SpringerLink
Log in

Detection of Tomato yellow leaf curl Thailand virus transmitted by Bemisia tabaci Asia I in tomato and pepper

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

Tomato yellow leaf curl Thailand virus (TYLCTHV) has caused serious yield loss of tomato in Thailand for more than three decades. Control of the virus is essential for successful integrated disease management (IDM) strategies. This study investigated the capability of whitefly (Bemisia tabaci) to transmit TYLCTHV on two host plants—tomato and pepper—and sought to detect the presence of viral DNA in the plants and whiteflies after two transmissions. The new TYLCTHV isolate used in this study (SPN-Tom1A) was 2756 nts long with typical characteristics of TYLCTHV DNA-A. Viral DNA-A (WF-SPN Tom2015) also was detected in viruliferous whiteflies; nucleotide sequence revealed 99% identity to TYLCTHV SPN-Tom1A sequence. In duplicated transmission test, vector B. tabaci Asia I was highly efficient in transmitting TYLCTHV from tomato to tomato by 90–100%, followed by the transmission from tomato to pepper by 55–90%. In contrast, the transmission rate of TYLCTHV pepper to tomato seedlings was nil. Tomato plants showed upward cup** and yellow leaves typical of TYLCTHV infection only when TYLCTHV was transmitted from tomato to tomato, but when transmitted to pepper, the infected peppers were symptomless. Bodies of viruliferous whiteflies fed on tomato and pepper were confirmed by PCR for the presence of TYLCTHV at 58.89–80% and 60–89.45%, respectively. Our results thus provide evidence that pepper infected with TYLCTHV is not a source plant for TYLCTHV transmission to tomato.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anokhe, A. (2015). Characterization of virus transmission in Asia I and Asia II-1 populations of whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). M.S. thesis, Indian Agricultural Research Institute at New Delhi, India.

  • Attathom, S., Chiemsombat, P., Sutabutra, T., & Pongpanitanond, R. (1990). Characterization of nucleic acid of Tomato yellow leaf curl virus. Kasetsart Journal: Natural Science. Supplement, 24(5), 1–5.

    Google Scholar 

  • Attathom, S., Chiemsombat, P., Kositratana, W., & Sae-Ung, N. (1994). Complete nucleotide sequence and genome analysis of bipartite Tomato yellow leaf curl virus in Thailand. Kasetsart Journal: Natural Science, 28, 632–639.

    CAS  Google Scholar 

  • Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G., & Thompson, J. D. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research, 31(13), 3497–3500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiemsombat, P., & Srikamphung, B. (2015). Genetic variation of Begomoviruses infecting tomato and pepper in Thailand and whitefly transmissibility, pp.109–118. The 12 th National Plant Protection Conference: Pragmatic Crop Protection for Food safety and sustainable Thai economy. 20–22 October 2015, Weed science society of Thailand. Chiang Rai, Thailand.

  • Chiemsombat, P., Srikamphung, B., & Yule, S. (2018). Begomoviruses associated to pepper yellow leaf curl disease in Thailand. Journal of Agricultural Research, 3(7), 000183.

    Google Scholar 

  • Chomdej, O., Whankaew, S., Chatchawankanpanich, O., Kositratana, W., & Chunwongse, J. (2008). Resistance to tomato yellow leaf curl Thailand virus, TYLCTHV-[2] from Solanum habrochaites accession 'L06112' in F1 and BC1F1 generations. Songklanakarin Journal of Science and Technology, 30, 441–446.

    Google Scholar 

  • Chomdej, O., Pongpayaklers, U., & Chunwongse, J. (2012). Resistance to tomato yellow leaf curl virus-Thailand isolate (TYLCTHV-[2]) and markers loci association in BC2F1 population from a cross between Seedathip 3 and a wild tomato, Solanum habrochaites' L06112'clone no. 1. Songklanakarin Journal of Science & Technology, 34, 31–36.

