Skip to main content
Log in

The population genetics of plant pathogens and breeding strategies for durable resistance

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

The durability of disease resistance is affected by the evolutionary potential of the pathogen population. Pathogens with a high evolutionary potential are more likely to overcome genetic resistance than pathogens with a low evolutionary potential. We will propose a set of guidelines to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure. Under our model of pathogen evolution, the two most important parameters to consider are reproduction/mating system and gene/genotype flow. Pathogens that pose the greatest risk of breaking down resistance genes are those that possess a mixed reproduction system, with at least one sexual cycle per growing season and asexual reproduction during the epidemic phase, and a high potential for gene flow. The lowest risk pathogens are those with strict asexual reproduction and low potential for gene flow. We will present examples of high- and low-risk pathogens. Knowledge of the population genetic structure of the pathogen may offer insight into the best breeding strategy for durable resistance. We will present broad guidelines suggesting a rational method for breeding durable resistance according to the population genetics of the pathogen.

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

  • Anderson, J.B. & L.M. Kohn, 1995. Clonality in soilborne, plantpathogenic fungi. Annu Rev Plant Pathol 33: 369–391.

    CAS  Google Scholar 

  • Biffen, R.H., 1905. Mendel's laws of inheritance and wheat breeding. J Agric Sci 1: 4–48.

    Article  Google Scholar 

  • Bourke, P.M.A., 1964. Emergence of potato blight, 1943-46. Nature (Lond.) 203: 805–808.

    Article  Google Scholar 

  • Brent, K.J. & D.W. Hollomon, 1998. Fungicide Resistance: The Assessment of Risk, pp. 48. FRAC Monograph No. 2, Global Protection Federation.

  • Brown, J.K.M., C.G. Simpson & M.S. Wolfe, 1993. Adaptation of barley powdery mildew populations in England to varieties with two resistance genes. Plant Pathol 42: 108–115.

    Google Scholar 

  • Brown, J.K.M., E.M. Foster & R.B. O'Hara, 1997. Adaptation of powdery mildew populations to cereal varieties in relation to durable and non-durable resistance. In: I.R. Crute, E.B. Holub & J.J. Burdon (Eds.), The Gene-for-Gene Relationship in Plant-Parasite Interaction, pp. 119–138. CAB International, UK.

    Google Scholar 

  • Browning, J.A. & K.J. Frey, 1969. Multiline cultivars as a means of disease control. Annu Rev Phytopathol 7: 355–382.

    Article  Google Scholar 

  • Burdon, J.J. & A.P. Roelfs, 1985. Isozyme and virulence variation in asexually reproducing populations of Puccinia graminis and Puccinia recondita on wheat. Phytopathology 75: 907–913.

    CAS  Google Scholar 

  • Caten, C.E., C. Person, J.V. Groth & S.J. Dhahi, 1983. The genetics of pathogenic aggressiveness in three dikaryons of Ustilago hordei. Can J Bot 62: 1209–1219.

    Google Scholar 

  • Chen, R.S. & B.A. McDonald, 1996. Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics 142: 1119–1127.

    PubMed  CAS  Google Scholar 

  • Chen, R.S. & J.M. Boeger & B.A. McDonald, 1994. Genetic stability in a population of a plant pathogenic fungus over time. Mol Ecol 3: 209–218.

    Google Scholar 

  • Ennos, R.A. & K.C. McConnell, 1995. Using genetic markers to investigate natural selection in fungal populations. Can J Bot 73 (Suppl. 1): S302–S310.

    Google Scholar 

  • Flor, H.H., 1956. The complementary genic systems in flax and flax rust. Adv Gen 8: 29–54.

    Article  Google Scholar 

  • Funnell, D.L., P.S. Matthews & H.D. VanEtten, 2000. Breeding for highly fertile isolates of Nectria haematococca MPVI that are highly virulent on pea and in planta selection for virulent recombinants. Phytopathology 91: 92–101.

