Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T12:48:37.440Z Has data issue: false hasContentIssue false

Does phloem-based resistance to aphid feeding affect host-plant acceptance for reproduction? Parturition of the pea aphid, Acyrthosiphon pisum, on two near-isogenic lines of Medicago truncatula

Published online by Cambridge University Press:  03 July 2013

K. Jung Nam*
Affiliation:
Department of Life Sciences, Faculty of Natural Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK
G. Powell
Affiliation:
Department of Life Sciences, Faculty of Natural Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK
J. Hardie
Affiliation:
Department of Life Sciences, Faculty of Natural Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK
*
*Author for correspondence Phone: +44 207594 22242 E-mail: [email protected]

Abstract

Probing behaviour (prior to parturition) and parturition of two clones (PS01 and N116) of the pea aphid, Acyrthosiphon pisum on two genotypes (near-isogenic lines (NILs)) (Q174_5.13 and Q174_9.10) of Medicago truncatula were investigated using electrical penetration graph (EPG) coupled with simultaneous visual monitoring for parturition. Line Q174_5.13 has been reported to show a phloem-based resistance to feeding in the clone PS01 but to be susceptible to the clone N116, whereas Q174_9.10 has shown to be susceptible to both aphid clones. The time taken to first parturition by clone PS01 was similar on Q174_5.13 and Q174_9.10. Prior to parturition, no aphids on Q174_5.13 contacted phloem, but 5% of the aphids on Q174_9.10 showed phloem salivation (recognized by EPG pattern E1). No phloem contact was observed with aphid clone N116 on either NILs of Medicago before first parturition occurred, and the time taken to first larviposition was similar on Q174_5.13 and Q174_9.10. The results indicate that the initiation of parturition of the clone PS01 and N116 on both NILs does not require the phloem contact and seems unchanged by a phloem-based resistance mechanism to feeding on Medicago. This finding suggests that host recognition and decisions about parturition occur before phloem contact or ingestion, and act independently on R-gene-mediated resistance.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bournoville, R., Simon, J.C., Badenhausser, I., Girousse, C., Guilloux, T. & André, S. (2000) Clones of pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae) distinguished using genetic markers, differ in their damaging effect on a resistant alfalfa cultivar. Bulletin of Entomological Research 90, 3339.Google Scholar
Caillaud, C.M. & Via, S. (2000) Specialised feeding behaviour influences both ecological specialisation and assortative mating in sympatric host races of pea aphids. American Naturalist 156, 606621.Google Scholar
Caillaud, C.M., Du Pietro, J.P., Chaubet, B. & Pierre, J.S. (1995) Application of discriminant analysis to electrical penetration graphs of the aphid Sitobion avenae feeding on resistant and susceptible wheat. Journal of Applied Entomology 119, 103106.Google Scholar
Cartier, J.J. & Painter, R.H. (1956) Differential reactions of two biotypes of the corn leaf aphid to resistant and susceptible varieties, hybrids, and selections of sorghums. Journal of Economical Entomology 46, 498508.Google Scholar
Chew, F.S. & Renwick, J.A.A. (1995) Chemical ecology of host-plant choice in Pieris butterflies. pp. 214238in Carde, R.T. & Bell, W.J. (Eds) Chemical Ecology of Insects. New York, USA, Chapman & Hall.Google Scholar
Del Campo, M.L., Via, S. & Caillaud, M.C. (2003) Recognition of host-specific chemical stimulants in two sympatric host races of the pea aphid Acyrthosiphon pisum. Ecological Entomology 28, 405412.CrossRefGoogle Scholar
Ferrari, J., Via, S. & Godfray, H.C.J. (2008) Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution 62, 25082524.CrossRefGoogle ScholarPubMed
Fraenkel, G. (1958) The raison d'etre of secondary plant substances. Science 129, 14661470.CrossRefGoogle Scholar
Gao, L.L., Klingler, J.P., Anderson, J.P., Edwards, O.R. & Singh, K.B. (2008) Characterization of pea aphid resistance to Medicago truncatula. Plant Physiology 146, 9961009.CrossRefGoogle ScholarPubMed
Goffreda, J.C., Mutschler, M.A., Ave, D.A., Tingey, W.A. & Steffens, J.C. (1989) Aphid deterrence by glucose esters in glandular trichome exudate of the wild tomato, Lycopersicon pennellii. Journal of Chemical Ecology 29, 261274.Google Scholar
Goggin, F.L. (2007) Plant-aphid interactions: molecular and ecological perspectives. Current Opinion in Plant Biology 10, 399408.Google Scholar
Isaak, F.A., Sorensen, E.P. & Painter, R.H. (1965) Stability of resistance to pea aphid and spotted alfalfa aphid in several alfalfa clones under various temperature regimes. Journal of Economic Entomology 58, 140143.Google Scholar
Kaloshian, I., Kinsey, M.G., Williamson, V.M. & Ullman, D.E. (2000) Mi-mediated resistance against the potato aphid Macrosiphum euphorbiae (Hemiptera: Aphididae) limits sieve element ingestion. Environmental Entomology 29, 690695.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.Google 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.Google Scholar
Lapointe, S.L. & Tingey, W.M. (1986) Glandular trichomes of Solanum neocardensasii confer resistance to green peach aphid (Homoptera, Aphididae). Journal of Economical Entomology 79, 12641268.Google Scholar
Moran, P.J. & Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology 125, 10741085.Google Scholar
Moran, P.J., Cheng, Y., Cassell, J.L. & Thompson, G.A. (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Archives of Insect Biochemistry and Physiology 51, 182203.Google Scholar
Pegadaraju, V., Louis, J., Singh, V., Reese, J.C., Bautor, J., Feys, B.J., Cook, G., Parker, J.E. & Shah, J. (2007) Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner enhanced disease susceptibility. Plant Journal 52, 332341.Google Scholar
Powell, G. & Hardie, J. (2001) A potent, morph-specific parturition stimulant in the overwintering host plant of the black bean aphid, Aphis fabae. Physiological Entomology 26, 194201.CrossRefGoogle Scholar
Powell, G., Tosh, C.R. & Hardie, J. (2006) Host plant selection by aphids: behavioural, evolutionary, and applied perspectives. Annual Review of Entomology 51, 309330.Google Scholar
Reinink, K., Dieleman, F.L., Jansen, J., Montenarie, A.M. (1989) Interactions between plant and aphid genotypes in resistance of lettuce to Myzus persicae and Macrosiphum euphorbiae. Euphytica 43, 215222.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.Google Scholar
Schoonhoven, L.M., Van Loon, J.J.A. & Dicke, M. (2005) pp. 135207in Insect-Plant Biology. Oxford, UK, Oxford University Press.Google Scholar
Stewart, S.A. (2010) Exploring effective, clone-specific resistance against the pea aphid (Acyrthosiphon pisum) in Medicago truncatula. PhD Thesis, Imperial College London.Google Scholar
Stewart, S.A., Hodge, S., Ismail, N., Mansfield, J.W., Feys, B.J., Prosperi, J.M., Huguet, T., Ben, C., Gentzbittel, L.M. & Powell, G. (2009) The RAP1 gene confers effective, race-specific resistance to the pea aphid in Medicago truncatula independent of the hypersensitive reaction. Molecular Plant-Microbe Interactions 22, 16451655.Google Scholar
Tjallingii, W.F. (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 739745.Google Scholar
Tjallingii, W.F. (1988) Electrical recording of stylet penetration activities. pp. 95108in Minks, A. & Harrewijn, P. (Eds.), Aphids, Their Biology, Natural Enemies and Control. Elsevier. Vol. 2B. Amsterdam, The Netherlands.Google Scholar
Tosh, C.R., Powell, G. & Hardie, J. (2002) Maternal reproductive decisions are independent of feeding in the black bean aphid, Aphis fabae. Journal of Insect Physiology 48, 619629.Google Scholar
Tosh, C.R., Powell, G., Holmes, N.D. & Hardie, J. (2003) Reproductive response of generalist and specialist aphid morphs with the same genotype to plant secondary compounds and amino acids. Journal of Insect Physiology 49, 11731182.CrossRefGoogle ScholarPubMed
Van Helden, M. & Tjallingii, W.F. (1993) Tissue localization of lettuce resistance to the aphid, Nusonoria ribisnigri, using electrical penetration graphs. Entomologia Experimentalis et Applicata 68, 269278.Google Scholar
Will, T., Tjallingii, W.F., Thönnessen, A. & van Bel, A.J.E. (2007) Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences of the United States of America 104, 1053610541.Google Scholar
Via, S. (1999) Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53, 14461457.Google Scholar
Via, S., Bouck, A.C. & Skillman, S. (2000) Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54, 16261637.Google Scholar