Africanus Compared to Other Aedes Species. Viruses, 16.","DOI":"10.20944\/preprints202406.0963.v1"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A Flexible Trimmer for Illumina Sequence Data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Nurk, S., Bankevich, A., Antipov, D., Gurevich, A., Korobeynikov, A., Lapidus, A., Prjibelsky, A., Pyshkin, A., Sirotkin, A., and Sirotkin, Y. (2013). Assembling Genomes and Mini-Metagenomes from Highly Chimeric Reads. Research in Computational Molecular Biology, Proceedings of the 17th Annual International Conference, RECOMB 2013, Beijing, China, 7\u201310 April 2013, Springer.","DOI":"10.1007\/978-3-642-37195-0_13"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L. (2009). BLAST+: Architecture and Applications. BMC Bioinform., 10.","DOI":"10.1186\/1471-2105-10-421"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1038\/s41587-020-00774-7","article-title":"CheckV Assesses the Quality and Completeness of Metagenome-Assembled Viral Genomes","volume":"39","author":"Nayfach","year":"2021","journal-title":"Nat. Biotechnol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and Sensitive Protein Alignment Using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Ondov, B.D., Bergman, N.H., and Phillippy, A.M. (2011). Interactive Metagenomic Visualization in a Web Browser. BMC Bioinform., 12.","DOI":"10.1186\/1471-2105-12-385"},{"key":"ref_43","unstructured":"Li, H. (2013). Aligning Sequence Reads, Clone Sequences and Assembly Contigs with BWA-MEM. arXiv."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"giab008","DOI":"10.1093\/gigascience\/giab008","article-title":"Twelve Years of SAMtools and BCFtools","volume":"10","author":"Danecek","year":"2021","journal-title":"Gigascience"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates","volume":"14","author":"Kalyaanamoorthy","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"D817","DOI":"10.1093\/nar\/gkad946","article-title":"ViralZone 2024 Provides Higher-Resolution Images and Advanced Virus-Specific Resources","volume":"52","author":"Hulo","year":"2024","journal-title":"Nucleic Acids Res."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Diop, S.I., Geering, A.D.W., Alfama-Depauw, F., Loaec, M., Teycheney, P.-Y., and Maumus, F. (2018). Tracheophyte Genomes Keep Track of the Deep Evolution of the Caulimoviridae. Sci. Rep., 8.","DOI":"10.1038\/s41598-017-16399-x"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"van de Vossenberg, B.T.L.H., Visser, M., Bruinsma, M., Koenraadt, H.M.S., Westenberg, M., and Botermans, M. (2020). Real-Time Tracking of Tomato Brown Rugose Fruit Virus (ToBRFV) Outbreaks in the Netherlands Using Nextstrain. PLoS ONE, 15.","DOI":"10.1101\/2020.06.02.129395"},{"key":"ref_51","unstructured":"de Koning, P.P.M., Fowkes, A.R., Zisi, Z., Beris, D., Oplaat, C., McGreig, S., Skelton, A., Adams, I.P., van Gemert, J., and de Krom, C. Tomato Brown Rugose Fruit Virus Nextstrain Build Version 4: Pathways of Introduction and Local Spread. PhytoFrontiersTM."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Zisi, Z., Ghijselings, L., Vogel, E., Vos, C., and Matthijnssens, J. (2024). Single Amino Acid Change in Tomato Brown Rugose Fruit Virus Breaks Virus-Specific Resistance in New Resistant Tomato Cultivar. Front. Plant Sci., 15.","DOI":"10.3389\/fpls.2024.1382862"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1146\/annurev-phyto-080614-120021","article-title":"Torradoviruses","volume":"53","author":"Verbeek","year":"2015","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Anikina, I., Kamarova, A., Issayeva, K., Issakhanova, S., Mustafayeva, N., Insebayeva, M., Mukhamedzhanova, A., Khan, S.M., Ahmad, Z., and Lho, L.H. (2023). Plant Protection from Virus: A Review of Different Approaches. Front. Plant Sci., 14.","DOI":"10.3389\/fpls.2023.1163270"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2071","DOI":"10.1111\/ppa.13968","article-title":"Detection of Tomato Brown Rugose Fruit Virus in Environmental Residues: The Importance of Contextualizing Test Results","volume":"73","author":"Giesbers","year":"2024","journal-title":"Plant Pathol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1111\/ppa.13771","article-title":"Detection of Tomato Brown Rugose Fruit Virus Is Influenced by Infection at Different Growth Stages and Sampling from Different Plant Parts","volume":"72","author":"Skelton","year":"2023","journal-title":"Plant Pathol."