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Characterization of resistance to multiple aphid species (Hemiptera: Aphididae) in Medicago truncatula

Published online by Cambridge University Press:  14 February 2007

L.-L. Gao
Affiliation:
CSIRO Plant IndustryPrivate Bag 5, Wembley, WA6913, Australia CSIRO Entomology, Private Bag 5, Wembley, WA6913, Australia
R. Horbury
Affiliation:
CSIRO Entomology, Private Bag 5, Wembley, WA6913, Australia
R.M. Nair
Affiliation:
South Australian Research and Development Institute, GPO Box 397, Adelaide, SA 5001, Australia
K.B. Singh
Affiliation:
CSIRO Plant IndustryPrivate Bag 5, Wembley, WA6913, Australia
O.R. Edwards*
Affiliation:
CSIRO Entomology, Private Bag 5, Wembley, WA6913, Australia
*
*Author for correspondence Fax: +61 8 9333 6646 E-mail: [email protected]

Abstract

Aphids are phloem-feeding insects that damage many important crops throughout the world yet, compared to plant–pathogen interactions, little is known about the mechanisms by which plants become resistant to aphids. Medicago truncatula (barrel medic) is widely considered as the pre-eminent model legume for genetic and biological research and in Australia is an important pasture species. Six cultivars of M. truncatula with varying levels of resistance to two pests of pasture and forage legumes, the bluegreen aphid Acyrthosiphon kondoi Shinji and the spotted alfalfa aphid Therioaphis trifolii f. maculata. (Buckton) are investigated. Two resistance phenotypes against T. trifolii f. maculata are described, one of which is particularly effective, killing most aphids within 24 h of infestation. Each resistance phenotype provided a similar but somewhat less effective degree of resistance to the closely-related spotted clover aphid Therioaphis trifolii (Monell). In the case of A. kondoi only one resistance phenotype was observed, which did not vary among different genetic backgrounds. None of the observed resistance against A. kondoiorT. trifolii f. maculata significantly affected the performance of green peach aphid Myzus persicae (Sulzer) or cowpea aphid Aphis craccivora Koch. The existence of multiple aphid resistance mechanisms in similar genetic backgrounds of this model plant provides a unique opportunity to characterize the fundamental basis of plant defence to these serious agricultural pests.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

