Abstract
Since the first report of the tobamovirus tomato brown rugose fruit virus (ToBRFV) in 2014, it has become globally distributed. Its rapid spread has been primarily attributed to seed-borne transmission. Here, the seed-borne nature of ToBRFV transmission was investigated in different cultivars of tomato, bell pepper, and eggplant. In situ hybridization to localize the virus in reproductive organs of ToBRFV-infected tomato plants revealed that the virus was not present in shoot apices, flower buds, or in ovules during flower opening, indicating the virus may be restricted to the outer integument and transported in the vascular bundles during seed development. However, during early fruit development, the virus was present in the integuments in the ovule. Seeds of tomato cultivars with or without tobamovirus resistance gene Tm-22 transmitted the virus to the progeny seedlings at rates that reflected the ineffectiveness of the gene against ToBRFV. Seeds of bell peppers transmitted ToBRFV at higher rates than tomato seeds, but a bell pepper cultivar that has resistance gene L3 was not systemically infected, and its seeds did not harbor the virus. Three eggplant cultivars were systemically infected with ToBRFV but without showing any obvious symptoms, and even though ToBRFV was present in their seeds, the seedlings were not infected. ToBRFV was detected in the seed coats of contaminated tomato and bell pepper seeds, but not in eggplant seed coats. These results indicate mechanistic differences in seed-borne transmission among the three Solanaceae crops.
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References
Abou Kubaa R, Choueiri E, Heinoun K, Cillo F, Saponari M (2022) First report of tomato brown rugose fruit virus infecting sweet pepper in Syria and Lebanon. J Plant Pathol 104:425. https://doi.org/10.1007/s42161-021-00987-y
Aghamohammadi V, Rakhshandehroo F, Shams-Bakhsh M, Palukaitis P (2013) Distribution and genetic diversity of tomato mosaic virus isolates in Iran. J Plant Pathol 95:339–347
Alkowni R, Alabdallah O, Fadda Z (2019) Molecular identification of tomato brown rugose fruit virus in tomato in Palestine. J Plant Pathol 101:719–723. https://doi.org/10.1007/s42161-019-00240-7
Avni B, Gelbart D, Sufrin-Ringwald T, Zemach H, Belausov E, Kamenetsky-Goldstein R, Lapidot M (2022) ToBRFV infects the reproductive tissues of tomato plants but is not transmitted to the progenies by pollination. Cells 11:2864. https://doi.org/10.3390/cells11182864
Bradamante G, Scheid OM, Incarbone M (2021) Under siege: virus control in plant meristems and progeny. Plant Cell 33:2523–2537. https://doi.org/10.1093/plcell/koab140
Broadbent L (1965) The epidemiology of tomato mosaic. XI. Seed transmission of TMV. Ann Appl Biol 56:177–205
Brukhin V, Hernould M, Gonzalez N, Chevalier C, Mouras A (2003) Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry. Sex Plant Reprod 15:311–320. https://doi.org/10.1007/s00497-003-0167-7
Chanda B, Gilliard A, Jaiswal N, Ling K-S (2021a) Comparative analysis of host range, ability to infect tomato cultivars with Tm-22 gene, and real-time reverse transcription PCR detection of tomato brown rugose fruit virus. Plant Dis 105:3643–3652. https://doi.org/10.1094/PDIS-05-20-1070-RE
Chanda B, Shamimuzzaman M, Gilliard A, Ling KS (2021b) Effectiveness of disinfectants against the spread of tobamoviruses: Tomato brown rugose fruit virus and Cucumber green mottle mosaic virus. Virol J 18:7. https://doi.org/10.1186/s12985-020-01479-8
Chapman SN (1998) Tobamovirus isolation and RNA extraction. In: Foster GD, Taylor SC (eds) Plant virology protocols: From virus isolation to transgenic resistance. Humana Press, Totowa, NJ, USA, pp 123–129
Cheng NH, Su CL, Carter SA, Nelson RS (2000) Vascular invasion routes and systemic accumulation patterns of tobacco mosaic virus in Nicotiana benthamiana. Plant J 23:349–362. https://doi.org/10.1046/j.1365-313x.2000.00788.x
Chitra TR, Prakash HS, Albrechtsen SE, Shetty HS, Mathur SB (1999) Infection of tomato and bell pepper by ToMV and TMV at different growth stages and establishment of virus in seeds. J Plant Pathol 81:123–126
Dall DJ, Lovelock DA, Penrose LDJ, Constable FE (2023) Prevalences of tobamovirus contamination in seed lots of tomato and capsicum. Viruses 15:883. https://doi.org/10.3390/v15040883
Davino S, Caruso AG, Bertacca S, Barone S, Panno S (2020) Tomato brown rugose fruit virus: seed transmission rate and efficacy of different seed disinfection treatments. Plants 9:1615. https://doi.org/10.3390/plants9111615
Dombrovsky A, Smith E (2017) Seed transmission of tobamoviruses: aspects of global disease distribution. In: Jimenez-Lopez JC (ed) Advances in seed biology. IntechOpen, London, UK, pp 233–260. https://doi.org/10.5772/intechopen.70244
Eldan O, Ofir A, Luria N, Klap C, Lachman O, Bakelman E, Beausov E, Smith E, Dombrovsky A (2022) Pepper plants harboring L resistance alleles showed tolerance toward manifestations of tomato brown rugose fruit virus disease. Plants 11:2378. https://doi.org/10.3390/plants11182378
EPPO (2019) Update of the situation of tomato brown rugose fruit virus in Mexico. EPPO Rep. Serv. 2019/192, European and Mediterranean Plant Protection Organization, Paris. https://gd.eppo.int/reporting/article-6622
FAOSTAT (2023) FAO statistical database. Available at: https://www.fao.org/faostat/en/#data/QCL (Accessed 11 Sept 2023).
