Abstract
We studied the presence of a potential transmission barrier that blocks Tomato yellow leaf curl virus in the nonvector greenhouse whitefly, Trialeurodes vaporariorum. Because T. vaporariorum can ingest and retain the virus after acquisition feeding on an infected plant, comparable to the vector whitefly Bemisia tabaci, circumstance evidence suggested that a transmission barrier presents at location(s) where the virus moves from the digestive tract lumen to the hemolymph. To provide direct evidence for the site of a transmission barrier in the nonvector insect, we compared the accumulation levels and localization of the virus between the two species of whiteflies. Quantitative real-time and conventional PCR analysis showed that accumulation of the virus during acquisition feeding and retention after a short acquisition period were indistinguishable between the two species, but the circulation of the virus within the whiteflies differed significantly between the species. In an immunofluorescence analysis using an antibody specific to the coat protein of the virus, the virus was restricted to the luminal surface of the midgut epithelial cells and did not enter their cytoplasm or that of the salivary glands in T. vaporariorum. In contrast, the virus was localized within the cytoplasm of the midgut epithelial cells and in the paired salivary glands of B. tabaci adults. This direct evidence shows that a selective transmission barrier at the luminal membrane surface of midgut epithelial cells in the nonvector whitefly blocks entrance of the virus into the midgut epithelial cells, resulting in incompetence as a vector of the virus.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Antignus Y, Perlsman M, Ben-Yoseph R, Cohen S (1993) The interaction of Tomato yellow leaf curl virus with its whitefly vector, Bemisia tabaci. Phytoparasitica 21:174–175
Brault V, Herrbach É, Reinbold C (2007) Electron microscopy studies on luteovirid transmission by aphids. Micron 38:302–312
Caciagli P, Bosco D (1997) Quantitation over time of Tomato yellow leaf curl geminivirus DNA in its whitefly vector. Phytopathology 87:610–613
Cohen S, Nitzany FE (1966) Transmission and host range of the Tomato yellow leaf curl virus. Phytopathology 56:1127–1131
Czosnek H (2007) Interaction of Tomato yellow leaf curl virus with its whitefly vector. In: Czosnek H (ed) Tomato yellow leaf curl virus disease: management, molecular biology, breeding for resistance. Springer, Berlin, pp 157–170
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
Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349
Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) (2005) Virus taxonomy. Classification and nomenclature of viruses. Family Geminiviridae. Eighth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, London, pp 301–326
Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821
Ghanim M, Medina V (2007) Localization of Tomato yellow leaf curl virus in its whitefly vector Bemisia tabaci. In: Czosnek H (ed) Tomato yellow leaf curl virus disease: management, molecular biology. breeding for resistance. Springer, Berlin, pp 171–183
Ghanim M, Morin S, Czosnek H (2001a) Rate of Tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91:188–196
Ghanim M, Rosell RC, Campbell LR, Czosnek H, Brown JK, Ullman DE (2001b) Digestive, salivary, and reproductive organs of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) B type. J Morphol 248:22–40
Ghanim M, Sobol I, Ghanim M, Czosnek H (2007) Horizontal transmission of begomoviruses between Bemisia tabaci biotypes. Arthropod Plant Interact 1:195–204
Gray S, Gildow FE (2003) Luteovirus–aphid interactions. Annu Rev Phytopathol 41:539–566
Harris KF, Pesic-Van Esbroeck Z, Duffus JE (1996) Morphology of the sweet potato whitefly, Bemisia tabaci (Homoptera, Aleyrodidae) relative to virus transmission. Zoomorphology 116:143–156
Kato K, Onuki M, Fuji S, Hanada K (1998) The first occurrence of Tomato yellow leaf curl virus in tomato (Lycopersicon esculentum Mill.) in Japan. Ann Phytopathol Soc Japan 64:552–559
Mason G, Caciagli P, Accotto GP, Noris E (2008) Real-time PCR for the quantitation of Tomato yellow leaf curl Sardinia virus in tomato plants and in Bemisia tabaci. J Virol Methods 147:282–289
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
Ohnishi J, Knight LM, Hosokawa D, Fujisawa I, Tsuda S (2001) Replication of Tomato spotted wilt virus after ingestion by adult Thrips setosus is restricted to midgut epithelial cells. Phytopathology 91:1149–1155
Rosell RC, Torres-Jerez I, Brown JK (1999) Tracing the geminivirus-whitefly transmission pathway by polymerase chain reaction in whitefly extracts, saliva, hemolymph, and honeydew. Phytopathology 89:239–246
Rouzé-Jouan J, Terradot L, Pasquer F, Tanguy S, Giblot Ducray-Bourdin D (2001) The passage of Potato leafroll virus through Myzus persicae gut membrane regulates transmission efficiency. J Gen Virol 82:17–23
Rubinstein G, Czosnek H (1997) Long-term association of Tomato yellow leaf curl virus with its whitefly vector Bemisia tabaci: effect on the insect transmission capacity, longevity and fecundity. J Gen Virol 78:2683–2689
Ueda S (2008) The epidemics of Tomato yellow leaf curl disease in Japan and its preventive managements. Plant Prot 62:414–417 (in Japanese)
Ueda S, Kimura T, Onuki M, Hanada K, Iwanami T (2004) Three distinct groups of isolates of Tomato yellow leaf curl virus in Japan and construction of an infectious clone. J Gen Plant Pathol 70:232–238
Zeidan M, Czosnek H (1991) Acquisition of Tomato yellow leaf curl virus by the whitefly Bemisia tabaci. J Gen Virol 72:2607–2614
Acknowledgments
This study was supported in part by a grant from the Research Project for Utilizing Advanced Technologies in Agriculture, Forestry, and Fisheries (No. 18002) from the Ministry of Agriculture, Forestry, and Fisheries of Japan.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ohnishi, J., Kitamura, T., Terami, F. et al. 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 (2009). https://doi.org/10.1007/s10327-009-0147-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-009-0147-3