},{"key":"ref_57","unstructured":"(2024, December 04). EPPO Global Database. Available online: https:\/\/gd.eppo.int\/taxon\/TOBRFV\/distribution."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/j.1365-3059.2009.02190.x","article-title":"Cross-Protection or Enhanced Symptom Display in Greenhouse Tomato Co-Infected with Different Pepino Mosaic Virus Isolates","volume":"59","author":"Hanssen","year":"2010","journal-title":"Plant Pathol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1094\/PHYTO-96-0274","article-title":"Genetic Structure of the Population of Pepino Mosaic Virus Infecting Tomato Crops in Spain","volume":"96","author":"Fraile","year":"2006","journal-title":"Phytopathology"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1094\/PHYTOFR-09-22-0090-A","article-title":"Tomato Brown Rugose Fruit Virus Nextstrain Build Version 3: Rise of a Novel Clade","volume":"3","author":"Botermans","year":"2022","journal-title":"PhytoFrontiers"},{"key":"ref_61","first-page":"211","article-title":"Population Genetic Dynamics of Southern Tomato Virus from Turkey","volume":"105","author":"Fox","year":"2023","journal-title":"Journal of Plant Pathology"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.virusres.2008.11.018","article-title":"Southern Tomato Virus: The Link between the Families Totiviridae and Partitiviridae","volume":"140","author":"Sabanadzovic","year":"2009","journal-title":"Virus Res."},{"key":"ref_63","first-page":"505","article-title":"Chapter 14\u2014Pepino Mosaic Virus and Tomato Torrado Virus: Two Emerging Viruses Affecting Tomato Crops in the Mediterranean Basin","volume":"Volume 84","author":"Loebenstein","year":"2012","journal-title":"Advances in Virus Research"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1094\/PDIS-91-10-1364A","article-title":"The First Report of Tomato Torrado Virus in Poland","volume":"91","author":"Pospieszny","year":"2007","journal-title":"Plant Dis."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.1094\/PDIS-93-12-1352C","article-title":"First Report of Tomato Torrado Virus in Tomato Crops in France","volume":"93","author":"Verdin","year":"2009","journal-title":"Plant Dis."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1094\/PDIS-93-5-0554C","article-title":"First Report of Tomato Torrado Virus Infecting Tomato in Hungary","volume":"93","author":"Bese","year":"2009","journal-title":"Plant Dis."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.1094\/PDIS-94-9-1172A","article-title":"First Report of Tomato Torrado Virus Infecting Tomato in Italy","volume":"94","author":"Davino","year":"2010","journal-title":"Plant Dis."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1111\/j.1439-0434.2009.01639.x","article-title":"Occurrence and Geographical Distribution of the \u2018Torrado\u2019 Disease in Spain","volume":"158","author":"Font","year":"2010","journal-title":"J. Phytopathol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/B978-0-12-394314-9.00002-6","article-title":"Chapter 2\u2014Major Tomato Viruses in the Mediterranean Basin","volume":"Volume 84","author":"Loebenstein","year":"2012","journal-title":"Advances in Virus Research"},{"key":"ref_70","unstructured":"(2024, December 04). EPPO Global Database. Available online: https:\/\/gd.eppo.int\/taxon\/TOTV00\/distribution."