Skip to main content
Log in

Resistance induction and herbivore virulence in the interaction between Myzus persicae (Sulzer) and a major aphid resistance gene (Rm2) from peach

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

In gene-for-gene host–enemy interactions, monogenic plant resistance results from pathogen recognition that initiates the induction of plant defense responses. Schematically, as the result of the on/off process of recognition, phenotypic variability in enemy virulence is expected to be qualitative, with either a failure or a success of host colonization. We focussed on a major gene from peach conferring avoidance resistance against the green peach aphid Myzus persicae. Measurements of herbivore density and time-dependent aspects of resistance induction were examined, as well as variability in the aphid’s ability to exploit the resistant host. Varying densities of infestation did not provoke differences in the aphid’s tendency to leave a plant, and a single aphid was sufficient to elicit a response. Similarly, the duration of infestation did not affect the aphid response. A brief aphid feeding time of 3 h triggered induced resistance, which became effective between 24 and 48 h after the initial attack. Induced resistance decayed over time in the absence of additional infestation. Thirty aphid genotypes collected from natural populations were tested in the laboratory. No clone could colonize the resistant host, suggesting that all of them triggered the induction of effective plant defense responses. However, we detected significant quantitative variation among clones in the tendency of aphids to leave plants. These results improve our understanding of induced resistance as a dynamic phenomenon and suggest that the potential for aphids to adapt to a major plant resistance gene may depend on factors other than the mere capacity to evade recognition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agrawal AA, Karban R (2000) Specificity of constitutive and induced resistance: pigment glands influence mites and caterpillars on cotton plants. Entomol Exp Appl 96:39–49. doi:10.1046/j.1570-7458.2000.00677.x

    Article  CAS  Google Scholar 

  • Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R (2002) Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56:2206–2213. doi:10.1111/j.0014-3820.2002.tb00145.x

    PubMed  Google Scholar 

  • Alston FH, Briggs JB (1977) Resistance genes in apple and biotypes of Dysaphis devecta. Ann Appl Biol 87:75–81

    Article  Google Scholar 

  • Bent AF, Mackey D (2007) Elicitors, effectors, and the R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436. doi:10.1146/annurev.phyto.45.062806.094427

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum MR, Zangerl AR (1998) Chemical phenotype matching between a plant and its insect herbivore. Proc Natl Acad Sci USA 95:13743–13748

    Article  PubMed  CAS  Google Scholar 

  • Brun H, Chèvre AM, Fitt BDL, Powers S, Besnard AL, Ermel M, Huteau V, Marquer B, Eber F, Renard M, Andrivon D (2010) Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 185:285–299. doi:10.1146/annurev.phyto.45.062806.094427

    Article  PubMed  Google Scholar 

  • Burd JD, Porter DR, Puterka GJ, Haley SD, Peairs FB (2006) Biotypic variation among North American Russian wheat aphid (Homoptera: Aphididae) populations. J Econ Entomol 99:1862–1866

    Article  PubMed  Google Scholar 

  • Cox DR (1972) Regression models and life-tables. J Roy Stat Soc B 34:187–220

    Google Scholar 

  • Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307. doi:10.1016/j.tree.2007.02.010

    Article  PubMed  Google Scholar 

  • Dogimont C, Bendahmane A, Pitrat M, Burget-Bigeard E, Hagen L, Le Menn A, Pauquet J, Rousselle P, Caboche M, Chovelon V (2007) Gene resistant to Aphis gossypii. United States of America patent no 0070016977

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Flor HH (1955) Host-parasite interaction in flax rust–its genetics and other implications. Phytopathology 45:680–685

    Google Scholar 

  • Gao LL, Anderson JP, Klingler JP, Nair RM, Edwards OR, Singh KB (2007) Involvement of the octadecanoid pathway in Bluegreen aphid resistance in Medicago truncatula. Mol Plant Microbe Interact 20:82–93. doi:10.1094/MPMI-20-0082

    Article  PubMed  CAS  Google Scholar 

  • Gassmann AJ, Onstad DW, Pittendrigh BR (2009) Evolutionary analysis of herbivorous insects in natural and agricultural environments. Pest Management Sci 65:1174–1181. doi:10.1002/ps.1844

