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Occurrence and characterization of tomato spotted wilt orthotospovirus isolated from cucumber

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Abstract

Diseases associated with tomato spotted wilt orthotospovirus (TSWV) are a serious threat to vegetable production worldwide. In 2019, leaf necrosis disease was observed on cucumber plants in Fukushima Prefecture, Japan. TSWV infection was identified in the diseased plants by immunostripe tests and RT-PCR analysis. Sequencing of the complete genome of this TSWV strain showed the highest identity with previously characterized TSWV isolates, and we therefore designated the cucumber-infecting variant as TSWV-Fukushima:cucumber 2019 (TS-FC19). Phylogenetic analyses based on the intergenic regions revealed that TS-FC19 and other TSWV isolates collected from the same area clustered in a distinct clade. Cucumber plants inoculated with TS-FC19 produced leaf necrosis symptoms, whereas other TSWV strains did not induce severe symptoms in this host. Together, our findings indicate that the cucumber leaf necrosis disease in Fukushima Prefecture is caused by a new strain of TSWV that appears to have evolved locally. This is the first detailed report on the biological characteristics of a cucumber-infecting TSWV.

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References

  • Abadkhah, M., Koolivand, D., & Eini, O. (2018). A new distinct clade for Iranian tomato spotted wilt virus isolates based on the polymerase, nucleocapsid, and non-structural genes. Plant Pathology Journal, 34, 514–531.

    Article  CAS  PubMed Central  Google Scholar 

  • Bezerra, I. C., Resende, R. D., Pozzer, L., Nagata, T., Kormelink, R., & de Avila, A. C. (1999). Increase of tospoviral diversity in Brazil with the identification of two new tospovirus species, one from chrysanthemum and one from zucchini. Phytopathology, 89, 823–830.

    Article  CAS  Google Scholar 

  • Butković, A., González, R., & Elena, S. F. (2021). Revisiting Orthotospovirus phylogeny using full-genome data and testing the contribution of selection, recombination and segment reassortment in the origin of members of new species. Archives of Virology, 166, 491–499.

    Article  Google Scholar 

  • Ciuffo, M., Kurowski, C., Vivoda, E., Copes, B., Masenga, V., Falk, B. W., & Turia, M. (2009). A new tospovirus sp in cucurbit crops in Mexico. Plant Disease, 93, 467–474.

    Article  CAS  Google Scholar 

  • de Haan, P., Wagemakers, L., Peters, D., & Goldbach, R. (1990). The S RNA segment of tomato spotted wilt virus has an ambisense character. Journal of General Virology, 71, 1001–1008.

    Article  Google Scholar 

  • de Haan, P., Kormelink, R., Resende, D., van Poelwijk, F., Peters, D., & Goldbach, R. (1991). Tomato spotted wilt virus L RNA encodes a putative RNA polymerase. Journal of General Virology, 72, 2207–2216.

    Article  Google Scholar 

  • Feng, M., Cheng, R., Chen, M., Guo, R., Li, L., Feng, Z., Wu, J., Xie, L., Hong, J., Zhang, Z., Kormelink, R., & Tao, X. (2020). Rescue of tomato spotted wilt virus entirely from complementary DNA clones. Proceedings of the National Academy of Sciences of the United States of America, 117, 1181–1190.

    Article  CAS  Google Scholar 

  • Fuji, S., Mochizuki, T., Okuda, M., Tsuda, S., Kagiwada, S., Sekine, K.-T., Ugaki, M., Natsuaki, K. T., Isogai, M., Maoka, T., Takeshita, M., Yoshikawa, N., Mise, K., Sasaya, T., Kondo, H., Kubota, K., Yamaji, Y., Iwanami, T., Ohshima, K., et al. (2022). Plant viruses and viroids in Japan. Journal of General Plant Pathology, 88, 105–127.

    Article  CAS  Google Scholar 

  • Hanada, K., Tsuda, S., Kameya-Iwaki, M., & Tochhara, H. (1993). Distinct properties of nucleocapsid of a watermelon isolate of tomato spotted wilt virus. Annals of the Phytopathological Society of Japan, 59, 500–506.

    Article  CAS  Google Scholar 

  • Hedil, M., & Kormelink, R. (2016). Viral RNA silencing suppression: The enigma of bunyavirus NSs proteins. Viruses, 8, 208.

    Article  PubMed Central  Google Scholar 

  • Heinze, C., Letschert, B., Hristova, D., Yankulova, M., Willingmann, P., Karadjova, O., Atanassov, A., & Adam, G. (2001). Variability of the N-protein and the intergenic region of the S-RNA of tomato spotted wilt tospovirus (TSWV). New Microbiologica, 24, 175–187.

    CAS  PubMed  Google Scholar 

  • Inoue, T., & Inoue, N. (1972). Tomato spotted wilt virus occurred in Dahlia plant. Nogaku-kennkyu, 54, 74–90.

    Google Scholar 

  • Karavina, C. & Gubba, A. (2017). Detection and characterization of Tomato spotted wilt virus infecting field and greenhouse-grown crops in Zimbabwe. European Journal of Plant Pathology, 49, 933–944.

  • Kato, K., & Hanada, K. (2000). A necrotic disease of chrysanthemum (Chrysanthemum morifolium Ramat) caused by tomato spotted wilt virus (TSWV) in Japan. Kyushu Plant Protection Research, 46, 61–65.

    Article  Google Scholar 

  • Kato, K., Hanada, K., & Kameya-Iwaki, M. (2000). Melon yellow spot virus: A distinct species of the genus Tospovirus isolated from melon. Phytopathology, 90, 422–426.

