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Features of the relationship between Tomato severe rugose begomovirus and Bemisa tabaci MEAM1 reveal that the virus is acquired during a probe lasting only one minute

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Abstract

Tomato severe rugose virus (ToSRV) is a begomovirus found only in Brazil and has been the prevalent species affecting tomato crops in southwest and midwest of the country. Although the virus is known to be transmitted by Bemisia tabaci MEAM1, this study was undertaken to better characterize the relationship between ToSRV and whiteflies on tomato plants. The minimum acquisition and inoculation access periods, latent period, and virus retention time in the vector were determined. The results of transmission experiments showed that the minimum acquisition and inoculation access periods (AAP and IAP) for transmission of ToSRV by MEAM1 were 1 min and 5 min, respectively. After monitoring 50 individual adult whiteflies during a one-minute AAP on ToSRV-infected tomato leaves, 21 insects (42%) were able to acquire the virus, as confirmed by PCR. In contrast, one hundred insects that were individually allowed one-minute AAP on Tomato chlorosis virus (ToCV)-infected tomato leaves, which is a phloem-limited crinivirus, were unable to acquire the virus. The latent period of ToSRV in MEAM1 was 12–15 h, with adult whiteflies retaining the virus for 25 days. Although the tissue distribution of ToSRV in tomato has not been determined, the short AAP suggests that the virus may be present in mesophyll cells, from where it may be acquired during a one-minute feeding probe.

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References

  • Alves-Júnior, M., Alfenas-Zerbini, P., Andrade, E. C., Esposito, D. A., Silva, F. N., Cruz, A. C. F., Ventrella, M. C., Otoni, W. C., & Zerbini, F. M. (2009). Synergism and negative interference during co-infection of tomato and Nicotiana benthamiana with two bipartite begomoviruses. Virology, 387, 257–266.

  • Barbosa, L. F., Yuki, V. A., Marubayashi, J. M., De Marchi, B. R., Perini, F. L., Pavan, M. A., Barros, D. R., Ghanim, M., Moriones, E., Navas-Castillo, J., & Krause-Sakate, R. (2015). First report of Bemisia tabaci Mediterranean (Q biotype) species in Brazil. Pest Management Science, 71, 501–504.

    Article  CAS  Google Scholar 

  • Brown, J. K., & Nelson, M. R. (1988). Transmission, host range, and virus-vector relationship of Chino del tomate virus, a whitefly-transmitted geminivirus from Sinaloa, Mexico. Plant Disease, 72, 866–869.

    Article  Google Scholar 

  • Caciagli, P., Bosco, D., & Al-Bitar, L. (1995). Relationship of the Sardinian isolate of Tomato yellow leaf curl geminivirus with its whitefly vector Bemisia tabaci Gen. European Journal of Plant Pathology, 101, 163–170.

    Article  Google Scholar 

  • Cohen, S., & Nitzany, F. E. (1966). Transmission and host range of Tomato yellow leaf curl virus. Phytopathology, 56, 1127–1131.

    Google Scholar 

  • Cohen, S., Duffus, J. E., Larsen, R. C., Liu, H., & Flock, R. A. (1983). Purification, serology and vector relationships of squash leaf curl virus, a whitefly-transmitted geminivirus. Phytopathology, 73, 1669–1673.

    Article  Google Scholar 

  • Costa, A. S., & Bennett, C. W. (1950). Whitefly-transmitted mosaic of Euphorbia prunifolia. Phytopathology, 40, 266–283.

    Google Scholar 

  • De Barro, P. J., Scott, K. D., Graham, G. C., Lange, C., & Schutze, M. K. (2003). Isolation and characterization of microsatellite loci in Bemisia tabaci. Molecular Ecology Notes, 3, 40–43.

    Article  Google Scholar 

  • Dovas, C. I., Katias, N. I., & Avgelis, A. D. (2002). Multiplex detection of criniviruses associated with epidemics of yellowing disease of tomato in Greece. Plant Disease, 86, 1345–1349.

