Composition of Secondary Endosymbiont Bacteria in Two Whitefly Species (Hemiptera: Aleyrodidae)
Year 2024,
Volume: 19 Issue: 2, 39 - 46, 31.12.2024
Zülal Tat
,
Erhan Koçak
Abstract
Tobacco whitefly Bemisia tabaci and greenhouse whitefly Trialeurodes vaporariorum, which have a wide host range, are among the most important plant protection problems in agricultural areas all over the world. Within the scope of the study, the infection status of endosymbiont bacteria Wolbachia, Rickettsia and Arsenophonus in the whiteflies was determined by molecular methods. Whiteflies T. vaporariorum and B. tabaci populations were collected from tomato greenhouses at five different locations in Antalya province. This study is the first for endosymbionts of Turkish T. vaporariorum populations. All the three endosymbionts were found in T. vaporariorum and B. tabaci populations. While Arsenophonus was the most frequently found endosymbiont in both whitefly populations, Wolbachia was found in high rates in T. vaporariorum and Rickettsia in B. tabaci. In addition, endosymbiont compositions in individuals belonging to both species were revealed as single, double and triple. Wolbachia (W) and Rickettsia (R) were not found together in any individual of both whitefly species. Out of WR, all single and other multiple endosymbiont combinations were detected in the individuals. However, any infection was not recorded for few individuals from the populations of both species.
Ethical Statement
As the authors of the article, we declare that we do not have any ethics committee approval information.
Supporting Institution
ISUBÜ
Project Number
2023-YL1-0205
Thanks
We would like to thank Isparta University of Applied Sciences, Scientific Research Projects Management Unit (BAP) for supporting the Master's thesis with Project No. 2023-YL1-0205.
References
- Alvarez, D. D. L., Hayashida, R., Cavallaro, M. C., Santos, D.M., Santos, L. M., Müller, C., Watanabe, L. F. M., Bello, V. H., Krause-Sakate, R., Hoback, W. W., & Oliveira, R. C. D. (2024). Susceptibility of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) Mediterranean Populations Found in São Paulo, Brazil to 11 Insecticides and Characterization of Their Endosymbionts. Insects, 15(9), 670.
- Barman, M., Samanta, S., Upadhyaya, G., Thakur, H., Chakraborty, S., Samanta, A., & Tarafdar, J. (2022). Unraveling the basis of neonicotinoid resistance in whitefly species complex: Role of endosymbiotic bacteria and insecticide resistance genes. Frontiers in Microbiology, 13, 901793.
- Bing, X. L., Yang, J., Zchori-Fein, E., Wang, X. W., & Liu, S. S. (2013). Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Applied of Environmental Microbiology, 79, 569–575.
- Brumin, M., Kontsedalov, S., & Ghanim, M. (2011). Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Science, 18(1), 57-66.
- Chiel, E., Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Katzir, N., Inbar, M., & Ghanim, M. (2007). Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bulletin of Entomological Research, 97(4), 407-413.
- Clark, M. A., Baumann, L., Munson, M. A., Baumann, P., Campbell, B. C., Duffus, J. E., Osborne, L. S., & Moran, N. A. (1992). The eubacterial endosymbionts of whiteflies (Homoptera: Aleyrodoidea) constitute a lineage distinct from the endosymbionts of aphids and mealybugs. Current Microbiology, 25, 119–123.
- Costa, H. S., Westcot, D. M., Ullman, D. E., Rosell, R., Brown, J. K., & Johnson, M. W. (1995). Morphological variation in Bemisia endosymbionts. Protoplasma, 189, 194–202.
- Erdogan, C., Velioglu, A. S., Gurkan, M. O., Denholm, I., & Moores, G. D. (2021). Detection of resistance to pyrethroid and neonicotinoid insecticides in the greenhouse whitefly, Trialeurodes vaporariorum (Westw.) (Hemiptera: Aleyrodidae). Crop Protection, 146, 105661.
- Ghanim, M., & Kontsedalov, S. (2009). Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Management Science: Formerly Pesticide Science, 65(9), 939-942.
