Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-05-10T21:45:13.631Z Has data issue: false hasContentIssue false
  • English
  • Français

Specificity of accumulation and transmission of tomato spotted wilt virus (TSWV) in two genera, Frankliniella and Thrips (Thysanoptera: Thripidae)

Published online by Cambridge University Press:  09 March 2007

T. Inoue ,
T. Sakurai ,
T. Murai  and
T. Maeda
T. Inoue
Affiliation:
Research Institute for Bioresources, Okayama University, Kurashiki 710-0046, Japan
T. Sakurai*
Affiliation:
Department of Biology and Environmental Sciences, National Agricultural Research Center for Tohoku Region, Morioka 020-0198, Japan
T. Murai
Affiliation:
Research Institute for Bioresources, Okayama University, Kurashiki 710-0046, Japan
T. Maeda
Affiliation:
Research Institute for Bioresources, Okayama University, Kurashiki 710-0046, Japan
*
*Fax: +81 19 643 3466 E-mail: tsakurai@affrc.go.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

The accumulation and transmission of tomato spotted wilt virus (TSWV) was examined in second instar larvae and adults of two thrips genera, Frankliniella and Thrips. The species tested were F. occidentalis (Pergande), F. intonsa (Trybom), T. tabaciLindeman, T. setosus Moulton, T. palmi Karny and T. hawaiiensis (Morgan). In a standard petunia leaf disc assay, the efficiencies of TSWV transmission by two species of Frankliniella were higher than those of any Thrips species in the adult stage. A triple antibody sandwich enzyme-linked immunosorbent assay (TAS-ELISA) showed that large amounts of the TSWV-nucleocapsid (N) protein were present in the ELISA-positive larvae of each species, with the exception of T. palmi. The ELISA titre of and the proportion of virus-infected individuals of the two Frankliniella species increased or did not significantly change from the larval to the adult stages, whereas those of the four Thrips species decreased significantly. These results show that the specificity of virus transmission by adult thrips is probably affected by the amount of viral N protein accumulation in the adults and that the accumulation pattern from the larval to the adult stages is in between the two genera tested in the present study.

