Epidemiological and evolutionary consequences of life-history trade-offs in pathogens

Plant Pathology

Volumn 62, Issue S1, 2013, Pages 96-105

  Laine, A L ^a   Barres B ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Aggressiveness; Cost of virulence; Fitness; Gene for gene; Infectivity; Plant pathogen interactions

Indexed keywords

AGGRESSION; EPIDEMIOLOGY; EVOLUTIONARY BIOLOGY; EXTINCTION RISK; FITNESS; HOST PLANT; LIFE HISTORY TRAIT; METAPOPULATION; TRADE-OFF; VIRULENCE;

FUNGI; OOMYCETES;

EID: 84890435545     PISSN: 00320862     EISSN: 13653059     Source Type: Journal    
DOI: 10.1111/ppa.12129     Document Type: Article

References (78)

1. Agudelo-Romero P, de la Iglesia F, Elena SF, 2008. The pleiotropic cost of host-specialization in Tobacco etch potyvirus. Infection, Genetics and Evolution 8, 806-14.
2. Anderson RM, May RM, 1982. Coevolution of hosts and parasites. Parasitology 85, 411-26.
3. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P, 2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution 19, 535-44.
4. Bahri B, Leconte M, de Vallavieille-Pope C, Enjalbert J, 2007. Cost of virulence: case of Puccinia striiformis f. sp tritici. Phytopathology 97, S6-7.
5. Bahri B, Kaltz O, Leconte M, de Vallavieille-Pope C, Enjalbert J, 2009. Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f. sp. tritici. BMC Evolutionary Biology 9, 26.
6. Bergelson J, Dwyer G, Emerson JJ, 2001. Models and data on plant-enemy coevolution. Annual Review of Genetics 35, 469-99.
7. Bronson CR, Ellingboe AH, 1986. The influence of four unnecessary genes for virulence on the fitness of Erysiphe graminis f. sp. tritici. Phytopathology 76, 154-8.
8. Carson ML, 1998. Aggressiveness and perennation of isolates of Cochliobolus heterostrophus from North Carolina. Plant Disease 82, 1043-7.
9. Caubel J, Launay M, Lannou C, Brisson N, 2012. Generic response functions to simulate climate-based processes in models for the development of airborne fungal crop pathogens. Ecological Modelling 242, 92-104.
10. Dangl JL, Jones JDG, 2001. Plant pathogens and integrated defence responses to infection. Nature 411, 826-33.
11. Desbiez C, Gal-On A, Girard M, Wipf-Scheibel C, Lecoq H, 2003. Increase in Zucchini yellow mosaic virus symptom severity in tolerant zucchini cultivars is related to a point mutation in P3 protein and is associated with a loss of relative fitness on susceptible plants. Phytopathology 93, 1478-84.
12. Doumayrou J, Avellan A, Froissart R, Michalakis Y, 2013. An experimental test of the transmission-virulence trade-off hypothesis in a plant virus. Evolution 67, 477-86.
13. Dybdahl MF, Storfer A, 2003. Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology and Evolution 18, 523-30.
14. Evans N, Baierl A, Semenov MA, Gladders P, Fitt BDL, 2008. Range and severity of a plant disease increased by global warming. Journal of the Royal Society Interface 5, 525-31.
15. Fisher MC, Henk DA, Briggs CJ et al., 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-94.
16. Flor HH, 1956. The complementary genetic systems in flax and flax rust. Advances in Genetics 8, 29-54.
17. Fraile A, Pagán I, Anastasio G, Sáez E, García-Arenal F, 2011. Rapid genetic diversification and high fitness penalties associated with pathogenicity evolution in a plant virus. Molecular Biology and Evolution 28, 1425-37.
18. Friesen TL, Stukenbrock EH, Liu Z et al., 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics 38, 953-6.
19. Fry JD, 1996. The evolution of host specialization: are trade-offs overrated? The American Naturalist 148, S84-107.
20. Futuyma DJ, Moreno G, 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 201-33.
21. Garrett KA, Mundt CC, 1999. Epidemiology in mixed host populations. Phytopathology 89, 984-90.
22. Geffroy V, Sicard D, de Oliveira JCF et al., 1999. Identification of an ancestral resistance gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum. Molecular Plant-Microbe Interactions 12, 774-84.
23. Grant MW, Archer SA, 1983. Calculation of selection coefficients against unnecessary genes for virulence from field data. Phytopathology 73, 547-51.
24. Héraudet V, Salvaudon L, Shykoff JA, 2008. Trade-off between latent period and transmission success of a plant pathogen revealed by phenotypic correlations. Evolutionary Ecology Research 10, 913-24.
