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Plant-mediated whitefly–begomovirus interactions: research progress and future prospects

Published online by Cambridge University Press:  19 February 2014

Jun-Bo Luan ,
Xiao-Wei Wang ,
John Colvin  and
Shu-Sheng Liu
Jun-Bo Luan
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China
Xiao-Wei Wang
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China
John Colvin
Affiliation:
Natural Resources Institute, University of Greenwich, Kent ME4 4TB, UK
Shu-Sheng Liu*
Affiliation:
Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China
*
*Author for correspondence Phone: +86 571 88982505 Fax: +86 571 8898235 E-mail: [email protected]
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Abstract

Plant-mediated interactions between begomoviruses and whiteflies exert important influences on the population dynamics of vectors and the epidemiology of plant diseases. In this article, we synthesize the relevant literature to identify patterns to the interactions. We then review studies on the ecological, biochemical and molecular mechanisms underlying the interactions and finally elaborate on the most interesting issues for future research. The interactions between begomoviruses and the insect vector, the whitefly Bemisia tabaci, via their shared host plants can be mutualistic, neutral or negative. However, in contrast to a pattern of improved performance of vectors on virus-infected plants that has been observed with persistently transmitted RNA viruses, the number of cases exhibiting mutualistic, neutral or negative effects in the indirect interactions between begomoviruses and whiteflies appear evenly distributed. With regard to the mechanisms of plant-mediated positive effects on whiteflies, two case studies indicate that suppression of plant defence and/or alteration in plant nutrition as a result of virus infection can be important. Our review shows that we are only just beginning to understand the tripartite interactions between begomoviruses, whiteflies and plants. Future efforts in this area should try to expand the number and diversity of pathosystems for investigation to reveal the patterns of interactions, to investigate the molecular and biochemical mechanisms of the interactions using a multidisciplinary approach, and to examine the virus–plant–vector interactions in the field and in natural plant communities.

Keywords

insect vectorplant virusplant–virus–vector interactionpersistently transmitted virusvector performancevector behaviour
Type
Review Article
Information
Bulletin of Entomological Research , Volume 104 , Issue 3 , June 2014 , pp. 267 - 276
Copyright
Copyright © Cambridge University Press 2014 

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References

Akman Gündüz, E. & Douglas, A.E. (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proceedings of the Royal Society B: Biological Sciences 276, 987–991.CrossRefGoogle ScholarPubMed
Belliure, B., Janssen, A., Maris, P.C., Peters, D. & Sabelis, M.W. (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters 8, 70–79.CrossRefGoogle Scholar
Berlinger, M.J. (1986) Host plant resistance to Bemisia tabaci . Agriculture, Ecosystems and Environment 17, 69–82.CrossRefGoogle Scholar
Bing, X.L., Yang, J., Zchori-Fein, E., Wang, X.W. & Liu, S.S. (2013) Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Applied and Environmental Microbiology 79, 569–575.CrossRefGoogle ScholarPubMed
Blanc, S., Uzest, M. & Drucker, M. (2011) New research horizons in vector-transmission of plant viruses. Current Opinion in Microbiology 14, 483–491.CrossRefGoogle ScholarPubMed
Boykin, L.M., Armstrong, K.F., Kubatko, L. & De Barro, P. (2012) Species delimitation and global biosecurity. Evolutionary Bioinformatics 8, 1–37.CrossRefGoogle ScholarPubMed
