Abstract
Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) were reported as the sole vectors for tomato severe rugose virus (ToSRV), the prevalent begomovirus infecting tomato (Solanum lycopersicum L., Solanaceae) in Brazil. To improve our understanding on the interactions between B. tabaci and ToSRV, we studied the effects of the virus on the performance of MEAM1 and MED. Comparing adults’ performance on non-infected and ToSRV-infected tomato plants, the number of hatched eggs and emerged adults decreased for both MEAM1 and MED in infected tomato plants. However, the negative effect was more evident for MED, where the emergence of adults was reduced by 90% on ToSRV-infected tomatoes. In addition, the developmental time and percentage survival of MED on ToSRV-infected plants were severely affected compared to non-infected plants, while no differences were observed for MEAM1. Preference assays showed that non-viruliferous MEAM1 adults preferred to settle on non-infected plants in initial times (from 1 h to 6 h) but did not show preference between non-infected and infected plants in other evaluated times (from 12 h to 72 h). Viruliferous MEAM1 adults did not show a preference for either ToSRV-infected or non-infected plants. In contrast, MED non-viruliferous and viruliferous adults preferred to settle on non-infected plants compared to ToSRV-infected tomato plants. Our results indicate that ToSRV differently influences the performance and behavior of the whitefly species MEAM1 and MED, negatively interfering with the life parameters of MED.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data supporting the findings of this study are available upon request from the corresponding author.
References
Alemandri, V., Medina, C. G. V., Dumón, A. D., Caro, E. B. A., Mattio, M. F., Medina, S. G., et al. (2015). Three members of the Bemisia tabaci (Hemiptera: Aleyrodidae) cryptic species complex occur sympatrically in argentine horticultural crops. Journal of Economic Entomology, 108(2), 405–413. https://doi.org/10.1093/jee/tov017
Bello, V. H., Fernando, L., Watanabe, M., Santos, B. R., Marubayashi, J. M., Yuki, V. A., et al. (2019). Evidence for increased efficiency of virus transmission by populations of Mediterranean species of Bemisia tabaci with high Hamiltonella prevalence. Phytoparasitica, 47, 293–300. https://doi.org/10.1007/s12600-019-00729-y
Bello, V. H., Watanabe, L. F. M., Fusco, L. M. H., De Marchi, B. R., Da Silva, F. B., Gorayeb, E. S., et al. (2020). Outbreaks of Bemisia tabaci Mediterranean species in vegetable crops in São Paulo and Paraná States, Brazil. Bulletin of Entomological Research, 110(4), 487–496. https://doi.org/10.1017/S0007485319000841
Bello, V. H., da Silva, F. B., Watanabe, L. F. M., Vicentin, E., Muller, C., de Freitas Bueno, R. C. O., et al. (2021). Detection of Bemisia tabaci Mediterranean cryptic species on soybean in São Paulo and Paraná states (Brazil) and interaction of cowpea mild mottle virus with whiteflies. Plant Pathology, 70(6), 1508–1520. https://doi.org/10.1111/ppa.13387
Chen, G., Pan, H., **e, W., Wang, S., Wu, Q., Fang, Y., et al. (2013). Virus infection of a weed increases vector attraction to and vector fitness on the weed. Scientific Reports, 3, 3–8. https://doi.org/10.1038/srep02253
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
Doyle, J. J., & Doyle, J. L. (1991). Isolation of plant DNA from fresh tissue. Focus, 1, 13–15
Fang, Y., Jiao, X., **e, W., Wang, S., Wu, Q., Shi, X., et al. (2013). Tomato yellow leaf curl virus alters the host preferences of its vector bemisia tabaci. Scientific Reports, 3, 1–5. https://doi.org/10.1038/srep02876
Fereres, A., & Moreno, A. (2009). Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Research, 141(2), 158–168. https://doi.org/10.1016/j.virusres.2008.10.020
Fereres, A., Peñaflor, M. F. G. V., Favaro, C. F., Azevedo, K. E. X., Landi, C. H., Maluta, N. K. P., et al. (2016). Tomato infection by whitefly-transmitted circulative and non-circulative viruses induce contrasting changes in plant volatiles and vector behaviour. Viruses, 8(8). https://doi.org/10.3390/v8080225
Fiallo-Olivé, E., Pan, L. L., Liu, S. S., & Navas-Castillo, J. (2020). Transmission of begomoviruses and other whitefly-borne viruses: Dependence on the vector species. Phytopathology, 110(1), 10–17. https://doi.org/10.1094/PHYTO-07-19-0273-FI
