Aphid-host plant interaction

Abstract

Black bean aphid, Aphis fabae (Homoptera; Aphididae) is a serious pest causing crop loss. Plant-aphid interaction is a dynamic system subjected to continual variation and changes. Host plants induce various biochemical and physical defense mechanisms due to aphid feeding. Aphids can overcome plant defenses by enzymatic adaptations and sequestering secondary metabolites produced by the plant within their bodies as a defense against their enemies. Many strategies were developed and evolved by aphids in order to overcome plant defense barriers which allowed them to feed, grow and reproduce on their host plants. This study aimed to aid in better understanding of the effect of altering host plant on specialist and generalist aphid fitness.The influence of plant defense on population development of Aphis fabae was also investigated. Analyses for insect enzymes were also demonstrated in addition to further biochemical studies on host plant defences. Generalists showed different ecological and enzymatic adaptations towards host plants than specialist Aphis fabae. The results were fully discussed in details.

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Sadek, R. , Elbanna, S. and Semida, F. (2013) Aphid-host plant interaction. Open Journal of Animal Sciences, 3, 16-27. doi: 10.4236/ojas.2013.32A003.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Powell, G. and Hardie, J. (2001) The chemical ecolgy of aphid host alternation: how do return migrants find the primary host plant? Applied Entomology and Zoology, 36, 259-267. doi:10.1303/aez.2001.259
[2] Thieme, T. (1987) Members of the complex Aphis fabae Scop. and their host plants. In: Holman, J., Pelikan, J., Dixon, A.F.G. and Weissman, L. (Eds.), Population Structure, Genetics and Taxonomy of Aphids and Thysanoptera, SPB Academic Publishing, The Hague, 314-323.
[3] Fereres, A., Avilla, C., Collar, J.L., Duque, M. and Fernandez-Quintanilla, C. (1996) Impact of various yieldreducing agents on open-field sweet peppers. Environmental Entomology, 25, 983-986.
[4] Müller, C.B., Williams, I.S. and Hardie, J. (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology, 26, 330-340. doi:10.1046/j.1365-2311.2001.00321.x
[5] Iwona, M., Van, C.M. and Beata, G. (2011) Phytohormonal signaling in plant responses to aphid feeding. Acta Physiol Plant, Springer.
[6] Tjallingii, W.F. and Hogen Esch, T.H. (1993) Fine-structure of aphid stylet routes in plant-tissues in correlation with EPG signals. Physiological Entomology, 18, 317328. doi:10.1111/j.1365-3032.1993.tb00604.x
[7] Smith, C.M. (1989) Plant resistance to insects: A fundamental approach. John Wiley and Sons, Inc., New York.
[8] Hartley, S.E. and Jones, C.G. (1999) Plant chemistry and herbivory, or why the world is green. In: Olff, V.K., Brown and Drent, R.H. (Eds.), Herbivores: Between Plants and Predators, Blackwell, Oxford.
[9] Shereen, M.E. (2007) Insect interactions of three trophic levels on milkweed plant, Asclepias sinaica (Boiss.) musch. International Journal of Agriculture and Biology, 9, 292293.
[10] Wagner, G.J., Wang, E. and Shepherd, R.W. (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany, 93, 3-11. doi:10.1093/aob/mch011
[11] Linda, L.W. (2008) Avoiding effective defenses: Strategies employed by phloem-feeding insects. Plant Physiology, 146, 859-866.
[12] Rosenthal, G.A. and Janzen, D.H. (1979) Herbivores: Their interaction with secondary plant metabolites. Academic Press, New York, 41.
[13] Feyereisen, R. (1999) Insect P450 enzymes. Annual Review of Entomology, 44, 507-533. doi:10.1146/annurev.ento.44.1.507
[14] Omodele, I., Runyararo, M.H. and Graeme, B. (2011) Understanding Aphid-Plant Physiological Interactions. University of Fort Hare Press, Alice, 17, 5-45.
[15] Silva, F., Marcia O.M. and Marcio, C. (2002) Plant-insect interactions: An evolutionary arms race between two distinct defense mechanisms. Brazilian Journal of Plant Physiology, 14, 71-81.
