Theoretical Ecology

, 2:229 | Cite as

Spatial deployment of gene-for-gene resistance governs evolution and spread of pathogen populations

  • Natalia SapoukhinaEmail author
  • Charles-Eric Durel
  • Bruno Le Cam
Original paper


We formulate a spatially realistic population-genetic model for ascertaining the synergetic effect between genetic and spatial composition of the host population on the pathogen spread reinforced by evolutionary processes. We show that spatial arrangement of host genotypes is crucial to the efficacy of host genetic diversification. In particular, the reductive effect of multigenic resistance on the pathogen density can be produced by a random patterning of monogenic resistances. Random patterns can reduce both density and genetic diversity of the pathogen population and delay invasion promoted by sexual recombination. By contrast, patchy distributions diversify pathogen population and, hence, reduce the efficacy of resistance genes. The proposed approach provides theoretical support for studying fast emergence and spread of novel pathogen genotypes carrying multiple virulence genes. It has a practical applicability to design innovative strategies for the most appropriate deployment of plant resistance genes.


Reaction–diffusion Spatial heterogeneity Spatial spread Recombination Gene-for-gene resistance 



We thank the three anonymous reviewers for detailed comments and useful suggestions that have greatly improved the manuscript. We thank Christian Jost, Jean-Pierre Paulin and James Dat for valuable comments on the manuscript. The research is supported by ‘Région Pays de la Loire’ and SPE Department of INRA.


