Skip to main content
SpringerLink
Log in

Evidence for increased efficiency of virus transmission by populations of Mediterranean species of Bemisia tabaci with high Hamiltonella prevalence

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

Bemisia tabaci is an important agriculture pests and vector of viruses. The MEAM1 species of B. tabaci, first described in Brazil in the 90s is now the most prevalent species and primary cause of the emergence of begomoviruses in tomatoes. The Mediterranean species (MED) was recently detected in Brazil and is a new concern for Brazilian agriculture. The potential impact of this species as a vector of economically important virus in Brazil is unknown. We therefore evaluated the ability of MED to transmit four whitefly transmitted viruses prevalent in Brazil, Cowpea mild mottle virus (CpMMV, carlavirus), Bean golden mosaic virus (BGMV, begomovirus) infecting beans; and the Tomato severe rugose virus (ToSRV, begomovirus), Tomato chlorosis virus (ToCV, crinivirus) infecting tomatoes. The colony of MED harbouring the secondary endosymbionts was tested: 14% positive for Hamiltonella and 29% positive for Rickettsia. After six months being maintained on cotton plants, this colony changed the frequency of endosymbionts (97% of Hamiltonella and 1% of Rickettsia) and was denominated as MEDH. Additionally, a colony of MEAM1 (98% positive for Hamiltonella and 91% positive for Rickettsia) was also tested. The viruses were efficiently transmitted by MED, but transmission efficiency varied among the MED and MEDH, being CpMMV, BGMV and ToCV better transmitted by MEDH. Moreover, transmission efficiency of ToSRV and ToCV by MEDH was even significantly better than MEAM1. We conclude that specimens from B. tabaci MED are good vectors of virus infecting tomato and beans in Brazil and populations with Hamiltonella prevalence increased the virus transmission.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Barbosa, L. F., Marubayashi, J. M., De Marchi, B. R., Yuki, V. A., Pavan, M. A., Moriones, E., et al. (2014). Indigenous American species of the Bemisia tabaci complex are still widespread in the Americas. Pest Management Science, 70(10), 1440–1445.

    Article  CAS  Google Scholar 

  • Barbosa, L. B., Yuki, V. A., Marubayashi, J. M., De Marchi, B. R., Perini, F. L., Pavan, M. A., et al. (2015). First report of Bemisia tabaci Mediterranean (Q biotype) species in Brazil. Pest Management Science, 71(4), 501–504. https://doi.org/10.1002/ps.3909.

    Article  CAS  Google Scholar 

  • Barreto, S. S., Hallwass, M., Aquino, O. M., & Inoue-Nagata, A. K. (2013). A study of weeds as potential inoculum sources for a tomato-infecting Begomovirus in Central Brazil. Phytopathology, 103(5), 436–444. https://doi.org/10.1094/PHYTO-07-12-0174-R.

    Article  CAS  PubMed  Google Scholar 

  • Bosco, D., Loria, A., Sartor, C., & Cenis, J. L. (2006). PCR-RFLP identification ofBemisia tabaci biotypes in the Mediterranean Basin. Phytoparasitica, 34(3), 243–251.

    Article  CAS  Google Scholar 

  • Boykin, L. M., & De Barro, P. J. (2014). A practical guide to identifying members of the Bemisia tabaci species complex: And other morphologically identical species. Frontiers in Ecology and Evolution, 2. https://doi.org/10.3389/fevo.2014.00045.

  • Costa, A. S., Oliveira, A. R., & Silva, D. M. (1977). Transmissao mecanica do agente causal do mosaico dourado do tomateiro [Lycopersicum esculentum]. Summa Phytopathologica (Brasil), 3(3), 194–200.

    Google Scholar 

  • Czosnek, H., & Ghanim, M. (2016). Management of insect pests to agriculture: Lessons learned from deciphering their genome, transcriptome and proteome. Management of Insect Pests to Agriculture: Lessons Learned from Deciphering their Genome, Transcriptome and Proteome, 1–290. https://doi.org/10.1007/978-3-319-24049-7.

  • De Barro, P. J., Liu, S.-S., Boykin, L. M., & Dinsdale, A. B. (2011). Bemisia tabaci : A statement of species status. Annual Review of Entomology, 56(1), 1–19. https://doi.org/10.1146/annurev-ento-112408-085504.

