Abstract
Begomoviruses are transmitted by a single species of vector insect, the whitefly Bemisia tabaci, in a circulative manner. However, the mechanisms of this strict vector specificity have not been clarified. By immunoelectron microscopy, we showed that a begomovirus, Tomato yellow leaf curl virus (TYLCV), can enter midgut epithelial cells of the vector whitefly B. tabaci but not those of a nonvector whitefly, Trialeurodes vaporariorum, belonging to the same family. In midgut epithelial cells of viruliferous B. tabaci, the virus was localized in vesicle-like structures, suggesting endocytosis as an entry mechanism. These structures were also observed in midgut cells of nonviruliferous B. tabaci that had fed on healthy plants and in those of the nonvector T. vaporariorum that had fed on virus-infected plants. Vesicles containing TYLCV particles were observed most frequently in cells in the anterior part of the descending midgut, suggesting that this is the major entry site. These results clearly demonstrated that the virus-containing vector and nonvector whiteflies differ in the cellular localization of the virus and strongly suggest that a critical step in determining the vector insect specificity of begomoviruses is the entry of the viruses into midgut epithelial cells.
Similar content being viewed by others
References
Abouzid AM, Barth A, Jeske H (1988) Immunogold labeling of the abutilon mosaic virus in ultrathin sections of epoxy resin embedded leaf tissue. J Ultrastruct Res 99:38–47
Acosta EG, Castilla V, Damonte EB (2008) Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin mediated endocytosis. J Gen Virol 89:474–484
Ammar El-D, Gargani D, Lett JM, Peterschmitt M (2009) Large accumulations of maize streak virus in the filter chamber and midgut cells of the leafhopper vector Cicadulina mbila. Arch Virol 154:255–262
Brault V, Herrbach E, Reinbold C (2007) Electron microscopy studies on luteovirid transmission by aphids. Micron 38:302–312
Brown JK, Fauquet CM, Briddon RW, Zerbini M, Moriones E, Navas-Castillo J (2012) Family Geminiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy, classification and nomenclature of viruses: ninth report of the international committee on taxonomy of viruses. Elsevier, San Diego, pp 351–373
Czosnek H (ed) (2007) Tomato yellow leaf curl virus disease: management, molecular biology, breeding for resistance. Springer, Dordrecht, The Netherlands
Czosnek H, Ghanim M, Ghanim M (2002) The circulative pathway of begomoviruses in the whitefly vector Bemisia tabaci—insights from studies with Tomato yellow leaf curl virus. Ann Appl Biol 140:215–231
Engel S, Heger T, Mancini R, Herzog F, Kartenbeck J, Hayer A, Helenius A (2011) Role of endosomes in Simian virus 40 entry and infection. J Virol 85:4198–4211
Ghanim M, Morin S, Czosnek H (2001) Rate of Tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91:188–196
Hunter WB, Hiebert E, Webb E, Tsai JH, Polston JE (1998) Location of geminiviruses in the whitefly Bemisia tabaci (Homoptera: Aleyrodidae). Plant Dis 82:1147–1151
Leshkowitz D, Gazit S, Reuveni E, Ghanim M, Czosnek H, McKenzie C, Shatters RL, Brown JK (2006) Whitefly (Bemisia tabaci) genome project: analysis of sequenced clones from egg, instar, and adult (viruliferous and non-viruliferous) cDNA libraries. BMC Genomics 7:79. doi:10.1186/1471-2164-7-79
Luisoni E, Milne RG, Vecchiati M (1995) Purification of tomato yellow leaf curl geminivirus. New Microbiol 18:253–260
Medina V, Pinner MS, Bedford ID, Achon MA, Gemeno C, Markham PG (2006) Immunolocalization of Tomato yellow leaf curl Sardinia virus in natural host plants and its vector Bemisia tabaci. J Plant Pathol 88:299–308
Morin S, Ghanim M, Zeidan M, Czosnek H, Verbeek M, van den Heuvel JFJM (1999) A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of Tomato yellow leaf curl virus. Virology 256:75–84
Morin S, Ghanim M, Sobol I, Czosnek H (2000) The GroEL protein of the whitefly Bemisia tabaci interacts with the coat protein of transmissible and nontransmissible begomoviruses in the yeast two-hybrid system. Virology 276:404–416
Ohnishi J, Kitamura T, Terami F, Honda K (2009) A selective barrier in the midgut epithelial cell membrane of the nonvector whitefly Trialeurodes vaporariorum to Tomato yellow leaf curl virus uptake. J Gen Plant Pathol 75:131–139
Rosell RC, Davidson EW, Jancovich JK, Hendrix DL, Brown JK (2003) Size limitations in the filter chamber and digestive tract of nymphal and adult Bemisia tabaci whiteflies (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 96:544–552
Seddas P, Boissinot S, Strub JM, Van Dorsselaer A, Van Regenmortel MHV, Pattus F (2004) Rack-1, GAPDH3, and actin: proteins of Myzus persicae potentially involved in the transcytosis of beet western yellows virus particles in the aphid. Virology 325:399–412
Wei T, Chen H, Ichiki-Uehara T, Hibino H, Omura T (2007) Entry of Rice dwarf virus into cultured cells of its insect vector involves clathrin-mediated endocytosis. J Virol 81:7811–7815
Yang X, Thannhauser TW, Burrows M, Cox-Foster D, Gildow FE, Gray SM (2008) Coupling genetics and proteomics to identify aphid proteins associated with vector-specific transmission of polerovirus (Luteoviridae). J Virol 82:291–299
Acknowledgments
We thank Shigenori Ueda from National Agriculture and Food Research Organization, Kyushu Okinawa Agricultural Research Center, for providing an infectious TYLCV clone. We thank Hiroshi Oida from Chiba Prefectural Agriculture and Forestry Research Center and Izumi Ohta from the National Institute of Vegetable and Tea Science for providing Bemisia tabaci biotype Q and Trialeurodes vaporariorum.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Uchibori, M., Hirata, A., Suzuki, M. et al. Tomato yellow leaf curl virus accumulates in vesicle-like structures in descending and ascending midgut epithelial cells of the vector whitefly, Bemisia tabaci, but not in those of nonvector whitefly Trialeurodes vaporariorum . J Gen Plant Pathol 79, 115–122 (2013). https://doi.org/10.1007/s10327-012-0426-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-012-0426-2