    CAS  Google Scholar 

  • Dader, B., Then, C., Berthelot, E., Ducousso, M., Ng, J. C. K., & Drucker, M. (2017). Insect transmission of plant viruses: Multilayered interactions optimize viral propagation. Insect Sci., 24, 929–946. https://doi.org/10.1111/1744-7917.12470.

    Article  PubMed  Google Scholar 

  • De Barro, P., Liu, S.-S., Boykin, L. M., & Dinsdale, A. B. (2011). Bemisia tabaci: A statement of species status. Annual Reviewof Entomology, 56, 1–19.

    Article  CAS  Google Scholar 

  • Dellaporta, S. L., Wood, J., & Hicks, J. B. (1983). A plant DNA mini preparation: Version II. Plant Molecular Biology Reporter, 1, 19–21.

    Article  CAS  Google Scholar 

  • Dinsdale, A., Cook, L., Riginos, C., Buckley, Y. M., & De Barro, P. (2010). Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America, 103(2), 196–208.

    Article  Google Scholar 

  • Fang, Y., Jiao, X., **e, W., Wang, S., Wu, Q., Shi, X., Chen, G., Su, Q., Yang, X., Pan, H., & Zhang, Y. (2013). Tomato yellow leaf curl virus alters the host preferences of its vector Bemisia tabaci. Scientific Reports, 3. https://doi.org/10.1038/srep02876.

  • Fanigliulo, A., Pacella, R., Comes, S., & Crescenzi, A. (2008). First record of Tomato yellow leaf curl Sardinia virus (TYLCSV) on pepper in Italy. Communications in Agricultural and Applied Biological Sciences, 73(2), 297–302.

    CAS  PubMed  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 

  • Ghanim, M., Sobol, I., Ghanim, M., & Czosnek, H. (2007). Horizontal transmission of begomoviruses between Bemisia tabaci. Arthropod-Plant Interactions, 1, 195–204.

    Article  Google Scholar 

  • Götz, M., & Winter, S. (2016). Diversity of Bemisia tabaci in Thailand and Vietnam and indications of species replacement. Journal of Asia-Pacific Entomology, 19, 537–543.

    Article  Google Scholar 

  • Green, S. K., Tsai, W. S., Shih, S. L., Rezaian, A., & Duangsong, U. (2003). Molecular characterization of a new begomovirus associated with tomato yellow leaf curl and eggplant yellow mosaic diseases in Thailand. Plant Disease, 87(4), 446.

    Article  CAS  PubMed  Google Scholar 

  • Hanssen, I. M., Lapidot, M., & Thomma, B. P. H. J. (2010). Emerging viral diseases of tomato crops. Molecular plant-microbe interaction, 23(5), 539–548.

    Article  CAS  Google Scholar 

  • Iida, H., Kitamura, T., & Honda, K.-I. (2009). Comparison of egg-hatching rate, survival rate and development time of the immature stage between B- and Q-biotypes of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on various agricultural crops. Applied Entomology and Zoology, 44(2), 267–273.

    Article  Google Scholar 

  • Ito, T., Sharma, P., Kittipakorn, K., & Ikegami, M. (2008). Complete nucleotide sequence of a new isolate of tomato leaf curl New Delhi virus infecting cucumber, bottle gourd and muskmelon in Thailand. Archives of Virology, 153(3), 611–613.

    Article  CAS  PubMed  Google Scholar 

  • Jiao, X., **e, W., Wang, S., Wu, Q., Zhou, L., Pan, H., Liu, B., & Zhang, Y. (2012). Host preference and nymph performance of B and Q putative species of Bemisia tabaci on three host plants. Journal of Pest Science, 85, 423–430.

    Article  Google Scholar 

  • Kenyon, L., Tsai, W.-S., Shih, S.-L., & Lee, L.-M. (2014). Emergence and diversity of begomoviruses infecting solanaceous crops in east and Southeast Asia. Virus Research, 186, 104–113.

