Skip to main content
Download PDF
  • I — Coévolution Hôtes Pathogènes: Caractérisation et Gestion de la Diversité Génétique des deux Partenaires / Co-Evolution Hosts Pathogens: Characterization and Management of Genetic Diversity of Both Partners
  • Open access
  • Published:

Spatial pattern for resistance to a pathogen. Theoretical approach and empirical approach at the phenotypic and molecular levels

Étude de la distribution spatiale des résistances à un agent pathogène, par des approches théorique et expérimentale aux niveaux phénotypique et moléculaire

Genetics Selection Evolution volume 33, Article number: S3 (2001) Cite this article

Abstract

A good understanding of the dynamics of host/pathogen interactions and of the factors that shape the spatial distribution of resistance genes is a prerequisite of metapopulation dynamic management of resistance genes. We studied the diversity and spatial structure of natural populations of common bean (Phaseolus vulgaris) for resistance to Colletotrichum lindemuthianum, the causal agent of anthracnose. This study was carried out in Mexico and Argentina both at the phenotypic level and at the molecular level for two families of resistance gene candidates (RGCs). Using a simulation model, we also investigated the effects of migration and selection on the spatial structure of resistance phenotypes in a metapopulation for two genetic determinisms of the interaction (gene-for-gene and matching allele). Our results showed a differentiation between the countries for all the markers and indicated that the RGC, polymorphic in both countries, do not behave as neutral markers. Comparison of the diversities for resistance to strains isolated from wild or cultivated plants suggested that, although there is local adaptation of C. lindemuthianum between the two countries, the coevolution process seems to occur at a very local scale with the maintenance of resistances to allopatric strains, a result consistent with simulations of the models.

Résumé

Un préalable à une gestion dynamique en métapopulation des résistances aux agents pathogènes est une meilleure connaissance des interactions hôte/pathogène et des facteurs qui modifient la répartition spatiale des gènes impliqués dans l’interaction. Nous avons étudié, au Mexique et en Argentine, la diversité et la structuration de populations naturelles de haricot commun (Phaseolus vulgaris) pour la résistance à Colletotrichum lindemuthianum, responsable de l’anthracnose. Cette approche a été menée au niveau phénotypique, au niveau de marqueurs moléculaires neutres (RAPD) et au niveau de deux familles de gènes candidats pour la résistance (RGC). Nos résultats indiquent qu’il existe une différenciation pour tous les marqueurs entre les deux pays et que les RGC, polymorphes dans les deux pays, ne se comportent pas comme des marqueurs neutres. La comparaison des diversités pour les résistances à des souches sauvages ou isolées de cultivars suggère que, bien qu’il existe une adaptation de C. lindemuthianum à l’échelle des deux pays, la coévolution se ferait à une échelle très locale et maintiendrait des résistances à des souches allopatriques. Par ailleurs, nous avons simulé sur une métapopulation l’effet de la migration et de la sélection sur la répartition spatiale des phénotypes de résistance pour deux déterminismes génétiques de l’interaction (gène pour gène et „matching allele”). Pour les mêmes valeurs de paramètres, le niveau de com-patibilité locale est moins élevé pour un déterminisme de type gène pour gène que „matching allele”, l’asymétrie du système gène pour gène favorisant l’hôte lorsque de nombreux loci sont en jeu. Globalement, le niveau d’adaptation locale du parasite diminue lorsque la migration de l’hôte augmente. Une maladaptation locale peut même être observée, en particulier dans un système gène pour gène, si les pressions de sélection réciproques sont fortes. Dans le détail, le test d’une population d’agents pathogènes sur l’ensemble des populations hôtes indique que certaines populations hôtes possèdent des résistances à des populations pathogènes éloignées, et ce quel que soit le niveau d’adaptation locale. Ce résultat est cohérent avec ce qui est observé dans les données expérimentales.

References

  1. Adam-Blondon A.F., Sévignac M., Dron M., A genetic map of common bean to localize specific resistance genes against anthracnose, Genome 37 (1994) 915–924.

    Article  CAS  Google Scholar 

  2. Allard R.W., The genetics of host-pathogen coevolution: Implications for genetic resource conservation, J. Hered. 81 (1990) 1–6.

    Article  CAS  Google Scholar 

  3. Antonovics J., Thrall P.H., Jarosz A.M., Genetics and the spatial ecology of species interactions: the Silene-Ustilago system, in: Tilman D., Kareiva P. (Eds.), Spatial ecology: the role of space in population dynamics and interspecific interactions., Princeton University Press, Princeton, 1997, pp. 146–170.

    Google Scholar 

  4. Beccera Velasquez L., Gepts P., RFLP diversity of common bean (Phaseolus vulgaris) in its centers of origin, Genome 37 (1994) 256–263.