- Ghosh, S., Bouvaine, S., & Maruthi, M. N. (2015). Prevalence and genetic diversity of endosymbiotic bacteria infecting cassava whiteflies in Africa. BMC Microbiology, 15, 93.
- Goto, S., Anbutsu, H., & Fukatsu, T. (2006). Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Applied and Environmental Microbiology, 72(7), 4805-4810.
- Gottlieb, Y., Ghanim, M., Chiel, E., Gerling, D., Portnoy, V., Steinberg, S., & Zchori-Fein, E. (2006). Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Applied and Environmental Microbiology, 72(5), 3646-3652.
- Guay, J. F., Boudreault, S., Michaud, D., & Cloutier, C. (2009). Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. Journal of Insect Physiology, 55(10), 919-926.
- Gueguen, G., Vavre, F., Gnankine, O., Peterschmitt, M., Charif, D., Chiel, E., & Fleury, F. (2010). Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Molecular Ecology, 19(19), 4365-4376.
- Guo, L., Lv, H., Tan, D., Liang, N., Guo, C., & Chu, D. (2020). Resistance to insecticides in the field and baseline susceptibility to cyclaniliprole of whitefly Bemisia tabaci (Gennadius) in China. Crop protection, 130, 105065.
- Hill, B. (1969). A morphological comparison between two species of whitefly, Trialeurodes vaporariorum (Westw.) and Bemisia tabaci (Genn.) (Homoptera: Aleurodidae) which occur on tobacco in the Transvaal. Phytophylactica, 1, 127-146.
- Jones D. R. (2003). Plant viruses transmitted by whiteflies. European Journal of Plant Pathology, 109(3), 195-219.
- Kareem, A. A., Logan, S. A., Port, G., & Wolff, K. (2020). Bemisia tabaci in Iraq: Population structure, endosymbiont diversity and putative species. Journal of Applied Entomology, 144(4), 297-307.
- Karut, K., & Tok, B. (2014). Secondary endosymbionts of Turkish Bemisia tabaci (Gennadius) populations. Phytoparasitica, 42, 413-419.
- 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.
- Kontsedalov, S., Zchori‐Fein, E., Chiel, E., Gottlieb, Y., Inbar, M., & Ghanim, M. (2008). The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science: Formerly Pesticide Science, 64(8), 789-792.
- Lapidot, M., Legg, J. P., Wintermantel, W. M., & Polston, J. E. (2014). Management of whitefly-transmitted viruses in open-field production systems. In Advances in virus research, 90, 147-206.
- Li, H., Jiang, Z., Zhou, J., Liu, X., Zhang, Y., & Chu, D., (2023). Ecological factors associated with the distribution of Bemisia tabaci cryptic species and their facultative endosymbionts. Insects, 14(3), 252.
- Liu, X. D. & Guo, H. F. (2019). Importance of endosymbionts Wolbachia and Rickettsia in insect resistance development. Current Opinion in Insect Science, 33, 84–90.
- 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.
- Milenovic, M., Ghanim, M., Hoffmann, L., & Rapisarda, C. (2022). Whitefly endosymbionts: IPM opportunity or tilting at windmills? Journal of Pest Science, 95(2), 543-566.
- Milenovic, M., Massimino Cocuzza, G. E., Suma, P., & Farina, A. (2023). Geographic distribution of Bemisia tabaci species in Sicily and patterns in facultative endosymbiont community composition. Journal of Applied Entomology, 147(10), 908-915.
- Nirgianiki, A., Banks, G. K., Frohlich, D. R., Veneti, Z., Braig, H. R., Miller, T. A., & Bourtzis, K. (2003). Wolbachia infections of the whitefly Bemisia tabaci. Current Microbiology, 47, 0093-0101.
- Opatovsky, I., Santos-Garcia, D., Ruan, Z., Lahav, T., Ofaim, S., Mouton, L., Barbe, V., Jiang, J., Zchori-Fein, E., & Freilich, S. (2018). Modeling trophic dependencies and exchanges among insects' bacterial symbionts in a host-simulated environment. BMC Genomics, 19, 1–14.