    Article  CAS  PubMed  Google Scholar 

  • De Marchi, B. R., Marubayashi, J. M., Favara, G. M., Yuki, V. A., Watanabe, L. F. M., Barbosa, L. F., et al. (2017). Comparative transmission of five viruses by Bemisia tabaci NW2 and MEAM1. Tropical Plant Pathology, 1, 495–499. https://doi.org/10.1007/s40858-017-0186-9.

    Article  Google Scholar 

  • Dellaporta, S. L., Wood, J., & Hicks, J. B. (1983). A plant DNA minipreparation: Version II. Plant Molecular Biology Reporter, 1(4), 19–21.

    Article  CAS  Google Scholar 

  • Dinsdale, A., Cook, L., Riginos, C., Buckley, Y. M., De Barro, P., & Barro, P. D. (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. https://doi.org/10.1603/AN09061.

    Article  Google Scholar 

  • Dovas, C. I., Katis, N. I., & Avgelis, A. D. (2002). Multiplex detection of Criniviruses associated with epidemics of a yellowing disease of tomato in Greece. Plant Disease, 86(12), 1345–1349. https://doi.org/10.1094/PDIS.2002.86.12.1345.

    Article  CAS  PubMed  Google Scholar 

  • Faria, J. C., Aragão, F. J. L., Souza, T. L. P. O., Quintela, E. D., Kitajima, E. W., & Ribeiro, S. G. (2016). Golden mosaic of common beans in Brazil : Management with a transgenic approach. APS Journal, 1–14. https://doi.org/10.1094/APSFeature-2016-10.Plant.

  • 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. https://doi.org/10.1016/j.virusres.2014.01.022.

    Article  CAS  PubMed  Google Scholar 

  • Ghanim, M., & Kontsedalov, S. (2009). Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Management Science, 65(9), 939–942. https://doi.org/10.1002/ps.1795.

    Article  CAS  PubMed  Google Scholar 

  • Ghosh, S., Bouvaine, S., Richardson, S. C. W., Ghanim, M., & Maruthi, M. N. (2018). Fitness costs associated with infections of secondary endosymbionts in the cassava whitefly species Bemisia tabaci. Journal of Pest Science, 91(1), 17–28. https://doi.org/10.1007/s10340-017-0910-8.

    Article  PubMed  Google Scholar 

  • Gilbertson, R. L., Batuman, O., Webster, C. G., & Adkins, S. (2015). Role of the insect Supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annual Review of Virology, 2(1), 67–93. https://doi.org/10.1146/annurev-virology-031413-085410.

    Article  CAS  PubMed  Google Scholar 

  • Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Kontsedalov, S., Skaljac, M., Brumin, M., Sobol, I., Czosnek, H., Vavre, F., Fleury, F., & Ghanim, M. (2010). The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. Journal of Virology, 84(18), 9310–9317. https://doi.org/10.1128/JVI.00423-10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gueguen, G., Vavre, F., Gnankine, O., Peterschmitt, M., Charif, D., Chiel, E., et al. (2010). Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Molecular Ecology, 19(19), 4365–4376.

    Article  PubMed  Google Scholar 

  • Hadjistylli, M., Roderick, G.K., & Brown, J.K. (2016). Global population structure of a worldwide Pest and virus vector : Genetic diversity and population history of the Bemisia tabaci sibling species group. https://doi.org/10.5061/dryad.h7s57.

  • Horowitz, A. R., Kontsedalov, S., Khasdan, V., & Ishaaya, I. (2005). Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Archives of Insect Biochemistry and Physiology, 58(4), 216–225. https://doi.org/10.1002/arch.20044.

    Article  CAS  PubMed  Google Scholar 

  • Inoue-Nagata, A. K., Lima, M. F., & Gilbertson, R. L. (2016). A review of geminivirus diseases in vegetables and other crops in Brazil: Current status and approaches for management. Horticultura Brasileira, 34(1), 8–18. https://doi.org/10.1590/S0102-053620160000100002.