    Article  CAS  PubMed  Google Scholar 

  • Kil, E.-J., Byun, H.-S., Kim, S., Kim, J., Park, J., Cho, S., Yang, D.-C., Lee, K.-Y., Choi, H.-S., Kim, J.-K., & Lee, S. (2014). Sweet pepper confirmed as a reservoir host for tomato yellow leaf curl virus by both agro-inoculation and whitefly-mediated inoculation. Archives of Virology, 159, 2387–2395.

    Article  CAS  PubMed  Google Scholar 

  • Knierim, D., & Maiss, E. (2007). Application of Phi29 DNA polymerase in identification and full-length clone inoculation of Tomato yellow leaf curlThailand virus and Tobacco leaf curlThailand virus. Archives of Virology, 152, 941–954.

    Article  CAS  PubMed  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(7), 1870–1874.

    Article  CAS  PubMed  Google Scholar 

  • Lapjit, F. P. (2014). Problems and needs of Sida tomato production of growers in Nakhonratchasima province. Khon Kaen Agriculture Journal, 42(3), 894–898.

    Google Scholar 

  • Li, M., Hu, J., Xu, F.-C., & Liu, S.-S. (2010a). Transmission of Tomato Yellow Leaf Curl Virus by two invasive biotypes and a Chinese indigenous biotype of the whitefly Bemisia tabaci. International Journal of Pest Management, 56(3), 275–280.

    Article  CAS  Google Scholar 

  • Li, M., Liu, J., & Liu, S.-S. (2010b). Tomato yellow leaf curl virus infection of tomato does not affect the performance of the Q and ZHJ2 biotypes of the viral vector Bemisia tabaci. Insect Sci., 18(1), 40–49.

    Article  CAS  Google Scholar 

  • Morilla, G., Janssen, D., García-Andrés, S., Moriones, E., Cuadrado, I. M., & Bejarano, E. R. (2005). Pepper (Capsicum annuum) is a dead-end host for Tomato yellow leaf curl virus. Phytopathology, 95, 1089–1097.

    Article  CAS  PubMed  Google Scholar 

  • Nikhil, R. K., Chang, J.-C., Manikanda Boopathi, N., & Srinivasan, R. (2017). Phylogeographical structure in mitochondrial DNA of whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) in southern India and Southeast Asia. Mitochondrial DNA Part A, 28(5), 621–631.

    Article  CAS  Google Scholar 

  • Ning, W., Shi, X., Liu, B., Pan, H., Wei, W., Zeng, Y., Sun, X., **e, W., , Wang, S., Wu, Q., Cheng, J., Peng, Z., & Zhang, Y. (2015). Transmission of Tomato Yellow Leaf Curl Virus by Bemisia tabaci as affected by whitefly sex and biotype. Scientific Reports, 5, 10744.

    Article  PubMed  PubMed Central  Google Scholar 

  • OAE (2016). Office of Agriculture Economics. Tomato production in Thailand in 2013–2015. Vegetable product. http://www.oae.go.th/ewtadmin/ewt/oae_web/download/prcai/vegetable/tomato.pdf. Accessed 23 December 2016.

  • Palangphukhieo, W., Patchanida, N., & Petcharat, T. (2012). Situation of pepper and tomato diseases in seed production fields in northeast of Thailand and Parksong district, Lao’s PDR. Khon Kaen Agriculture Journal, 40 supplement, 522–531.

  • Polston, J. E., Cohen, L., Sherwood, T. A., Ben-Joseph, R., & Lapidot, M. (2006). Capsicum species: Symptomless hosts and reservoirs of tomato yellow leaf curl virus. Phytopathology, 96, 447–452.

    Article  CAS  PubMed  Google Scholar 

  • Rotbi, M., De Castro, A. P., Diez, M. J., & Elmtili, N. (2014). Identification and distribution of tomato yellow leaf curl virus TYLCV and tomato yellow leaf curl Sardinia virus TYLCSV infection vegetable crops in Morocco. African Journal of Biotechnology, 13(13), 1476–1483.

