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Molecular characterization of clones of the Myzus persicae complex (Hemiptera: Aphididae) differing in their ability to transmit the potato leafroll luteovirus (PLRV)

Published online by Cambridge University Press:  09 March 2007

L. Terradot
Affiliation:
Station de Pathologie végétale, Domaine de la Motte au Vicomte, 35653 Le Rheu Cédex, France
J.-C. Simon*
Affiliation:
Laboratoire de Zoologie, Institut National de la Recherche Agronomique, Domaine de la Motte au Vicomte, 35653 Le Rheu Cédex, France
N. Leterme
Affiliation:
Laboratoire de Zoologie, Institut National de la Recherche Agronomique, Domaine de la Motte au Vicomte, 35653 Le Rheu Cédex, France
D. Bourdin
Affiliation:
Station de Pathologie végétale, Domaine de la Motte au Vicomte, 35653 Le Rheu Cédex, France
A.C.C. Wilson
Affiliation:
Department of Biological Sciences, Macquarie University NSW 2109, Australia
J.-P. Gauthier
Affiliation:
Laboratoire de Zoologie, Institut National de la Recherche Agronomique, Domaine de la Motte au Vicomte, 35653 Le Rheu Cédex, France
Y. Robert
Affiliation:
Laboratoire de Zoologie, Institut National de la Recherche Agronomique, Domaine de la Motte au Vicomte, 35653 Le Rheu Cédex, France
*
* Fax: + 33 (0) 2 99 28 51 50 E-mail: [email protected]

Abstract

A prerequisite to studying the specific interactions involved in the persistent transmission of luteoviruses such as the potato leafroll virus (PLRV) is the characterization of both the virus and its vectors. A range of techniques was used to assess genetic differentiation among 27 clones belonging to the Myzus persicae complex (M. persicae (Sulzer), M. antirrhinii (Macchiati) and M. nicotianaeBlackman) and showing different efficiencies in transmitting PLRV isolates. All M. persicae/M. nicotianae clones belonged to one of two karyotypes, both 2n = 12, either normal or carrying an autosomal translocation (A1,3), and all M. antirrhinii clones had 13 or 14 chromosomes. Amplified esterase 4 genes were detected by PCR–REN assay in M. persicae/M. nicotianae taxa, with gene expression being modified by methylation. Similarly, amplified E4 genes were revealed in M. antirrhinii but they all showed unmethylated. Two allozyme and 11 microsatellite loci discriminated 10 different genotypic classes among the 27 clones. Analysis of genetic relatedness between these genotypic classes revealed that M. nicotianae clones were very closely related to M. persicaeclones, whereas the genetic differentiation between M. antirrhinii and M. persicae was greater. The implications of these results for the taxonomic status of these genotypes within the complex, and the transmission of PLRV, are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1999

