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Infection by the semi-persistently transmitted Tomato chlorosis virus alters the biology and behaviour of Bemisia tabaci on two potato clones

Published online by Cambridge University Press:  08 January 2019

L.S. Pereira ,
A.L. Lourenção ,
F.J.S. Salas ,
J.M.S. Bento ,
J.A.M. Rezende  and
M.F.G.V. Peñaflor Open the ORCID record for M.F.G.V. Peñaflor [Opens in a new window]
L.S. Pereira
Affiliation:
Instituto Agronômico (IAC), Centro de Fitossanidade, Av. Barão de Itapura, 1481, 13020-902 Campinas, SP, Brazil
A.L. Lourenção
Affiliation:
Instituto Agronômico (IAC), Centro de Fitossanidade, Av. Barão de Itapura, 1481, 13020-902 Campinas, SP, Brazil
F.J.S. Salas
Affiliation:
Instituto Biológico (IB), Laboratório de Estudo Vetores, Av. Conselheiro Rodrigues Alves, 1.252, 04014-900 São Paulo, SP, Brazil
J.M.S. Bento
Affiliation:
Departamento de Entomologia e Acarologia, Escola Superior de Agricultura ‘Luiz de Queiroz’ Universidade de São Paulo (ESALQ-USP), Av. Pádua Dias, 11, 13418-900 Piracicaba, SP, Brazil
J.A.M. Rezende
Affiliation:
Departamento de Fitopatologia e Nematologia, Escola Superior de Agricultura ‘Luiz de Queiroz’ Universidade de São Paulo (ESALQ-USP), Av. Pádua Dias, 11, 13418-900 Piracicaba, SP, Brazil
M.F.G.V. Peñaflor*
Affiliation:
Departamento de Entomologia, Universidade Federal de Lavras (UFLA), Campus Universitário, 37200-00 Lavras, MG, Brazil
*
*Author for correspondence Phone: 55 35 3829-1287 Fax: 55 35 3829-1502 E-mail: fernanda.penaflor@den.ufla.br
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Abstract

Insect-borne plant viruses usually alter the interactions between host plant and insect vector in ways conducive to their transmission (‘host manipulation hypothesis’). Most studies have tested this hypothesis with persistently and non-persistently transmitted viruses, while few have examined semi-persistently transmitted viruses. The crinivirus Tomato chlorosis virus (ToCV) is semi-persistently transmitted virus by whiteflies, and has been recently reported infecting potato plants in Brazil, where Bemisia tabaci Middle East Asia Minor 1 (MEAM1) is a competent vector. We investigated how ToCV infection modifies the interaction between potato plants and B. tabaci in ways that increase the likelihood of ToCV transmission, in two clones, one susceptible (‘Agata’) and the other moderately resistant (Bach-4) to B. tabaci. Whiteflies alighted and laid more eggs on ToCV-infected plants than mock-inoculated plants of Bach-4. When non-viruliferous whiteflies were released on ToCV-infected plants near mock-inoculated plants, adults moved more intensely towards non-infected plants than in the reverse condition for both clones. Feeding on ToCV-infected plants reduced egg-incubation period in both clones, but the egg–adult cycle was similar for whiteflies fed on ToCV-infected and mock-inoculated plants. Our results demonstrated that ToCV infection in potato plants alters B. tabaci behaviour and development in distinct ways depending on the host clone, with potential implications for ToCV spread.