    Article  Google Scholar 

  • Salati, R., Shorey, M., Briggs, A., Calderon, J., Rojas, M. R., Chen, L. F., Gilbertson, R. L., & Palmieri, M. (2010). First report of Tomato yellow leaf curl virus infecting tomato, tomatillo, and peppers in Guatemala. Plant Disease, 94(4), 482.

    Article  CAS  PubMed  Google Scholar 

  • Samretwanich, K., Chiemsombat, P., Kittipakorn, K., & Ikegami, M. (2000a). Yellow leaf disease of cantaloupe and wax gourd from Thailand. Plant Disease, 84, 200.

    Article  CAS  PubMed  Google Scholar 

  • Samretwanich, K., Chiemsombat, P., Kittipakorn, K., & Ikegami, M. (2000b). Tomato leaf curl Geminivirus associated with cucumber yellow leaf disease in Thailand. Journal of Phytopathology, 148, 615–617.

    Google Scholar 

  • Sawangjit, S. (2009). The complte nucleotide sequence of Squash leaf curl China virus-[wax gourd] and its phylogenetic relationship to other geminiviruses. ScienceAsia, 35, 131–136.

    Article  CAS  Google Scholar 

  • Sawangjit, S., Chatchawankanphanich, O., Chiemsombat, P., Attathom, T., Dale, J., & Attathom, S. (2005). Molecular characterization of tomato infecting begomoviruses in Thailand. Virus Research, 109, 1–8.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, M., & Budha, P. B. (2015). Host preference vegetables of tobacco whitefly Bemisia tabaci (Gennadius, 1889) in Nepal. Journal of Institute of Science and Technology, 20(1), 133–137.

    Article  Google Scholar 

  • Shih, S. L., Tsai, W. S., Lee, L. M., Wang, J. T., Green, S. K., & Kenyon, L. (2010). First report of tomato yellow leaf curl Thailand virus associated with pepper leaf curl disease in Taiwan. Plant Disease, 94, 637.

    Article  CAS  PubMed  Google Scholar 

  • Shih, S.-L., Tsai, W.-S., Lee, L.-M., & Kenyon, L. (2013). Molecular characterization of Begomoviruses infecting Sauropus androgynus in Thailand. Journal of Phytopathology, 161(2), 78–85.

    Article  CAS  Google Scholar 

  • Simon, C., Frati, F., Beckenbach, A., Crespi, B., Lui, H., & Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction “primers”. Annals of the Entomological Society of America, 87, 651–701.

    Article  CAS  Google Scholar 

  • Sinisterra, X. H., McKenzie, C. L., Hunter, W. B., Powell, C. A., & Shatters, R. G. (2005). Differential transcriptional activity of plantpathogenic begomoviruses in their whitefly vector (Bemisia tabaci, Gennadius: Hemiptera Aleyrodidae). Journal of General Virology, 86, 1525–1532.

    Article  CAS  Google Scholar 

  • Srinivasan, R., Hsu, Y.-C., Kadirvel, P., & Lin, M.-Y. (2013). Analysis of Bemisia tabaci (Hemiptera: Aleyrodidae) species complex in Java, Indonesia based on mitochondrial cytochrome oxidase I sequences. The Philippine Agricultural Scientist, 96(3), 290–295.

    Google Scholar 

  • Su, Q., Pan, H., Liu, B., Chu, D., **e, W., Wu, Q., Wang, S., Xu, B., & Zhang, Y. (2013). Insect symbiont facilitates vector acquisition, retention, and transmission of plant virus. Scientific Reports, 3. https://doi.org/10.1038/srep01367.

  • Sun, D.-B., Liu, Y.-Q., Qin, L., Xu, J., Li, F.-F., & Liu, S.-S. (2013). Competitive displacement between two invasive whiteflies: Insecticide application and host plant effects. Bulletin of Entomological Research, 103(3), 344–353.

    Article  CAS  PubMed  Google Scholar 

  • Tantiwanich, Y., & Chiemsombat, P. (2002). Gene cloning and genome structure of geminivirus causing yellow leaf curl disease of angled luffa. Thai Phytopathol, 16, 1–14.

