The jack of all trades is master of none: A pathogen's ability to infect a greater number of host genotypes comes at a cost of delayed reproduction

Evolution

Volumn 68, Issue 9, 2014, Pages 2453-2466

  Bruns, Emily ^a,b   Carson, Martin L ^a   May, Georgiana ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Gene for gene; Host range; Life history; Puccinia coronata; Trade offs; Virulence

Indexed keywords

ALLELE; EVOLUTIONARY BIOLOGY; FUNGUS; GENE EXPRESSION; GENOTYPE; HOST PLANT; HOST-PATHOGEN INTERACTION; LIFE HISTORY; PATHOGEN; VIRULENCE;

UNITED STATES;

PUCCINIA CORONATA;

ADAPTATION; BASIDIOMYCETES; EVOLUTION; FUNGUS SPORE; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; HOST RANGE; MICROBIOLOGY; OAT; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; REPRODUCTIVE FITNESS; UNITED STATES; VIRULENCE;

ADAPTATION, PHYSIOLOGICAL; AVENA SATIVA; BASIDIOMYCOTA; BIOLOGICAL EVOLUTION; GENETIC FITNESS; GENOTYPE; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; SPORES, FUNGAL; UNITED STATES; VIRULENCE;

EID: 84908004584     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12461     Document Type: Article

References (94)