Keywords

host manipulation hypothesisplant–pathogen–vector interactionsilverleaf whiteflyToCVvector-borne plant viruses
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 5 , October 2019 , pp. 604 - 611
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Copyright
Copyright © Cambridge University Press 2019 

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References

Alvarez, A.E., Garzo, E., Verbeek, M., Vosman, B., Dicke, M. & Tjallingii, W.F. (2007) Infection of potato plants with potato leafroll virus changes attraction and feeding behavior of Myzus persicae. Entomologia Experimentalis et Applicata 125, 135–144.Google Scholar
Barbosa, L.D.F., Yuki, V.A., Marubayashi, J.M., De Marchi, B.R., Perini, F.L., Pavan, M.A., Barros, D.R., Ghanim, M., Moriones, E., Navas-Castillo, J. & Krause-Sakate, R. (2015) First report of Bemisia tabaci Mediterranean (Q biotype) species in Brazil. Pest Management Science 71, 501–504.Google Scholar
Bleeker, P.M., Diergaarde, P.J., Ament, K., Guerra, J., Weidner, M., Schütz, S., de Both, M.T.J., Haring, M.A. & Schuurink, R.C. (2009) The role of specific tomato volatiles in tomato-whitefly interaction. Plant Physiology 151, 925–935.Google Scholar
Bleeker, P.M., Diergaarde, P.J., Ament, K., Schütz, S., Johne, B., Dijkink, J., Hiemstra, H., de Gelder, R., de Both, M.T.J., Sabelis, M.W., Haring, M.A. & Schuurink, R.C. (2011) Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies. Phytochemistry 72, 68–73.Google Scholar
Bosque-Pérez, N.A. & Eigenbrode, S.D. (2011) The influence of virus-induced changes in plants on aphid vectors: insights from luteovirus pathosystems. Virus Research 159, 201–205.Google Scholar
Buckner, J.S., Freeman, T.P., Ruud, R.L., Chu, C.C. & Henneberry, T.J. (2002) Characterization and functions of the whitefly egg pedicel. Archives of Insect Biochemistry and Physiology 49, 22–33.Google Scholar
De Barro, P.J., Scott, K.D., Graham, G.C., Lange, C. L. & Schutze, M. K. (2003) Isolation and characterization of microsatellite loci in Bemisia tabaci. Molecular Ecology Notes 3, 40–43.Google Scholar
De Barro, P. J., Liu, S. S., Boykin, L.M. & Dinsdale, A.B. (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1–19.Google Scholar
Dovas, C.I., Katis, N.I. & Avgelis, A.D. (2002) Multiplex detection of criniviruses associated with epidemics of yellowing disease of tomato in Greece. Plant Disease 86, 1345–1349.Google Scholar
Fang, Y., Jiao, X., Xie, W., Wang, S., Wu, Q., Shi, X., Chen, G., Su, Q., Yang, X., Pan, H. & Zhang, Y. (2013) Tomato yellow leaf curl virus alters the host preferences of its vector Bemisia tabaci. Scientific Reports 3, 2876.Google Scholar
Fereres, A., Peñaflor, M.F.G.V., Favaro, C. F., Azevedo, K.E., Landi, C.H., Maluta, N.K., Bento, J.M.S. & Lopes, J.R. (2016) Tomato infection by whitefly-transmitted circulative and non-circulative viruses induce contrasting changes in plant volatiles and vector behavior. Viruses 8, 225.Google Scholar
Fortes, I.M. & Navas-Castillo, J. (2012) Potato, an experimental and natural host of the crinivirus Tomato chlorosis virus. European Journal of Plant Pathology 134, 81–86.Google Scholar
Freitas, D.M.S. (2012). Tomato severe rugose virus (ToSRV) e Tomato chlorosis virus (ToCV): relações com a Bemisia tabaci biótipo B e eficiência de um inseticida no controle da transmissão do ToSRV. Doctoral dissertation, Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Freitas, D.M.S., Nardin, I., Shimoyama, N., Souza-Dias, J.A.C. & Rezende, J.A.M. (2012) First report of Tomato chlorosis virus in potato in Brazil. Plant Disease 96, 593.Google Scholar