Fiallo-Olivé, E., Lett, J. M., Martin, D. P., Roumagnac, P., Varsani, A., Zerbini, F. M., & Navas-Castillo, J. (2021). ICTV virus taxonomy profile: Geminiviridae 2021. Journal of General Virology, 102(12), 1696. https://doi.org/10.1099/jgv.0.001696
Gadhave, K. R., Gautam, S., Rasmussen, D. A., & Srinivasan, R. (2020). Aphid transmission of potyvirus: The largest plant-infecting RNA virus genus. Viruses, 12(7), 1–22. https://doi.org/10.3390/v12070773
García-Arenal, F., & Zerbini, F. M. (2019). Life on the edge: Geminiviruses at the Interface between crops and wild plant hosts. Annual Review of Virology, 6, 411–433. https://doi.org/10.1146/annurev-virology-092818-015536
Gautam, S., Gadhave, K. R., Buck, J. W., Dutta, B., Coolong, T., Adkins, S., & Srinivasan, R. (2020). Virus-virus interactions in a plant host and in a hemipteran vector: Implications for vector fitness and virus epidemics. Virus Research, 286(June), 198069. https://doi.org/10.1016/j.virusres.2020.198069
Gautam, S., Buck, J. W., Dutta, B., Coolong, T., Sanchez, T., Smith, H. A., et al. (2023). Sida Golden mosaic virus, an emerging pathogen of snap bean (Phaseolus vulgaris L.) in the southeastern United States. Viruses, 15(2). https://doi.org/10.3390/v15020357
Ghosh, S., & Ghanim, M. (2021). Factors determining transmission of persistent viruses by bemisia tabaci and emergence of new virus–vector relationships. Viruses, 13(9). https://doi.org/10.3390/v13091808
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
Gorayeb, E. S., Bello, V. H., Cruciol, G. C. D., Watanabe, L. F. M., Dovigo, L. H., Sartori, M. M. P., et al. (2020). Evaluation of Datura stramonium and Nicandra physaloides as reservoirs of tomato severe rugose virus and whiteflies. Plant Pathology, 69(3), 569–575. https://doi.org/10.1111/ppa.13139
Guo, L., Su, Q., Yin, J., Yang, Z., **e, W., Wang, S., et al. (2019). Amino acid utilization may explain why Bemisia tabaci Q and B differ in their performance on plants infected by the tomato yellow leaf curl virus. Frontiers in Physiology, 10(MAY), 1–8. https://doi.org/10.3389/fphys.2019.00489
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
Johnston, N., & Martini, X. (2020). The influence of visual and olfactory cues in host selection for Bemisia tabaci biotype B in the presence or absence of tomato yellow leaf curl virus. Insects, 11(2), 115. https://doi.org/10.3390/INSECTS11020115.
Kanakala, S., Ghanim, M., Kanakala, S., & Ghanim, M. (2019). Global genetic diversity and geographical distribution of Bemisia tabaci and its bacterial endosymbionts. PLoS One, 14(3). https://doi.org/10.1371/journal.pone.0213946
Krause-Sakate, R., Watanabe, L. F., Gorayeb, E. S., da Silva, F. B., Alvarez, D. D., Bello, V. H., et al. (2020). Population dynamics of whiteflies and associated viruses in South America: Research Progress and perspectives. Insects. https://doi.org/10.3390/insects11120847
Lapidot, M., Friedmann, M., Pilowsky, M., Ben-Joseph, R., & Cohen, S. (2001). Effect of host plant resistance to tomato yellow leaf curl virus (TYLCV) on virus acquisition and transmission by its whitefly vector. Phytopathology, 91(12), 1209–1213. https://doi.org/10.1094/PHYTO.2001.91.12.1209
Legarrea, S., Barman, A., Marchant, W., Diffie, S., & Srinivasan, R. (2015). Temporal effects of a Begomovirus infection and host plant resistance on the preference and development of an insect vector, Bemisia tabaci, and implications for epidemics. PLoS One, 10(11), 1–19. https://doi.org/10.1371/journal.pone.0142114
Liu, B., Preisser, E. L., Chu, D., Pan, H., **e, W., Wang, S., et al. (2013). Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and tomato yellow leaf curl virus. Journal of Virology, 87(9), 4929–4937. https://doi.org/10.1128/jvi.03571-12
Luan, J. B., Wang, X. W., Colvin, J., & Liu, S. S. (2014). Plant-mediated whitefly-begomovirus interactions: Research progress and future prospects. Bulletin of Entomological Research, 104(3), 267–276. https://doi.org/10.1017/S000748531400011X
Maluta, N. K. P., Fereres, A., & Lopes, J. R. S. (2017). Settling preferences of the whitefly vector Bemisia tabaci on infected plants varies with virus family and transmission mode. Entomologia Experimentalis et Applicata, 165(2–3), 138–147. https://doi.org/10.1111/eea.12631
Maluta, N., Fereres, A., & Lopes, J. R. S. (2018). Plant-mediated indirect effects of two viruses with different transmission modes on Bemisia tabaci feeding behavior and fitness. Journal of Pest Science, 92(2), 405–416. https://doi.org/10.1007/s10340-018-1039-0