Fidan H, Sarikaya P, Yildiz K, Topkaya B, Erkis G, Calis O (2021) Robust molecular detection of the new tomato brown rugose fruit virus in infected tomato and pepper plants from Turkey. J Integr Agric 20:2170–2179. https://doi.org/10.1016/S2095-3119(20)63335-4
Klap C, Luria N, Smith E, Bakelman E, Belausov E, Laskar O, Lachman O, Gal-On A, Dombrovsky A (2020) The potential risk of plant-virus disease initiation by infected tomatoes. Plants 9:623. https://doi.org/10.3390/plants9050623
Kubota K, Takeyama S, Ishibashi K, Matsushita Y, Tomitaka Y, Matsuyama M, Shinosaka H, Osaki K (2023a) Host range and pathogenicity of tomato brown rugose fruit virus (in Japanese with English abstract). Jpn J Phytopathol 89:225–234
Kubota K, Takeyama S, Matsushita Y, Tomitaka Y, Matsuyama M, Ishibashi K, Shinosaka H, Osaki K (2023b) Evaluation of control measures against tomato brown rugose fruit virus: disinfestation of equipment and seeds and use of attenuated strain of tomato mosaic virus (in Japanese with English abstract). Jpn J Phytopathol 89:235–244
Lee WS, Fu SF, Li Z, Murphy AM, Dobson EA, Garland L, Chaluvadi SR, Lewsey MG, Nelson RS, Carr JP (2016) Salicylic acid treatment and expression of an RNA-dependent RNA polymerase 1 transgene inhibit lethal symptoms and meristem invasion during tobacco mosaic virus infection in Nicotiana benthamiana. BMC Plant Biol 16:15. https://doi.org/10.1186/s12870-016-0705-8
Liu HW, Luo LX, Li JQ, Liu PF, Chen XY, Hao JJ (2014) Pollen and seed transmission of Cucumber green mottle mosaic virus in cucumber. Plant Pathol 63:72–77. https://doi.org/10.1111/ppa.12065
Luria N, Smith E, Reingold V, Bekelman I, Lapidot M, Levin I, Elad N, Tam Y, Sela N, Abu-Ras A, Erza N, Haberman A, Yitzhak L, Lachman O, Dombrovsky A (2017) A new Israeli Tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PLoS ONE 12:e0170429. https://doi.org/10.1371/journal.pone.0170429
Matsushita Y, Tsuda S (2014) Distribution of potato spindle tuber viroid in reproductive organs of petunia during its developmental stages. Phytopathology 104:964–969. https://doi.org/10.1094/PHYTO-10-13-0294-R
Matsushita Y, Usugi T, Tsuda S (2011) Distribution of tomato chlorotic dwarf viroid in floral organs of tomato. Eur J Plant Pathol 130:441–447. https://doi.org/10.1007/s10658-011-9766-6
Panno S, Ruiz-Ruiz S, Caruso AG, Alfaro-Fernandez A, San Ambrosio MIF, Davino S (2019) Real-time reverse transcription polymerase chain reaction development for rapid detection of tomato brown rugose fruit virus and comparison with other techniques. Peer J 7:e7928. https://doi.org/10.7717/peerj.7928
Panno S, Caruso AG, Blanco G, Davino S (2020) First report of tomato brown rugose fruit virus infecting sweet pepper in Italy. New Dis Rep 41:20. https://doi.org/10.5197/j.2044-0588.2020.041.020
Panno S, Davino S, Caruso AG, Bertacca S, Crnogorac A, Mandić A, Noris E, Matić S (2021) A review of the most common and economically important diseases that undermine the cultivation of tomato crop in the Mediterranean Basin. Agronomy 11:2188. https://doi.org/10.3390/agronomy11112188
Qu F, Ye X, Hou G, Sato S, Clemente TE, Morris TJ (2005) RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J Virol 79:15209–15217. https://doi.org/10.1128/JVI.79.24.15209-15217.2005
Reingold V, Lachman O, Blaosov E, Dombrovsky A (2015) Seed disinfection treatments do not sufficiently eliminate the infectivity of Cucumber green mottle mosaic virus (CGMMV) on cucurbit seeds. Plant Pathol 64:245–255. https://doi.org/10.1111/ppa.12260
