Relationships of virus titers and transmission rates among sympatric and allopatric virus isolates and thrips vectors support local adaptation

Gray, S. M. & Banerjee, N. Mechanisms of arthropod transmission of plant and animal viruses. MMBR. 63, 128–148 (1999).

Agarwal, A., Parida, M. & Dash, P. K. Impact of transmission cycles and vector competence on global expansion and emergence of arboviruses. Rev. Med. Virol. 27, e1941 (2017).

• Google Scholar

Stumpf, C. F. & Kennedy, G. G. Effects of tomato spotted wilt virus (TSWV) isolates, host plants, and temperature on survival, size, and development time of Frankliniella fusca. Entomol. Exp. Appl. 114, 215–225 (2005).

• Google Scholar

Stumpf, C. F. & Kennedy, G. G. Effects of tomato spotted wilt virus isolates, host plants, and temperature on survival, size, and development time of Frankliniella occidentalis. Entomol. Exp. Appl. 123, 139–147 (2007).

• Google Scholar

Hogenhout, S. A., Ammar, E. -D., Whitfield, A. E., & Redinbaugh, M. G. Insect Vector Interactions with Persistently Transmitted Viruses. Ann. Rev. Entomol. 46, 327–359 (2008).

Ammar, E.-D., Gingery, R. E. & Madden, L. Transmission efficiency of three isolates of maize stripe tenuivirus in relation to virus titre in the planthopper vector. Plant Pathol. 44, 239–243 (1995).

• Google Scholar

Ammar, E.-D. Effect of European wheat striate mosaic, acquired transovarially, on the biology of its planthopper vector Javesella pellucida. Ann. Appl. Biol. 79, 203–213 (1975).

• Google Scholar

Gill, C. C. Cyclical transmissibility of barley yellow dwarf virus from oats with increasing age of infection. Phytopathol. 59, 23–28 (1969).

• Google Scholar

Gray, S. M., Power, A. G., Smith, D. M., Seaman, A. J. & Altman, N. S. Aphid transmission of barley yellow dwarf virus: acquisition access periods and virus concentration requirements. Phytopathol. 81, 539–545 (1991).

• Google Scholar

Pereira, A.-M., Lister, R. M., Barbara, P. J. & Shaner, G. E. Relative transmissibility of barley yellow dwarf virus from sources with differing virus contents. Phytopathol. 79, 1353–1358 (1989).

• Google Scholar

Lett, J.-M. et al. Spatial and temporal distribution of geminiviruses in leafhoppers of the genus Cicadulina monitored by conventional and quantitative polymerase chain reaction. Phytopathol. 92, 65–74 (2002).

• Google Scholar

Whitfield, A. E., Falk, B. W. & Rotenberg, D. Insect vector-mediated transmission of plant viruses. Virol. 479, 278–289 (2015).

• Google Scholar

Inoue, T., Sakurai, T., Murai, T. & Maeda, T. Specificity of accumulation and transmission of tomato spotted wilt virus (TSWV) in two genera, Frankliniella and Thrips (Thysanoptera: Thripidae). Bull. of Entomol. Res. 94, 501–507 (2004).

• CAS
• Google Scholar

Nagata, T., Almeida, A. C. L., Resende, R. O. & DeÁvila, A. C. The competence of four thrips species to transmit and replicate four tospoviruses. Plant Pathol. 53, 136–140 (2004).

• Google Scholar

Okazaki, O. et al. The effect of virus titre on acquisition efficiency of Tomato spotted wilt virus by Frankliniella occidentalis and the effect of temperature on detectable period of the virus in dead bodies. Australasian. Plant Pathol. 40, 120–125 (2011).

• Google Scholar

Rotenberg, D. et al. Variation in Tomato spotted wilt virus titer in Frankliniella occidentalis and its association with frequency of transmission. Phytopathol. 99, 404–10 (2009).

• CAS
• Google Scholar

Jacobson, A. L. & Kennedy, G. G. Specific insect-virus interactions are responsible for variation in competency of different Thrips tabaci isolines to transmit different tomato spotted wilt virus isolates. PLoS ONE 8, e54567 (2013).

Morgan, A. D., Gandon, S. & Buckling, A. The effect of migration on local adaptation in a coevolving host-parasite system. Nature. 437, 253–256 (2005).

Boonham, N. et al. The detection of Tomato spotted wilt virus (TSWV) in individual thrips using real time fluorescent RT-PCR (Taqman). J. Virol. Meth. 101, 37–48 (2002).