    Article  Google Scholar 

  • Doyle, J. J., & Doyle, J. L. (1990). Isolation of DNA from fresh tissue. Focus, 12, 13–15.

    Google Scholar 

  • FAOSTAT - Food and Agriculture Organization of the United Unions (2017). Retrieved 29 June 2017, from http://www.fao.org/faostat/en/#home.

  • Fernandes, F. R., Albuquerque, L. C., & Inoue-Nagata, A. K. (2010). Development of a species-species detection method for three Brazilian tomato begomoviruses. Tropical Plant Pathology, 35, 43–47.

    Article  Google Scholar 

  • Firmino, A. C., Yuki, V. A., Moreira, A. G., & Rezende, J. A. M. (2009). Tomato yellow vein streak virus: Relationship with Bemisia tabaci biotype B and host range. Scientia Agricola, 66, 793–799.

    Article  Google Scholar 

  • Ghanim, M. (2014). A review of the mechanisms and components that determine the transmission efficiency of Tomato yellow leaf curl virus (Geminiviridae: Begomovirus) by its whitefly vector. Virus Research, 186, 47–54.

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez, C. (2000). DNA replication and cell cycle in plants: Learning from geminiviruses. The EMBO Journal, 19(5), 792–799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Idris, A. M., & Brown, J. K. (1998). Sinaloa tomato leaf curl virus geminivirus: Biological and molecular evidence for a new sub-group III virus. Phytopathology, 88, 648–657.

    Article  CAS  PubMed  Google Scholar 

  • Idris, A. M., Smith, S. E., & Brown, J. K. (2001). Ingestion, transmission, and persistence of Chino del tomate virus (CdTV), a new world begomovirus, by old and new world biotypes of the whitefly vector Bemisia tabaci. Annals of Applied Biology, 139, 145–154.

    Article  Google Scholar 

  • Inoue-Nagata, A. K., Carvalho, C. M., Zerbini, F. M., Rezende, J. A. M., Krause-Sakate, R., & Nagata, T. (2016a). Vírus transmitidos por moscas-brancas no Brasil: vetores, principais doenças e manejo. Revisão Anual de Patologia de Plantas, 24, 7–29.

    Google Scholar 

  • Inoue-Nagata, A. K., Lima, M. F., & Gilbertson, R. L. (2016b). A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: Current status and approaches for management. Horticultura Brasileira, 34, 8–18.

    Article  Google Scholar 

  • Kim, K. S., Shock, T. L., & Goodman, R. M. (1978). Infection of Phaseolus vulgaris by Bean golden mosaic virus: Ultrastructural aspects. Virology, 89, 22–33.

    Article  CAS  PubMed  Google Scholar 

  • Maluta, N. K. P., Garzo, E., Moreno, A., Navas-Castillo, J., Fiallo-Olivé, E., Lopes, J. R. S., & Fereres, A. (2017). Stylet penetration activities of the whitefly Bemisia tabaci associated with inoculation of the crinivirus Tomato chlorosis virus. Journal of General Virology, 98, 1515–1520.

    Article  CAS  Google Scholar 

  • Mansour, A., & Al-Musa, A. (1992). Tomato yellow leaf curl virus: Host range and virus vector relationship. Plant Pathology, 41, 122–125.

    Article  Google Scholar 

  • Medina, V., Rodrigo, G., Tian, T., Juarez, M., Dolja, V. V., Achon, M. A., & Falk, B. W. (2003). Comparative cytopathology of Crinivirus infections in different plant hosts. Annals of Applied Biology, 143, 99–110.

    Article  Google Scholar 

  • Mehta, P., Wyman, J. A., Nakhla, M. K., & Maxwell, D. P. (1994). Transmission of tomato yellow leaf curl geminivirus by Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology, 87, 1291–1297.

    Article  Google Scholar 

  • Morra, M. R., & Petty, I. T. D. (2000). Tissue specificity of gemininivirus infection is genetically determinated. The Plant Cell, 12, 2250–2270.