Type
Research Article
Information
Bulletin of Entomological Research , Volume 94 , Issue 6 , December 2004 , pp. 501 - 507
Copyright
Copyright © Cambridge University Press 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adkins, S. (2000) Tomato spotted wilt virus – positive stgif towards negative success. Molecular Plant Pathology 1, 151–157.CrossRefGoogle ScholarPubMed
Ammar, E.D. (1994) Propagative transmission of plant and animal viruses by insects: factors affecting vector specificity and competence. Advances in Disease Vector Research 10, 289–331.CrossRefGoogle Scholar
Anon. (1993) Distribution maps of pests. Series A: Map No. 538, Frankliniella occidentalis. International Institute of Entomology, London, CAB International.Google Scholar
Brødsgaard, H.F. (1989) Frankliniella occidentalis (Thysanoptera: Thripidae) – a new pest in Danish glasshouses. A review. Tidsskrift for Planteavl 93, 83–91.Google Scholar
Chatzivassiliou, E.K., Peters, D. & Katis, N.I. (2002) The efficiency by which Thrips tabaci populations transmit Tomato spotted wilt virus depends on their host preference and reproductive strategy. Phytopathology 92, 603–609.CrossRefGoogle ScholarPubMed
Clark, M.F. & Adams, A.N. (1977) Characteristics of the microplate method of enzyme linked immunosorbent assay for the detection of plant viruses. Journal of General Virology 34, 475–483.CrossRefGoogle ScholarPubMed
Fujisawa, I., Tanaka, K. & Ishii, M. (1988) Tomato spotted wilt virus transmission by three species of thrips, Thrips setosus, Thrips tabaci, Thrips palmi. Annals of the Phytopathological Society of Japan 54 (Abstract), 392 (in Japanese).Google Scholar
German, T.L., Ullman, D.E. & Moyer, J.W. (1992) Tospoviruses: diagnosis, molecular biology, phylogeny, and vector relationships. Annual Review of Phytopathology 30, 315–348.CrossRefGoogle ScholarPubMed
Goldbach, R. & Peters, D. (1994) Possible cause of the emergence of tospovirus diseases. Seminars in Virology 5, 113–120.CrossRefGoogle Scholar
Lakshmi, K.V., Wightman, J.A., Reddy, D.V.R., Ranga, Rao, G.V., Buiel, A.A.M., Reddy D.D.R. (1995) Transmission of peanut bud necrosis virus by Thrips palmi in India. pp. 179–184Parker, B.L., Skinner, M., Lewis, T.(Eds) Thrips biology and management. New York, Plenum Press.CrossRefGoogle Scholar
Matsuoka, Y., Chen, S.Y. & Compans, R.W. (1991) Bunyavirus protein transport and assembly. pp. 161–179 in Kolakofsky, D.. (Ed.) Bunyaviridae. Berlin Heidelberg, Springer-Verlag.Google ScholarPubMed
Mau, R.F.L., Bautista, R., Cho, J.J., Ullman, D.E., Gusukuma-Minuto, L. & Custer, D.M. (1991) Factors affecting the epidemiology of TSWV in field crops: comparative virus acquisition efficiency of vectors and suitability of alternate hosts to Frankliniella occidentalis (Pergande). 21–27 in Hus, H.T., Lawson, R.H. (Eds) Virus–thrips–plant interaction of tomato spotted wilt virus, Proceedings of a USDA Workshop, Maryland, 18–19. April 1990, Springfield, National Technical Information Service, United States Department of Agriculture, Agricultural Research Service, ARS-87.Google Scholar
Mound, L.A. (1996) The Thysanoptera vector species of tospoviruses. pp. 298–309Kuo, C.G. (Ed.) Proceedings of the International Symposium on Tospoviruses and Thrips of Floral and Vegetable Crops, Taichung, Taiwan,7–10 November 1995Leiden, Netherlands,ISHI Acta Horticulturae 431.CrossRefGoogle Scholar
Mumford, R.A., Barker, I. & Wood, K.R. (1996) The biology of the tospoviruses. Annals of Applied Biology 128, 159–183.CrossRefGoogle Scholar
Murai, T. & Loomans, A.J.M. (2001) Evaluation of an improved method for mass-rearing of thrips and a thrips parasitoid. Entomologia Experimentalis et Applicata 101, 281–289.CrossRefGoogle Scholar
Murphy, F.A., Fauquet, C.M., Bishop, P.H.L., Ghabrial, S.A., Jarvis, A.W., Martelli, G.P., Mayo, M.A. & Summers, M.D. (1995) Virus taxonomy. Sixth report of the international committee on taxonomy of viruses. Archives of Virology 10, 313–314.Google Scholar
Nagata, T., Inoue-Nagata, A.K., Smid, H.M., Goldbach, R. & Peters, D. (1999) Tissue tropism related to vector competence of Frankliniella occidentalis for tomato spotted wilt tospovirus. Journal of General Virology 80, 507–515.CrossRefGoogle ScholarPubMed
Nagata, T., Inoue-Nagata, A.K., van Lent, J., Goldbach, R., Peters, D. (2002) Factors determining vector competence and specificity for transmission of Tomato spotted wilt virus. Journal of General Virology 83, 663–671.CrossRefGoogle ScholarPubMed
Nault, L.R. (1997) Arthropod transmission of plant viruses: a new synthesis. Annals of the Entomological Society of America 90, 521–541.CrossRefGoogle Scholar
Ohnishi, J., Tsuda, S., Fujisawa, I., Hosokawa, D. & Tomaru, K. (1996) Immunolocalization of tomato spotted wilt virus nucleocapsid protein in larval and pupal thrips (Thrips setosus): a time-course analysis. 325–332 in Kuo, C.G. (Ed.) Proceedings of the International Symposium on Tospoviruses and Thrips of Floral and Vegetable Crops, Taichung, Taiwan7–10 November 1995,Leiden, Netherlands,ISHI, Acta Horticulturae 431.Google Scholar
Ohnishi, J., Hosokawa, D., Murai, T. & Tsuda, S. (1999) A simple rearing system for Thrips setosus Moulton (Thysanoptera: Thripidae) using a leaf cage method for the transmission experiment of tomato spotted wilt tospovirus. Applied Entomology and Zoology 34, 497–500.CrossRefGoogle Scholar