    Article  Google Scholar 

  5. Berglund Brucher O., Brücher H., The South American wild bean (Phaseolus aborigineus BurK.) as ancestor of the common bean, Econ. Bot. 30 (1976) 257–272.

    Article  Google Scholar 

  6. Burdon J.J., Diseases and plant population biology, Cambridge University Press, 1987.

    Google Scholar 

  7. Burdon J.J., Phenotypic and genetic patterns of resistance to the pathogen Phakopsora pachyrhizi in populations of Glycine canecens, Oecologia 73 (1987b) 257–267.

    Article  CAS  Google Scholar 

  8. Burdon J.J., The structure of pathogen populations in natural plant communities, Ann. Rev. Phytopathol. 31 (1993) 305–323.

    Article  Google Scholar 

  9. Burdon J.J., The distribution and origin of genes for race-specific resistance to Melampsora lini in Linum marginale, Evolution 48 (1994) 1564–1575.

    Article  CAS  Google Scholar 

  10. Burdon J.J., Jarosz A.M., Temporal variation in the racial structure of flax rust (Melampsora lini) populations growing on natural stands of wild flax (Linum marginale): local versus metapopulation dynamics, Plant Pathol. 41 (1991) 165–179.

    Article  Google Scholar 

  11. Burdon J.J., Thompson J.N., Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini, J. Ecol. 83 (1995) 199–206.

    Article  Google Scholar 

  12. Burdon J.J., Thrall P.H., Spatial and temporal patterns in coevolving plants and pathogen associations, Amer. Nat. 153 (1999) S15–S33.

    Article  CAS  Google Scholar 

  13. Burdon J.J., Oats J.D., Marshall D.R., Interactions between Avena and Puccinia species. I The wild hosts: Avena barbata Pott. ex Link, A. fatua L., A. ludoviciana Durieu, J. Appl. Ecol. 20 (1983) 571–584.

    Article  Google Scholar 

  14. Caicedo A.L., Schaal B.A., Kunkel B.N., Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA 96 (1999) 302–306.

    Article  CAS  Google Scholar 

  15. Cattan-Toupance I., Diversité et répartition de la résistance à Colletotrichum lindemuthianum dans des populations naturelles de Phaseolus vulgaris LM., Thèse de l’Institut national agronomique Paris-Grignon, 1997, 110 p.

    Google Scholar 

  16. Cattan-Toupance I., Michalakis Y., Neema C., Genetic structure of wild bean populations in their south Andean center of origin, Theor. Appl. Genet. 96 (1998) 844–851.

    Article  CAS  Google Scholar 

  17. Cheng J., Smith-Becker J., Keen N.T., Genetics of plant-pathogen interactions, Curr. Opin. Biotechnol. 9 (1998) 202–207.

    Article  Google Scholar 

  18. Christ B.J., Person C.O., Pope D.D., The genetic determination of variation in pathogenicity, in: Wolfe M.S., Caten C.E. (Eds.), Populations of plant pathogens: their dynamics and genetics, Blackwell Scientific Publications, Oxford, 1987, pp. 7–19.

    Google Scholar 

  19. Clarke D.D., Bevan J.R., Crute I.R., Genetic interactions between wild plants and their parasites, in: Day P.R., Ellis G.J. (Eds), Genetic and plant pathogenesis, Blackwell Scientific Publications, Oxford, 1987, pp. 195–206.

    Google Scholar 

  20. Delmotte F., Bucheli E., Shykoff J.A., Host and parasite populations structure in a natural plant-pathosystem, Heredity 82 (1999) 300–308.

    Article  Google Scholar 

  21. Ebert D., Virulence and local adaptation of a horizontally transmitted parasite, Science 265 (1994) 1084–1086.

    Article  CAS  Google Scholar 

  22. Ferrier-Cana E., Caractérisation d’analogues de gènes de résistance chez le haricot commun Phaseolus vulgaris, regroupés à des locus contenant des spécificités de résistance vis-à-vis du champignon phytopathogène Colletotrichum lindemuthianum. Thèse de Doctorat Université Paris 11, 2000, 196 p.

    Google Scholar 

  23. Flor H.H., Host-parasite interaction in flax rust. Its genetics and other implications, Phytopathol. 45 (1955) 680–685.

    Google Scholar 

  24. Frank S.A., Ecological and genetic models of host-pathogen coevolution, Heredity 67 (1991) 73–83.

    Article  Google Scholar 

  25. Frank S.A., Coevolutionary genetics of plants and pathogens, Evol. Ecol. 7 (1993) 45–75.

    Article  Google Scholar 

  26. Frank S.A., Recognition and polymorphism in host-parasite genetics, Phil. Trans. Roy. Soc. London B 346 (1994) 283–293.