25. Hoeksema JD, Forde SE, 2008. A meta-analysis of factors affecting local adaptation between interacting species. The American Naturalist 171, 275-90.
26. Huang YJ, Li ZQ, Evans N, Rouxel T, Fitt BDL, Balesdent MH, 2006. Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). European Journal of Plant Pathology 114, 77-89.
27. Huang Y-J, Balesdent M-H, Li Z-Q, Evans N, Rouxel T, Fitt BDL, 2010. Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). European Journal of Plant Pathology 126, 279-91.
28. Janzac B, Montarry J, Palloix A, Navaud O, Moury B, 2010. A point mutation in the polymerase of Potato virus Y confers virulence toward the Pvr4 resistance of pepper and a high competitiveness cost in susceptible cultivar. Molecular Plant-Microbe Interactions 23, 823-30.
29. Jenner CE, Tomimura K, Ohshima K, Hughes SL, Walsh JA, 2002a. Mutations in Turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. Virology 300, 50-9.
30. Jenner CE, Wang XW, Ponz F, Walsh JA, 2002b. A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Research 86, 1-6.
31. Joshi A, Thompson JN, 1995. Trade-offs and the evolution of host specialization. Evolutionary Ecology 9, 82-92.
32. Kawecki TJ, Ebert D, 2004. Conceptual issues in local adaptation. Ecology Letters 7, 1225-41.
33. Kolmer JA, 1993. Selection in a heterogeneous population of Puccinia recondita f. sp. tritici. Phytopathology 83, 909-14.
34. Kover PX, Clay K, 1998. Trade-off between virulence and vertical transmission and the maintenance of a virulent plant pathogen. The American Naturalist 152, 165-75.
35. Laine A-L, 2004. Resistance variation within and among host populations in a plant-pathogen metapopulation: implications for regional pathogen dynamics. Journal of Ecology 92, 990-1000.
36. Laine A-L, 2007. Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant-pathogen association. Journal of Evolutionary Biology 20, 2371-8.
37. Laine A-L, Hanski I, 2006. Large-scale spatial dynamics of a specialist plant pathogen in a fragmented landscape. Journal of Ecology 94, 217-26.
38. Laine A-L, Tellier A, 2008. Heterogeneous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos 117, 1281-8.
39. Leach JE, Vera Cruz CM, Bai JF, Leung H, 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annual Review of Phytopathology 39, 187-224.
40. Leonard KJ, 1969. Selection in heterogenous populations of Puccinia graminis f. sp. avenae. Phytopathology 59, 1851-7.
41. López-Villavicencio M, Jonot O, Coantic A, Hood ME, Enjalbert J, Giraud T, 2007. Multiple infections by the anther smut pathogen are frequent and involve related strains. PLoS Pathogens 3, e176.
42. Luderer R, Joosten MHAJ, 2001. Avirulence proteins of plant pathogens: determinants of victory and defeat. Molecular Plant Pathology 2, 355-64.
43. Maynard Smith J, 1966. Sympatric speciation. The American Naturalist 100, 637-50.
44. Montarry J, Corbière R, Andrivon D, 2007. Is there a trade-off between aggressiveness and overwinter survival in Phytophthora infestans? Functional Ecology 21, 603-10.
45. Montarry J, Hamelin FM, Glais I, Corbière R, Andrivon D, 2010. Fitness costs associated with unnecessary virulence factors and life history traits: evolutionary insights from the potato late blight pathogen Phytophthora infestans. BMC Evolutionary Biology 10, 283.
46. Montarry J, Cartier E, Jacquemond M, Palloix A, Moury B, 2012. Virus adaptation to quantitative plant resistance: erosion or breakdown? Journal of Evolutionary Biology 25, 2242-52.
47. Mundt CC, 2002. Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology 40, 381-410.
48. van Noordwijk AJ, de Jong G, 1986. Acquisition and allocation of resources: their influence on variation of life history tactics. The American Naturalist 128, 137-42.
49. Pagán I, Alonso-Blanco C, García-Arenal F, 2007. The relationship of within-host multiplication and virulence in a plant-virus system. PLoS ONE 2, e786.
50. Pariaud B, Ravigné V, Halkett F, Goyeau H, Carlier J, Lannou C, 2009. Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathology 58, 409-24.