Bragard, C., Caciagli, P., Lemaire, O., Lopez-Moya, J.J., MacFarlane, S., Peters, D., Susi, P. & Torrance, L. 2013. Status and prospects of plant virus control through interference with vector transmission. Annual Review of Phytopathology 51, 177–201.CrossRefGoogle ScholarPubMed
Brown, J.K., Frohlich, D.R. & Rosell, R.C. (1995) The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annual Review of Entomology 40, 511–534.CrossRefGoogle Scholar
Caspi-Fluger, A., Inbar, M., Mozes-Daube, N., Katzir, N., Portnoy, V., Belausov, E., Hunter, M.S. & Zchori-Fein, E. (2011) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proceedings of the Royal Society B: Biological Sciences 279, 1791–1796.CrossRefGoogle ScholarPubMed
Casteel, C.L., Hansen, A.K., Walling, L.L. & Paine, T.D. (2012) Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter Psyllaurous. PLoS ONE 7, e35191.CrossRefGoogle ScholarPubMed
Colvin, J., Omongo, C.A., Maruthi, M.N., Otim-Nape, G.W., & Thresh, J.M. (2004) Dual begomovirus infections and high Bemisia tabaci populations: two factors driving the spread of a cassava mosaic disease pandemic. Plant Pathology 53, 577–584.CrossRefGoogle Scholar
Colvin, J., Omongo, C.A., Govindappa, M.R., Stevenson, P. C., Maruthi, M.N., Gibson, G., Seal, S.E. & Muniyappa, V. (2006) Host–plant viral infection effects on arthropod–vector population growth, development and behaviour: management and epidemiological implications. pp. 419–452 in Karl Maramorosch, A.J.S. & Thresh, J.M. (Eds) Advances in Virus Research. San Diego, Academic Press.Google Scholar
Costa, H.S., Brown, J.K. & Byrne, D.N. (1991) Life history traits of the whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) on six virus-infected or healthy plant species. Environmental Entomology 20, 1102–1107.CrossRefGoogle Scholar
Czosnek, H. & Ghanim, M. (2012) Back to basics: are begomoviruses whitefly pathogens? Journal of Integrative Agriculture 11, 225–234.CrossRefGoogle Scholar
da Silva, S.C., Castillo-Urquiza, G., Hora Júnior, B.T., Assuncão, I.P., Lima, G.S.A., Pio-Ribeiro, G., Mizubuti, E.S.G. & Murilo Zerbini, F. (2011) High genetic variability and recombination in a begomovirus population infecting the ubiquitous weed Cleome affinis in northeastern Brazil. Archives of Virology 156, 2205–2213.CrossRefGoogle Scholar
Dale, C. & Moran, N.A. (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126, 453–465.CrossRefGoogle ScholarPubMed
De Barro, P.J., Hidayat, S.H., Frohlich, D., Subandiyah, S. & Ueda, S. (2008) A virus and its vector, pepper yellow leaf curl virus and Bemisia tabaci, two new invaders of Indonesia. Biological Invasions 10, 411–433.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Douglas, A.E. (2009) The microbial dimension in insect nutritional ecology. Functional Ecology 23, 38–47.CrossRefGoogle Scholar
Firdaus, S., Vosman, B., Hidayati, N., Supena, E.D.J., Visser, R.G.F. & van Heusden, A.W. (2013) The Bemisia tabaci species complex: additions from different parts of the world. Insect Science 20, 723–733.CrossRefGoogle ScholarPubMed
Frago, E., Dicke, M. & Godfray, H.C.J. (2012) Insect symbionts as hidden players in insect–plant interactions. Trends in Ecology & Evolution 27, 705–711.CrossRefGoogle ScholarPubMed
Gill, R.J. & Brown, J.K. (2010) Systematics of Bemisia and Bemisia relatives: can molecular techniques solve the Bemisia tabaci complex conundrum – a taxonomist's viewpoint. pp. 5–29 in Stansly, P.A. & Narahjo, S.E. (Eds) Bemisia: Bionomics and Management of a Global Pest. Dordrecht, Springer.Google Scholar
Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Kontsedalov, S., Skaljac, M., Brumin, M., Sobol, I., Czosnek, H., Vavre, F., Flury, F. & Ghanim, M. (2010) The transmission efficiency of Tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. Journal of Virology 84, 9310–9317.CrossRefGoogle ScholarPubMed
Götz, M., Popovski, S., Kollenberg, M., Gorovits, R., Brown, J.K., Cicero, J.M., Czosnek, H., Winter, S. & Ghanim, M. (2012) Implication of Bemisia tabaci heat shock protein 70 in begomovirus-whitefly interactions. Journal of Virology 86, 13241–13252.CrossRefGoogle ScholarPubMed
Guo, J.Y., Ye, G.Y., Dong, S.Z. & Liu, S.S. (2010) An invasive whitefly feeding on a virus-infected plant increased its egg production and realized fecundity. PLoS ONE 5, e11713.CrossRefGoogle ScholarPubMed
Guo, J.Y., Dong, S.Z., Yang, X.L., Cheng, L., Wan, F.H., Liu, S.S., Zhou, X.P. & Ye, G.Y. (2012) Enhanced vitellogenesis in a whitefly via feeding on a begomovirus-infected plant. PLoS ONE 7, e43567.CrossRefGoogle Scholar
Gutiérrez, S., Michalakis, Y., Munster, M. & Blanc, S. (2013) Plant feeding by insect vectors can affect life cycle, population genetics and evolution of plant viruses. Functional Ecology 27, 610–622.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Hu, J., De Barro, P.J., Zhao, H., Wang, J., Nardi, F. & Liu, S.S. (2011) An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE 6, e16061.CrossRefGoogle ScholarPubMed
Huot, O.B., Nachappa, P. & Tamborindeguy, C. (2013) The evolutionary strategies of plant defenses have a dynamic impact on the adaptations and interactions of vectors and pathogens. Insect Science 20, 297–306.CrossRefGoogle ScholarPubMed
Inbar, M. & Gerling, D. (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annual Review of Entomology 53, 431–448.CrossRefGoogle ScholarPubMed
Ingwell, L.L., Eigenbrode, S.D. & Bosque-Pérez, N.A. (2012) Plant viruses alter insect behaviour to enhance their spread. Scientific Reports 2, 578.CrossRefGoogle ScholarPubMed
Jiu, M., Zhou, X.P., Tong, L., Xu, J., Yang, X., Wan, F.H. & Liu, S.S. (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE 2, e182.CrossRefGoogle ScholarPubMed
Lapidot, M., Friedmann, M., Pilowsky, M., Ben-Joseph, R. & Cohen, S. (2001) Effect of host plant resistance to Tomato yellow leaf curl virus (TYLCV) on virus acquisition and transmission by its whitefly vector. Phytopathology 91, 1209–1213.CrossRefGoogle ScholarPubMed
Li, M., Liu, J. & Liu, S.S. (2011) Tomato yellow leaf curl virus infection of tomato does not affect the performance of the Q and ZHJ2 biotypes of the viral vector Bemisia tabaci. Insect Science 18, 40–49.CrossRefGoogle Scholar
Liu, B.M., Preisser, E.L., Chu, D., Pan, H.P., Xie, W., Wang, S.L., Wu, Q.J., Zhou, X.G. & Zhang, Y.J. (2013) Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and Tomato yellow leaf curl virus . Journal of Virology 87, 4929–4937.CrossRefGoogle ScholarPubMed
Liu, J. (2009) An investigation on the interactions of Bemisia tabaci–TYLCCNV–plant and the underlying nutritional mechanisms. PhD Thesis, Zhejiang University, Hangzhou, China.Google Scholar
Liu, J., Zhao, H., Jiang, K., Zhou, X.P. & Liu, S.S. (2009) Differential indirect effects of two plant viruses on an invasive and an indigenous whitefly vector: implications for competitive displacement. Annals of Applied Biology 155, 439–448.CrossRefGoogle Scholar
Liu, J., Li, M., Li, J.M., Huang, C.J., Zhou, X.P., Xu, F.C. & Liu, S.S. (2010) Viral infection of tobacco plants improves performance of Bemisia tabaci but more so for an invasive than for an indigenous biotype of the whitefly. Journal of Zhejiang University Scencei B 11, 30–40.CrossRefGoogle ScholarPubMed
Liu, S.S., De Barro, P.J., Xu, J., Luan, J.B., Zang, L.S., Ruan, Y.M. & Wan, F.H. (2007) Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318, 1769–1772.CrossRefGoogle Scholar