    Google Scholar 

  • Goodwin, S.B., 1997. The population genetics of Phytophthora. Phytopathology 87: 462–473.

    PubMed  CAS  Google Scholar 

  • Goodwin, S.B., B.A. Cohen & W.A. Fry, 1994. Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proc Natl Acad Sci USA 91: 11591–11595.

    Article  PubMed  CAS  Google Scholar 

  • Gordon, T.R. & R.D. Martyn, 1997. The evolutionary biology of Fusarium oxysporum. Annu Rev Phytopathol 35: 111–128.

    Article  PubMed  CAS  Google Scholar 

  • Hall, R., 1992. Epidemiology of blackleg of oilseed rape. Can J Plant Pathol 14: 46–55.

    Article  Google Scholar 

  • Hohl, H.R. & K. Iselin, 1984. Strains of Phytophthora infestans from Switzerland with A2 mating type behaviour. Trans Br Mycol Soc 83: 529–531.

    Article  Google Scholar 

  • Hulbert, S.H., P.C. Lyons & J.L. Bennetzen, 1991. Reactions of maize lines carrying Rp resistance genes to isolates of the common rust pathogen, Puccinia sorghi. Plant Dis 75: 1130–1133.

    Article  Google Scholar 

  • Johnson, R., 1992. Reflections of a plant pathologist on breeding for disease resistance, with emphasis on yellow rust and eyespot of wheat. Plant Pathol 41: 239–254.

    Google Scholar 

  • Keller, S.M., J.M. McDermott, R.E. Pettway, M.S. Wolfe & B.A. McDonald, 1997. Gene flow and sexual reproduction in the wheat glume blotch pathogen Phaeosphaeria nodorum (anamorph Stagonospora nodorum). Phytopathology 87: 353–358.

    PubMed  CAS  Google Scholar 

  • Koenig, H.C., R.C. Ploetz & H.C. Kistler, 1997. Fusarium oxysporum f.sp. cubense consists of a small number of divergent and globally distributed clonal lineages. Phytopathology 87: 915–923.

    PubMed  CAS  Google Scholar 

  • Kohli, Y., L.J. Brunner, H. Yoell, M.G. Milgroom, J.B. Anderson, R.A.A. Morrall & L.M. Kohn, 1995. Clonal dispersal and spatial mixing in populations of the plant pathogenic fungus, Sclerotinia sclerotiorum. Mol Ecol 4: 69–77.

    Google Scholar 

  • Kolmer, J.A., 1992. Diversity of virulence phenotypes and effect of host sampling between and within populations of Puccinia recondita f. sp. tritici in Canada. Plant Dis 76: 618–621.

    Article  Google Scholar 

  • Martens, J.W. & P.L. Dyck, 1989. Genetics of resistance to rust in cereals from a Canadian perspective. Can J Plant Pathol 11: 78–85.

    Article  Google Scholar 

  • McDonald, B.A., 1997. The population genetics of fungi: tools and techniques. Phytopathology 87: 448–453.

    PubMed  CAS  Google Scholar 

  • McDonald, B.A., 1999. The population genetics of plant pathogens and resistance breeding strategies. Vortrage für Pflanzenzüchtung, pp. 235-244. Proc German Soc of Plant Breeders and Plant Pathologists.

  • McDonald, B.A. R.E. Pettway, R.S. Chen, J.M. Boeger & J.P. Martinez, 1995. The population genetics of Septoria tritici (teleomorph Mycosphaerella graminicola). Can J Bot 73(Suppl): S292–S301.

    Google Scholar 

  • McDonald, B.A., J. Zhan, O. Yarden, K. Hogan, J. Garton & R.E. Pettway, 1999. The population genetics of Mycosphaerella graminicola and Phaesphaeria nodorum. In: J.A. Lucas, P. Bowyer & H.M. Anderson (Eds.), Septoria on Cereals: A Study of Pathosystems, pp. 44–69. CAB International, UK.