- Pan, H. P., Chu, D., Liu, B. M., Xie, W., Wang, S. L., Wu, Q. J., Xu, B. Y., Zhang, Y. J. (2013). Relative amount of symbionts in insect hosts changes with host-plant adaptation and insecticide resistance. Environmental entomology, 42(1), 74-78.
- Raina, H. S., Rawal, V., Singh, S., Daimei, G., Shakarad, M., & Rajagopal, R. (2015). Elimination of Arsenophonus and decrease in the bacterial symbionts diversity by antibiotic treatment leads to increase in fitness of whitefly, Bemisia tabaci. Infection, Genetics and Evolution, 32, 224-230.
- Rossitto De Marchi, B., & Smith, H. A. (2020). Bacterial endosymbiont diversity among Bemisia tabaci (Hemiptera: Aleyrodidae) populations in Florida. Insects, 11(3), 179.
- Shi, P. Q., Wang, L., Chen, X. Y., Wang, K., Wu, Q. J., Turlings, T. C., Zhang, P. J., & Qiu, B. L. (2024). Rickettsia transmission from whitefly to plants benefits herbivore insects but is detrimental to fungal and viral pathogens. Mbio, 15(3), 02448-23.
- Singh, S.T., Priya, N.G., Kumar, J., Rana, V.S., Ellango, R., Joshi, A., Priyadarshini, G., Asokan, R., & Rajagopal, R. (2012). Diversity and phylogenetic analysis of endosymbiotic bacteria from field caught Bemisia tabaci from different locations of North India based on 16S rDNA library screening. Infection, Genetics and Evolution, 12(2), 411-419.
- Sivasupramaniam, S., & Watson, T. F. (2000). Selection for fenpropathrin and fenpropathrinacephate resistance in the silverleaf whitefly (Homoptera: Aleyrodidae). Journal of Economic Entomology, 93(3), 949-954.
- Skaljac, M., Zanic, K., Ban, S. G., Kontsedalov, S., & Ghanim, M. (2010). Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiology, 10(1), 1-15.
- Skaljac, M., Kanakala, S., Zanic, K., Puizina, J., Lepen Pleic, I., & Ghanim, M. (2017). Diversity and phylogenetic analyses of bacterial symbionts in three whitefly species from Southeast Europe. Insects, 8(4), 113.
- Tang, X. T., Cai, L., Shen, Y., & Du, Y. Z. (2018). Diversity and evolution of the endosymbionts of Bemisia tabaci in China. PeerJ, 6, 5516.
- Thao, M. L., & Baumann, P. (2004a). Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Applied and Environmental Microbiology, 70(6), 3401-3406.
- Thao, M. L., & Baumann, P. (2004b). Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Current Microbiology, 48, 140-144.
- Tsagkarakou, A., Mouton, L., Kristoffersen, J. B., Dokianakis, E., Grispou, M., & Bourtzis, K. (2012). Population genetic structure and secondary endosymbionts of Q Bemisia tabaci (Hemiptera: Aleyrodidae) from Greece. Bulletin of Entomological Research, 102(3), 353-365
- Xue, X., Li, S. J., Ahmed, M. Z., De Barro, P. J., Ren, S. X., & Qiu, B. L. (2012). Inactivation of Wolbachia reveals its biological roles in whitefly host. PLoS One, 7(10), 48148.
- Zchori-Fein, E., & Brown, J. K. (2002). Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Annals of the Entomological Society of America, 95(6), 711-718.
- Zchori-Fein, E., Lahav, T., & Freilich, S. (2014). Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Frontiers in Microbiology, 5, 310. doi: 10.3389/fmicb.2014.00310.