Liu, S.S., Colvin, J. & De Barro, P.J. (2012) Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there? Journal of Integrative Agriculture 11, 176–186.CrossRefGoogle Scholar
Luan, J.B., Li, J.M., Varela, N., Wang, Y.L., Li, F.F., Bao, Y.Y., Zhang, C.X., Liu, S.S. & Wang, X.W. (2011) Global analysis of the transcriptional response of whitefly to Tomato yellow leaf curl China virus reveals the relationship of coevolved adaptations. Journal of Virology 85, 3330–3340.CrossRefGoogle ScholarPubMed
Luan, J.B., Ghanim, M., Liu, S.S. & Czosnek, H. (2013 a) Silencing the ecdysone synthesis and signaling pathway genes disrupts nymphal development in whitefly. Insect Biochemistry and Molecular Biology 43, 740–746.CrossRefGoogle ScholarPubMed
Luan, J.B., Wang, Y.L., Wang, J., Wang, X.W. & Liu, S.S. (2013 b) Detoxification activity and energy cost is attenuated in the whiteflies feeding on begomovirus-infected tobacco plants. Insect Molecular Biology 22, 597–607.CrossRefGoogle Scholar
Luan, J.B., Yao, D.M., Zhang, T., Walling, L.L., Yang, M., Wang, Y.J. & Liu, S.S. (2013 c) Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecology Letters 16, 390–398.CrossRefGoogle ScholarPubMed
Mann, R.S., Sidhu, J.S., Butter, N.S., Sohi, A.S. & Sekhon, P.S. (2008) Performance of Bemisia tabaci (Hemiptera: Aleyrodidae) on healthy and Cotton leaf curl virus infected cotton. Florida Entomologist 91, 249–255.CrossRefGoogle Scholar
Mann, R.S., Sidhu, J.S. & Butter, N.S. (2009) Settling preference of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) on healthy versus cotton leaf curl virus-infected cotton plants. International Journal of Tropical Insect Science 29, 57–61.CrossRefGoogle Scholar
Mansoor, S., Briddon, R.W., Zafar, Y. & Stanley, J. (2003) Geminivirus disease complexes: an emerging threat. Trends in Plant Science 8, 128–134.CrossRefGoogle ScholarPubMed
Matsuura, S. & Hoshino, S. (2009) Effect of tomato yellow leaf curl disease on reproduction of Bemisia tabaci Q biotype (Hemiptera: Aleyrodidae) on tomato plants. Applied Entomology and Zoology 44, 143–148.CrossRefGoogle Scholar
Mauck, K., 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.CrossRefGoogle Scholar
Mayer, R.T., Inbar, M., McKenzie, C.L., Shatters, R., Borowicz, V., Albrecht, U., Powell, C.A. & Doostdar, H. (2002) Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivores, and phytopathogens. Archives of Insect Biochemistry and Physiology 51, 151–169.CrossRefGoogle ScholarPubMed
McKenzie, C. (2002) Effect of tomato mottle virus (ToMoV) on Bemisia tabaci biotype B (Homoptera: Aleyrodidae) oviposition and adult survivorship on healthy tomato. Flarida Entomologist 85, 367–368.CrossRefGoogle Scholar
Moffat, A.S. (1999) Geminiviruses emerge as serious crop threat. Science 286, 1835.CrossRefGoogle Scholar
Moreno-Delafuente, A., Garzo, E., Moreno, A. & Fereres, A. (2013) A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLoS ONE 8, e61543.CrossRefGoogle ScholarPubMed
Mugerwa, H., Rey, M.E.C., Alicai, T., Ateka, E., Atuncha, H., Ndunguru, J. & Sseruwagi, P. (2012) Genetic diversity and geographic distribution of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) genotypes associated with cassava in East Africa. Ecology and Evolution 2, 2749–2762.CrossRefGoogle ScholarPubMed
Navas-Castillo, J., Fiallo-Olivé, E. & Sánchez-Campos, S. (2011) Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology 49, 219–248.CrossRefGoogle ScholarPubMed
Nawaz-ul-Rehman, M.S. & Fauquet, C.M. (2009) Evolution of geminiviruses and their satellites. FEBS Letters 583, 1825–1832.CrossRefGoogle ScholarPubMed
Pan, D., Li, Y.X., Luan, J.B., Liu, S.S. & Liu, Y.Q. (2014) Olfactory responses of the whitefly Bemisia tabaci and its parasitoid Eretmocerus hayati to Tomato yellow leaf curl China virus-infected tobacco. Chinese Journal of Applied Entomology 51(1) in press, doi: 10.7679/j.issn.2095-1353.2014.004 (in Chinese with English summary).Google Scholar