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References

Abdel-Aal, Y.A.I., Lampert, E.P., Roe, R.M. & Semtner, P.J. (1992) Diagnostic esterases and insecticide resistance in the tobacco aphid Myzus nicotianae Blackman (Homoptera: Aphididae). Pesticide Biochemistry and Physiology 43, 123133.CrossRefGoogle Scholar
Al-Aboodi, A. & ffrench-Constant, R.H. (1995) RAPD PCR confirms absence of genetic variation between insecticide resistant variants of the green peach aphid, Myzus persicae (Homoptera: Aphididae). Great Lakes Entomologist 28, 127133.Google Scholar
Blackman, R.L. (1971) Chromosomal abnormalities in an anholocyclic biotype of Myzus persicae (Sulzer). Experientia 27, 704706.CrossRefGoogle Scholar
Blackman, R.L. (1974) Life-cycle variation of Myzus persicae (Sulz.) (Hom., Aphididae) in different parts of the world, in relation to genotype and environment. Bulletin of Entomological Research 63, 595607.CrossRefGoogle Scholar
Blackman, R.L. (1980) Chromosome numbers in the Aphididae and their taxonomic significance. Systematic Entomology 5, 725.CrossRefGoogle Scholar
Blackman, R.L. (1987) Morphological discrimination of a tobacco-feeding form from Myzus persicae (Sulzer) (Hemiptera: Aphididae), and a key to New World Myzus (Nectarosiphon) species. Bulletin of Entomological Research 77, 713730.CrossRefGoogle Scholar
Blackman, R.L. & Paterson, A.J.C. (1986) Separation of Myzus (Nectarosiphon) antirrhinii (Macchiati) from Myzus (N.) persicae (Sulzer) and related species in Europe (Homoptera: Aphididae). Systematic Entomology 11, 267276.CrossRefGoogle Scholar
Blackman, R.L. & Spence, J.M. (1992) Electrophoretic distinction between the peach-potato aphid, Myzus persicae, and the tobacco aphid, M. nicotianae (Homoptera: Aphididae). Bulletin of Entomological Research 82, 161165.CrossRefGoogle Scholar
Blackman, R.L., Spence, J.M., Field, L.M. & Devonshire, A.L. (1995) Chromosomal location of the amplified esterase genes conferring resistance to insecticides in Myzus persicae (Homoptera: Aphididae). Heredity 75, 297302.CrossRefGoogle Scholar
Blackman, R.L., Spence, J.M., Field, L.M., Javed, N., Devine, G.D. & Devonshire, A.L. (1996) Inheritance of the amplified esterase genes responsible for insecticide resistance in Myzus persicae (Homoptera: Aphididae). Heredity 77, 154167.CrossRefGoogle Scholar
Bourdin, D., Rouzé, J., Tanguy, S. & Robert, Y. (1998) Variation among clones of Myzus persicae (Sulzer) and Myzus nicotianae Blackman in the transmission of a poorly- and a highly-aphid-transmissible isolate of potato leafroll luteovirus (PLRV). Plant Pathology 47, 794800.Google Scholar
Brookes, C.P. & Loxdale, H.D. (1987) Survey of enzyme variation in British populations of Myzus persicae (Sulzer) (Hemiptera: Aphididae) on crops and weed hosts. Bulletin of Entomological Research 77, 8389.CrossRefGoogle Scholar
Cavalli-Sforza, L.L. & Edwards, A.W.F. (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics 19, 233257.Google ScholarPubMed
Chakraborty, R. & Jin, L. (1993) A unified approach to study hypervariable polymorphisms: statistical considerations of determining relatedness and population distances, pp. 153175in Pena, S.D.J., Chakraborty, R., Epplen, J.T. & Jeffreys, A.J.(Eds) DNA fingerprinting: state of science. Basel, Birkhauser Verlag.CrossRefGoogle Scholar
Devonshire, A.L. (1977) The properties of a carboxylesterase from the peach-potato aphid, Myzus persicae (Sulz.), and its role in conferring insecticide resistance. Biochemical Journal 167, 675683.CrossRefGoogle ScholarPubMed
Devonshire, A.L. & Field, L.M. (1991) Gene amplification and insecticide resistance. Annual Review of Entomology 36, 123.CrossRefGoogle ScholarPubMed
Devonshire, A.L. & Moores, G.D. (1984) Immunoassay of carboxylesterase activity for identifying insecticide resistant Myzus persicae. Proceedings of the British Crop Protection Conference – Pests and Diseases 6A, 515520.Google Scholar
Devonshire, A.L., Field, L.M., Foster, S.P., Moores, G.D., Williamson, M.S. & Blackman, R.L. (1998) The evolution of insecticide resistance in the peach-potato aphid, Myzus persicae. Philosophical Transactions of the Royal Society of London, Series B 353, 16771684.CrossRefGoogle Scholar
Estoup, A., Garnery, L., Solignac, M., & Cornuet, J.-M. (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140, 679695.CrossRefGoogle ScholarPubMed
Fenton, B., Woodford, J.A.T. & Malloch, G. (1998) Analysis of clonal diversity of the peach-potato aphid, Myzus persicae (Sulzer), in Scotland, UK and evidence for the existence of a predominant clone. Molecular Ecology 7, 14751487.CrossRefGoogle ScholarPubMed