İki Beyazsinek Türünde (Hemiptera: Aleyrodidae) Sekonder Endosimbiyont Bakterilerin Kompozisyonu
Year 2024,
Volume: 19 Issue: 2, 39 - 46, 31.12.2024
Zülal Tat
,
Erhan Koçak
Abstract
Geniş konukçu dizisine sahip olan Tütün beyazsineği Bemisia tabaci ve Sera beyazsineği Trialeurodes vaporariorum tüm dünyada tarımsal alanlarda var olan en önemli bitki koruma sorunları içerisinde ilk sıralarda yer almaktadır. Çalışma kapsamında Antalya İlinde beş farklı lokasyondaki seralarda domateslerden toplanan beyazsinekler T. vaporariorum ve B. tabaci popülasyonlarında endosimbiyont bakteriler Wolbachia, Rickettsia ve Arsenophonus’un bulaşı durumu moleküler yöntemlerle saptanmıştır. Bu çalışma, Türkiye’de T. vaporariorum popülasyonlarındaki endosimbiyontlar için yapılan ilk çalışmadır. Her üç endosymbiont T. vaporariorum ve B. tabaci populasyonlarında saptanmıştır. Her iki beyazsinek popülasyonunda en sık bulunan endosimbiont Arsenophonus olurken Wolbachia, T. vaporariorum’da ve Rickettsia ise B. tabaci’de yüksek oranda belirlenmiştir. Ayrıca, her iki türe ait bireylerdeki endosimbiyont kompozisyonları tekli, ikili ve üçlü olarak ortaya konulmuştur. Wolbachia (W) and Rickettsia (R) her iki beyazsinek türünde de birlikte bulunmamıştır. Buna karşın tekli, üçlü ve diğer ikili kombinasyonlar bireylerde belirlenmiştir. Ancak her iki türün popülasyonlarından birkaç bireyde herhangi bir enfeksiyon görülmemiştir.
Ethical Statement
Bu çalışmanın yazarları olarak herhangi bir etik kurul onay bilgileri beyanımız bulunmadığını bildiririz.
Supporting Institution
ISUBÜ
Project Number
2023-YL1-0205
Thanks
We would like to thank Isparta University of Applied Sciences, Scientific Research Projects Management Unit (BAP) for supporting the Master's thesis with Project No. 2023-YL1-0205.
References
- Alvarez, D. D. L., Hayashida, R., Cavallaro, M. C., Santos, D.M., Santos, L. M., Müller, C., Watanabe, L. F. M., Bello, V. H., Krause-Sakate, R., Hoback, W. W., & Oliveira, R. C. D. (2024). Susceptibility of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) Mediterranean Populations Found in São Paulo, Brazil to 11 Insecticides and Characterization of Their Endosymbionts. Insects, 15(9), 670.
- Barman, M., Samanta, S., Upadhyaya, G., Thakur, H., Chakraborty, S., Samanta, A., & Tarafdar, J. (2022). Unraveling the basis of neonicotinoid resistance in whitefly species complex: Role of endosymbiotic bacteria and insecticide resistance genes. Frontiers in Microbiology, 13, 901793.
- Bing, X. L., Yang, J., Zchori-Fein, E., Wang, X. W., & Liu, S. S. (2013). Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Applied of Environmental Microbiology, 79, 569–575.
- Brumin, M., Kontsedalov, S., & Ghanim, M. (2011). Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Science, 18(1), 57-66.
- Chiel, E., Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Katzir, N., Inbar, M., & Ghanim, M. (2007). Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bulletin of Entomological Research, 97(4), 407-413.
- Clark, M. A., Baumann, L., Munson, M. A., Baumann, P., Campbell, B. C., Duffus, J. E., Osborne, L. S., & Moran, N. A. (1992). The eubacterial endosymbionts of whiteflies (Homoptera: Aleyrodoidea) constitute a lineage distinct from the endosymbionts of aphids and mealybugs. Current Microbiology, 25, 119–123.
- Costa, H. S., Westcot, D. M., Ullman, D. E., Rosell, R., Brown, J. K., & Johnson, M. W. (1995). Morphological variation in Bemisia endosymbionts. Protoplasma, 189, 194–202.