    Article  CAS  Google Scholar 

  • Gómez S, van Dijk W, Stuefer JF (2009) Timing of induced resistance in a clonal plant network. Plant Biol 12:512–517. doi:10.1111/j.1438-8677.2009.00234.x

    Article  Google Scholar 

  • Guillemaud T, Mieuzet L, Simon JC (2003a) Spatial and temporal genetic variability in French populations of the peach-potato aphid, Myzus persicae. Heredity 91:143–152. doi:10.1038/sj.hdy.6800292

    Article  PubMed  CAS  Google Scholar 

  • Guillemaud T, Brun A, Anthony N, Sauge MH, Boll R, Delorme R, Fournier D, Lapchin L, Vanlerberghe-Masutti F (2003b) Incidence of insecticide resistance alleles in sexually-reproducing populations of the peach-potato aphid Myzus persicae (Hemiptera: Aphididae) from southern France. Bull Entomol Res 93:289–297. doi:10.1079/BER2003241

    Article  PubMed  CAS  Google Scholar 

  • Haccou P, Devlas SJ, Van Alphen JJM, Visser ME (1991) Information-processing by foragers–Effects of intra-patch experience on the leaving tendency of Leptopilina heterotoma. J Anim Ecol 60:93–106

    Article  Google Scholar 

  • Harrington DP, Fleming TR (1982) A class of rank test procedures for censored survival data. Biometrika 69:553–566

    Article  Google Scholar 

  • Harris MO, Stuart JJ, Mohan M, Nair S, Lamb RJ, Rohfritsch O (2003) Grasses and gall midges: plant defense and insect adaptation. Annu Rev Entomol 48:549–577. doi:10.1146/annurev.ento.48.091801.112559

    Article  PubMed  CAS  Google Scholar 

  • Hebert SL, Jia L, Goggin FL (2007) Quantitative differences in aphid virulence and foliar symptom development on tomato plants carrying the Mi resistance gene. Environ Entomol 36:458–467

    Article  PubMed  Google Scholar 

  • Kaloshian I, Walling LL (2005) Hemipterans as plant pathogens. Annu Rev Phytopathol 43:491–521. doi:10.1146/annurev.phyto.43.040204.135944

    Article  PubMed  CAS  Google Scholar 

  • Klingler J, Creasy R, Gao L, Nair RM, Calix AS, Spafford Jacob H, Edwards OR, Singh KB (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 Physiol 137:1445–1455. doi:10.1146/annurev.phyto.43.040204.135944

    Article  PubMed  CAS  Google Scholar 

  • Kniskern J, Rausher MD (2001) Two modes of host-enemy coevolution. Popul Ecol 43:3–14. doi:10.1111/j.1365-3040.2008.01823.x

    Article  Google Scholar 

  • Lambert P, Pascal T (2011) Mapping Rm2 gene conferring resistance to the green peach aphid (Myzus persicae Sulzer) in the peach cultivar “Rubira®”. Tree Genet Genomes. doi: 10.1007/s11295-011-0394-2

  • Li Y, Zou J, Li M, Bilgin DD, Vodkin LO, Hartman GL, Clough SJ (2008) Soybean defense responses of the soybean aphid. New Phytol 179:185–195. doi:10.1111/j.1469-8137.2008.02443.x

    Article  PubMed  CAS  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. Entomol Exp Appl 133:46–56. doi:10.1111/j.1570-7458.2009.00904.x

    Article  Google Scholar 

  • Ma Z, Bechinski EJ (2008) A survival-analysis-based simulation model for Russian wheat aphid population dynamics. Ecol Model 216:323–332. doi:10.1016/j.ecolmodel.2008.04.011

    Article  Google Scholar 

  • Massey FP, Roland Ennos A, Hartley SE (2007) Herbivore specific induction of silica-based defences. Oecologia 152:677–683. doi:10.1007/s00442-007-0703-5

    Article  PubMed  Google Scholar 

  • Nikolakakis NN, Margaritopoulos JT, Tsitsipis JA (2003) Performance of Myzus persicae (Hemiptera: Aphididae) clones on different host-plants and their host preference. Bull Entomol Res 93:235–242. doi:10.1079/BER2003230