    Article  CAS  Google Scholar 

  27. Freyre R., Skroch P., Geffroy V., Adam-Blondon A.F., Shirmohamadali A., Johnson W.C., Llca V., Nodari R.O., Pereira P.A., Tsai S.M., Tohme J., Dron M., Nienhuis J., Vallejos C.E., Gepts P., Towards an integrated linkage map of common bean 4. Development of a core linkage map and alignment of RFLP maps, Theor. Appl. Genet. 97 (1998) 847–856.

    Article  CAS  Google Scholar 

  28. Gandon S., Capowiez Y., Dubois Y., Michalakis Y., Olivieri I., Local adaptation and gene for gene coevolution in a metapopulation model, Proc. Roy. Soc. London B. 263 (1996) 1003–1009.

    Article  Google Scholar 

  29. Gandon S., Ebert D., Olivieri I., Michalakis Y., Differential adaptation in spacially heterogeneous environments and host-parasite coevolution, in: Mopper S., Strauss S.Y. (Eds.), Genetic structure and local adaptation in natural insect populations, Chapman & Hall, New York, 1998, pp. 325–342.

    Chapter  Google Scholar 

  30. Geffroy V., Creusot F., Falquet J., Sévignac M., Adam-Blondon A.F., Bannerot H., Gepts P., Dron M., A family of LRR sequences in the vicinity of the Co—2 locus for anthracnose resistance in Phaseolus vulgaris and its potential use in marker assisted selection, Theor. Appl. Genet. 96 (1998) 494–502.

    Article  CAS  Google Scholar 

  31. Geffroy V., Sicard D., de Oliveira J.C.F., Sévignac M., Cohen S., Gepts P., Neema C., Langin T., Dron M., Identification of an ancestral gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum, Mol. Plant-Microbe Interact. 12 (1999) 774–784.

    Article  CAS  Google Scholar 

  32. Henry J.P., Pontis C., David J.L., Gouyon P.H., An experiment on dynamic conservation of genetic resources with metapopulations, in: Seitz A., Loeschcke V. (Eds.), Species conservation: A populational-biological approach, Birkhaüser Verlag, Basel, 1991.

    Google Scholar 

  33. Ibrahim K.M., Barret J.A., Evolution of mildew resistance in a hybrid bulk population of barley, Heredity 67 (1991) 247–256.

    Article  Google Scholar 

  34. Jarosz A.M., Burdon J.J., Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: IL Local and regional variation in patterns of resistance and racial structure, Evolution 45 (1991) 1618–1627.

    CAS  PubMed  Google Scholar 

  35. Jarosz A.M., Burdon J.J., Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini III Influence of pathogen epidemics on host survivorship and flower production, Oecologia 89 (1992) 53–61.

    Article  CAS  Google Scholar 

  36. Kaltz O., Shykoff J.A., Local adaptation in host-parasite systems, Heredity 81 (1998) 361–370.

    Article  Google Scholar 

  37. Kaltz O., Gandon S., Michalakis Y., Shykoff J.A., Local maladaptation in the anther-smut fungus Microbotryum violaceum to its host plant Silene latifolia: evidence from a cross-inoculation experiment, Evolution 53 (1999) 395–407.

    PubMed  Google Scholar 

  38. Kelly J.D., Young R.A., Proposed symbols for anthracnose resistance genes, Annu. Rep. Bean Coop. 39 (1996) 20–24.

    Google Scholar 

  39. Le Boulc’h V., David J.L., Brabant P., de Vallavieille-Pope C., Dynamic conservation of variability: responses of wheat populations to different selective forces including powdery mildew, Genet. Sel. Evol. 26 (1994) 221s–240s.

    Article  Google Scholar 

  40. Leister D., Kurth J., Laurie D.A., Yano M., Sasaki T., Devos K., Graner A., Schulze-Lefert P., Rapid reorganization of resistance gene homologues in cereal genomes, Proc. Natl. Acad. Sci. USA 95 (1998) 370–375.

    Article  CAS  Google Scholar 

  41. Lenné J.M., Variation in reaction to anthracnose within native Stylosanthes capitata populations in Minas Gerais, Brazil, Phytopathol. 78 (1988) 131–134.

    Article  Google Scholar 

  42. Lively CM., Jokela J., Clinal variation for local adaptation in a host-parasite interaction, Proc. Roy. Soc. London B 263 (1996) 891–897.

    Article  Google Scholar 

  43. Manning S.D., Woolhouse M.E.J., Ndamba J., Geographic compatibility of the freshwater snail Bulinus globosus and schistosomes for the Zimbabwe Highveld, Int. J. Parasit. (1995) 37–42.