[16] Karban, R. and Baldwin, I.T. (1997) Induced responses to herbivory. University Chicago Press, Chicago, 33-38. doi:10.7208/chicago/9780226424972.001.0001
[17] Arimura, G., Kost, C. and Boland, W. (2005) Herbivoreinduced, indirect plant defences. Biochimica et Biophysica Acta, 1734, 91-111. doi:10.1016/j.bbalip.2005.03.001
[18] Joan, C.S. and Maydianne, A. (1994) An investigation of the behavior of the pea aphid, Acyrthosiphon pisum. In: Goldman, C.A., Ed., Tested Studies for Laboratory Teaching, Volume 15 (Goldman, C.A.), Reprinted from: Sharp, J. C. and M. Andrade, Proceedings of the 15th Workshop/ Conference of the Association Biology for Biology Laboratory Education (ABLE), 335-346.
[19] Fred, E.F., Georges, L. and Eric, H. (2004) Olfactory responses to Aphid and host plant volatile releases: (E)-βFarnesene an effective kairomone for the predator Adalia bipunctata. Journal of Chemical Ecology, 30, 741-755. doi:10.1023/B:JOEC.0000028429.13413.a2
[20] Hartley, E.A. (1923) A useful cage for the rearing of small insects on growing plants. New York State College of Forestry, Syracuse, 201-203.
[21] Halimona, J. and Jankevical, L. (2011) The influence of entomophtorales isolates on Aphis fabae and Metopeurum fuscoviride. Latvijas Entomologs, 50, 55-60.
[22] Vetter, et al. (1958) Quantitative determination of peroxidase in sweet corn. Journal of Agricultural and Food Chemistry, 6, 39-41. doi:10.1021/jf60083a006
[23] Ishaaya, I. (1971) Observation on the phenolixidase system in the armored scales Aonidiella aurantii and Chrysomphalus aonidium. Comparative Biochemistry and Physiology, 39, 935-943.
[24] Lindroth, R.L. (1988) Hydrolysis of phenolic glycosides by mid gut B-glucosidases in papilo glaucus subspecies. Insect Biochemistry, 18, 789-792. doi:10.1016/0020-1790(88)90102-3
[25] Van Asperen, K. (1962) A study of house fly esterase by means of sensitive colourimetric method. Journal of Insect Physiology, 8, 401-416. doi:10.1016/0022-1910(62)90074-4
[26] Simpson, D.R., Bulland, D.L. and Linquist, D.A. (1964) A semi microtechnique for estimation of cholinesterase activity in boll weevils. Annals of the Entomological Society of America, 57, 367-371.
[27] Blackman, R.L. and Eastop, V.F. (2000) Aphids on the world’s crops: An identification and information guide. 2nd Edition, Wiley, London.
[28] Hansen, L.M., Lorenstsen, L. and Boelt, B. (2008) How to reduce the incidence of black bean aphids (Aphis fabae Scop.) attacking organic growing field beans (Vicia faba L.) by growing partially resistant bean varieties and by intercropping field beans with cereals. Acta Agriculturae Scandinavica, 58, 359-364.
[29] Goszczynski, W., Cichocka, E. and Leszczynski, B. (2002) Beetroot damage due to the black bean aphid (Aphis fabae Scop) infestation. Electronic Journal of Polish Agricultural Universities, 5, 2.
[30] Cichocka, E., Leszczynski, B., Ciepiela, A.P. and Goszczynski, W. (2002) Response of Aphis fabae Scop. to different broad bean cultivars. Electronic Journal of Polish Agricultural Universities, 5, 1.
[31] Razmjou, J. and Fallahi, A. (2009) Effects of sugar beet cultivar on development and reproductive capacity of Aphis fabae. Bulletin of Insectology, 62, 197-201.
[32] Gazi, G., Cecilia, L. and Aulay, M. (2005) Phenotypic plasticity in host-plant specialization in Aphis fabae. Ecological Entomology, 30, 657-664. doi:10.1111/j.0307-6946.2005.00742.x
[33] Sticher, L., Mauch Mani, B. and Metraux, J.P. (1997) Systemic acquired resistance. Annual Review of Phytopatheology, 35, 235-270.
