Transmission of Tomato chlorotic dwarf viroid by bumblebees (Bombus ignitus) in tomato plants

  • Shohei MatsuuraEmail author
  • Yosuke Matsushita
  • Reiko Kozuka
  • Sachiko Shimizu
  • Shinya Tsuda
Short Communications


Quantitative PCR revealed that Tomato chlorotic dwarf viroid (TCDVd) was present in substantial amounts in viroid-infected tomato flowers. Healthy tomato plants were arranged in two different glasshouses, and plants were mechanically inoculated with TCDVd. Bumblebees (Bombus ignitus) were then introduced into the glasshouses to reveal whether the viroid was transmitted from infected source plants to neighbouring healthy plants. TCDVd infection was found in neighbouring tomato plants more than 1 month after the introduction of the bees, some of which expressed symptoms, in both glasshouses. Thus, bumblebees transmitted TCDVd from tomato to tomato by pollination activities.


Anther Pollination Potato spindle tuber viroid Quantitative PCR Rutgers 



We are grateful to Dr. Taeko Takeuchi of Chiba Prefectural Agriculture and Forestry Research Centre, Japan for her advice. This work was supported in part by Research Project (No. 1976) for the Utilisation of Advanced Technologies in Agriculture, Forestry and Fisheries, of the Ministry of Agriculture, Forestry and Fisheries of Japan.


  1. Antignus, Y., Lachman, O., Pearlsman, M., Gofman, R., & Bar-Joseph, M. (2002). A new disease of greenhouse tomatoes in Israel caused by a distinct strain of Tomato apical stunt viroid (TASVd). Phytoparasitica, 30, 502–510.CrossRefGoogle Scholar
  2. Antignus, Y., Lachman, O., & Pearlsman, M. (2007). Spread of Tomato apical stunt viroid (TASVd) in greenhouse tomato crops is associated with seed transmission and bumble bee activity. Plant Disease, 91, 47–50.CrossRefGoogle Scholar
  3. Behjatnia, S. A. A., Dry, I. B., Krake, L. R., Conde, B. D., Connelly, M. I., Randles, J. W., et al. (1996). New Potato spindle tuber viroid and Tomato leaf curl geminivirus strains from a wild Solanum sp. Phytopathology, 86, 880–886.CrossRefGoogle Scholar
  4. Diener, T. O. (2001). The viroid: biological oddity or evolutionary fossil? Advances in Virus Research, 57, 137–184.CrossRefPubMedGoogle Scholar
  5. Galindo, J., Smith, D. R., & Diener, T. O. (1982). Etiology of planta macho, a viroid disease of tomato. Phytopathology, 72, 49–54.CrossRefGoogle Scholar
  6. James, T., Mulholland, V., Jeffries, C., & Chard, J. (2008). First report of Tomato chlorotic dwarf viroid infecting commercial petunia stocks in the United Kingdom. Plant Pathology, 57, 400.CrossRefGoogle Scholar
  7. Kryczyński, S., Paduch-Cichal, E., & Skrzeczkowski, L. J. (1988). Transmission of three viroids through seed and pollen of tomato plants. Journal of Phytopathology, 121, 51–57.CrossRefGoogle Scholar
  8. Matsushita, Y., Kanda, A., Usugi, T., & Tsuda, S. (2008). First report of a Tomato chlorotic dwarf viroid disease on tomato plants in Japan. Journal of General Plant Pathology, 74, 182–184.CrossRefGoogle Scholar
  9. Matsushita, Y., Usugi, T., & Tsuda, S. (2009). Host range and properties of Tomato chlorotic dwarf viroid. European Journal of Plant Pathology, 124, 349–352.CrossRefGoogle Scholar
  10. Mumford, R. A., Jarvis, B., & Skelton, A. (2004). The first report of Potato spindle tuber viroid (PSTVd) in commercial tomatoes in the UK. Plant Pathology, 53, 242.CrossRefGoogle Scholar
  11. Okada, K., Kusakari, S., Kawaratani, M., Neguro, J., Ohki, S. T., & Osaki, T. (2000). Tobacco mosaic virus is transmissible from tomato to tomato by pollinating bumblebees. Journal of General Plant Pathology, 66, 71–74.CrossRefGoogle Scholar
  12. Shipp, J. L., Buitenhuis, R., Stobbs, L., Wang, K., Kim, W. S., & Ferguson, G. (2008). Vectoring of Pepino mosaic virus by bumble-bees in tomato greenhouses. Annals of Applied Biology, 153, 149–155.Google Scholar
  13. Singh, R. P., Nie, X., & Singh, M. (1999). Tomato chlorotic dwarf viroid: an evolutionary link in the origin of pospiviroids. Journal of General Virology, 80, 2823–2828.PubMedGoogle Scholar
  14. Singh, R. P. (2006). Reassessment of the presence of viroid species of the genus Pospiviroid in infected floral parts, using reverse transcription-polymerase chain reaction and infectivity assays. Canadian Journal of Plant Pathology, 28, 242–249.Google Scholar
  15. Singh, R. P., & Dilworth, A. D. (2009). Tomato chlorotic dwarf viroid in the ornamental plant Vinca minor and its transmission through tomato seed. European Journal of Plant Pathology, 123, 111–116.CrossRefGoogle Scholar
  16. Velthuis, H. H. W., & van Doorn, A. (2006). A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37, 421–451.CrossRefGoogle Scholar
  17. Verhoeven, J. Th J., Jansen, C. C. C., Willemen, T. M., Kox, L. F. F., Owens, R. A., & Roenhorst, J. W. (2004). Natural infections of tomato by Citrus exocortis viroid, Columnea latent viroid, Potato spindle tuber viroid and Tomato chlorotic dwarf viroid. European Journal of Plant Pathology, 110, 823–831.CrossRefGoogle Scholar

Copyright information

© KNPV 2009

Authors and Affiliations

  • Shohei Matsuura
    • 1
    Email author
  • Yosuke Matsushita
    • 2
  • Reiko Kozuka
    • 3
  • Sachiko Shimizu
    • 1
  • Shinya Tsuda
    • 4
  1. 1.Hiroshima Prefectural Technology Research Institute, Agriculture Research CentreHigashihiroshimaJapan
  2. 2.National Institute of Floricultural ScienceTsukubaJapan
  3. 3.Chiba Prefectural Agriculture and Forestry Research CentreChiba-shiJapan
  4. 4.National Agricultural Research CentreTsukubaJapan

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