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1146\/annurev-phyto-021622-120703","article-title":"Tomato Brown Rugose Fruit Virus Pandemic","volume":"61","author":"Salem","year":"2023","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Moodley, V., Gubba, A., and Mafongoya, P.L. (2020). Emergence and Full Genome Analysis of Tomato Torrado Virus in South Africa. Viruses, 12.","DOI":"10.3390\/v12101167"},{"key":"ref_73","first-page":"1738","article-title":"ICTV Virus Taxonomy Profile: Potyviridae 2022","volume":"103","author":"Jordan","year":"2022","journal-title":"J. Gen. Virol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1111\/j.1365-3059.1994.tb01638.x","article-title":"A Potyvirus Isolated from Solanaceous Hosts","volume":"43","author":"Walkey","year":"1994","journal-title":"Plant Pathol."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Luigi, M., Tiberini, A., Taglienti, A., Bertin, S., Dragone, I., Sybilska, A., Tarchi, F., Goggioli, D., Lewandowski, M., and Simoni, S. (2024). Molecular Methods for the Simultaneous Detection of Tomato Fruit Blotch Virus and Identification of Tomato Russet Mite, a New Potential Virus\u2013Vector System Threatening Solanaceous Crops Worldwide. Viruses, 16.","DOI":"10.3390\/v16050806"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2271","DOI":"10.1094\/PDIS-07-21-1392-PDN","article-title":"First Report of Tomato Fruit Blotch Virus Infecting Tomatoes in Brazil","volume":"106","author":"Nakasu","year":"2022","journal-title":"Plant Dis."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"e12219","DOI":"10.1002\/ndr2.12219","article-title":"First Report of Tomato Fruit Blotch Fruit Virus Infecting Tomato in Greece","volume":"48","author":"Beris","year":"2023","journal-title":"New Dis. Rep."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/s10493-023-00777-4","article-title":"Genetic Analysis of the Tomato Russet Mite Provides Evidence of Oligophagy and a Widespread Pestiferous Haplotype","volume":"89","author":"Duarte","year":"2023","journal-title":"Exp. Appl. Acarol."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Perring, T., and Farrar, C. (1986). Historical Perspective and Current World Status of the Tomato Russet Mite (Acari: Eriophyidae), Entomological Society of America.","DOI":"10.4182\/CCMM7124.63.1"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1111\/j.1364-3703.2011.00749.x","article-title":"Cucumber Mosaic Virus: Viral Genes as Virulence Determinants","volume":"13","author":"Mochizuki","year":"2012","journal-title":"Mol. Plant Pathol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/S0065-3527(08)60039-1","article-title":"Cucumber Mosaic Virus","volume":"Volume 41","author":"Maramorosch","year":"1992","journal-title":"Advances in Virus Research"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1094\/PHYTO-05-22-0167-RVW","article-title":"Plant Viruses of Agricultural Importance: Current and Future Perspectives of Virus Disease Management Strategies","volume":"113","author":"Tatineni","year":"2022","journal-title":"Phytopathology"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1007\/s007050050280","article-title":"The Universal System of Virus Taxonomy of the International Committee on Virus Taxonomy (ICTV), Including New Proposals Ratified since Publication of the Sixth ICTV Report in 1995","volume":"143","author":"Pringle","year":"1998","journal-title":"Arch. Virol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1099\/0022-1317-81-6-1579","article-title":"Characterization and Genomic Analysis of Tobacco Vein Clearing Virus, a Plant Pararetrovirus That Is Transmitted Vertically and Related to Sequences Integrated in the Host Genome","volume":"81","author":"Lockhart","year":"2000","journal-title":"J. Gen. Virol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"77","DOI":"10.22268\/AJPP-41.1.077084","article-title":"High-Throughput Sequencing and Bioinformatic Analysis Reveal Presence of the Endogenous Pararetrovirus Tobacco Vein Clearing Virus Genome in the Tomato (Solanum lycopersicum) Host Genome","volume":"41","author":"Abass","year":"2023","journal-title":"Arab. J. 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