    Article  Google Scholar 

  • Kliot, A., Cilia, M., Czosnek, H., & Ghanim, M. (2014). Implication of the bacterial endosymbiont rickettsia spp. in interactions of the whitefly Bemisia tabaci with tomato yellow leaf curl virus. Journal of Virology, 88(10), 5652–5660. https://doi.org/10.1128/JVI.00071-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lourencao, A. L., & Nagai, H. (1994). Surtos populacionais de Bemisia tabaci no Estado de Sao Paulo. Bragantia, 53(1), 53–59. https://doi.org/10.1590/S0006-87051994000100006.

    Article  Google Scholar 

  • Macedo, M., Barreto, S., Hallwass, M., & Inoue-nagata, A. (2014). High incidence of Tomato chlorosis virus alone and in mixed infection with begomoviruses in two tomato fields in the Federal District and Goiás state , Brazil. Tropical Plant Pathology, 39(6), 449–452. https://doi.org/10.1590/S1982-56762014000600005.

    Article  Google Scholar 

  • Marubayashi, J. M., Yuki, V. A., Rocha, K. C. G., Mituti, T., Pelegrinotti, F. M., Ferreira, F. Z., Moura, M. F., Navas-Castillo, J., Moriones, E., Pavan, M. A., & Krause-Sakate, R. (2013). At least two indigenous species of the Bemisia tabaci complex are present in Brazil. Journal of Applied Entomology, 137(1–2), 113–121. https://doi.org/10.1111/j.1439-0418.2012.01714.x.

    Article  Google Scholar 

  • Marubayashi, J. M., Kliot, A., Yuki, V. A., Rezende, J. A. M., Krause-Sakate, R., Pavan, M. A., & Ghanim, M. (2014). Diversity and localization of bacterial endosymbionts from whitefly species collected in Brazil. PLoS One, 9(9), e108363. https://doi.org/10.1371/journal.pone.0108363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moraes, L. A., Marubayashi, J. M., Yuki, V. A., Ghanim, M., Bello, V. H., De Marchi, B. R., et al. (2017). New invasion of Bemisia tabaci Mediterranean species in Brazil associated to ornamental plants. Phytoparasitica, 45, 1–525. https://doi.org/10.1007/s12600-017-0607-9.

    Article  CAS  Google Scholar 

  • Moraes, L. A., Muller, C., Bueno, R. C. O. F., Santos, A., Bello, V. H., De Marchi, B. R., et al. (2018). Distribution and phylogenetics of whiteflies and their endosymbiont relationships after the Mediterranean species invasion in Brazil. Scientific Reports, 8(1), 14589. https://doi.org/10.1038/s41598-018-32913-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno-Delafuente, A., Garzo, E., Moreno, A., & Fereres, A. (2013). A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLoS One, 8(4), e61543. https://doi.org/10.1371/journal.pone.0061543.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navas-Castillo, J., Fiallo-Olivé, E., & Sánchez-Campos, S. (2011). Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology, 49, 219–248. https://doi.org/10.1146/annurev-phyto-072910-095235.

    Article  CAS  PubMed  Google Scholar 

  • Ning, W., Shi, X., Liu, B., Pan, H., Wei, W., Zeng, Y., Sun, X., Xie, 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(1), 10744. https://doi.org/10.1038/srep10744.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan, H., Chu, D., Yan, W., Su, Q., Liu, B., Wang, S., & Wu, Q. (2012). Rapid Spread of Tomato Yellow Leaf Curl Virus in China Is Aided Differentially by Two Invasive Whiteflies, 7(4), e34817. https://doi.org/10.1371/journal.pone.0034817.

  • RDevelopment, C. (2018). R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Ribeiro, S. G., De Ávila, A. C., Bezerra, I. C., Fernandes, J. J., Faria, J. C., Lima, M. F., et al. (1998). Widespread occurrence of tomato geminiviruses in Brazil, associated with the new biotype of the whitefly vector. Plant Disease, 82(7), 830.

    Article  CAS  PubMed  Google Scholar 

  • Rojas, M. R., Gilbertson, R. L., Russell, D. R., & Maxwell, D. P. (1993). Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted Geminiviruses. Plant Disease, 77, 340. https://doi.org/10.1094/PD-77-0340.