    Article  Google Scholar 

  • Nozaki, D.N. (2007). Molecular and biological analysis of begomovirus infecting pepper (Capsicum annuum) in São Paulo State. Ph.D. Thesis, FCA/UNESP, Botucatu, SP, Brazil.

  • Rojas, M. R., Gilbertson, R. L., Russel, D. R., & Maxwell, D. P. (1993). Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Disease, 77, 340–347.

    Article  CAS  Google Scholar 

  • Rushing, A. E., Sunter, G., Gardiner, W. E., Dute, R. R., & Bisaro, D. M. (1987). Ultrastructural aspects of Tomato golden mosaic virus infection in tobacco. Phytopathology, 77, 1231–1236.

    Article  Google Scholar 

  • Santos, C. D. G., Ávila, A. C., & Resende, R. O. (2003). Estudo da interação de um Begomovírus isolado de tomateiro com a mosca branca. Fitopatologia Brasileira, 28, 664–673.

    Article  Google Scholar 

  • Santos, C. D. G., Ávila, A. C., Inoue-Nagata, A. K., & Resende, R. O. (2004). Espécies vegetais hospedeiras de begomovírus isolados de tomateiro em Goiás e no Distrito Federal. Fitopatologia Brasileira, 29, 450–455.

    Article  Google Scholar 

  • Stenger, D. C., Duffus, J. E., & Villalon, B. (1990). Biological and genomic properties of a geminivirus isolated from pepper. Phytopathology, 80, 704–709.

    Article  CAS  Google Scholar 

  • Timmermans, M. C. P., Prem Das, O., & Messing, J. (1994). Geminiviruses and their uses as extrachromosomal replicons. Annual Review of Plant Physiology and Plant Molecular Biology, 45, 79–112.

    Article  CAS  Google Scholar 

  • Wisler, G. C., Li, R. H., Liu, H.-Y., Lowry, D. S., & Duffus, J. E. (1998). Tomato chlorosis virus: A new whitefly-transmitted, phloem-limited, bipartite closterovirus of tomato. Phytopathology, 88, 402–409.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by Fundação de Amparo à Pesquisa no Estado de São Paulo (FAPESP), Project No. 2012/51771-4.

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Authors and Affiliations

  1. Department of Plant Pathology and Nematology, University of São Paulo, PO Box 09, Piracicaba, São Paulo, 13418-900, Brazil

    Rodrigo Solci Toloy, Tatiana Mituti, Talita Nicola Zocca Silva & Jorge Alberto Marques Rezende

  2. DuPont Pioneer, PO Box 3020, Palmas, 77500-000, Tocantins, Brazil

    Rodrigo Solci Toloy

  3. EMBRAPA Semiárido, PO Box 23, Petrolina, Pernambuco, 56302-970, Brazil

    Debora Maria Sansini Freitas

  4. Department of Entomology and Acarology, University of São Paulo, PO Box 09, Piracicaba, São Paulo, 13418-900, Brazil

    Nathalie Kristine Prado Maluta & João Roberto Spotti Lopes

  5. Instituto de Ciencias Agrarias, CSIC, 28006, Madrid, Spain

    Alberto Fereres

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  1. Rodrigo Solci Toloy
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  2. Tatiana Mituti
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  3. Debora Maria Sansini Freitas
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  4. Nathalie Kristine Prado Maluta
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  5. Talita Nicola Zocca Silva
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  6. João Roberto Spotti Lopes
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  7. Alberto Fereres
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  8. Jorge Alberto Marques Rezende
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Correspondence to Jorge Alberto Marques Rezende.

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Toloy, R.S., Mituti, T., Freitas, D.M.S. et al. Features of the relationship between Tomato severe rugose begomovirus and Bemisa tabaci MEAM1 reveal that the virus is acquired during a probe lasting only one minute. Eur J Plant Pathol 151, 541–547 (2018). https://doi.org/10.1007/s10658-017-1388-1

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