[34] Dugravot, S., Brunissen, L., Letocart, E., Tjallingii, W.F., Vincent, C., Giordanengo, P. and Cherqui, A. (2007) Local and systemic responses induced by aphids in Solanum tuberosum plants. Entomologia Experimentalis et Applicata, 123, 271-277. doi:10.1111/j.1570-7458.2007.00542.x
[35] Will, T., Tjallingii, W.F., Thönnessen, A. and van Bel, A.J.E. (2007) Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences of USA, 104, 10536-10541. doi:10.1073/pnas.0703535104
[36] Pegadaraju, V., Knepper, C., Reese, J. and Shah, J. (2005) Premature leaf senescence modulated by the arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defence against the phloem-feeding green peach aphid. Plant Physiology, 139, 1927-1934. doi:10.1104/pp.105.070433
[37] Francis, F., Haubruge, E. and Gaspaar, C. (2000) Influence of host plants on specialist/generalist aphids on the development of Adalia bipunctata (Coleoptera: Coccinillidae). European Journal of Entomology, 97, 481-485.
[38] Dixon, A.F.G. (1985) Aphid ecology. 2nd Edition. Chapman & Hall, London.
[39] Cole, R.A. (1997) The relative importance of glucosenolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated brassica species. Entomologia Experimentalis et Applicata, 85, 121-133. doi:10.1046/j.1570-7458.1997.00242.x
[40] Fenwick, G.R., Heaney, R.K. and Mullin, W.J. (1983) Glucosinolates and their breakdown products in food and food plants. Critical Reviews in Food Science and Nutrition, 18, 123-201.
[41] Singh, K.B., et al. (2005) Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs. Plant Physiology, 137, 1445-1455. doi:10.1104/pp.104.051243
[42] Kaloshian, I., Kinsey, M.G., Ullman, D.E. and Williamson, V.M. (1997) The impact of Meu1-mediated resistance in tomato on longevity, fecundity and behavior of the potato aphid, Macrosiphum euphorbiae. Entomologia Experimentalis et Applicata, 83, 181-187. doi:10.1046/j.1570-7458.1997.00170.x
[43] Kennedy, G.G. and Kishaba, A.N. (1977) Response of alate melon aphids to resistant and susceptible muskmelon lines. Journal of Economic Entomology, 70, 407410.
[44] Mewis, I., Tokuhisa, J.G., Schultz, J.C., Appel, H.M., Ulrichs, C. and Gershenzon, J. (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry, 67, 2450-2462. doi:10.1016/j.phytochem.2006.09.004
[45] Kempema, L.A., Cui, X., Holzer, F.M. and Walling, L.L. (2007) Arabidopsis transcriptome changes in response to phloem-feeding silver leaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology, 143, 849-865. doi:10.1104/pp.106.090662
[46] Kim, J.H. and Jander, G. (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. The Plant Journal, 49, 1008-1019. doi:10.1111/j.1365-313X.2006.03019.x
[47] Hunter, M.D. and McNeil, J.N. (1997) Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology, 78, 977-986. doi:10.1890/0012-9658(1997)078[0977:HPQIDA]2.0.CO;2
[48] Tikkanen, O,-P., Niemel, P. and Kernen, J. (2000) Growth and development of a generalist insect herbivore, Operophtera brumata, on original and alternative host plants. Oecologia, 122, 529-536. doi:10.1007/s004420050976
[49] Silva, F., Marcia, O.M. and Marcio, C. (2002) Plant-insect interactions: An evolutionary arms race between two distinct defense mechanisms. Brazilian Journal of Plant Physiology, 14, 71-81.
[50] Jongsma, M.A. and Bolter, C. (1997) The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology, 43, 885-895. doi:10.1016/S0022-1910(97)00040-1
[51] Price, P.W. (1997) Insect ecology. 3rd Edition, John Wiley & Sons, Inc., New York.
[52] Patankar, A.G., Giri, A.P., Harsulkar, A.M., Sainani, M.N., Deshpande, V.V., Ranjekar, P.K. and Gupta, V.S. (2001) Complexity in specificities and expression of Helicoverpa armigera gut proteinases explains polyphagous nature of the insect pest. Insect Biochemistry and Molecular Biology, 31, 453-464. doi:10.1016/S0965-1748(00)00150-8
[53] Shen, B.Z., Zheng, Z.W. and Dooner, H.K. (2000) A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: Characterization of wild-type and mutant alleles. Proceedings of the National Academy of Sciences of the United States of America, 97, 1480714812. doi:10.1073/pnas.240284097
[54] Ohshima, T., Hayashi, H. and Chino, M. (1990) Collection and chemical composition of pure phloem sap from Zea mays L. Plant & Cell Physiology, 31, 735-737.