    Article  PubMed  CAS  Google Scholar 

  • Palloix A, Ayme V, Moury B (2009) Durability of plant major resistance genes to pathogens depends on the genetic background: experimental evidence and consequences for breeding strategies. New Phytol 183:190–199. doi:10.1111/j.1469-8137.2009.02827.x

    Article  PubMed  CAS  Google Scholar 

  • Pascal T, Pfeiffer F, Kervella J, Lacroze JP, Sauge MH (2002) Inheritance of green peach aphid resistance in the peach cultivar ‘Rubira’. Plant Breed 121:459–461. doi:10.1111/j.1439-0523.2002.tb02053.x

    Article  Google Scholar 

  • Poëssel JL, Sauge MH, Corre MN, Renaud C, Gaudillère M, Maucourt M, Deborde C, Dufour C, Loonis M, Lacroze JP, Pascal T, Moing A (2006) Metabolic profiling of shoot apices infested by the peach-potato aphid in susceptible and resistant peach cultivars. Metabolomics 2:288

    Google Scholar 

  • Porter DR, Burd JD, Shufran KA, Webster JA, Teetes GL (1997) Greenbug (Homoptera: Aphididae) biotypes: selected by resistant cultivars or preadapted opportunists? J Econ Entomol 90:1055–1065

    Google Scholar 

  • Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95:9750–9754

    Article  PubMed  CAS  Google Scholar 

  • Sauge MH, Lacroze JP, Poëssel JL, Pascal T, Kervella J (2002) Induced resistance by Myzus persicae in the peach cultivar ‘Rubira’. Entomol Exp Appl 102:29–37. doi:10.1046/j.1570-7458.2002.00922.x

    Article  Google Scholar 

  • Sauge MH, Mus F, Lacroze JP, Pascal T, Kervella J, Poëssel JL (2006) Genotypic variation in induced resistance and induced susceptibility in the peach-Myzus persicae aphid system. Oikos 113:305–313

    Article  Google Scholar 

  • Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16. doi:10.1111/j.1570-7458.2006.00503.x

    Article  CAS  Google Scholar 

  • Stahl EA, Bishop JG (2000) Plant-pathogen arms race at the molecular level. Curr Opin Plant Biol 3:299–304. doi:10.1016/S1369-5266(00)00083-2

    Article  PubMed  CAS  Google Scholar 

  • Stevens MT, Lindroth RL (2005) Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306. doi:10.1007/s00442-005-0128-y

    Article  PubMed  Google Scholar 

  • R Development Core Team (2010) R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing, Vienna, Austria Available at http://wwwR-projectorg. Accessed 22 April 2010

  • Underwood N (2000) Density dependence in induced plant resistance to herbivore damage: threshold, strength and genetic variation. Oikos 89:295–300. doi:10.1034/j.1600-0706.2000.890210.x

    Article  Google Scholar 

  • Weber G (1985) Genetic variability in host plant adaptation of the green peach aphid, Myzus persicae. Entomol Exp Appl. 38:49–56

    Article  Google Scholar 

  • Wittstock U, Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5:300–307. doi:10.1016/S1369-5266(02)00264-9

    Article  PubMed  CAS  Google Scholar 

  • Zangerl AR, Berenbaum MR (1990) Furanocoumarin induction in wild parsnip–Genetics and populational variation. Ecology 7:1933–1940

    Article  Google Scholar 

  • Zehnder CB, Hunter MD (2007) Interspecific variation within the genus Asclepias in response to herbivory by a phloem-feeding insect herbivore. J Chem Ecol 33:2044–2053. doi:10.1007/s10886-007-9364-4

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge J.P. Lacroze for technical assistance, S. Simon for aphid sampling, and C. Favret for English correction of an earlier draft. Part of this work received financial supports from the Institut Français de la Biodiversité and Département Santé des Plantes et Environnement, Institut National de la Recherche Agronomique.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marie-Hélène Sauge.

Additional information

Handling Editor: Michael Smith.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sauge, MH., Poëssel, JL., Guillemaud, T. et al. 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 (2011). https://doi.org/10.1007/s11829-011-9141-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-011-9141-8

Keywords

Navigation