    Article  CAS  Google Scholar 

  • Shi, X., Pan, H., Xie, W., Jiao, X., Fang, Y., Chen, G., Yang, X., Wu, Q., Wang, S., & Zhang, Y. (2014). Three-Way Interactions Between the Tomato Plant, Tomato Yellow Leaf Curl Virus, and Bemisia tabaci (Hemiptera: Aleyrodidae) Facilitate Virus Spread. Journal of Economic Entomology, 107(3), 920–926. https://doi.org/10.1603/EC13476.

    Article  PubMed  Google Scholar 

  • Shi, X., Chen, G., Pan, H., Xie, W., Wu, Q., Wang, S., et al. (2018). Plants pre-infested with viruliferous MED/Q cryptic species promotes subsequent Bemisia tabaci infestation. Frontiers in Microbiology, 9(JUN), 1–8. https://doi.org/10.3389/fmicb.2018.01404.

    Article  Google Scholar 

  • Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, 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(6), 651–701.

    Article  CAS  Google Scholar 

  • Su, Q., Pan, H., Liu, B., Chu, D., Xie, W., Wu, Q., Wang, S., Xu, B., & Zhang, Y. (2013). Insect symbiont facilitates vector acquisition, retention, and transmission of plant virus. Scientific Reports, 3, 1–6. https://doi.org/10.1038/srep01367.

    Article  CAS  Google Scholar 

  • 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(03), 344–353. https://doi.org/10.1017/S0007485312000788.

    Article  CAS  PubMed  Google Scholar 

  • Walsh, P. S., Metzger, D. A., & Higuchi, R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques, 10(4), 506–513.

    CAS  PubMed  Google Scholar 

  • Yao, F. L., Zheng, Y., Huang, X. Y., Ding, X. L., Zhao, J. W., Desneux, N., He, Y. X., & Weng, Q. Y. (2017). Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005-2014. Scientific Reports, 7(December 2016), 1–12. https://doi.org/10.1038/srep40803.

    Article  CAS  Google Scholar 

  • Zambrano, K., Carballo, O., Geraud, F., Chirinos, D., Fernández, C., & Marys, E. (2007). First report of tomato yellow leaf curl virus in Venezuela. Plant Disease, 91(6), 768.

    Article  CAS  PubMed  Google Scholar 

  • Zanardo, L. G., Silva, F. N., Lima, A. T. M., Milanesi, D. F., Castilho-Urquiza, G. P., Almeida, A. M. R., Zerbini, F. M., & Carvalho, C. M. (2014). Molecular variability of cowpea mild mottle virus infecting soybean in Brazil. Archives of Virology, 159(4), 727–737. https://doi.org/10.1007/s00705-013-1879-0.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financed in party by the Coordenaçao de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001. BRM and BRS received a CNPq/Brazil scholarship. Financial support was received from FAPESP 2017/21588-7, 2017/50222, -2014/047289-4 and CNPq479101/2013-2. RKS and MAP received CNPq fellowships.

Author information

Authors and Affiliations

  1. UNESP – Faculdade de Ciências Agronômicas, Botucatu, Brazil

    Vinicius Henrique Bello, Luís Fernando Maranho Watanabe, Beatriz Rosa Santos, Julio Massaharu Marubayashi, Bruno Rossitto De Marchi, Marcelo Agenor Pavan & Renate Krause-Sakate

  2. Centro de Fitossanidade, Instituto Agronômico de Campinas, Campinas, Brazil

    Valdir Atsushi Yuki

Authors
  1. Vinicius Henrique Bello
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luís Fernando Maranho Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beatriz Rosa Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julio Massaharu Marubayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Valdir Atsushi Yuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bruno Rossitto De Marchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcelo Agenor Pavan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Renate Krause-Sakate
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renate Krause-Sakate.

Ethics declarations

The authors declare that the work is in compliance with ethical standards.

Conflict of interest

The authors declare no conflict of interests.

Research involving human participants and/or animals

The authors declare that the manuscript does not contain research involving Human Participants and/or Animals.

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

Bello, V.H., Watanabe, L.F.M., Santos, B.R. et al. Evidence for increased efficiency of virus transmission by populations of Mediterranean species of Bemisia tabaci with high Hamiltonella prevalence. Phytoparasitica 47, 293–300 (2019). https://doi.org/10.1007/s12600-019-00729-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-019-00729-y

Keywords

Search

Navigation