[55] Tjallingii, W.F. (1995) Regulation of phloem sap feeding by aphids. In: Chapman, R.F. and De Boer, G., Eds., Regulatory mechanisms in insect feeding, Chapman and Hall, New York, 190-209. doi:10.1007/978-1-4615-1775-7_7
[56] Prado, E. and Tjallingii, W.F. (1994) Aphid activities during sieve element punctures. Entomologia Experimentalis et Applicata, 72, 157-165. doi:10.1111/j.1570-7458.1994.tb01813.x
[57] Tjallingii, W.F. (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany, 57, 739-745. doi:10.1093/jxb/erj088
[58] Bridges, M., Jones, A.M.E., Bones, A.M., Hodgson, C., Cole, R., Bartlet, E., Wallsgrove, R., Karapapa, V.K., Watts, N. and Rossiter, J.T. (2002) Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. The Royal Society Proceedings. B, Biological Sciences, 269, 187-191. doi:10.1098/rspb.2001.1861
[59] De Bruxelles, G.L. and Roberts, M.R. (2001) Signals regulating multiple responses to wounding and herbivores. Critical Reviews in Plant Sciences, 20, 487-521.
[60] Nishida, R. (2002) Sequestration of defensive substances from plants by lepidoptera. Annual Review of Entomology, 47, 57-92. doi:10.1146/annurev.ento.47.091201.145121
[61] Miles, P.W. (1999) Aphid saliva. Biological Reviews of the Cambridge Philosophical Society, 74, 41-85.
[62] Miles, P.W. and Harrewijn, P. (1991) Discharge by aphids of soluble secretions into dietary sources. Entomologia Experimentalis et Applicata, 59, 123-134. doi:10.1111/j.1570-7458.1991.tb01495.x
[63] Baumann, L. and Baumann, B. (1995) Soluble salivary protein secreted by Schizaphis graminum. Entomologia Experimentalis et Applicata, 77, 57-60. doi:10.1111/j.1570-7458.1995.tb01985.x
[64] Urbanska, A., Tjallingii, W.F. and Leszczynski, B. (1994) Application of agarose-sucrose gels for investigation of aphid salivary enzymes. In: Hamilton, K., et al., Eds., Aphids and Other Homopterous Insects, Vol. 4, Polish Academy of Science, Skiernewice, 81-87.
[65] Madhusudhan, V.V. and Miles, P.W. (1998) Mobility of salivary components as a possible reason for differences in response of alfalfa to the spotted alfalfa aphid and pea aphid. Entomologia Experimentalis et Applicata, 86, 2539. doi:10.1046/j.1570-7458.1998.00262.x
[66] Kornemann, S. (2005) Untersuchung zu einem allgemeinen Modell der Siebelementwund-verschlus-sunterdru¨ckung durch Blattla¨use. Ph.D. Thesis, Justus Liebig University, Gießen.
[67] Kus′nierczyk, A., Winge, P., Jørstad, T.M., Troczyn′ska, J., Rossiter, J.T. and Bones, A.M. (2008) Towards global understanding of plant defence against aphids-timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant, Cell & Environment, 31, 1097-1115. doi:10.1111/j.1365-3040.2008.01823.x
[68] Goggin, F.L. (2007) Plant-aphid interactions: Molecular and ecological perspectives. Current Opinion in Plant Biology, 10, 399-408. doi:10.1016/j.pbi.2007.06.004
[69] Hori, K. (1976) Plant growth-regulating factor in the Salivary gland of several heteropterous insects. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 53, 435-438.
[70] Urbanska, A., Tjallingii, W.F., Dixon, A.F.G. and Leszczynski (1998) Phenol oxidising enzymes in the grain aphid’s saliva. Entomologia Experimentalis et Applicata, 86, 197-203. doi:10.1046/j.1570-7458.1998.00281.x
[71] Harmel, N., Le′tocart, E., Cherqui, A., Giordanengo, P., Mazzucchetlli, G., Guillonneau, F., De Pauw, E., Haubruge, E. and Francis, F. (2008) Identification of pahid salivary proteins: A proteomic investigation of Myzus persicae. Insect Molecular Biology, 17, 165-174. doi:10.1111/j.1365-2583.2008.00790.x
[72] Ni, X., Quisenberry, S.S., Pornkulwat, S., Figarola, J., Skoda, S.R. and Foster, J.E. (2000) Hydrolase and oxidoreductase activities in Diuraphis noxia and Rhopalosiphum padi (Hemiptera: Aphididae). Annals of the Entomological Society of America, 93, 595-601. doi:10.1603/0013-8746(2000)093[0595:HAORAI]2.0.CO;2
[73] Miles, P.W. and Peng, Z. (1989) Studies on the salivary physiology of plant bugs: Detoxification of phytochemicals by the salivary peroxidase of aphids. Journal of Insect Physiology, 35, 865-872. doi:10.1016/0022-1910(89)90102-9
[74] Peng, Z. and Miles, P.W. (1991) Oxidases in the gut of an aphid, Macrosiphum rosae (L.) and their relation to dietary phenolics. Journal of Insect Physiology, 37, 779-787. doi:10.1016/0022-1910(91)90113-E
[75] Lamabadusuriya, M.R. (2009) Development of sample collection methods and preliminary identifications of Aphid salivary proteins. Master of Science Thesis, Kansas State University, Manhattan.