    Google Scholar 

  • McIntosh, R.A., N.H. Luig, D.L. Minle & J. Cusick, 1983. Vulnerability of triticales to wheat stem rust. Can J Plant Pathol 5: 61–69.

    Article  Google Scholar 

  • Park, F.F., D.D. Oates & S. Meldrum, 2000. Recent pathogenic changes in the leaf (brown) rust pathogen of wheat and the crown rust pathogen of oats in Australia in relation to host resistance. Acta Phytopathol Entomol Hung 35: 387–394.

    Google Scholar 

  • Pope, D.D. & C.F. Wehrhan, 1990. Quantitative genetics of disease incidence in Ustilago hordei controlled by virulence and aggressiveness genes. Can J Bot 69: 420–427.

    Google Scholar 

  • Roelfs, A.P. & J.V. Groth, 1980. A comparison of virulence phenotypes in wheat stem rust populations reproducing sexually and asexually. Phytopathology 70: 855–862.

    Google Scholar 

  • Rosewich, U.J., 1996. The Population Genetics of Colletotrichum graminicola from Different Ecosystems of Sorghum, pp. 139. Texas A&M University.

  • Rosewich, U.L., R.E. Pettway, B.A. McDonald & H.C. Kistler, 1999. High levels of gene flow and heterozygote excess characterize Rhizoctonia solani AG-1 1A (Thanatephorus cucumeris) from Texas. Fungal Genet Biol 28: 148–159.

    Article  PubMed  CAS  Google Scholar 

  • Rosewich, U.L., R.E. Pettway, B.A. McDonald, R.R. Duncan & R.A. Frederiksen, 1998. Genetic structure and temporal dynamics of a Colletotrichum graminicola population in a sorghum disease nursery. Phytopathology 88: 1087–1093.

    CAS  PubMed  Google Scholar 

  • Salamati, S., J. Zhan, J.J. Burdon & B.A. McDonald, 2000. The genetic structure of field populations of Rhynchosporium secalis from three continents suggests moderate gene flow and regular recombination. Phytopathology 90: 901–908.

    CAS  PubMed  Google Scholar 

  • Samborski, D.J., 1985. Wheat leaf rust. In: A.P. Roelfs & W.R. Bushnell (Eds.), Cereal Rusts, Vol II, pp. 39–59. Academic Press, New York, London.

    Google Scholar 

  • Stevens, N.E., 1933. The dark ages in plant pathology in America: 1830-1870. J Wash Acad Sci 23: 435–446.

    Google Scholar 

  • Tegtmeier, K.J. & H.D. VanEtten, 1982. The role of pisatin tolerance and degradation in the virulence of Nectria haematococca on peas: A genetic analysis. Phytopathology 72: 608–612.

    Article  CAS  Google Scholar 

  • Torres-Montalvo, J.H., 1998. The Population Genetics of Sporisorium reilianum, the Head Smut Pathogen of Sorghum and Maize, pp. 90. Texas A&M University.

  • Wolfe, M.S., 1984. Trying to understand and control powdery mildew. Plant Pathol 33: 451–466.

    Google Scholar 

  • Wolfe, M.S., 1985. The current status and prospects of multiline cultivars and cultivar mixtures for disease resistance. Annu Rev Phytopathol 23: 251–273.

    Article  Google Scholar 

  • Wolfe, M.S. & J.M. McDermott, 1994. Population genetics of plant pathogen interactions: the example of Erysiphe graminis-Hordeum vulgare pathosystems. Annu Rev Phytopathol 32: 89–113.

    Google Scholar 

  • Zhu, Y., H. Chen, J. Fan, Y. Wang, Y. Li, J. Chen, J. Fan, S. Yang, L. Hu, H. Leung, T.W. Mew, P.S. Teng, Z. Wang & C.C. Mundt, 2000. Genetic diversity and disease control in rice. Nature 406: 718–722.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

McDonald, B.A., Linde, C. The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124, 163–180 (2002). https://doi.org/10.1023/A:1015678432355

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1015678432355

Navigation