- Erdogan, C., Velioglu, A. S., Gurkan, M. O., Denholm, I., & Moores, G. D. (2021). Detection of resistance to pyrethroid and neonicotinoid insecticides in the greenhouse whitefly, Trialeurodes vaporariorum (Westw.) (Hemiptera: Aleyrodidae). Crop Protection, 146, 105661.
- Ghanim, M., & Kontsedalov, S. (2009). Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Management Science: Formerly Pesticide Science, 65(9), 939-942.
- Ghosh, S., Bouvaine, S., & Maruthi, M. N. (2015). Prevalence and genetic diversity of endosymbiotic bacteria infecting cassava whiteflies in Africa. BMC Microbiology, 15, 93.
- Goto, S., Anbutsu, H., & Fukatsu, T. (2006). Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Applied and Environmental Microbiology, 72(7), 4805-4810.
- Gottlieb, Y., Ghanim, M., Chiel, E., Gerling, D., Portnoy, V., Steinberg, S., & Zchori-Fein, E. (2006). Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Applied and Environmental Microbiology, 72(5), 3646-3652.
- Guay, J. F., Boudreault, S., Michaud, D., & Cloutier, C. (2009). Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. Journal of Insect Physiology, 55(10), 919-926.
- Gueguen, G., Vavre, F., Gnankine, O., Peterschmitt, M., Charif, D., Chiel, E., & Fleury, F. (2010). Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Molecular Ecology, 19(19), 4365-4376.
- Guo, L., Lv, H., Tan, D., Liang, N., Guo, C., & Chu, D. (2020). Resistance to insecticides in the field and baseline susceptibility to cyclaniliprole of whitefly Bemisia tabaci (Gennadius) in China. Crop protection, 130, 105065.
- Hill, B. (1969). A morphological comparison between two species of whitefly, Trialeurodes vaporariorum (Westw.) and Bemisia tabaci (Genn.) (Homoptera: Aleurodidae) which occur on tobacco in the Transvaal. Phytophylactica, 1, 127-146.
- Jones D. R. (2003). Plant viruses transmitted by whiteflies. European Journal of Plant Pathology, 109(3), 195-219.
- Kareem, A. A., Logan, S. A., Port, G., & Wolff, K. (2020). Bemisia tabaci in Iraq: Population structure, endosymbiont diversity and putative species. Journal of Applied Entomology, 144(4), 297-307.
- Karut, K., & Tok, B. (2014). Secondary endosymbionts of Turkish Bemisia tabaci (Gennadius) populations. Phytoparasitica, 42, 413-419.
- 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.
- Kontsedalov, S., Zchori‐Fein, E., Chiel, E., Gottlieb, Y., Inbar, M., & Ghanim, M. (2008). The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science: Formerly Pesticide Science, 64(8), 789-792.
- Lapidot, M., Legg, J. P., Wintermantel, W. M., & Polston, J. E. (2014). Management of whitefly-transmitted viruses in open-field production systems. In Advances in virus research, 90, 147-206.
- Li, H., Jiang, Z., Zhou, J., Liu, X., Zhang, Y., & Chu, D., (2023). Ecological factors associated with the distribution of Bemisia tabaci cryptic species and their facultative endosymbionts. Insects, 14(3), 252.
- Liu, X. D. & Guo, H. F. (2019). Importance of endosymbionts Wolbachia and Rickettsia in insect resistance development. Current Opinion in Insect Science, 33, 84–90.
- 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.
- Milenovic, M., Ghanim, M., Hoffmann, L., & Rapisarda, C. (2022). Whitefly endosymbionts: IPM opportunity or tilting at windmills? Journal of Pest Science, 95(2), 543-566.
- Milenovic, M., Massimino Cocuzza, G. E., Suma, P., & Farina, A. (2023). Geographic distribution of Bemisia tabaci species in Sicily and patterns in facultative endosymbiont community composition. Journal of Applied Entomology, 147(10), 908-915.
- Nirgianiki, A., Banks, G. K., Frohlich, D. R., Veneti, Z., Braig, H. R., Miller, T. A., & Bourtzis, K. (2003). Wolbachia infections of the whitefly Bemisia tabaci. Current Microbiology, 47, 0093-0101.