Paliwal, Y.C. (1976) Some characteristics of the thrips vector relationship of tomato spotted wilt virus in Canada. Canadian Journal of Botany 54, 402–405.CrossRefGoogle Scholar
Portela, A. & Digard, P. (2002) The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. Journal of General Virology 83, 723–734.CrossRefGoogle ScholarPubMed
R Development Core Team (2003) R: A language and environment for statistical computing, version 1.7.1. Vienna Austria. R Foundation for Statistical Computing.Google Scholar
Richmond, K.E., Chenault, K., Sherwood, J.L. & German, T.L. (1998) Characterization of nucleic acid binding properties of tomato spotted wilt virus nucleocapsid protein. Virology 248, 6–11.CrossRefGoogle ScholarPubMed
Sakimura, K. (1962) The present status of thrips-borne viruses. 33–40Maramorosch, K. (Ed.) Biological transmission of disease agents. New York, Academic Press.CrossRefGoogle Scholar
Sakimura, K. (1963) Frankliniella fusca, an additional vector for the tomato spotted wilt virus, with notes on Thrips tabaci, another vector. Phytopathology 53, 412–415.Google Scholar
Sakimura, K. (1969) A comment on the colour forms of Frankliniella schultzei (Thysanoptera: Thripidae) in relation to transmission of the tomato-spotted wilt virus. Pacific Insects 11, 761–762.Google Scholar
Sakurai, T. (2004) Transmission of Tomato spotted wilt virus by the dark form of Frankliniella schultzei (Thysanoptera: Thripidae) originating in tomato fields in Paraguay. Applied Entomology and Zoology 39, 189–194.CrossRefGoogle Scholar
Sakurai, T., Murai, T., Maeda, T., Tsumuki, H. (1998) Sexual differences in transmission and accumulation of tomato spotted wilt virus in its vector Frankliniella occidentalis (Thysanoptera: Thripidae). Applied Entomology and Zoology 33, 583–588.CrossRefGoogle Scholar
SAS, Institute Inc. (1998) StatView version 5. Cary, North Carolina, SAS Institute Inc.Google Scholar
Smith, K.M. (1931) Thrips tabaci as a vector of plant virus disease. Nature 127, 852–853.CrossRefGoogle Scholar
Sokal, R.R. & Rohlf, F.J. (1995) Biometry: the principles and practice of statistics in biological research 3rd edn. New YorkW.H. Freeman and Company.Google Scholar
Steinecke, P., Heinze, C., Oehmen, E., Adam, G. & Schreier, P.H. (1998) Early events of tomato spotted wilt transcription and replication in protoplasts. Microbiologica 21, 263–268.Google ScholarPubMed
Tordo, N., de Haan, P., Goldbach, R., Poch, O. (1992) Evolution of negative-stranded RNA genomes. Seminars in Virology 3, 341–357.Google Scholar
Tsuda, S., Hanada, K., Minobe, Y., Kameya-Iwaki, M. & Tomaru, K. (1993) Tomato spotted wilt virus isolated in Japan are grouped into two strains. Annals of the Phytopathological Society of Japan 59, 626–634.CrossRefGoogle Scholar
Tsuda, S., Fujisawa, I., Ohnishi, J., Hosokawa, D. & Tomaru, K. (1996) Localization of tomato spotted wilt tospovirus in larvae and pupae of the insect vector Thrips setosus. Phytopathology 86, 1199–1203.CrossRefGoogle Scholar
Uhrig, J.F., Soellick, T.-R., Minke, C.J., Philipp, C., Kellmann, J.-W. & Schreier, P.H. (1999) Homotypic interaction and multimerization of nucleocapsid protein of tomato spotted wilt tospovirus: identification and characterization of two interacting domains. Proceedings of the National Academy of Sciences of the United States of America 96, 55–60.CrossRefGoogle ScholarPubMed
Ullman, D.E., Cho, J.J., Mau, R.F.L., Westcot, D.M. & Custer, D.M. (1992) A midgut barrier to tomato spotted wilt virus acquisition by adult western flower thrips. Phytopathology 82, 1333–1342.CrossRefGoogle Scholar
Ullman, D.E., German, T.L., Sherwood, J.L., Westcot, D.M. & Cantone, F.A. (1993) Tospovirus replication in insect vector cells: immunocytochemical evidence that the nonstructural protein encoded by the S RNA of tomato spotted wilt tospovirus is present in thrips vector cells. Phytopathology 83, 456–463.CrossRefGoogle Scholar
Ullman, D.E., Sherwood, J.L. & German, T.L. (1997) Thrips as vectors of plant pathogens. pp. 539–565 in Lewis, T. (Ed.) Thrips as crop pests. Wallingford, CAB International.Google Scholar
Ullman, D.E., Meideros, R., Campbell, L.R., Whitfield, A.E., Sherwood, J.L. & German, T.L. (2002) Thrips as vectors of tospoviruses. Advances in Botanical Research 36, 113–140.CrossRefGoogle Scholar
van de Wetering, F., Goldbach, R. & Peters, D. (1996) Tomato spotted wilt tospovirus ingestion by first instar larvae of Frankliniella occidentalis is a prerequisite for transmission. Phytopathology 86, 900–905.CrossRefGoogle Scholar
Webb, S.E., Kok-Yokomi, M.L. & Tsai, J.H. (1997) Evaluation of Frankliniella bispinosa as a potential vector of tomato spotted wilt virus. Phytopathology 87S, 102.Google Scholar
Wijkamp, I., Peters, D. (1993) Determination of the median latent period of two tospoviruses in Frankliniella occidentalis, using a novel leaf disk assay. Phytopathology 83, 986–991.CrossRefGoogle Scholar
Wijkamp, I., van Lent, J., Kormelink, R., Goldbach, R., Peters, D. (1993) Multiplication of tomato spotted wilt virus in its insect vector, Frankliniella occidentalis. Journal of General Virology 74, 341–349.CrossRefGoogle ScholarPubMed
Wijkamp, I., Almarza, N., Goldbach, R. & Peters, D. (1995) Distinct levels of specificity in thrips transmission of tospoviruses. Phytopathology 85, 1069–1074.CrossRefGoogle Scholar
Yeh, S.-D., Lin, Y.-C., Cheng, Y.-H., Jih, C.-L., Chen, M.-J. & Chen, C.-C. (1992) Identification of tomato spotted wilt-like virus on watermelon in Taiwan. Plant Disease 76, 835–840.CrossRefGoogle Scholar