  1. Alphey N, Coleman PG, Bonsall MB, Alphey L (2008) Proportions of different habitat types are critical to the fate of a resistant allele. Theor Ecol 1:103–105CrossRefGoogle Scholar
  2. Boots M, Sasaki A (1999) ‘Small worlds’ and the evolution of virulence: Infection occurs locally and at a distance. Proc R Soc Lond B Biol Sci 266:1933–1938CrossRefGoogle Scholar
  3. Boots M, Hudson PJ, Sasaki A (2004) Large shifts in pathogen virulence relate to host population structure. Science 303:842–844CrossRefPubMedGoogle Scholar
  4. Castagnone-Sereno P, Bongiovanni M, Wajnberg E (2007) Selection and parasite evolution: a reproductive fitness cost associated with virulence in the parthenogenetic nematode Meloidogyne incognita. Evol Ecol 21:259–270CrossRefGoogle Scholar
  5. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833CrossRefPubMedGoogle Scholar
  6. Didelot F, Brun L, Parisi L (2007) Effects of cultivar mixtures on scab control in apple orchards. Plant Pathol 56:1014–1022CrossRefGoogle Scholar
  7. Ellstrand NC, Schierenbeck KA (2000) Hybridisation as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci U S A 97:7043–7050CrossRefPubMedGoogle Scholar
  8. Finckh MR (2008) Integration of breeding and technology into diversification strategies for disease control in modern agriculture. Eur J Plant Pathol 121:399–409CrossRefGoogle Scholar
  9. Flor HH (1956) The complementary genic systems in flax and flax rust. Adv Genet 8:29–54CrossRefGoogle Scholar
  10. Frank SA (1993) Coevolutionary genetics of plants and pathogens. Evol Ecol 7:45–75CrossRefGoogle Scholar
  11. Galvani AP (2003) Epidemiology meets evolutionary ecology. Trends Ecol Evol 18:132–139CrossRefGoogle Scholar
  12. Guérin F, Gladieux P, Le Cam B (2007) Origin and colonization history of newly virulent strains of the phytopathogenic fungus Venturia inaequalis. Fungal Genet Biol 44:284–292CrossRefPubMedGoogle Scholar
  13. Hall RJ, Hastings A, Ayres D (2006) Explaining the explosion: modeling hybrid invasions. Proc R Soc Lond B Biol Sci 273:1385–1389CrossRefGoogle Scholar
  14. Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A et al (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101CrossRefGoogle Scholar
  15. Huang R, Kranz J, Welz HG (1994) Selection of pathotypes of Erisyphe graminis f. sp. hordei in pure and mixed stands of spring barley. Plant Pathol 43:458–470CrossRefGoogle Scholar
  16. Huang Y-L, Li Z-Q, Evans N, Rouxel T, Fitt BDL, Balesdent M-H (2006) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur J Plant Path 114:77–89CrossRefGoogle Scholar
  17. Kinezaki N, Kawasaki K, Takasu F, Shigesada N (2003) Modeling biological invasions into periodically fragmented environments. Theor Popul Biol 64:291–302CrossRefPubMedGoogle Scholar
  18. Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci U S A 104:3883–3888CrossRefPubMedGoogle Scholar
  19. Leach JE, Vera Cruz CM, Bai J, Leung H (2001) Pathogen fitness penalty as a predictor of durability of disease resistance genes. Ann Rev Phytopathol 39:187–224CrossRefGoogle Scholar
  20. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  21. Levene H (1953) Genetic equilibrium when more than one ecological niche is available. Am Nat 87:331–333CrossRefGoogle Scholar
  22. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Ann Rev Phytopathol 40:349–379CrossRefGoogle Scholar
  23. Melbourne BA, Howard VC, Davies KF, Dugaw CJ, Elmendorf S, Freestone AL et al (2007) Invasion in a heterogeneous world: resistance, coexistence or hostile takeover? Ecol Let 10:77–94CrossRefGoogle Scholar
  24. Mundt CC (1990) Probability of mutation to multiple virulence and durability of resistance gene pyramids. Phytopathology 80:221–223CrossRefGoogle Scholar
  25. Mundt CC (2002) Use of multiline cultivars and cultivar mixtures for disease management. Ann Rev Phytopathol 40:381–410CrossRefGoogle Scholar
  26. Murray JD (1993) Mathematical Biology, 3rd edn. Springer, HeidelbergGoogle Scholar
  27. Ohtsuki A, Sasaki A (2006) Epidemiology and disease-control under gene-for-gene plant-pathogen interaction. J Theor Biol 238:780–794CrossRefPubMedGoogle Scholar
  28. Okubo A, Levin SA (2002) Diffusion and ecological problems: Modern perspectives, 2nd edn. Springer, New YorkGoogle Scholar
  29. Otten W, Bailey DJ, Gilligan CA (2004) Empirical evidence of spatial thresholds to control invasion of fungal parasites and saprotrophs. New Phytol 163:125–132CrossRefGoogle Scholar
  30. Parlevliet JE (2002) Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica 124:147–156CrossRefGoogle Scholar
  31. Pietravalle S, Lemarié S, van den Bosch F (2006) Durability of resistance and cost of virulence. Eur J Plant Path 114:107–116CrossRefGoogle Scholar
  32. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical Recipes in C: The Art of Scientific Computing, 2nd edn. Cambridge University Press, LondonGoogle Scholar
  33. Richter O, Seppelt R (2004) Flow of genetic information through agricultural ecosystems: a generic modelling framework with application to pesticide-resistance weeds and genetically modified crops. Ecol Model 171:55–66CrossRefGoogle Scholar
  34. Sapoukhina N, Tyutyunov Y, Arditi R (2003) The role of prey taxis in biological control: a spatial theoretical model. Am Nat 162:61–76CrossRefPubMedGoogle Scholar
  35. Sasaki A (2000) Host-parasite coevolution in a multilocus gene-for-gene system. Proc R Soc Lond B Biol Sci 267:2183–2188CrossRefGoogle Scholar
  36. Segarra J (2005) Stable polymorphism in a two-locus gene-for-gene system. Phytopathology 95:728–736CrossRefPubMedGoogle Scholar
  37. Shigesada N, Kawasaki K (1997) Biological invasions: Theory and practice. Oxford University Press, OxfordGoogle Scholar
  38. Sivasithamparam K, Barbetti MJ, Li H (2005) Recurring challenges from a necrotrophic fungal plant pathogen: a case study with Leptosphaeria maculans (causal agent of blackleg disease in Brassicas) in Western Australia. Ann Bot 96:363–377CrossRefPubMedGoogle Scholar
  39. Stukenbrock EH, McDonald BA (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopatol 46:75–100CrossRefGoogle Scholar
  40. Svirezhev Y, Passekov VP (1990) Fundamentals of Mathematical Evolutionary Genetics. Kluwer, DordrechtGoogle Scholar
  41. Thrall PH, Burdon JJ (2002) Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathology 51:169–184CrossRefGoogle Scholar
  42. Thrall PH, Burdon JJ (2003) Evolution of virulence in a plant host–pathogen metapopulation. Science 299:1735–1737CrossRefPubMedGoogle Scholar
  43. van den Bosch F, Gilligan CA (2003) Measures of durability of resistance. Phytopathology 93:616–625CrossRefPubMedGoogle Scholar
  44. Zhao J-Z, Cao J, Collins HL, Bates SL, Roush RT, Earle ED, Shelton AM (2005) Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc Natl Acad Sci U S A 102:8426–8430CrossRefPubMedGoogle Scholar
  45. Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Fan J, Yang S, Hee L, Zeung H et al (2000) Genetic diversity and disease control in rice. Nature 406:718–722CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Natalia Sapoukhina
    • 1
    Email author
  • Charles-Eric Durel
    • 2
  • Bruno Le Cam
    • 1
  1. 1.UMR077 INRA/AGROCAMPUS OUEST/UA-Plant Pathology-PaVéINRA AngersBeaucouzéFrance
  2. 2.UMR1259 INRA/AGROCAMPUS OUEST/UA-Genetics and Horticulture-GenhortINRA AngersBeaucouzéFrance

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