51. Pariaud B, van den Berg F, van den Bosch F, Powers SJ, Kaltz O, Lannou C, 2013. Shared influence of pathogen and host genetics on a trade-off between latent period and spore production capacity in the wheat pathogen, Puccinia triticina. Evolutionary Applications 6, 303-12.
52. Parker IM, Gilbert GS, 2004. The evolutionary ecology of novel plant-pathogen interactions. Annual Review of Ecology Evolution and Systematics 35, 675-700.
53. Rausher MD, 1984. Tradeoffs in performance on different hosts: evidence from within- and between-site variation in the beetle Deloyala guttata. Evolution 38, 582-95.
54. Roff DA, 1992. The Evolution of Life Histories. London, UK: Chapman and Hall.
55. Sacristán S, García-Arenal F, 2008. The evolution of virulence and pathogenicity in plant pathogen populations. Molecular Plant Pathology 9, 369-84.
56. Sacristán S, Fraile A, Malpica JM, García-Arenal F, 2005. An analysis of host adaptation and its relationship with virulence in Cucumber mosaic virus. Phytopathology 95, 827-33.
57. Salvaudon L, Héraudet V, Shykoff JA, 2005. Parasite-host fitness trade-offs change with parasite identity: genotype-specific interactions in a plant-pathogen system. Evolution 59, 2518-24.
58. Salvaudon L, Héraudet V, Shykoff JA, 2007. Genotype-specific interactions and the trade-off between host and parasite fitness. BMC Evolutionary Biology 7, 189.
59. Salvaudon L, Giraud T, Shykoff JA, 2008. Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Current Opinion in Plant Biology 11, 135-43.
60. Sgrò CM, Hoffmann AA, 2004. Genetic correlations, tradeoffs and environmental variation. Heredity 93, 241-8.
61. Sicard D, Pennings PS, Grandclément C, Acosta J, Kaltz O, Shykoff JA, 2007. Specialization and local adaptation of a fungal parasite on two host plant species as revealed by two fitness traits. Evolution 61, 27-41.
62. Skamnioti P, Ridout CJ, 2005. Microbial avirulence determinants: guided missiles or antigenic flak? Molecular Plant Pathology 6, 551-9.
63. Soubeyrand S, Laine A-L, Hanski I, Penttinen A, 2009. Spatiotemporal structure of host-pathogen interactions in a metapopulation. The American Naturalist 174, 308-20.
64. Stearns SC, 1989. Trade-offs in life-history evolution. Functional Ecology 3, 259-68.
65. Stevens RB, 1960. Cultural practices in disease control. In: Horsfall JG, Dimond AE, eds. Plant Pathology - an Advanced Treatise. New York, USA: Academic Press, 357-429.
66. Susi H, Laine AL, 2013. Pathogen life-history trade-offs revealed in allopatry. Evolution. doi:10.1111/evo.12182.
67. Tack AJM, Thrall PH, Barrett LG, Burdon JJ, Laine A-L, 2012. Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences. Journal of Evolutionary Biology 25, 1918-36.
68. Thrall PH, Burdon JJ, 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299, 1735-7.
69. Thrall PH, Laine AL, Ravensdale M et al., 2012. Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecology Letters 15, 425-35.
70. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J, 2003. Fitness costs of R-gene mediated resistance in Arabidopsis thaliana. Nature 423, 74-7.
71. Toffolatti SL, Venturini G, Maffi D, Vercesi A, 2012. Phenotypic and histochemical traits of the interaction between Plasmopara viticola and resistant or susceptible grapevine varieties. BMC Plant Biology 12, 124.
72. Tollenaere C, Susi H, Nokso-Koivisto J et al., 2012. SNP design from 454 sequencing of Podosphaera plantaginis transcriptome reveals a genetically diverse pathogen metapopulation with high levels of mixed-genotype infection. PLoS ONE 7, e52492.
73. Vanderplank JE, 1968. Disease Resistance in Plants. New York, NY, USA: Academic Press.
74. Vera Cruz CM, Bai JF, Ona I et al., 2000. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proceedings of the National Academy of Sciences, USA 97, 13500-5.
75. White FF, Yang B, Johnson LB, 2000. Prospects for understanding avirulence gene function. Current Opinion in Plant Biology 3, 291-8.
76. Wolfe MS, 1985. The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Annual Review of Phytopathology 23, 251-73.
77. Wolinska J, King KC, 2009. Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236-44.
78. Zhan J, Mundt CC, Hoffer ME, McDonald BA, 2002. Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem. Journal of Evolutionary Biology 15, 634-47.