• CAS
• Google Scholar

Gandon, S. & Michalakis, Y. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. J. Evol. Biol. 15, 451–462 (2002).

• Google Scholar

Jacobson, A. L., Booth, W., Vargo, E. L. & Kennedy, G. G. Thrips tabaci population genetic structure and polyploidy in relation to competency as a vector of tomato spotted wilt virus. PLoS ONE 8, e54484 (2013).

Cabrera-La Rosa, J. C. & Kennedy, G. G. Thrips tabaci and tomato spotted wilt virus: inheritance of vector competence. Entomol. Expt. et Appl. 124, 161–166 (2007).

• Google Scholar

Halaweh, N. & Poehling, H. M. Inheritance of vector competence by the thrips Ceratothripoides claratris (Shumsher) (Thysanoptera: Thripidae). J. Appl. Entomol. 133, 386–393 (2009).

• Google Scholar

Ogada, P. A., Debener, T. & Poehling, H. M. Inheritance genetics of the trait vector competence in Frankliniella occidentalis (western flower thrips) in the transmission of tomato spotted wilt virus. Ecol. & Evol. 6, 7911–7920 (2016).

• Google Scholar

Rotenberg, D., Jacobson, A. L., Schneweis, D. J. & Whitfield, A. E. Thrips transmission of tospoviruses. Curr. Opin. Virol. 15, 80–89 (2015).

• PubMed
• Google Scholar

Oliver, J. E. & Whitfield, A. E. The genus Tospovirus: Emerging Bunyaviruses that threaten food security. Annu. Rev. Virol. 3, 101–24 (2016).

Ullman, D. E., German, T., Sherwood, J. L., Wescot, D. M. & Cantone, F. A. Immunocytochemical evidence that the nonstructural protein encoded by the S RNA of tomato spotted wilt tospovirus is present in thrips vector cells. Phytopathol. 83, 456–463 (1993).

• CAS
• Google Scholar

Ullman, D. E., Wescot, D. M., Chenaut, K. D., Sherwood, J. L. & German, T. Compartmentalization, intracellular transport, and autophagy of tomato spotted wilt tospovirus proteins in infected thrips cells. Phytopathol. 85, 644–654 (1995).

• Google Scholar

Sin, S. H., McNulty, B. C., Kennedy, G. G. & Moyer, J. W. Viral genetic determinants for thrips transmission of Tomato spotted wilt virus. PNAS. 102, 5168–5173 (2005).

Margaria, P., Bosco, L. & Vallino, M. The NSs protein of Tomato spotted wilt virus is required for persistent infection and transmission by Frankliniella occidentalis. J. Virol. 88, 5788–5802 (2014).

Montero-Astúa, M. et al. Disruption of vector transmission by a plant-expressed viral glycoprotein. MPMI. 27(3), 296–304 (2014).

Montero-Astúa, M., Ullman, D. E. & Whitfield, A. E. Salivary gland morphology, tissue tropism and the progression of tospovirus infection in Frankliniella occidentalis. Virol. 493, 39–51 (2016).

• Google Scholar

Nagata., T., Inoue-Nagata, A. K., Smid, H. M., Goldbach, R. & Peters, D. Tissue tropism related to vector competence of Frankliniella occidentalis for tomato spotted wilt tospovirus. J. Gen. Virol. 80, 507–515 (1999).

Kritzman, A. et al. The route of tomato spotted wilt virus inside the thrips body in relation to transmission efficiency. Archives Virol. 147, 2143–2156 (2002).

• CAS
• Google Scholar

Whitfield, A. E. et al. A soluble form of the tomato spotted wilt virus (TSWV) glycoprotein G_N (G_N -S) inhibits transmission of TSWV by Frankliniella occidentalis. Phyopathol. 98, 45–50 (2008).

• CAS
• Google Scholar

Bandla, M. D., Campbell, L. R., Ullman, D. E. & Sherwood, J. L. Interaction of tomato spotted wilt tospovirus (TSWV) glycoproteins with a thrips midgut protein, a potential cellular receptor for TSWV. Phytopathol 88(2), 98–104 (1998).

• CAS
• Google Scholar

Kikkert, M. et al. Binding of tomato Spotted wilt virus to a 94-kDa thrips protein. Phytopathol. 88, 63–69 (1998).