[76] Mattiacci, L., Dicke, M. and Posthumus, M.A. (1995) β-Glucosidase: An elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America, 92, 2036-2040. doi:10.1073/pnas.92.6.2036
[77] Sales, M.P., Gerhardt, I.R., Grossi-de-Sá, M.F. and Xavier-Filho, J. (2000) Do legume storage proteins play a role in defending seeds against bruchids? Plant Physiology, 124, 515-522. doi:10.1104/pp.124.2.515
[78] Franco, O.L., Rigden, D.J., Melo, F.R. and Grossi-de-Sá, M.F. (2002) Plant alpha-amylase inhibitors and their interaction with insect alpha-amylases-structure, function and potential for crop protection. European Journal of Biochemistry, 269, 397-412. doi:10.1046/j.0014-2956.2001.02656.x
[79] Scott, J.G. and Wen, Z.M. (2001) Cytochromes P450 of insects: The tip of the iceberg. Pest Management Science, 57, 958-967. doi:10.1002/ps.354
[80] Urbanska, A., Leszczynski, B., Tjallingii, W.F. and Matok, H. (2002) Probing behavior and enzymatic defence of the grain aphid against cereal phenolics. Electronic Journal of Polish Agricultural Universities, 5. http://www.ejpau.media.pl
[81] Classen, D., Arnason, J.T., Serratos, J.A., Lambert, J.D.H., Nozzolillo, C. and Philogène, B.J.R. (1990) Correlation of phenolic acid content of maize to resistance to Sitophilus zeamais, the maize weevil, in CIMMYT’s collections. Journal of Chemical Ecology, 16, 301-315. doi:10.1007/BF01021766
[82] Dreyer, D.L. and Jones, K. (1981) Feeding deterrence of flavonoids and related phenolics toward Schizaphis graminum and Myzus persicae: Aphid feeding deterrents from wheat. Phytochemistry, 20, 2489-2493. doi:10.1016/0031-9422(81)83078-6
[83] Todd, G.W., Getahun, A. and Cress, D.C. (1971) Resistance in barley to the greenbug Schizaphis graminum. 1. Toxicity of phenolic and flavonoid compounds and related substances. Annals of the Entomological Society of America, 64, 718-722.
[84] De Bruxelles, G.L. and Roberts, M.R. (2001) Signals regulating multiple responses to wounding and herbivores. Critical Reviews in Plant Sciences, 20, 487-521.
[85] Alborn, H.T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. and Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science, 276, 945-949. doi:10.1126/science.276.5314.945
[86] Way, M.J., Cammell, M.E., Taylor, L.R. and Woiwod, I.P. (1981) The use of egg counts and suction trap samples to forecast the infestation of spring-sown field beans, Vicia faba, by the black bean aphid, Aphis fabae. Annals of Applied Biology, 98, 21-34. doi:10.1111/j.1744-7348.1981.tb00419.x
[87] Hoover, D. (1990) Cholinesterases and cholinesterase inhibitors. In: Craig, C.R. and Stitzel, R.E., Eds., Modern Pharmacology, Little, Brown and Co., Boston, 165-178.
[88] Zahavi, M., Tahori, A.S. and Klimer, F. (1972) An acetylcholinesterase sensitive to sulfhydryl inhibitors. Biochimica et Biophysica Acta, 276, 577-583. doi:10.1016/0005-2744(72)91024-8
[89] Ogenga-Latego, M.W., Baliddawa, C.W. andAmpofo, J.K.O. (1993) Factors influencing the incidence of black bean aphid Aphis fabae scop. On common beans intercropped with Maize. African Crop Science Journal, 1, 49-58.

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