1. Abang, M. M., M. Baum, S. Ceccarelli, S. Grando, C. C. Linde, A. Yahyaoui, J. Zhan, and B. A. McDonald. 2006. Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 96:1214-1222.
2. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image processing with ImageJ. Biophotonics Int. 11:36-42.
3. Agrawal, A., and C.M. Lively. 2002. Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol. Ecol. Res. 4:79-90.
4. Alizon, S., A. Hurford, N. Mideo, and M. Van Baalen. 2009. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22:245-259.
5. Antonovics, J., and H. M. Alexander. 1989. The concept of fitness in plantfungal pathogen systems. Pp. 185-214 in K. J. Leonard and J. Fry, eds. Plant disease epidemiology: genetics, resistance, and management. Vol. 2. McGraw-Hill, New York.
6. Antonovics, J., and P. H. Thrall. 1994. The cost of resistance and maintenance of genetic polymorphism in host-pathogen systems. Proc. R. Soc. Lond. B 257:105-110.
7. Baart, P. G. J., J. E. Parlevliet, and H. Limburg. 1991. Effects of infection density on the size of barley and wheat leaf rust colonies before and on the size of uredina after the start of sporulation. J. Phytopathol. Zeitschrift 131:59-64.
8. Bahri, B., O. Kaltz, M. Leconte, C. de Vallavieille-Pope, and J. Enjalbert. 2009. Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f.sp.tritici. BMC Evol. Biol. 9:26.
9. Barrett, L. G., and M. Heil. 2012. Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci. 17:282-292.
10. Bent, A. F., and D. Mackey. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:399-436.
11. Brown, J. K. M., and M. S. Hovmøller. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537-541.
12. Brown, J. K. M., and A. Tellier. 2011. Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu. Rev. Phytopathol. 49:345-367.
13. Brown, J. K. M., E. M. Foster, and R. B. O'Hara. 1997. Adaptation of powdery mildew populations to cereal varieties in relation to durable and non-durable resistance. Pp. 119-138 in I. R. Crute, E. B. Holub, and J. J. Burdon, eds. The gene-for-gene relationship in plant-parasite interactions. CAB International, Wallingford.
14. Browning, J. A., and K. J. Frey. 1981. The multiline concept in theory and practice. Pp. 37-46 in J. F. Jenkyn and R. T. Plumb, eds. Strategies for the control of cereal disease. Blackwell, Oxford, U.K.
15. Bruns, E. 2012. Constraints to pathogen evolution. Ph.D. dissertation, Department of Ecology, Evolution and Behavior, University of Minnesota, Minneapolis, MN.
16. Bruns, E., M. Carson, and G. May. 2012. Pathogen and host genotype differently affect pathogen fitness through their effects on different life-history stages. BMC Evol. Biol. 12:135.
17. Buckling, A., and P. B. Rainey. 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. Biol. Sci. 269:931-936.
18. Caffier, V., F. Didelot, B. Pumo, D. Causeur, C. E. Durel, and L. Parisi. 2010. Aggressiveness of eight Venturia inaequalis isolates virulent or avirulent to the major resistance gene Rvi6 on a non-Rvi6 apple cultivar. Plant Pathol. 59:1072-1080.
19. Carius, H. J., T. J. Little, and D. Ebert. 2001. Genetic variation in a hostparasite association: potential for coevolution and frequency-dependent selection. Evolution 55:1136-1145.
20. Carson, M. L. 2008. Virulence frequencies in oat crown rust in the United States from 2001 through 2005. Plant Dis. 92:379-384.
21. Carson, M. L. 2009. Crown rust development and selection for virulence in Puccinia coronata f. sp avenae in an oatmultiline cultivar. Plant Dis. 93:347-353.
22. Carson, M. L. 2011. Virulence in oat crown rust (Puccinia coronata f.sp. avenae) in the United States from 2006 through 2009. Plant Dis. 95:1528-1534.
23. Chisholm, S. T., G. Coaker, B. Day, and B. J. Staskawicz. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-814.
24. Chong, J., and J. A. Kolmer. 1993. Virulence dynamics and phenotypic diversity of Puccinia coronata f.sp. avenae in Canada from 1974 to 1990. Can. J. Bot. 71:248-255.
25. Clarke, D. D. 1997. The genetic structure of natural populations. Pp. 231-244 in I. R. Crute, E. B. Holub, and J. J. Burdon, eds. The gene-for-gene relationship in plant-parasite interactions. CAB International, Wallingford.
26. Decaestecker, E., S. Gaba, J. A. M. Raeymaekers, R. Stoks, L. Van Kerckhoven, D. Ebert, and L. De Meester. 2007. Host-parasite "Red Queen" dynamics archived in pond sediment. Nature 450:870-873.
27. Dodds, P. N., G. J. Lawrence, A. Catanzariti, T. Teh, C. A.Wang, M. A. Ayliffe, B. Kobe, and J. G. Ellis. 2006. Direct protein interaction underlies genefor-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA 103:8888-8893.
28. Ellis, J., P. Dodds, and T. Pryor. 2000. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3:278-284.
29. Ellis, J. G., P. N. Dodds, and G. J. Lawrence. 2007. The role of secreted proteins in diseases of plants caused by rust, powdery mildew and smut fungi. Curr. Opin. Microbiol. 10:326-331.
30. Estey, R. H. 1994. Essays on the early history of plant pathology andmycology in Canada. McGill-Queen's Press, Montreal.
31. Fabre, F., E. Rousseau, L. Mailleret, and B. Moury. 2012. Durable strategies to deploy plant resistance in agricultural landscapes. New Phytol. 193:1064-1075.
32. Fleischmann, G., and R. Baker. 1971. Oat crown rust race differentiation: replacement of the standard differential varieties with a new set of single resistance gene lines derived from Avena sterilis. Can. J. Bot. 49:1433-1437.
33. Flor, H. H. 1956. The complementary genic systems in flax and flax rust. Adv. Genet. 8:29-54.
34. Fry, D. 1996. The evolution of host specialization: are trade-offs overrated. Am. Nat. 148(Suppl.):S84-S107.
35. Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19:207-233.
36. Gandon, S., A. Buckling, E. Decaestecker, and T. Day. 2008. Host-parasite coevolution and patterns of adaptation across time and space. J. Evol. Biol. 21:1861-1866.
37. García-arenal, F., and B. A. Mcdonald. 2003. An analysis of the durability of resistance to plant viruses. Phytopathology 93:941-952.
38. Giraud, T., P. Gladieux, and S. Gavrilets. 2010. Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol. Evol. 25:387-395.
39. Grant, M., and S. Archer. 1983. Calculation of selection coefficients against unnecessary genes for virulence from field data. Phytopathology 73:547-551.