- Opatovsky, I., Santos-Garcia, D., Ruan, Z., Lahav, T., Ofaim, S., Mouton, L., Barbe, V., Jiang, J., Zchori-Fein, E., & Freilich, S. (2018). Modeling trophic dependencies and exchanges among insects' bacterial symbionts in a host-simulated environment. BMC Genomics, 19, 1–14.
- Pan, H. P., Chu, D., Liu, B. M., Xie, W., Wang, S. L., Wu, Q. J., Xu, B. Y., Zhang, Y. J. (2013). Relative amount of symbionts in insect hosts changes with host-plant adaptation and insecticide resistance. Environmental entomology, 42(1), 74-78.
- Raina, H. S., Rawal, V., Singh, S., Daimei, G., Shakarad, M., & Rajagopal, R. (2015). Elimination of Arsenophonus and decrease in the bacterial symbionts diversity by antibiotic treatment leads to increase in fitness of whitefly, Bemisia tabaci. Infection, Genetics and Evolution, 32, 224-230.
- Rossitto De Marchi, B., & Smith, H. A. (2020). Bacterial endosymbiont diversity among Bemisia tabaci (Hemiptera: Aleyrodidae) populations in Florida. Insects, 11(3), 179.
- Shi, P. Q., Wang, L., Chen, X. Y., Wang, K., Wu, Q. J., Turlings, T. C., Zhang, P. J., & Qiu, B. L. (2024). Rickettsia transmission from whitefly to plants benefits herbivore insects but is detrimental to fungal and viral pathogens. Mbio, 15(3), 02448-23.
- Singh, S.T., Priya, N.G., Kumar, J., Rana, V.S., Ellango, R., Joshi, A., Priyadarshini, G., Asokan, R., & Rajagopal, R. (2012). Diversity and phylogenetic analysis of endosymbiotic bacteria from field caught Bemisia tabaci from different locations of North India based on 16S rDNA library screening. Infection, Genetics and Evolution, 12(2), 411-419.
- Sivasupramaniam, S., & Watson, T. F. (2000). Selection for fenpropathrin and fenpropathrinacephate resistance in the silverleaf whitefly (Homoptera: Aleyrodidae). Journal of Economic Entomology, 93(3), 949-954.
- Skaljac, M., Zanic, K., Ban, S. G., Kontsedalov, S., & Ghanim, M. (2010). Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiology, 10(1), 1-15.
- Skaljac, M., Kanakala, S., Zanic, K., Puizina, J., Lepen Pleic, I., & Ghanim, M. (2017). Diversity and phylogenetic analyses of bacterial symbionts in three whitefly species from Southeast Europe. Insects, 8(4), 113.
- Tang, X. T., Cai, L., Shen, Y., & Du, Y. Z. (2018). Diversity and evolution of the endosymbionts of Bemisia tabaci in China. PeerJ, 6, 5516.
- Thao, M. L., & Baumann, P. (2004a). Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Applied and Environmental Microbiology, 70(6), 3401-3406.
- Thao, M. L., & Baumann, P. (2004b). Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Current Microbiology, 48, 140-144.
- Tsagkarakou, A., Mouton, L., Kristoffersen, J. B., Dokianakis, E., Grispou, M., & Bourtzis, K. (2012). Population genetic structure and secondary endosymbionts of Q Bemisia tabaci (Hemiptera: Aleyrodidae) from Greece. Bulletin of Entomological Research, 102(3), 353-365
- Xue, X., Li, S. J., Ahmed, M. Z., De Barro, P. J., Ren, S. X., & Qiu, B. L. (2012). Inactivation of Wolbachia reveals its biological roles in whitefly host. PLoS One, 7(10), 48148.
- Zchori-Fein, E., & Brown, J. K. (2002). Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Annals of the Entomological Society of America, 95(6), 711-718.
- Zchori-Fein, E., Lahav, T., & Freilich, S. (2014). Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Frontiers in Microbiology, 5, 310. doi: 10.3389/fmicb.2014.00310.