Field, L.M. & Devonshire, A.L. (1998) Evidence that the E4 and FE4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer) are part of a gene family. Biochemistry Journal 330, 169–73.CrossRefGoogle ScholarPubMed
Field, L.M., Devonshire, A.L., ffrench-Constant, R.H. & Forde, B.G. (1989) Changes in DNA methylation are associated with loss of insecticide resistance in the peach-potato aphid Myzus persicae (Sulz.). FEBS Letters 243, 323327.CrossRefGoogle Scholar
Field, L.M., Javed, N., Stribley, M.F. & Devonshire, A.L. (1994) The peach-potato aphid Myzus persicae and the tobacco aphid Myzus nicotianae have the same esterase-based mechanisms of insecticide resistance. Insect Molecular Biology 3, 143148.CrossRefGoogle ScholarPubMed
Field, L.M., Crick, S.E. & Devonshire, A.L. (1996) Polymerase chain reaction-based identification of insecticide resistance genes and DNA methylation in the aphid Myzus persicae (Sulzer). Insect Molecular Biology 5, 197202.CrossRefGoogle ScholarPubMed
Gildow, F.E. (1987) Virus-membrane interactions involved in circulative transmission of luteoviruses by aphids. pp. 93120in Harris, K.F.(Ed.) Current topics in vector research. Vol. 4, New York, Springer Verlag.Google Scholar
Hales, D.F., Tomiuk, J., Wöhrmann, K. & Sunnucks, P. (1997) Evolutionary and genetic aspects of aphid biology: a review. European Journal of Entomology 94, 155.Google Scholar
Hebert, P.D.N. & Beaton, M.J. (1989) Methodologies for allozymes analysis using cellulose acetate electrophoresis. Helena Laboratories, Beaumont, Texas.Google Scholar
Heuvel, J.F.J.M.van den, Verbeek, M. & Wilk, F.van der (1994) Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. Journal of General Virology 75, 25592565.CrossRefGoogle ScholarPubMed
Hick, C.A., Field, L.M. & Devonshire, A.L. (1996) Changes in the methylation of amplified esterase DNA during loss and reselection of insecticide resistance in peach-potato aphids, Myzus persicae. Insect Biochemistry and Molecular Biology 26, 4147.CrossRefGoogle ScholarPubMed
Jolly, C.A. & Mayo, M.A. (1994) Changes in the amino acid sequence of the coat protein readthrough domain of potato leafroll luteovirus affect the formation of an epitope and aphid transmission. Virology 201, 182185.CrossRefGoogle ScholarPubMed
Margaritopoulos, J.T., Mamuirs, A. & Tsitsipis, J.A. (1998) Attempted discrimination of Myzus persicae and Myzus nicotianae (Homoptera: Aphididae) by random amplified polymorphic DNA polymerase chain reaction technique. Annals of the Entomological Society of America 91, 602607.CrossRefGoogle Scholar
Martinez-Torres, D., Carrió, R., Latorre, A., Simon, J.-C., Hermoso, A. & Moya, A. (1997) Assessing the nucleotide diversity of three aphid species by RAPD. Journal of Evolutionary Biology 10, 459477.CrossRefGoogle Scholar
Nei, M. (1978) Estimation of average heterozygosity and genetic distances from a small number of individuals. Genetics 89, 583590.CrossRefGoogle ScholarPubMed
Robert, Y. (1971) Epidémiologie de l'enroulement de la pomme de terre: capacité vectrice de stades et de formes des pucerons Aulacorthum solani Kltb, Macrosiphum euphorbiae Thomas et Myzus persicae Sulz. Potato Research 14, 130139.CrossRefGoogle Scholar
Robert, Y. & Maury, Y. (1970) Capacités vectrices comparées de plusieurs souches de Myzus persicae Sulz., Aulacorthum solani Kltb et Macrosiphum euphorbiae Thomas dans l'étude de la transmission de l'enroulement de la pomme de terre. Potato Research 13, 199209.CrossRefGoogle Scholar
Robert, Y., Maury, Y. & Quéméner, J. (1969) Transmission du virus de l'enroulement de la pomme de terre par différentes formes et stades d'une souche de Myzus persicae (Sulz.) (Homoptera: Aphididae): résultats comparés sur Physalis floridana Rydberg et Solanum tuberosum L. var. Claudia. Annales de Phytopathologie 1, 167179.Google Scholar
Rochow, W.F. (1972) Dependent transmission by aphids of barley yellow dwarf luteoviruses from mixed infections. Phytopathology 72, 302305.Google Scholar
Simon, J.-C., Baumann, S., Sunnucks, P., Hebert, P.D.N., Pierre, J.-S., Le Gallic, J.-F. & Dedryver, C.-A. (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Molecular Ecology 8, 531545.CrossRefGoogle ScholarPubMed
Sunnucks, P., England, P.R., Taylor, A.C. & Hales, D.F. (1996) Microsatellite and chromosome evolution of parthenogenetic Sitobion aphids in Australia. Genetics 144, 747756.CrossRefGoogle ScholarPubMed
Sunnucks, P., De Barro, P.J., Lushai, G., Maclean, N. & Hales, D.F. (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology 6, 10591073.CrossRefGoogle Scholar
Wilson, A., Sunnucks, P. & Hales, D.F. (1999) Microevolution, low clonal diversity and genetic affinities of parthenogenetic Sitobion aphids in New Zealand. Molecular Ecology, in press.CrossRefGoogle Scholar