Hogenhout, S.A., Ammar, E.D., Whitfield, A.E. & Redinbaugh, M.G. (2008) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology 46, 327–359.Google Scholar
Ingwell, L.L., Eigenbrode, S.D. & Bosque-Pérez, N.A. (2012) Plant viruses alter insect behavior to enhance their spread. Scientific Reports 2, 578.Google Scholar
Jiménez-Martínez, E.S., Bosque-Pérez, N.A., Berger, P.H., Zemetra, R.S., Ding, H. & Eigenbrode, S.D. (2004a) Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to barley yellow dwarf virus-infected transgenic and untransformed wheat. Environmental Entomology 33, 1207–1216.Google Scholar
Jiménez-Martínez, E.S., Bosque-Pérez, N.A., Berger, P.H. & Zemetra, R.S. (2004b) Life history of the bird cherry-oat aphid, Rhopalosiphum padi (Homoptera: Aphididae), on transgenic and untransformed wheat challenged with barley yellow dwarf virus. Journal of Economic Entomology 97, 203–212.Google Scholar
Li, Y., Zhong, S., Qin, Y., Zhang, S., Gao, Z., Dang, Z. & Pan, W. (2014) Identification of plant chemicals attracting and repelling whiteflies. Arthropod-Plant Interactions 8, 183–190.Google Scholar
Luan, J.B., Yao, D.M., Zhang, T., Walling, L.L., Yang, M., Wang, Y.J. & Liu, S.S. (2013) Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecology Letters 16, 390–398.Google Scholar
Macias, W. & Mink, G.I. (1969) Preference of green peach aphids for virus-infected sugarbeet leaves. Journal of Economic Entomology 62, 28–29.Google Scholar
Maluta, N.K.P., Fereres, A. & Lopes, J.R.S. (2017) Settling preferences of the whitefly vector Bemisia tabaci on infected plants varies with virus family and transmission mode. Entomologia Experimentalis et Applicata 165, 138–147.Google Scholar
Maluta, N., Fereres, A. & Lopes, J.R.S. (2018) Plant-mediated indirect effects of two viruses with different transmission modes on Bemisia tabaci feeding behavior and fitness. Journal of Pest Science, 1–12.Google Scholar
Mauck, K.E. (2016) Variation in virus effects on host plant phenotypes and insect vector behavior: what can it teach us about virus evolution? Current Opinion in Virology 21, 114–123.Google Scholar
Mauck, K.E., De Moraes, C.M. & Mescher, M.C. (2010) Deceptive chemical signals by a plant virus attract insect vectors to inferior hosts. Proceedings of the National Academy of Sciences of the USA 107, 3600–3605.Google Scholar
Mauck, K.E., Bosque-Pérez, N.A., Eigenbrode, S.D., De Moraes, C.M. & Mescher, M.C. (2012) Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses. Functional Ecology 26, 1162–1175.Google Scholar
Mauck, K.E., De Moraes, C.M. & Mescher, M.C. (2014) Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host-plant traits that mediate transmission by aphid vectors. Plant, Cell & Environment 37, 1427–1439.Google Scholar
Musser, R.O., Hum-Musser, S.M., Felton, G.W. & Gergerich, R.C. (2003) Increased larval growth and preference for virus-infected leaves by the Mexican bean beetle, Epilachna varivestis Mulsant, a plant virus vector. Journal of Insect Behavior 16, 247–256.Google Scholar
Navas-Castillo, J., Camero, R., Bueno, M. & Moriones, E. (2000) Severe yellowing outbreaks in tomato in Spain associated with infections of Tomato chlorosis virus. Plant Disease 84, 835–837.Google Scholar
Navas-Castillo, J., Olivé, E.F. & Campos, S.C. (2011) Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology 49, 219–248.Google Scholar