    Google Scholar 

  44. Morand S., Manning S.D., Woolhouse M.E.J., Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility, Proc. Roy. Soc. London B 263 (1996) 119–128.

    Article  CAS  Google Scholar 

  45. Nei M., Estimation of average heterozygocity and genetic distance from a small number of individuals, Genetics 89 (1978) 583–590.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Paillard S., Goldringer I., Enjalbert J., Doussinault G., de Vallavieille-Pope C., Brabant P., Evolution of resistance against powdery mildew in winter wheat populations conducted under dynamic management. I- Is specific seedling resistance selected?, Theor. Appl. Genet. 101 (2000) 449–456.

    Article  CAS  Google Scholar 

  47. Paillard S., Goldringer I., Enjalbert J., Trottet M., David J., de Vallavieille-Pope C., Brabant P., Evolution of resistance against powdery mildew in winter wheat populations conducted under dynamic management. II- Adult plant resistance, Theor. Appl. Genet. 101 (2000) 457–462.

    Article  CAS  Google Scholar 

  48. Parker M.A., Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen, Evolution 39 (1985) 713–723.

    Article  Google Scholar 

  49. Parker M.A., The nature of plant-parasite specificity, Evol. Ecol. 10 (1996) 319–322.

    Article  Google Scholar 

  50. Parniske M., Hammond Kosack K.E., Golstein C., Thomas C.M., Jones D.A., Harrison K., Wulff B.B., Jones J.D.G. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the C f — 4/9 locus of tomato, Cell 91 (1997) 821–832.

    Article  CAS  Google Scholar 

  51. Pastor-Corrales M.A., Tu J.C., Anthracnose, in: Schwartz H.F., Pastor-Corrales M.A. (Eds.), Bean production problems in the tropics, Columbia, CIAT, 1989, pp. 77–105.

    Google Scholar 

  52. Pryor T., Ellis J., The genetic complexity of fungal resistance genes in plants, Adv. Plant Pathol. 10 (1993) 281–305.

    Google Scholar 

  53. Raymond M., Rousset F., A population genetics software for exact tests and ecumenicism, J. Hered. 86 (1995) 248–249.

    Article  Google Scholar 

  54. Sicard D., Buchet S., Michalakis Y., Neema C., Genetic variability of Colletotrichum lindemuthianum in wild populations of common bean, Plant Pathol. 46 (1997) 355–365.

    Article  Google Scholar 

  55. Song W.Y., Pi L.Y., Wang G.L., Gardner J., Holsten T., Ronald P.C. Evolution of the rice Xa21 disease resistance gene family, Plant Cell 9 (1997) 1279–1287.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Thompson J.N., The coevolutionary process, University of Chicago Press, Chicago, 1994.

    Book  Google Scholar 

  57. Thompson J.N., Burdon J.J., Gene-for-gene coevolution between plants and parasites, Nature 360 (1992) 121–125.

    Article  Google Scholar 

  58. Thrall P.H., Antonovics J., Theoretical and empirical studies of metapopulations: population and genetic dynamics of the Silene- Ustilago system., Can. J. Bot. 73 (1995) S1249–S1258.

    Article  Google Scholar 

  59. Thrall P.H., Burdon J.J., Host-pathogen dynamics in a metapopulation context: the ecological and evolutionary consequences of being spatial, J. Ecol. 85 (1997) 743–753.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de pathologie végétale, INAPG, 16 rue Claude Bernard, 75231, Paris Cedex 05, France

    Claire Neema & Juliette de Meaux

  2. Laboratoire de phytopathologie moléculaire, IBP-Bât 630, Université Paris 11, 91405, Orsay, France

    Claire Lavigne, Juliette de Meaux, Isabelle Cattan-Toupance & Thierry Langin

  3. Laboratoire d’Écologie, Systématique et Évolution, Bât. 362, UPRES-A 8079, Université Paris XI, 91405, Orsay, France

    Julio Franco de Oliveira & Alexandra Deville

Authors
  1. Claire Neema
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claire Lavigne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juliette de Meaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabelle Cattan-Toupance
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Julio Franco de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alexandra Deville
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thierry Langin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claire Neema.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Cite this article

Neema, C., Lavigne, C., de Meaux, J. et al. Spatial pattern for resistance to a pathogen. Theoretical approach and empirical approach at the phenotypic and molecular levels. Genet Sel Evol 33 (Suppl 1), S3 (2001). https://doi.org/10.1186/BF03500870

Download citation

  • Published:

  • DOI: https://doi.org/10.1186/BF03500870

Keywords

Mots clés

Genetics Selection Evolution

ISSN: 1297-9686