    Google Scholar 

  • Thanapase, V., Poolpol, P., Sutabutra, T., & Attathom, S. (1983). Causal agent and some important characteristics of Tomato yellow leaf curl disease. Kasetsart Journal: Natural Science, 17, 65–73.

    Google Scholar 

  • Tsai, W. S., Shih, S. L., Green, S., Rauf, A., Hidayat, S., & Jan, F. J. (2006). Molecular characterization of Pepper yellow leaf curl Indonesia virus in leaf curl and yellowing diseased tomato and pepper in Indonesia. Plant Disease, 90(2), 247.

    Article  CAS  PubMed  Google Scholar 

  • Tsai, W. S., Shih, S. L., Venkatesan, S. G., Aquino, M. U., Green, S. K., Keyon, L., & Jan, F. J. (2011). Distribution and genetic diversity of begomoviruses in fecting tomato and pepper plants in the Philippines. The Annals of Applied Biology, 158(3), 275–287.

    Article  CAS  Google Scholar 

  • Tsai, W. S., Shih, S. L., Lee, L. M., Wang, J. T., Duangsong, U., & Kenyon, L. (2012). First report of Bhendi yellow vein mosaic virus associated with yellow vein mosaic of okra (Abelmoschus esculentus) in Thailand. Plant Disease, 97(2), 291.

    Article  Google Scholar 

  • Weng, V., Tsai, W. S., Kenyon, L., & Tsai, C. W. (2015). Different transmission efficiencies may drive displacement of tomato begomoviruses in the fields in Taiwan. Annals of Applied Biology, 166, 321–330.

    Article  Google Scholar 

  • Xu, J., Lin, K. K., & Liu, S. S. (2011). Performance on different host plants of an alien and an indigenous Bemisia tabaci from China. Journal of Applied Entomology, 135, 771–779.

    Article  Google Scholar 

  • Zang, L.-S., Chen, W.-Q., & Liu, S.-S. (2006). Comparison of performance on different host plants between the B biotype and a non-B biotype of Bemisia tabacifrom Zhejiang, China. Entomologia Experimentalis et Applicata, 121, 221–227.

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful for financial support provided for the Beating Begomoviruses project (11.7860.7-001.00) by the Federal Ministry for Economic Cooperation and Development (BMZ) through Deutsche Gesellschaft für Internationale Zusammenarbeit (GIZ) GmbH and from core donors to the World Vegetable Center: Republic of China (Taiwan), UK aid from the UK government, United States Agency for International Development (USAID), Australian Centre for International Agricultural Research (ACIAR), Germany, Thailand, Philippines, Korea, and Japan. We appreciate the use of laboratory facilities at the World Vegetable Center, East and Southeast Asia and the Molecular Plant Pathology Laboratory, Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Kamphaeng Saen Campus. Thanks are also expressed to Ms. Jutarat Lidjun, PhD in Agricultural Biotechnology, for technical support in molecular analysis.

Author information

Authors and Affiliations

  1. KasetsartUniversity, Kamphaeng Saen Campus, Kamphaeng Saen, Nakhon Pathom, 73140, Thailand

    S. Yule & P. Chiemsombat

  2. World Vegetable Center, East andSoutheast Asia, Research and Training Station, Kasetsart University, Kamphaeng Saen Campus, Kamphaeng Saen, Nakhon Pathom, 73140, Thailand

    S. Yule

  3. World Vegetable Center, Shanhua, Tainan, 74151, Taiwan

    Ramasamy Srinivasan

Authors
  1. S. Yule
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Chiemsombat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ramasamy Srinivasan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ramasamy Srinivasan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yule, S., Chiemsombat, P. & Srinivasan, R. Detection of Tomato yellow leaf curl Thailand virus transmitted by Bemisia tabaci Asia I in tomato and pepper. Phytoparasitica 47, 143–153 (2019). https://doi.org/10.1007/s12600-018-00712-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-018-00712-z

Keywords

Search

Navigation