Sainte-Marie G (1962) A paraffin embedding technique for studies employing immunofluorescence. J Histochem Cytochem 10:250–256
Salem N, Mansour A, Ciuffo M, Falk BW, Turina M (2016) A new tobamovirus infecting tomato crops in Jourdan. Arch Virol 161:503–506
Salem NM, Cao MJ, Odeh S, Turina M, Tahzima R (2020) First report of tobacco mild green mosaic virus and tomato brown rugose fruit virus infecting Capsicum annuum in Jordan. Plant Dis 104:601. https://doi.org/10.1094/PDIS-06-19-1189-PDN
Salem NM, Abumuslem M, Turina M, Samarah N, Sulaiman A, Abu-Irmaileh B, Ata Y (2022a) New weed hosts for tomato brown rugose fruit virus in wild Mediterranean vegetation. Plants 11:2287. https://doi.org/10.3390/plants11172287
Salem NM, Sulaiman A, Samarah N, Turina M, Vallino M (2022b) Localization and mechanical transmission of tomato brown rugose fruit virus in tomato seeds. Plant Dis 106:275–281. https://doi.org/10.1094/PDIS-11-20-2413-RE
Salem NM, Jewehan A, Aranda MA, Fox A (2023) Tomato brown rugose fruit virus pandemic. Annu Rev Phytopathol 61:14.1–14.18. https://doi.org/10.1146/annurev-phyto-021622-120703
Samarah N, Sulaiman A, Salem NM, Turina M (2021) Disinfection treatments eliminated tomato brown rugose fruit virus in tomato seeds. Eur J Plant Pathol 159:153–162. https://doi.org/10.1007/s10658-020-02151-1
Sastry KS (2013) Seed-borne plant virus diseases. Springer, Berlin
Smith E, Dombrovsky A (2019) Aspects in Tobamovirus management in intensive agriculture. In: Topolovec-Pintaric S (ed) Plant diseases: current threats and management trends. IntechOpen, London, UK, pp 31–47. https://doi.org/10.5772/intechopen.87101
Suehiro N, Matsuda K, Okuda S, Natsuaki T (2005) A simplified method for obtaining plant viral RNA for RT-PCR. J Virol Methods 125:67–73. https://doi.org/10.1016/j.jviromet.2005.01.002
Taylor RH, Grogan RG, Kimble KA (1961) Transmission of tobacco mosaic virus in tomato seed. Phytopathology 51:837–842
Tóbiás I, Rast ATB, Maat DZ (1982) Tobamoviruses of pepper, eggplant and tobacco: comparative host reactions and serological relationships. Neth J Pl Path 88:257–268
Yan Z, Zhao M, Ma H, Liu L, Yang G, Geng C, Tian Y, Li X (2021) Biological and molecular characterization of tomato brown rugose fruit virus and development of quadruplex RT-PCR detection. J Integr Agric 20:1871–1879. https://doi.org/10.1016/S2095-3119(20)63275-0
Zhang S, Griffiths JS, Marchand G, Bernards MA, Wang A (2022) Tomato brown rugose fruit virus: an emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide. Mol Plant Pathol 23:1262–1277. https://doi.org/10.1111/mpp.13229
Acknowledgements
The authors thank Y. Narita, K. Nakata, and Y. Matsumura for preparing the experimental materials and T. Sakurai for statistical analysis. This work was supported by Regulatory research projects for food safety, animal health and plant protection (JP J008617. 20320466) funded by the Ministry of Agriculture, Forestry and Fisheries of Japan.
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Ministry of Agriculture, Forestry and Fisheries of Japan, JP J008617. 20320466, Kenji Kubota.
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Matsushita, Y., Takeyama, S., Tomitaka, Y. et al. Elucidating the nature of seed-borne transmission of tomato brown rugose fruit virus in tomato, bell pepper, and eggplant. J Gen Plant Pathol 90, 23–34 (2024). https://doi.org/10.1007/s10327-023-01159-9
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DOI: https://doi.org/10.1007/s10327-023-01159-9