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References

Assad, M.T., Behrabi, A.M., Pakniyat, H. & Nematollahy, M.R. (2004) The effect of resistance components on reducing yield and its related characters in wheat as infected by Diuraphis noxia (Hemiptera: Aphididae). Cereal Research Communications 32, 6973.CrossRefGoogle Scholar
Berlandier, F.A., Edwards, O.R., Nichols, P.G.H. & Blake, A. (1999) Aphid resistance in annual pasture legumes. pp. 299304in Matthiessen, J.N. (Ed.) Proceedings of the 7th Australasian Grassland Invertebrate Ecology Conference, October 4–6, 1999. CSIRO Entomology, Perth, Australia.Google Scholar
Blackman, R.L. & Eastop, V.F. (1984) Aphids on the world's crops: an identification guide. Chichester, UK, Wiley-Interscience.Google Scholar
Bournoville, R., Carre, S., Landre, B., Aupinel, P., Grimaud, E. & Epardaud, M. (2003) Effects of French populations of the pea aphid Acyrthosiphon pisum (Homoptera: Aphididae) on alfalfa resistance. Phytoprotection 84, 917.CrossRefGoogle Scholar
Cabrera y Poch, H.L., Ponz, F. & Fereres, A. (1998) Searching for resistance in Arabidopsis thaliana to the green peach aphid Myzus persicae. Plant Science 38, 209216.CrossRefGoogle Scholar
Cook, D.R. (1999) Medicago truncatula – a model in the making! Current Opinion in Plant Biology 2, 301304.CrossRefGoogle Scholar
Crawford, E., Lake, A. & Boyce, K. (1989) Breeding annual Medicago species for semiarid conditions in Southern Australia. Advances in Agronomy 42, 399437.CrossRefGoogle Scholar
Dixon, A. (1998) Aphid ecology: an optimization approach. London, Chapman and Hall.Google Scholar
Du Toit, F. (1987) Resistance in wheat (Triticum aestivum) to Diuraphis noxia (Hemiptera: Aphididae). Cereal Research Communications 15, 175179.Google Scholar
Edwards, O.R. (2001) Interspecific and intraspecific variation in the performance of three pest aphid species on five grain legume hosts. Entomologia Experimentalis et Applicata 100, 2130.CrossRefGoogle Scholar
Edwards, O. & Singh, K.B. (2006) Resistance to insect pests: what do legumes have to offer? Euphytica 147, 273285.CrossRefGoogle Scholar
Farrell, J.A. & Stufkens, M.W. (1981) Field evaluation of lucerne cultivars for resistance to blue-green lucerne aphid and pea aphid (Acyrthosiphon spp.) in New Zealand. New Zealand Journal of Agricultural Research 24, 217220.CrossRefGoogle Scholar
Ferry, N., Edwards, M.G., Gatehouse, J.A. & Gatehouse, A.M.R. (2004) Plant–insect interactions: molecular approaches to insect resistance. Current Opinion in Biotechnology 15, 155161.CrossRefGoogle ScholarPubMed
Gao, L.-L., Anderson, J.P., Klingler, J.P., Nair, R.M., Edwards, O.R. & Singh, K.B. (2006) Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Molecular Plant–Microbe Interactions, in press.Google Scholar
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.CrossRefGoogle Scholar
Gorz, H.J., Manglitz, G.R. & Haskins, F.A. (1979) Selection for yellow clover aphid and pea aphid resistance in red clover. Crop Science 19, 257260.CrossRefGoogle Scholar
Gutierrez, A.P., Nix, H.A., Havenstein, D.E. & Moore, P.A. (1974) The ecology of Aphis craccivora Koch and subterranean clover stunt virus in southeast Australia. II. A model of cowpea aphid populations in temperate pastures. Journal of Applied Ecology 1, 120.CrossRefGoogle Scholar
Hill, J.R. (2000) Jester. Plant Varieties Journal 13, 40.Google Scholar
Holt, B.F., Hubert, D.A. & Dangl, J.L. (2003) Resistance gene signaling in plants – complex similarities to animal innate immunity. Current Opinion in Immunology 15, 2025.CrossRefGoogle ScholarPubMed
Irwin, J.A.G., Lloyd, D.L. & Lowe, K.F. (2001) Lucerne biology and genetic improvement – an analysis of past activities and future goals in Australia. Australian Journal of Agricultural Research 52, 699712.CrossRefGoogle Scholar
Jimenez, H.O., Caddel, J.L. & Berberet, R.C. (1988) Selection and characterization of tolerance to the spotted alfalfa aphid (Homoptera: Aphididae) in alfalfa. Journal of Economic Entomology 81, 17681774.CrossRefGoogle Scholar
Kaloshian, I. & Walling, L.L. (2005) Hemipterans as plant pathogens. Annual Review of Phytopathology 43, 491521.CrossRefGoogle ScholarPubMed
Kessler, A. & Baldwin, I.T. (2002) Plant responses to insect herbivory. Annual Review of Plant Biology 53, 299328.CrossRefGoogle ScholarPubMed
Klingauf, F.A. (1987) Host plant finding and acceptance. pp. 209223in Minks, A.K. & Harrewijn, P. (Eds) Aphids: their biology, natural enemies and control. Vol. 2A. Amsterdam, Elsevier.Google Scholar
Klingler, J., Powell, G., Thompson, G.A. & Isaacs, R. (1998) Phloem specific aphid resistance in Cucumis melo line AR 5: effects on feeding behaviour and performance of Aphis gossypii. Entomologia Experimentalis et Applicata 86, 7988.CrossRefGoogle Scholar
Klingler, J., Creasy, R., Gao, L., Nair, R.M., Calix, A.S., Jacob, H.S., Edwards, O.R. & Singh, K.B. (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, 14451455.CrossRefGoogle ScholarPubMed
Lake, A.W.H. (1989) Spotted alfalfa aphid survival and reproduction on annual medics with various levels of aphid resistance. Australian Journal of Agricultural Research 40, 117123.CrossRefGoogle Scholar
Lake, A.W.H. (1993) Register of Australian herbage plant cultivars: Medicago truncatula cvv. Caliph, Mogul. Australian Journal of Experimental Agriculture 33, 821824.CrossRefGoogle Scholar
Leather, S.R. & Dixon, A.F.G. (1984) Aphid growth and reproductive rates. Entomologia Experimentalis et Applicata 35, 137140.CrossRefGoogle Scholar
Loi, A., Nutt, B.J., McRobb, R. & Ewing, M.A. (2000) Potential new alternative annual pasture legumes for Australian Mediterranean farming systems. Option Mediterraneennes 45, 5154.Google Scholar
Manglitz, G.R. & Russell, L.M. (1974) Cross matings between Therioaphis maculata (Buckton) and T. trifolii (Monell) (Hemiptera: Homoptera: Aphididae) and their implications in regard to the taxonomic status of the insects. Proceedings of the Entomological Society of Washington 76, 290297.Google Scholar
Martin, G.B., Bogdanove, A.J. & Sessa, G. (2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology 54, 2361.CrossRefGoogle ScholarPubMed
May, G.D. & Dixon, R.A. (2004) Medicago truncatula. Current Biology 14, 180181.CrossRefGoogle ScholarPubMed
Milne, W.M. (1998) Comparative performance of spotted clover aphid and spotted alfalfa aphid on annual medic cultivars. Australian Journal of Experimental Agriculture 38, 247252.CrossRefGoogle Scholar
Nair, R.M., Craig, A.D., Auricht, G.C., Edwards, O.R., Robinson, S.S., , M.J., , O. & Jones, J.A. (2003) Evaluating pasture legumes for resistance to aphids. Australian Journal of Experimental Agriculture 43, 13451349.CrossRefGoogle Scholar
Ng, J.C.K. & Perry, K.L. (2004) Transmission of plant viruses by aphid vectors. Molecular Plant Pathology 5, 505511.CrossRefGoogle ScholarPubMed
Nielson, M.W. & Kuehl, R.O. (1982) Screening efficacy of spotted alfalfa aphid biotypes and genic systems for resistance in alfalfa. Environmental Entomology 11, 989996.CrossRefGoogle Scholar
Nombela, G., Williamson, V.M. & Muniz, 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.CrossRefGoogle ScholarPubMed
Oerke, E.C. & Dehne, H.W. (2004) Safeguarding production – losses in major crops and the role of crop protection. Crop Protection 23, 275285.CrossRefGoogle Scholar
Oldroyd, G.E. & Geurts, R. (2001) Medicago truncatula, going where no plant has gone before. Trends in Plant Science 6, 552554.CrossRefGoogle ScholarPubMed
Porter, D.R., Burd, J.D., Shufran, K.A. & Webster, J.A. (2000) Efficacy of pyramiding greenbug (Homoptera: Aphididae) resistance genes in wheat. Journal of Economic Entomology 93, 13151318.CrossRefGoogle ScholarPubMed
Ridland, P.M. & Berg, G.N. (1981) Seedling resistance to spotted alfalfa aphid of lucerne and annual medic species in Victoria. Australian Journal of Experimental Agriculture and Animal Husbandry 21, 5962.CrossRefGoogle Scholar
Roche, P., van Arkel, G. & van Heusden, A.W. (1997) A specific PCR assay for resistance to biotypes 1 and 2 of the rosy leaf curling aphid in apple based on an RFLP marker closely linked to the Sd(1) gene. Plant Breeding 116, 567572.Google Scholar
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.CrossRefGoogle ScholarPubMed
Ruggle, P. & Gutierrez, A.P. (1995) Use of life tables to assess host plant resistance in alfalfa to Therioaphis trifolii f. maculata (Homoptera: Aphididae): hypothesis for maintenance of resistance. Environmental Entomology 24, 313325.CrossRefGoogle Scholar
Sunnucks, P., Driver, F., Brown, W.V., Carver, M., Hales, D.F. & Milne, W.M. (1997) Biological and genetic characterisation of morphologically similar Therioaphis trifolii (Hemiptera: Aphididae) with different host utilization. Bulletin of Entomological Research 87, 425436.CrossRefGoogle Scholar
Thatcher, L.F., Anderson, J.P. & Singh, K.B. (2005) Plant defence responses: what have we learnt from Arabidopsis? Functional Plant Biology 32, 119.CrossRefGoogle ScholarPubMed
Thoquet, P., Gherardi, M., Journet, E.-P., Kereszt, A., Ane, J.-M., Prosperi, J.-M. & Huguet, T. (2002) Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biology 2, 1.CrossRefGoogle ScholarPubMed
Vos, P., Simons, G., Jesse, T., Wijbrandi, J., Heinen, L., Hogers, R., Frijters, A., Groenendijk, J., Diergaarde, P., Reijans, M., Fierens-Onstenk, J., de Both, M., Peleman, J., Peleman, J., Liharska, T., Hontelez, J., & Zabeau, M. (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnology 16, 13651370.CrossRefGoogle ScholarPubMed
Webster, J.A., Baker, C.A. & Porter, D.R. (1991) Detection and mechanisms of Russian wheat aphid (Homoptera: Aphididae) resistance in barley. Journal of Economic Entomology 84, 669673.CrossRefGoogle Scholar
Wellings, P.W. (1985) Growth, development, and survival of Acyrthosiphon kondoi (Homoptera: Aphididae) on five cultivars of lucerne. Journal of the Australian Entomological Society 24, 155160.CrossRefGoogle Scholar
Weng, Y., Lazar, M.D., Michels, G.J. & Rudd, J.C. (2004) Phenotypic mechanisms of host resistance against greenbug (Homoptera: Aphididae) revealed by near isogenic lines of wheat. Journal of Economic Entomology 97, 654660.CrossRefGoogle ScholarPubMed
Zarrabi, A.A., Berberet, R.C., Payton, M.E. & Hoard, G.E. (2004) Within-plant distribution of Acyrthosiphon kondoi (Homoptera: Aphididae) on alfalfa. Environmental Entomology 34, 193198.CrossRefGoogle Scholar