• CAS
• Google Scholar

Thomas, R. E., Wu, W. K., Verleye, D. & Rai, K. S. Midgut basal lamina thickness and dengue-1 virus dissemination rates in laboratory strains of Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 30, 326–331 (1993).

Ullman, D. E., Cho, J. J., Mau, R. F. L., Westcot, D. M. & Custer, D. M. A midgut barrier to Tomato spotted wilt virus acquisition by adult western flower thrips. Phytopathol. 82, 1333–1342 (1992).

• Google Scholar

de Assis Filho, F. M., Stavisky, J., Reitz, S. R., Deom, C. M. & Sherwood, J. L. Midgut infection by tomato spotted wilt virus and vector incompetence of Frankliniella tritici. J. Appl. Entomol. 129, 548–550 (2005).

• Google Scholar

Gildow, F. E. & Grey, S. M. The aphid salivary-gland basal lamina as a selective barrier associated with vector-specific transmission of barley yellow dwarf luteoviruses. Phytopathol. 83, 1293–1302 (1993).

• Google Scholar

Peiffer, M. L., Gildow, F. E. & Gray, S. M. Two distinct mechanisms regulate luteovirus transmission efficiency and specificity at the aphid salivary gland. J. Gen. Virol. 78, 595–503 (1997).

• Google Scholar

Gray, S. & Gildow, F. E. Luteovirus-aphid interactions. Annu. Rev. Phytapathol. 41, 539–566 (2003).

• CAS
• Google Scholar

Wei, J. et al. Specific cells in the primary salivary glands of the whitefly Bemisia tabaci control retention and transmission of Begomoviruses. J. Virol. 88, 13460–13468 (2014).

Medeiros, R. B., Resende, R. D. O. & Ávila, C. D. The plant virus tomato spotted wilt tospovirus activates the immune system of its main vector, Frankliniella occidentalis. J. Virol. 78, 4976–4982 (2004).

Schneweis, D. J., Whitfield, A. E. & Rotenberg, D. Thrips developmental stage-specific transcriptome response to tomato spotted wilt virus during the virus infection cycle in Frankliniella occidentalis, the primary vector. Virol. 500, 226–237 (2017).

• CAS
• Google Scholar

Shrestha, A. et al. Transcriptome changes associated with Tomato spotted wilt virus infection in various life stages of its thrips vector, Frankliniella fusca (Hinds). J. Gen. Virol. 98, 2156–2170 (2017).

Stafford, C. A., Walker, G. P. & Ullman, D. E. Infection with a plant virus modifies vector feeding behavior. PNAS. 108, 9350–9355 (2011).

Kindt, F., Joosten, N. N., Peters, D. & Tjallingii, W. F. Characterization of the feeding behavior of western flower thrips in terms of electrical penetration graph (EPG) waveforms. J. Insect Physiol. 49, 183–191 (2003).

Eigenbrode, S. D., Bosque-Pérez, N. A. & Davis, T. S. Insect-borne pathogens and their vectors: ecology, evolution, and complex interactions. Annu. Rev. Entomol. 63, 169–191 (2018).

Mason, G., Roggero, P. & Tavella, L. Detection of tomato spotted wilt virus in its vector Frankliniella occidentalis by reverse transcription-polymerase chain reaction. J. Virol. Meth. 109, 69–73 (2003).

• CAS
• Google Scholar

Yang, C. C. et al. Validation of reference genes for gene expression studies in nonviruliferous and viruliferous Frankliniella occidentalis (Thysanoptera: Thripidae). PeerJ PrePrints. 2, e662v1 (2014).

• Google Scholar

Zheng., Y. T., Li, H. B., Lu, M. X. & Du, Y. Z. Evaluation and validation of reference genes for qRT-PCR normalization in Frankliniella occidentalis (Thysanoptera: Thripidae). PLoS ONE. 9, e111369 (2014).

Roberts, C. A., Dietzgen, R. G., Heelan, L. A. & Maclean, D. J. Real-time RT-PCR fluorescent detection of tomato spotted wilt virus. J. Virol. Meth. 88, 1–8 (2000).

• CAS
• Google Scholar

Mortimer-Jones, S. M., Jones, M. G. K., Jones, R. A. C., Thomson, G. & Dwyer, G. I. A single tube, quantitative real-time RT-PCR assay that detects four potato viruses simultaneously. J. Virol. Meth. 161, 289–296 (2009).

• CAS
• Google Scholar

Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nature Protocols. 3, 1101–1108 (2008).

Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).