Fitness Costs of Plant Disease Resistance

James K M Brown, John Innes Centre, Norwich, UK

Published online: September 2007

DOI: 10.1002/9780470015902.a0020094

Disease is a major agent of evolution by natural selection because infection by a parasite reduces the fitness of its host, yet all plants suffer from disease. This paradox can be explained if host resistance to disease is most beneficial when most plants are susceptible, and if resistance reduces a plant's fitness in the absence of the parasite. Fitness costs of disease resistance may arise in several ways: physiological and metabolic costs of defence against parasites, developmental traits which allow plants to escape disease but are sub-optimal for seed production, and trade-offs between resistance and responses to other microbes.

Keywords: co evolution; frequency-dependent selection; plant disease; plant breeding; fungi; disease resistance

Figure 1. Natural selection in a coevolving host–parasite interaction.
Figure 2. A gene-for-gene interaction illustrated by barley powdery mildew. The plant has a resistance (RES) gene which is effective only against parasites with an avirulence (AVR) gene (meaning that the parasite cannot cause disease on a host plant with the corresponding RES gene). If the plant has the susceptibility allele (res) of the resistance gene, it cannot recognize the parasite, whether it is avirulent or virulent, and if the parasite has the virulence allele (avr) of the avirulence gene, it cannot be detected by the host. In either case, the host's resistance mechanism fails to detect parasite avirulence and induce effective defences, which results in the plant becoming diseased.
Figure 3. Dynamics of gene-for-gene coevolution. (a) A simple model, lacking direct frequency-dependent selection, in which the graph of allele frequencies spirals outwards from an unstable equilibrium point. (b) A model in which direct frequency-dependent selection is generated by disease being polycyclic; the graph of allele frequencies spirals inwards towards a stable equilibrium.
Figure 4. Forces acting on frequencies of resistance and virulence. An increased cost of resistance reduces the frequency of resistance, which reduces selection for virulence. The increased frequency of virulence reduces selection against resistance, so raising the frequency of resistance to its original value; the net outcome is a reduced frequency of virulence but no change in that of resistance. An increased cost of virulence reduces the frequency of virulence, which increases selection for resistance. The increased frequency of resistance increases selection for virulence, so raising the frequency of virulence to its original level; the net outcome is a higher frequency of resistance but no change in that of virulence.
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 References
    Ayliffe MA, Frost DV, Finnegan EJ et al. (1999) Analysis of alternative transcripts of the flax L6 rust resistance gene. Plant Journal 17: 287–292.
    Bergelson J and Purrington CB (1996) Surveying patterns in the cost of resistance in plants. American Naturalist 148: 536–558.
    van Beuningen LT and Kohli MM (1990) Deviation from the regression of infection on heading and height as a measure of resistance to Septoria tritici blotch in wheat. Plant Disease 74: 488–493.
    Brown JKM (2002) Yield penalties of disease resistance in crops. Current Opinion in Plant Biology 5: 339–344.
    Brown JKM (2003) A cost of disease resistance: paradigm or peculiarity? Trends in Genetics 19: 667–671.
    Brown JKM and Hovmøller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297: 537–541.
    Frank SA (1992) Models of plant pathogen coevolution. Trends in Genetics 8: 213–219.
    Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205–227.
    Halterman DA, Wei FS and Wise RP (2003) Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames. Plant Physiology 131: 558–567.
    Heil M, Hilpert A, Kaiser W and Linsenmair KE (2000) Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology 88: 645–654.
    Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nature Reviews Genetics 2: 516–527.
    Jarosch B, Kogel K-H and Schaffrath U (1999) The ambivalence of the barley Mlo locus: mutations conferring resistance against powdery mildew (Blumeria graminis f. sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Molecular Plant–Microbe Interactions 12: 508–514.
    Johnson R (1984) A critical analysis of durable resistance. Annual Review of Phytopathology 22: 309–330.
    Kjær B, Jensen HP, Jensen J and Jørgensen JH (1990) Associations between three ml-o powdery mildew resistance genes and agronomic traits in barley. Euphytica 46: 185–193.
    Kumar J, Hückelhoven R, Beckhove U et al. (2001) A compromised Mlo pathway affects the response of barley to the necrotrophic fungus Bipolaris sorokiniana (teleomorph: Cochliobolus sativus) and its toxins. Phytopathology 91: 127–133.
    Laine AL (2004) Resistance variation within and among host populations in a plant-pathogen metapopulation: implications for regional pathogen dynamics. Journal of Ecology 92: 990–1000.
    Lovell DJ, Parker SR, Hunter T et al. (1997) Influence of crop growth and structure on the risk of epidemics by Mycospaerella graminicola (Septoria tritici) in winter wheat. Plant Pathology 46: 126–138.
    other Makepeace JC, Oxley SJP, Havis ND et al. (2007) Associations between fungal and abiotic leaf spotting and the presence of mlo alleles in barley. Plant Pathology (in press).
    Purrington CB (2000) Costs of resistance. Current Opinion in Plant Biology 3: 305–308.
    Ruiz-Lozano JM, Gianinazzi S and Gianinazzi-Pearson V (1999) Genes involved in resistance to powdery mildew in barley differentially modulate root colonization by the mycorrhizal fungus Glomus mossae. Mycorrhiza 9: 237–240.
    Smedegaard-Petersen V and Stølen O (1981) Effect of energy-requiring defense reactions on yield and grain quality in a powdery mildew resistant barley cultivar. Phytopathology 71: 396–399.
    Stahl EA, Dwyer G, Mauricio R et al. (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667–671.
    Tellier A and Brown JKM (2007) Stability of genetic polymorphism in host–parasite interactions. Proceedings of the Royal Society B 274: 809–817.
    Thompson JN and Burdon JJ (1992) Gene-for-gene coevolution between plants and parasites. Nature 360: 121–125.
    Thrall PH, Burdon JJ and Young A (2001) Variation in resistance and virulence among demes of a plant host-pathogen metapopulation. Journal of Ecology 89: 736–748.
    Tian D, Traw MB, Chen JQ et al. (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74–77.
    book Vanderplank JE (1963) Plant Diseases: Epidemics and Control. London: Academic Press.
 Further Reading
    Brown JKM (2003) Little else but parasites. Science 299: 1680–1681.
    other Crute IR, Holub EB and Burdon JJ (eds) (1997) The Gene-for-Gene Relationship in Plant-Parasite Interactions. Wallingford: CAB International.
    Jones JDG and Dangl JL (2006) The plant immune system. Nature 444: 323–329.

Related Sub-Topics:

Adaptive Evolution | Coevolution | Selection and Variation | Evolutionary Ecology | Plant Evolution | Plant Disease
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Article Title: Fitness Costs of Plant Disease Resistance
 
How to Cite close
Brown, James K M(Sep 2007) Fitness Costs of Plant Disease Resistance. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020094]