Mauck, K. E. (2016). Variation in virus effects on host plant phenotypes and insect vector behavior: What can it teach us about virus evolution? Current Opinion in Virology, 21, 114–123. https://doi.org/10.1016/j.coviro.2016.09.002
Mauck, K. E., Chesnais, Q., & Shapiro, L. R. (2018). Evolutionary determinants of host and vector manipulation by plant viruses. In Advances in virus research (Vol. 101, 1st ed.). Elsevier Inc.. https://doi.org/10.1016/bs.aivir.2018.02.007
Mituti, T., Moura, M. F., Macedo, M. A., Silva, T. N. Z., Pinto, L. R., Costa, H., et al. (2019). Survey of begomoviruses and the crinivirus, tomato chlorosis virus, in solanaceous in southeast/Midwest of Brazil. Tropical Plant Pathology, 44(5), 468–472. https://doi.org/10.1007/s40858-019-00294-z
Moraes, L. A., Muller, C., de Freitas Bueno, R. C. O., 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), 1–13. https://doi.org/10.1038/s41598-018-32913-1
Ng, J. C. K., & Falk, B. W. (2006). Virus-vector interactions mediating nonpersistent and Semipersistent transmission of plant viruses. Annual Review of Phytopathology, 44(1), 183–212. https://doi.org/10.1146/annurev.phyto.44.070505.143325
Pan, H., Chu, D., Yan, W., Su, Q., Liu, B., Wang, S., et al. (2012). Rapid spread of tomato yellow leaf curl virus in China is aided differentially by two invasive whiteflies. PLoS One, 7(4), e34817. https://doi.org/10.1371/journal.pone.0034817
Pan, H., Chu, D., Liu, B., Shi, X., Guo, L., **e, W., et al. (2013). Differential effects of an exotic plant virus on its two closely related vectors. Scientific Reports, 3(1), 2230. https://doi.org/10.1038/srep02230
Rocha, C. S., Castillo-Urquiza, G. P., Lima, A. T. M., Silva, F. N., Xavier, C. A. D., Hora-Junior, B. T., et al. (2013). Brazilian Begomovirus populations are highly recombinant, rapidly evolving, and segregated based on geographical location. Journal of Virology, 87(10), 5784–5799. https://doi.org/10.1128/jvi.00155-13
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(4), 340–347. https://doi.org/10.1094/PD-77-0340
Rojas, M. R., Macedo, M. A., Maliano, M. R., Soto-Aguilar, M., Souza, J. O., Briddon, R. W., et al. (2018). World Management of Geminiviruses. Annual Review of Phytopathology, 56(1), 637–677. https://doi.org/10.1146/annurev-phyto-080615-100327
Shi, X., Chen, G., Pan, H., **e, W., Wu, Q., Wang, S., et al. (2018a). 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
Shi, X., Tang, X., Zhang, X., Zhang, D., Li, F., Yan, F., et al. (2018b). Transmission efficiency, preference and behavior of Bemisia tabaci MEAM1 and MED under the influence of tomato chlorosis virus. Frontiers in Plant Science, 8(January), 1–9. https://doi.org/10.3389/fpls.2017.02271
Su, Q., Preisser, E. L., Zhou, X. M., **e, W., Liu, B. M., Wang, S. L., et al. (2015). Manipulation of host quality and defense by a plant virus improves performance of whitefly vectors. Journal of Economic Entomology, 108(1), 11–19. https://doi.org/10.1093/jee/tou012
Toloy, R. S., Mituti, T., Freitas, D. M. S., Maluta, N. K. P., Silva, T. N. Z., Lopes, J. R. S., et al. (2018). 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. European Journal of Plant Pathology, 151(2), 541–547. https://doi.org/10.1007/s10658-017-1388-1
Whitfield, A. E., Falk, B. W., & Rotenberg, D. (2015). Insect vector-mediated transmission of plant viruses. Virology, 479–480(August 2016), 278–289. https://doi.org/10.1016/j.virol.2015.03.026
Acknowledgements
This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001; Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP (grant number 2017/21588-7, 2018/18274-3, 2019/18639-4, 2020/05563-7) and CNPq (405684/2018-5). RKS, MMS, MAP and JAMR received CNPq fellowships.
Author information
Authors and Affiliations
Contributions
Conceptualization, Methodology, Formal analysis and investigation: V.H.B., A.M.N., M.A.P., J.A.M.R., M.G. and R.K.S. Statistical analysis: V.H.B. and M.M.P.S. Writing – original draft preparation: V.H.B. Writing – review and editing: V.H.B., J.A.M.R., M.G. and R.K.S. Funding acquisition: R.K.S. and J.A.M.R. Supervision: R.K.S.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is 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
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bello, V.H., Nogueira, A.M., Sartori, M.M.P. et al. Performance and preference of Bemisia tabaci on tomato severe rugose virus infected tomato plants. Phytoparasitica 51, 403–413 (2023). https://doi.org/10.1007/s12600-023-01079-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12600-023-01079-6