Ng, J.C.K. & Perry, K.L. (2004) Transmission of plant viruses by aphid vectors. Molecular Plant Pathology 5, 505–511.Google Scholar
Ngumbi, E., Eigenbrode, S.D., Bosque-Pérez, N.A., Ngumbi, E., Eigenbrode, S.D., Bosque-Pérez, N.A., Ding, H. & Rodriguez, A. (2007) Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV-infected potato. Journal of Chemical Ecology 33, 1733–1747.Google Scholar
Peñaflor, M.F.G., Mauck, K.E., Alves, K.J., De Moraes, C.M. & Mescher, M.C. (2016) Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host-plant chemistry and host–vector interactions. Functional Ecology 30, 1648–1659.Google Scholar
Poulin, R. (1998) Evolutionary Ecology of Parasites. From Individuals to Communities. London, Chapman & Hall.Google Scholar
Prado, J.C., Peñaflor, M.F.G.V., Cia, E., Vieira, S.S., Silva, K.I., Carlini-Garcia, L.A. & Lourenção, A.L. (2016) Resistance of cotton genotypes with different leaf colour and trichome density to Bemisia tabaci biotype B. Journal of Applied Entomology 140, 405–413.Google Scholar
Raij, B., Cantarella, H., Quaggio, J.A. & Furlani, A.M.C. (1997) Recomendações de adubação e calagem para o estado de São Paulo. Campinas, Instituto Agronômico/Fundação IAC.Google Scholar
Rajabaskar, D., Bosque-Pérez, N.A. & Eigenbrode, S.D. (2014) Preference by a virus vector for infected plants is reversed after virus acquisition. Virus Research 186, 32–37.Google Scholar
Rocha, A.B.O., Lourenção, A.L., Miranda-Filho, H.S., Hayashi, P.C. & Ramos, V.J. (2012) Resistência de clones de batata a Bemisia tabaci biótipo B. Horticultura Brasileira 30, 32–38.Google Scholar
Shi, X., Tang, X., Zhang, D., Li, F., Yan, F., Zhang, Y., Zhou, X. & Liu, Y. (2018) Transmission efficiency, preference and behavior of Bemisia tabaci MEAM1 and MED under the influence of Tomato chlorosis virus. Frontiers in Plant Science 8, 2271.Google Scholar
Shrestha, D., McAuslane, H.J., Adkins, S.T., Smith, H.A., Dufault, N., Colee, J. & Webb, S.E. (2017) Host-mediated effects of semipersistently transmitted squash vein yellowing virus on sweetpotato whitefly (Hemiptera: Aleyrodidae) behavior and fitness. Journal of Economic Entomology 110, 1433–1441.Google Scholar
Silva, M.S., Lourenção, A.L., Souza-Dias, J.A.C., Miranda Filho, H.S., Ramos, V.J. & Schammass, E.A. (2008) Resistance of potato genotypes (Solanum spp.) to Bemisia tabaci biotype B. Horticultura Brasileira 26, 221–226.Google Scholar
Su, Q., Preisser, E.L., Zhou, X.M., Xie, W., Liu, B.M., Wang, S.L., Wu, Q.J. & Zhang, Y.J. (2015) Manipulation of host quality and defense by a plant virus improves performance of whitefly vectors. Journal of Economic Entomology 108, 11–19.Google Scholar
Walker, G.P., Perring, T.M. & Freeman, T.P. (2010) Life history, functional anatomy, feeding and mating behavior. pp. 109–161 in Stansly, P.A. & Naranjo, S.E. (Eds) Bemisia: Bionomics and Management of a Global Pest. Dordrecht, Springer.Google Scholar
Webb, S.E., Adkins, S. & Reitz, S.R. (2012) Semipersistent whitefly transmission of Squash vein yellowing virus, causal agent of viral watermelon vine decline. Plant Disease 96, 839–844.Google Scholar
Wintermantel, W.M. & Wisler, G.C. (2006) Vector specificity, host range, and genetic diversity of Tomato chlorosis virus. Plant Disease 90, 814–819.Google Scholar
Wisler, G.C., Li, R.H., Liu, H.Y., Lowry, D.S. & Duffus, J.E. (1998) Tomato chlorosis virus: a new whitefly transmitted phloem-limited, bipartite closterovirus of tomato. Phytopathology 88, 402–409.Google Scholar
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