Skip to main content Accessibility help

Preinfestations of tomato plants by whiteflies (Bemisia tabaci) or aphids (Macrosiphum euphorbiae) induce variable resistance or susceptibility responses

  • G. Nombela (a1), E. Garzo (a1), M. Duque (a2) and M. Muñiz (a1)


In addition to constitutive plant resistance against pests or pathogens, plants can activate protective mechanisms upon contact with an invader or a chemical elicitor. Studies on induced plant resistance to herbivores, especially piercing-sucking insects, are less abundant than those devoted to pathogens. Several experiments under controlled conditions have been conducted to demonstrate that infestations by Macrosiphum euphorbiae induce plant resistance to Bemisia tabaci in susceptible tomato plants. After three days of exposure to 20 apterous adult aphids, the plants acquired a transiently induced resistance to B. tabaci when aphid removal occurred one or 18 hours prior to B. tabaci infestation; the effect disappeared when four days passed between aphid and whitefly infestations. The resistance observed was both locally and systemically induced. Other assays were performed to evaluate the effect of preinfestation with ten adults of B. tabaci during 48 h on the tomato responses to two different clones (Sp and Nt) of M. euphorbiae. The numbers of nymph and adult aphids were counted after the same time interval as the pre-reproductive period and 20 (Sp clone) or 22 (Nt clone) days after adult aphid removal. The tomato responses induced by whitefly feeding depend on the aphid clone. For the Sp clone, the number of aphid nymphs ten days after adult removal was significantly higher on whitefly preinfested plants than on uninfested plants. However, no significant differences were observed when the aphid clone Nt was tested. The duration of plant response to a previous infestation by B. tabaci is apparently limited.


Corresponding author

*Author for correspondence Fax: +1(34) 915640800 E-mail:


Hide All
Agrawal, A. (2005) Future directions in the study of induced plant responses to herbivory. Entomologia Experimentalis et Applicata 115, 97105.
Agrawal, A., Tuzun, S. & Bent, E. (1999) Induced Plant Defenses against Pathogens and Herbivores. 390 pp. St. Paul, Minnesota, APS Press.
Agrawal, A., Karban, R. & Colfer, R.G. (2000) How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89, 7080.
Bostock, R.M., Karban, R., Thaler, J.S., Weyman, P.D. & Gilchrist, D. (2001) Signal interactions in induced resistance to pathogens and insect herbivores. European Journal of Plant Pathology 107, 103111.
Cooper, W.C., Jia, L. & Goggin, F.L. (2004) Acquired and R-gene-mediated resistance against the potato aphid in tomato. Journal of Chemical Ecology 30, 25272542.
Correa, R.S.B., Moraes, J.C., Auad, A.M. & Carvalho, G.A. (2005) Silicon and acibenzolar-S-methyl as resistance inducers in cucumber, against the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B. Neotropical Entomology 34, 429433.
Costa, H.S., Westcot, D.M., Ullman, D.E., Rosell, R., Brown, J.K. & Johnson, M.W. (1995) Morphological variation in Bemisia endosymbionts. Protoplasma 189, 194202.
De Barro, P.J., Sherratt, T.N., David, O. & Maclean, N. (1995) An investigation of the differential performance of clone of the aphid Sitobion avenae on two host species. Oecologia 104, 379385.
Douglas, A.E. (1998) Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology 43, 1737.
Dugravot, S., Brunissen, L., Létocart, E., Tjallingii, W.F., Vicent, C., Giordanengo, P. & Cherqui, A. (2007) Local and systemic responses induced by aphids in Solanum tuberosum plants. Entomologia Experimentalis et Applicata 123, 271277.
Engelberth, J., Alborn, H.T., Schmelz, E.A. & Tumlinson, J.H. (2004) Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences USA 101, 17811785.
Fereres, A., Lister, R.M., Araya, J.E. & Foster, J.E. (1989) Development and reproduction of the English grain aphid (Homoptera: Aphididae) on wheat cultivars infected with Barley Yellow Dwarf Virus. Environmental Entomology 18, 388393.
Goggin, F.L., Williamson, V.M. & Ullman, D.E. (2001) Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environmental Entomology 30, 101106.
Goundoudaki, S., Tsitsipis, J.A., Margaritopoulos, J.T., Zarpas, K.D. & Divanidis, S. (2003) Performance of the tobacco aphid Myzus persicae (Hemiptera: Aphididae) on Oriental and Virginia tobacco varieties. Agricultural and Forest Entomology 5, 285291.
Hammerschmidt, R., Métraux, J.P. & van Loon, L.C. (2001) Inducing resistance: a summary of papers presented at the First International Symposium on Induced Resistance to Plant Diseases, Corfu, May 2000. European Journal of Plant Pathology 107, 16.
Heil, M. & Kost, C. (2006) Priming of indirect defences. Ecological Letters 9, 813817.
Hunter, M.D. (2000) Mixed signals and cross-talk: interactions between plants, insect herbivores and plant pathogens. Agricultural and Forest Entomology 2, 155160.
Hunter, M.D. (2002) A breath of fresh-air: beyond laboratory studies of plant volatile-natural enemy interactions. Agricultural and Forest Entomology 4, 8186.
Inbar, M., Doostdar, H., Leibee, G.L. & Mayer, R.T. (1999) The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. Journal of Chemical Ecology 25, 19611979.
Jiang, Y.X., Nombela, G. & Muñiz, M. (2001) Analysis by DC-EPG of the resistance to Bemisia tabaci on an Mi-tomato line. Entomologia Experimentalis et Applicatta 99, 295302.
Karban, R. & Baldwin, I.T. (1997) Induced Responses to Herbivory. 319 pp. University of Chicago Press, Chicago, IL, USA.
Karban, R., Agrawal, A.A., Thaler, J.S. & Adler, L.S. (1999) Induced plant responses and information content about risk of herbivory. Tree 14, 443447.
Kfoury, L. & Masonie, G. (1995) Characteristics of the resistance of the peach cultivar Rubira to Myzus persicae Sulzer. Agronomie 15, 277284.
Kunz, W., Schurter, R. & Maetzke, T. (1997) The chemistry of benzothiadiazole plant activators. Pesticide Science 50, 275282.
Martínez de Ilarduya, O., Xie, Q. & Kaloshian, I. (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant Microbe Interactions 16, 699708.
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 pathogens. Archives of Insect Biochemistry and Physiology 51, 151169.
Messina, F.J., Taylor, R. & Karren, M.E. (2002) Divergent responses of two cereal aphids to previous infestation of their host plant. Entomologia Experimentalis et Applicata 16, 4350.
Muñiz, M. & Nombela, G. (2001) Bemisia tabaci: A new clip-cage for biological studies. European Whitefly Studies Network A2, 12.
Murugan, M. & Dhandapani, N. (2006) Induced systemic resistance activates defense responses to interspecific insect infestations on tomato. Journal of Vegetable Science 12, 4362.
Nombela, G., Williamson, V.M. & Muñiz, M. (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular Plant-Microbe Interactions 16, 645649.
Nombela, G., Pascual, S., Aviles, M., Guillard, E. & Muñiz, M. (2005) Benzothiadiazole (BTH) induces local resistance to Bemisia tabaci in tomato plants. Journal of Economic Entomology 98, 22662271.
Oostendorp, M., Kunz, W., Dietrich, B. & Staub, T. (2001) Induced resistance in plants by chemicals. European Journal of Plant Pathology 107, 1928.
Prado, E. & Tjallingii, W.F. (1997) Effects of previous plant infestation on sieve element acceptance by two aphids. Entomologia Experimentalis et Applicatta 82, 189200.
Quiroz, A., Petterson, J., Pickett, J.A., Wadhams, L.J. & Niemeyer, H.M. (1997) Semiochemicals mediating spacing behavior of bird cherry-oat aphid, Rhopalosiphum padi feeding on cereals. Journal of Chemical Ecology 23, 25992607.
Rabbinge, R., Drees, E.M., van Der Graaf, M., Verberne, F.C.M. & Wesselo, A. (1981) Damage effects of cereal aphids in wheat. Netherland Journal of Plant Pathology 87, 217232.
Roberts, P.A. & Thomason, I.J. (1986) Variability in reproduction of isolates of Meloidogyne incognita and M. javanica on resistant tomato genotypes. Plant Disease 70, 547551.
Rodríguez-Saona, C., Crafts-Brandner, S.J. & Cañas, L.A. (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. Journal of Chemical Ecology 29, 25392550.
Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, I., Ullman, D.E. & Williamson, V.M. (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences of the United States of America 95, 97509754.
Sauge, M.H., Lacroze, J.P., Poëssel, J.L., Pascal, T. & Kervella, J. (2002) Induced resistance by Myzus persicae in the peach cultivar ‘Rubira’. Entomologia Experimentalis et Applicata 102, 2937.
Siddiqui, I.A. & Shaukat, S.S. (2004) Systemic resistance in tomato induced by biocontrol bacteria against the root-knot nematode, Meloidogyne javanica is independent of salicylic acid production. Journal of Phytopathology 152, 4854.
Smith, C.M. & Boyko, E.V. (2006) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 122, 116.
Smith-Becker, J., Keen, N.T. & Becker, J.O. (2003) Acibenzolar-S-metyl induces resistance to Colletotrichum lagenarium and cucumber mosaic virus in cantaloupe. Crop Protection 22, 769774.
Statgraphics (1997) Statgraphics Plus for Windows 3.1. Statistical Graphics Corp.
Stout, M.J., Workman, K.V., Bostock, R.M. & Duffey, S.S. (1998) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113, 7481.
Thaler, J.S., Stout, M.J., Karban, R. & Duffey, S.S. (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecological Entomology 26, 312324.
Thompson, G.A. & Goggin, F.L. (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. Journal of Experimental Botany 57, 755766.
Tjallingii, W.F. (1988) Electrical recording of stylet penetration activities. pp. 95108in Minks, A.K. & Harrewijn, P. (Eds) Aphids, Their Biology, Natural Enemies and Control, Vol. 2B. Amsterdam, Elsevier.
Walling, L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195216.
Wool, D. & Hales, D.F. (1996) Previous infestation affects recolonization of cotton by Aphis gossypii: induced resistance or plant damage? Phytoparasitica 24, 3948.
Zhu-Salzman, K., Bi, J.L. & Liu, T.X. (2005) Molecular strategies of plant defense and insect counter-defense. Insect Science 12, 315.


Preinfestations of tomato plants by whiteflies (Bemisia tabaci) or aphids (Macrosiphum euphorbiae) induce variable resistance or susceptibility responses

  • G. Nombela (a1), E. Garzo (a1), M. Duque (a2) and M. Muñiz (a1)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed