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Performance and feeding behaviour of two biotypes of the black currant-lettuce aphid, Nasonovia ribisnigri, on resistant and susceptible Lactuca sativa near-isogenic lines

Published online by Cambridge University Press:  13 March 2013

Cindy J.M. ten Broeke ,
Marcel Dicke  and
Joop J.A. van Loon
Cindy J.M. ten Broeke*
Affiliation:
Laboratory of Entomology, Wageningen, University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands
Marcel Dicke
Affiliation:
Laboratory of Entomology, Wageningen, University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands
Joop J.A. van Loon
Affiliation:
Laboratory of Entomology, Wageningen, University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands
*
*Author for correspondence Phone: 031317482320 E-mail: cindytenbroeke@gmail.com
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Abstract

The black currant-lettuce aphid, Nasonovia ribisnigri, is an important pest of cultivated lettuce, Lactuca sativa. Since 1982, the control of this aphid on lettuce is largely based on host plant resistance, conferred by the Nr gene, introgressed from Lactuca virosa. The resistance mechanism remains to be identified. N. ribisnigri populations virulent on the Nr-based resistance in lettuce have emerged in several locations in Europe since 2007. The objective of this study was to investigate the resistance mechanism mediated by the Nr gene in lettuce by detailed studies of aphid feeding behaviour and performance. Both avirulent (Nr:0) and virulent (Nr:1) biotypes of N. ribisnigri were studied on five resistant and two susceptible near isogenic lines (NILs). In addition, survival and colony development were quantified. Nr:0 aphids showed a strong decrease in sieve element ingestion and took longer to accept a sieve element on resistant NILs compared with susceptible NILs, and no aphids survived on the resistant NIL. Nr:1 aphids fed and performed equally well on the resistant and susceptible NILs. The resistance mechanism against Nr:0 aphids encoded by the Nr gene seems to be located in the phloem, although we also observed differences in feeding behaviour during the pathway phase to the phloem. Nr:1 aphids were highly virulent to the resistance conferred by the Nr gene. The consequences of the appearance of Nr:1 aphids for control of N. ribisnigri are discussed.

Keywords

lettuceelectrical penetration graphhost plant resistancephloem sap ingestionsurvivalisogenic line
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 5 , October 2013 , pp. 511 - 521
Copyright
Copyright © Cambridge University Press 2013 

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References

Alvarez, A.E., Tjallingii, W.F., Garzo, E., Vleeshouwers, V., Dicke, M. & Vosman, B. (2006) Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomologia Experimentalis et Applicata 121, 145–157.CrossRefGoogle Scholar
Annan, I.B., Tingey, W.M., Schaefers, G.A., Tjallingii, W.F., Backus, E.A. & Saxena, K.N. (2000) Stylet penetration activities by Aphis craccivora (Homoptera : Aphididae) on plants and excised plant parts of resistant and susceptible cultivars of cowpea (Leguminosae). Annals of the Entomological Society of America 93, 133–140.CrossRefGoogle Scholar
Barber, M.D., Moores, G.D., Tatchell, G.M., Vice, W.E. & Denholm, I. (1999) Insecticide resistance in the currant-lettuce aphid, Nasonovia ribisnigri (Hemiptera: Aphididae) in the UK. Bulletin of Entomological Research 89, 17–23.Google Scholar
Blackman, R.L. & Eastop, V.W. (2000) Aphids on the World's Crops: An Indentification and Information Guide. Chichester, Wiley & Sons Ltd., pp. 466.Google Scholar
Boissot, N., Thomas, S., Marchal, C. & Dogimont, C. (2010) Mapping and validation of QTLs for resistance to aphids and whiteflies in melon. Theoretical and Applied Genetics 121, 9–20.Google Scholar
Caillaud, C.M. & Niemeyer, H.M. (1996) Possible involvement of the phloem sealing system in the acceptance of a plant as host by an aphid. Experientia 52, 927–931.Google Scholar
Caillaud, C.M., Pierre, J.S., Chaubet, B. & Di Pietro, J.P. (1995) Analysis of wheat resistance to the cereal aphid Sitobion avenae using electrical penetration graphs and flow charts combined with correspondence analysis. Entomologia Experimentalis et Applicata 75, 9–18.CrossRefGoogle Scholar
Casteel, C.L., Walling, L.L. & Paine, T.D. (2006) Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomologia Experimentalis et Applicata 121, 67–72.CrossRefGoogle Scholar
Chen, J.Q., Rahbé, Y., Delobel, B., Sauvion, N., Guillaud, J. & Febvay, G. (1997) Melon resistance to the aphid Aphis gossypii: behavioural analysis and chemical correlations with nitrogenous compounds. Entomologia Experimentalis et Applicata 85, 33–44.Google Scholar
Cole, R.A. (1994) Locating a resistance mechanism to the cabbage aphid in two wild Brassicas. Entomologia Experimentalis et Applicata 71, 23–31.Google Scholar
Crompton, D.S. & Ode, P.J. (2010) Feeding behavior analysis of the soybean aphid (Hemiptera: Aphididae) on resistant soybean 'Dowling'. Journal of Economic Entomology 103, 648–653.Google Scholar
Davis, R.M., Subbarao, K.V., Raid, R.N. & Kurtz, E.A. (1997) Compendium of lettuce diseases. MN, USA, St. Paul: APS press, pp. 79.Google Scholar
Dieleman, F.L. & Eenink, A.H. (1980) Breeding lettuce (Lactuca sativa) for resistance tot the aphid Nasonovia ribisnigriin Minks, A.K. & Gruyss, P. (Eds) Integrated Control of Insect Pests in The Netherlands. Wageningen, Centre for Agricultural Publishing and Documentation. 183–185Google Scholar
Dogimont, C., Bendahmane, A., Chovelon, V. & Boissot, N. (2010) Host plant resistance to aphids in cultivated crops: genetic and molecular bases, and interactions with aphid populations. Comptes Rendus Biologies 333, 566–573.Google Scholar
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586–608.Google Scholar
Flor, H.H. (1955) Host-parasite interaction in flax-rust – its genetics and other implications. Phytopathology 45, 680–685.Google Scholar
Goffreda, J.C., Mutschler, M.A. & Tingey, W.M. (1988) Feeding behavior of potato aphid affected by glandular trichomes of wild tomato. Entomologia Experimentalis et Applicata 48, 101–107.Google Scholar
Haile, F.J., Kerns, D.L., Richardson, J.M. & Higley, L.G. (2000) Impact of insecticides and surfactant on lettuce physiology and yield. Journal of Economic Entomology 93, 788–794.Google Scholar
Hogenhout, S.A. & Bos, J.I.B. (2011) Effector proteins that modulate plant-insect interactions. Current Opinion in Plant Biology 14, 422–428.Google Scholar
Jacquet, M., Bongiovanni, M., Martinez, M., Verschave, P., Wajnberg, E. & Castagnone-Sereno, P. (2005) Variation in resistance to the root-knot nematode Meliodogyne incognita in tomato genotypes bearing the Mi gene. Plant Pathology 54, 93–99.Google Scholar
Jones, J.D.G. & Dangl, J.L. (2006) The plant immune system. Nature 444, 323–329.Google Scholar
Kaloshian, I., Kinsey, M.G., Ullman, D.E. & 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.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, 690–695.Google Scholar
Kift, N.B., Mead, A., Reynolds, K., Sime, S., Barber, M.D., Denholm, I. & Tatchell, G.M. (2004) The impact of insecticide resistance in the currant-lettuce aphid, Nasonovia ribisnigri, on pest management in lettuce. Agricultural and Forest Entomology 6, 295–309.Google Scholar
Kim, K.S., Hill, C.B., Hartman, G.L., Mian, M.A.R. & Diers, B.W. (2008) Discovery of soybean aphid biotypes. Crop Science 48, 923–928.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, 79–88.Google Scholar
Liu, Y.B. (2004) Distribution and population development of Nasonovia ribisnigri (Homoptera: Aphididae) in iceberg lettuce. Journal of Economic Entomology 97, 883–890.Google Scholar
Liu, Y.B. & McCreight, J.D. (2006) Responses of Nasonovia ribisnigri (Homoptera: Aphididae) to susceptible and resistant lettuce. Journal of Economic Entomology 99, 972–978.Google Scholar
Lombaert, E., Carletto, J., Piotte, C., Fauvergue, X., Lecoq, H., Vanlerberghe-Masutti, F. & Lapchin, L. (2009) Response of the melon aphid, Aphis gossypii, to host-plant resistance: evidence for high adaptive potential despite low genetic variability. Entomologia Experimentalis et Applicata 133, 46–56.Google Scholar
McCreight, J.D. (2008) Potential sources of genetic resistance in Lactuca spp. to the lettuce aphid, Nasanovia ribisnigri (Mosely) (Homoptera: Aphididae). HortScience 43, 1355–1358.Google Scholar
McDougall, S. & Creek, A. (2007) Current lettuce aphid Nasonovia ribisnigri (Mosley). Primefact 155, 1–4.Google Scholar
McHale, L., Tan, X., Koehl, P. & Michelmore, R.W. (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biology 7, 212.CrossRefGoogle ScholarPubMed
Mentink, P.J.M., Kimmins, F.M., Harrewijn, P., Dieleman, F.L., Tjallingii, W.F., van Rheenen, B. & Eenink, A.H. (1984) Electrical penetration graphs combined with stylet cutting in the study of host plant resistance to aphids. Entomologia Experimentalis et Applicata 35, 210–213.Google Scholar
Milligan, S.B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P., & Williamson, V.M. (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell Online 10, 1307–1319.Google Scholar
Mitchell, C., Johnson, S.N., Gordon, S.C., Birch, A.N.E. & Hubbard, S.F. (2009) combining plant resistance and a natural enemy control Amphorophora idaei. BioControl 55, 1–7.Google Scholar
Montllor, C.B. & Tjallingii, W.F. (1989) Stylet penetration by two aphid species on susceptible and resistant lettuce. Entomologia Experimentalis et Applicata 52, 103–111.Google Scholar
Pallipparambil, G.R., Reese, J.C., Avila, C.A., Louis, J.M. & Goggin, F.L. (2010) Mi-mediated aphid resistance in tomato: tissue localization and impact on the feeding behavior of two potato aphid clones with differing levels of virulence. Entomologia Experimentalis et Applicata 135, 295–307.Google Scholar
Parker, I.M. & Gilbert, G.S. (2004) The evolutionary ecology of novel plant-pathogen interactions. Annual Review of Ecology, Evolution, and Systematics 35, 675–700.Google Scholar
Pauquet, J., Burget, E., Hagen, L., Chovelon, V., Menn, A.L., Valot, N., Desloire, S., Caboche, M., Rousselle, P., Pitrat, M., Bendahmane, A. & Dogimont, C. (2004). Map-based cloning of the Vat gene from melon conferring resistance to both aphid colonization and aphid transmission of several viruses. pp. 325–329 in Progress in cucurbit genetics and breeding research. Proceedings of Cucurbitaceae 2004, the 8th EUCARPIA Meeting on Cucurbit Genetics and Breeding, 12–17 July 2004, Olomouc, Czech Republic.Google Scholar
Pompon, J. & Pelletier, Y. (2012) Changes in aphid probing behaviour as a function of insect age and plant resistance level. Bulletin of Entomological Research 104, 1–8.Google Scholar
Reinink, K. & Dieleman, F.L. (1989) Comparison of sources of resistance to leaf aphids in lettuce (Lactuca sativa L.). Euphytica 40, 21–29.CrossRefGoogle Scholar
Sarria, E., Cid, M., Garzo, E. & Fereres, A. (2009) Excel workbook for automatic parameter calculation of EPG data. Computers and Electronics in Agriculture 67, 35–42.Google Scholar
Sauge, M.H., Poëssel, J.L., Guillemaud, T. & Lapchin, L. (2011) Resistance induction and herbivore virulence in the interaction between Myzus persicae (Sulzer) and a major aphid resistance gene (Rm2) from peach. Arthropod-Plant Interactions 5, 369–377.Google Scholar
Sauge, M.H., Lambert, P. & Pascal, T. (2012) Co-localisation of host plant resistance QTLs affecting the performance and feeding behaviour of the aphid Myzus persicae in the peach tree. Heredity 108, 292–301.Google Scholar
Stufkens, M.A.W. & Wallace, A.R. (2004) Effectiveness and persistence of six insecticides for control of lettuce aphid on field lettuce in Canterbury. New Zealand Plant Protection 57, 233–238.CrossRefGoogle Scholar
Thabius, A.P.P., Teekens, K.C. & Van Herwijnen, Z.O. (2011) Lettuce that is resistant to the lettuce aphid Nasonovia ribisnigri biotype 1. World Intellectual Property Organization. PCT/EP2010/067588.Google Scholar
Thomas, S., Dogimont, C. & Boissot, N. (2012) Association between Aphis gossypii genotype and phenotype on melon accessions. Arthropod-Plant Interactions 6, 93–101.Google Scholar
Tjallingii, W.F. (1985) Electrical nature of recorded signals during stylet penetration by aphids. Entomologia Experimentalis et Applicata 38, 177–186.Google Scholar
Tjallingii, W.F. (1986) Wire effects on aphids during electrical recording of stylet penetration. Entomologia Experimentalis et Applicata 40, 89–98.Google Scholar
Tjallingii, W.F. (1988) Electrical recording of stylet penetration activities. pp. 95–108in Minks, A.K. & Harrewijn, P. (Eds) Aphids: Their Biology, Natural Enemies and Control 2B. Amsterdam, Elsevier Science Publishers.Google Scholar
Tjallingii, W.F. (1994) Sieve element acceptance by aphids. European Journal of Entomology 91, 47–52.Google Scholar
Tjallingii, W.F. (1995) Aphid-plant interactions: what goes on in the depth of the tissues? Proceedings of Experimental and Applied Entomology 6, 163–169.Google Scholar
Tolmay, V.L., Lindeque, R.C. & Prinsloo, G.J. (2007) Preliminary evidence of a resistance-breaking biotype of the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), in South Africa. African Entomology 15, 228–230.CrossRefGoogle Scholar
Tzortzakakis, E., Trudgill, D. & Phillips, M. (1998) Evidence for a dosage effect of the Mi gene on partially virulent isolates of Meloidogyne javanica. Journal of nematology 30, 76–80.Google Scholar
Van der Arend, A.J.M. (2003) The possibility of Nasonovia ribisnigri resistance breaking biotype development due to plant host resistance: a literature study. in Van Hintum, T.J.L., Lebeda, D., Pink, D. & Schut, J.W. (Eds) Proceedings of the EUCARPIA Meeting on Leafy Vegetables Genetics and Breeding, Noordwijkerhout, The Netherlands, 75–81Google Scholar
van Helden, M. & Tjallingii, W.F. (1993) Tissue localisation of lettuce resistance to the aphid Nasonovia ribisnigri using electrical penetration graphs. Entomologia Experimentalis et Applicata 68, 269–278.Google Scholar
van Helden, M. & Tjallingii, W.F. (2000) Experimental design and analysis and EPG experiments with emphasis on plant resistance research. pp. 144–171in Walker, G.P. & Backus, E.A. (Eds) Principles and Applications of electronic Monitoring and other Techniques in the Study of Homopteran Feeding Behaviour. Lanham, Thomas Say Publications in Entomology.Google Scholar
van Helden, M., Tjallingii, W.F. & Dieleman, F.L. (1993) The resistance of lettuce (Lactuca sativa L.) to Nasonovia ribisnigri: bionomics of N. ribisnigri on near isogenic lettuce lines. Entomologia Experimentalis et Applicata 66, 53–58.CrossRefGoogle Scholar
van Helden, M., Tjallingii, W.F. & Van Beek, T.A. (1994) Phloem sap collection from lettuce (Lactuca sativa L.): Methodology and yield. Journal of Chemical Ecology 20, 3173–3190.Google Scholar
van Helden, M., van Heest, H.P., van Beek, T.A. & Tjallingii, W.F. (1995) Development of a bioassay to test phloem sap samples from lettuce for resistance to Nasonovia ribisnigri (Homoptera, Aphididae). Journal of Chemical Ecology 21, 761–774.Google Scholar
Walker, G.P. (2000) A biginner's guide to electonic monitoring of homopteran probing behavior. pp. 14–40in Walker, G.P. & Backus, E.A. (Eds) Principles and Applications of Electronic Monitoring and other Techniques in the Study of Homopteran Feeding Behaviour. Lanham, Thomas Say Publications in Entomology.Google Scholar
Wilkinson, T.L. & Douglas, A.E. (1998) Plant penetration by pea aphids (Acyrthosiphon pisum) of different plant range. Entomologia Experimentalis et Applicata 87, 43–50.Google Scholar