    Article  CAS  Google Scholar 

  • Kobatake, H., Osaki, T., Yoshioka, A., & Inoue, T. (1976). Spotted wilt disease of tomatoes in Japan. Annals of the Phytopathological Society of Japan, 42, 287–294.

    Article  Google Scholar 

  • Kormelink, R., de Haan, P., Meurs, C., Peters, D., & Goldbach, R. (1992). The nucleotide sequence of the M RNA segment of tomato spotted wilt virus, a bunyavirus with two ambisense RNA segments. Journal of General Virology, 73, 2795–2804.

    Article  CAS  Google Scholar 

  • Kormelink, R., Storms, M., van Lent, J., Peters, D., & Goldbach, R. (1994). Expression and subcellular location of the NSm protein of tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology, 200, 56–65.

    Article  CAS  Google Scholar 

  • Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33, 1870–1874.

  • Margaria, P., Bosco, L., Vallino, M., Ciuffo, M., Mautino, G. C., Tavella, L., & Turina, M. (2014a). The NSs protein of tomato spotted wilt virus is required for persistent infection and transmission by Franklinella occidentalis. Journal of Virology, 88, 5788–5802.

    Article  CAS  PubMed Central  Google Scholar 

  • Margaria, P., Miozzi, L., Ciuffo, M., Pappu, H., & Turina, M. (2014b). The complete genome sequence of polygonum ring spot virus. Archives of Virology, 159, 3149–3152.

    Article  CAS  Google Scholar 

  • Margaria, P., Ciuffo, M., Rosa, C., & Turina, M. (2015). Evidence of a tomato spotted wilt virus resistance-breaking strain originated through natural reassortment between two evolutionary-distinct isolates. Virus Research, 196, 157–161.

    Article  CAS  Google Scholar 

  • Massumi, H., Samei, A., Hosseini Pour, A., Shaabanian, M., & Rahimian, H. (2007). Occurrence, distribution, and relative incidence of seven viruses infecting greenhouse-grown cucurbits in Iran. Plant Disease, 91, 159–163.

    Article  Google Scholar 

  • Okuda, M. (2016). Tospoviruses occurring in and outside Japan. Japanese Journal of Phytopathology, 82, 169–184.

    Article  Google Scholar 

  • Okuda, M., Takeuchi, S., Taba, S., Kato, K., & Hanada, K. (2002). Melon yellow spot virus and watermelon silver mottle virus: Outbreak of cucurbit infecting tospovirus in Japan. Acta Horticulturae, 588, 143–148.

    Article  CAS  Google Scholar 

  • Oliver, J. E., & Whitfield, A. E. (2016). The genus Tospovirus: Emerging bunyaviruses that threaten food security. Annual Review of Virology, 3, 101–124.

    Article  CAS  Google Scholar 

  • Rotenberg, D., Jacobson, A. L., Schneweis, D. J., & Whitfield, A. E. (2015). Thrips transmission of tospoviruses. Current Opinion in Virology, 15, 80–89.

    Article  Google Scholar 

  • Shimada, R., Okuda, M., & Uekusa, H. (2019). Characteristics of watermelon silver mottle virus (WSMoV) found in Kanagawa prefecture and reproduction of symptoms on cucumber caused by WSMoV. Japanese Journal of Phytopathology, 85, 108–111.

    Article  CAS  Google Scholar 

  • Soellick, T. R., Uhrig, J. F., Bucher, G. L., Kellmann, J. W., & Schreier, P. H. (2000). The movement protein NSm of tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. Proceedings of the National Academy of Sciences of the United States of America, 97, 2373–2378.

    Article  CAS  PubMed Central  Google Scholar 

  • Takeda, A., Sugiyama, K., Nagano, H., Mori, M., Kaido, M., Mise, K., Tsuda, S., & Okuno, T. (2002). Identification of a novel RNA silencing suppressor, NSs protein of tomato spotted wilt virus. FEBS Letters, 532, 75–79.

    Article  CAS  Google Scholar 

  • Turina, M., Kormelink, R., & Resende, R. O. (2016). Resistance to tospovirusus in vegetable crops: Epidemiological and molecular aspects. Annual Review of Phytopathology, 54, 347–371.

    Article  CAS  Google Scholar 

  • van Knippenberg, I., Goldbach, R., & Kormelink, R. (2005). Tomato spotted wilt virus S-segment mRNAs have overlapping 3′-ends containing a predicted stem-loop structure and conserved sequence motif. Virus Research, 110, 125–131.

    Article  Google Scholar 

  • Whitfield, A. E., Ullman, D. E., & German, T. L. (2004). Expression and characterization of a soluble form of tomato spotted wilt virus glycoprotein GN. Journal of Virology, 78, 13197–13206.

    Article  CAS  PubMed Central  Google Scholar 

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Acknowledgments

We thank the NARO Genebank for providing the TSWV-P2 strain.

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Correspondence to Shin-ichi Fuji.

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This article does not contain any studies with human participants or animals.

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The authors declare that there is no conflict of interest.

Additional information

The GenBank/EMBL/DDBJ accession number for the sequence reported in this paper is LC652640, LC652641, and LC652642 (TS-FC19).

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Kon, T., Watanabe, N., Ootake, H. et al. Occurrence and characterization of tomato spotted wilt orthotospovirus isolated from cucumber. Eur J Plant Pathol 163, 789–797 (2022). https://doi.org/10.1007/s10658-022-02515-9

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