Pan, H.P., Chu, D., Liu, B.M., Shi, X.B., Guo, L.T., Xie, W., Carrière, Y., Li, X.C. & Zhang, Y.J. (2013) Differential effects of an exotic plant virus on its two closely related vectors. Scientific Reports 3, 2230.CrossRefGoogle ScholarPubMed
Péréfarres, F., Thierry, M., Becker, N., Lefeuvre, P., Reynaud, B., Delatte, H. & Lett, J.-M. (2012) Biological invasions of Geminiviruses: case study of TYLCV and Bemisia tabaci in Reunion Island. Viruses 4, 3665–3688.CrossRefGoogle ScholarPubMed
Renteria-Canett, I., Xoconostle-Cazares, B., Ruiz-Medrano, R. & Rivera-Bustamante, R. (2011) Geminivirus mixed infection on pepper plants: synergistic interaction between PHYVV and PepGMV. Virology Journal 8, 104.CrossRefGoogle ScholarPubMed
Rodelo-Urrego, M., Pagán, I., González-Jara, P., Betancourt, M., Moreno-Letelier, A., Ayllón, M.A., Fraile, A., Piñero, D. & García-Arenal, F. (2013) Landscape heterogeneity shapes host–parasite interactions and results in apparent plant–virus codivergence. Molecular Ecology 22, 2325–2340.CrossRefGoogle ScholarPubMed
Rodríguez-López, M.J., Garzo, E., Bonani, J.P., Fereres, A., Fernández-Muñoz, R. & Moriones, E. (2011) Whitefly resistance traits derived from the wild tomato Solanum pimpinellifolium affect the preference and feeding behaviour of Bemisia tabaci and reduce the spread of Tomato yellow leaf curl virus . Phytopathology 101, 1191–1201.CrossRefGoogle Scholar
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. Journal of General Virology 78, 2683–2689.CrossRefGoogle ScholarPubMed
Sidhu, J.S., Mann, R.S. & Butter, N.S. (2009) Deleterious effects of Cotton leaf curl virus on longevity and fecundity of whitefly, Bemisia tabaci (Gennadius). Journal of Entomology 6, 62–66.CrossRefGoogle Scholar
Sloan, D.B. & Moran, N.A. 2012. Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biology Letters 8, 986–989.CrossRefGoogle ScholarPubMed
Stout, M.J., Thaler, J.S. & Thomma, B.P.H.J. (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annual Review of Entomology 51, 663–689.CrossRefGoogle ScholarPubMed
Thompson, W.M.O. (2002) Comparison of Bemisia tabaci (Homoptera: Aleyrodidae) development on uninfected cassava plants and cassava plants infected with East African cassava mosaic virus . Annals of the Entomological Society of America 95, 387–394.CrossRefGoogle Scholar
Thompson, W.M.O. (2011) The performance of viruliferous and non-viruliferous cassava biotype Bemisia tabaci on amino acid diets. pp. 165–180 in Thompson, W.M.O. (Ed.) The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) Interaction with Geminivirus-Infected Host Plants. Dordrecht, Springer.CrossRefGoogle Scholar
Varma, A., Mandal, B. & Singh, M.K. (2011) Global emergence and spread of whitefly (Bemisia tabaci) transmitted geminiviruses. pp. 205–292 in Thompson, W.M.O. (Ed.) The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) Interaction with Geminivirus-Infected Host Plants. Dordrecht, Springer.CrossRefGoogle Scholar
Wang, J., Bing, X.L., Li, M., Ye, G.Y. & Liu, S.S. (2012) Infection of tobacco plants by a begomovirus improves nutritional assimilation by a whitefly. Entomologia Experimentalis et Applicata 144, 191–201.CrossRefGoogle Scholar
Zhang, T., Luan, J.B., Qi, J.F., Huang, C.J., Li, M., Zhou, X.P. & Liu, S.S. (2012) Begomovirus–whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Molecular Ecology 21, 1294–1304.CrossRefGoogle ScholarPubMed
Zhou, X.P., Liu, Y.L., Calvert, L., Munoz, C., Otim-Nape, G.W., Robinson, D.J. & Harrison, B.D. (1997) Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. Journal of General Virology 78, 2101–2111.CrossRefGoogle ScholarPubMed