40. Groth, J. V. 1976. Multilines and "super races": a simple model. Phytopathology 66:937-939.
41. Hill, J. P., and R. R. Nelson. 1983. Genetic control of two parasitic fitness attributes of Helminthosporium maydis Race T. Genetics 73:455-457.
42. Hoffman, D. L., J. Chong, E. W. Jackson, and D. E. Obert. 2006. Characterization and mapping of a crown rust resistance gene complex (Pc58) in TAM O-301. Crop Sci. 46:2630-2635.
43. Huang, Y.-J., M.-H. Balesdent, Z.-Q. Li, N. Evans, T. Rouxel, and B. D. L. Fitt. 2009. Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur. J. Plant Pathol. 126:279-291.
44. Jones, J. D. G., and J. L. Dangl. 2006. The plant immune system. Nature 444:323-329.
45. Joshi, A., and J. Thompson. 1995. Trade-offs and the evolution of host specialization. Evol. Ecol. 9:82-92.
46. Kamoun, S. 2007. Groovy times: filamentous pathogen effectors revealed. Curr. Opin. Plant Biol. 10:358-365.
47. Kardin, M. K., and J. V. Groth. 1989. Density-dependent fitness interactions in the bean rust fungus. Phytopathology 79:409-412.
48. Kolmer, J. A. 1993. Selection in a heterogeneous population of Puccinia recondita f.sp. tritici. Phytopathology 82:909-914.
49. Kolmer, J. A. 1997. Virulence dynamics and genetics of cereal rust populations in NorthAmerica. Pp. 139-156 in I. R. Crute, E. B. Holum, and J. J.Burdon, eds. The gene-for-gene relationship in plant-parasite interactions. CAB International, Wallingford.
50. Laine, A. 2004. Resistance variation within and among host populations in a plant pathogen metapopulation: implications for regional pathogen dynamics. J. Ecol. 92:990-1000.
51. Laine, A.-L., and A. Tellier. 2008. Heterogeneous selection promotes maintenance of polymorphism in host parasite interactions. Oikos 117:1281-1288.
52. Lambrechts, L., J. Halbert, P. Durand, L. C. Gouagna, and J. C. Koella. 2005. Host genotype by parasite genotype interactions underlying the resistance of Anopheline mosquitoes to Plasmodium falciparum. Malar. J. 4:3.
53. Lannou, C. 2012. Variation and selection of quantitative traits in plant pathogens. Annu. Rev. Phytopathol. 50:319-338.
54. Lannou, C., and C. C. Mundt. 1996. Evolution of a pathogen population in host mixtures: simple race-complex race competition. Plant Pathol. 45:440-453.
55. Lannou, C., and C. C. Mundt. 1997. Evolution of a pathogen population in host mixtures: rate of emergence of complex races. Theor. Appl. Genet. 94:991-999.
56. Leach, J. E., C. M. Vera Cruz, J. Bai, and H. Leung. 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 39:187-224.
57. Legros, M., and J. C. Koella. 2010. Experimental evolution of specialization by a microsporidian parasite. BMC Evol. Biol. 10:159.
58. Lehman, J. S., and G. Shaner. 1996. Genetic variation in latent period among isolates of Puccinia triticina f.sp. tritici on partially resistant wheat cultivars. Phytopathology 86:633-641.
59. Lehman, J. S., and G. Shaner. 2007. Heritability of latent period estimated from wild-type and selected populations of Puccinia triticina. Phytopathology 97:1022-1029.
60. Leonard, K. J. 1969. Selection in heterogeneous populations of Puccinia graminis f. sp. avenae. Phytopathology 59:1851-1856.
61. Leonard, K. J. 1977. Selection pressures and plant pathogens. Ann. NY Acad. Sci. 287:207-222.
62. Leonard, K. J. 1994. Stability of equilibria in a gene-for-gene coevolution model of host-parasite interactions. Phytopathology 84:70-77.
63. Leonard, K. J. 2003. Regional frequencies of virulence in oat crown rust in the United States from 1990 through 2000. Plant Dis. 87:1301-1310.
64. Leonard, K. J., and C. C. Mundt. 1984. Methods for estimating epidemiological effects of quantitative resistance to plant diseases. Theor. Appl. Genet. 67:219-230.
65. Leonard, K. J., Y. Anikster, and J. Manisterski. 2004. Patterns of virulence in natural populations of Puccinia coronata on wild oat in Israel and in agricultural populations on cultivated oat in the United States. Phytopathology 94:505-514.
66. Little, T. J., and D. Ebert. 2001. Temporal patterns of genetic variation for resistance and infectivity in a Daphnia-microparasite system. Evolution 55:1146-1152.
67. May, R. M., and R. Anderson. 1983. Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. Lond. B 219:281-313.
68. McDonald, B. 2010. How can we achieve durable disease resistance in agricultural ecosystems? New Phytol. 185:3-5.
69. McDonald, B. A., and C. Linde. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-379.
70. Montarry, J., F. M. Hamelin, I. Glais, R. Corbi, and D. Andrivon. 2010. Fitness costs associated with unnecessary virulence factors and life history traits: evolutionary insights from the potato late blight pathogen Phytophthora infestans. BMC Evol. Biol. 10:283.
71. Nagarajan, S., and D. V. Singh. 1990. Long-distance dispersion of rust pathogens. Annu. Rev. Phytopathol. 28:139-1953.
72. Newton, M. R., L. L. Kinkel, and K. J. Leonard. 1997. Competition and density-dependent fitness in a plant parasitic fungus. Ecology 78:1774-1784.
73. Pariaud, B., C. Robert, H. Goyeau, and C. Lannou. 2009. Aggressiveness components and adaptation to a host cultivar in wheat leaf rust. Phytopathology 99:869-878.
74. Parker, J. E., and J. G. Ellis. 2010. Plant-biotic interactions: advances on all fronts. Curr. Opin. Plant Biol. 13:363-365.
75. Poullain, V., S. Gandon, M. A. Brockhurst, A. Buckling, and M. E. Hochberg. 2008. The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution 62:1-11.
76. Pringle, A., and J. W. Taylor. 2002. The fitness of filamentous fungi. Trends Microbiol. 10:474-481.
77. Remold, S. 2012. Understanding specialism when the Jack of all trades can be the master of all. Proc. Biol. Sci. 279:4861-4869.
78. Sacristan, S., and F. Garcia-Arenal. 2008. The evolution of virulence and pathogenicity in plant pathogen populations. Mol. Plant Pathol. 9:369-384.
79. Sasaki, A. 2000. Host-parasite coevolution in a multilocus gene-for-gene system. Proc. Biol. Sci. 267:2183-2188.
80. Simons, M. D. 1985. Oat crown rust. In A. P. Roelfs and W. R. Bushnell, eds. The cereal rusts. Diseases, distribution, epidemiology, and control. Academic Press, Inc., Orlando.
81. Stahl, E. A., G. Dwyer, R. Mauricio, M. Kreitman, and J. Bergelson. 1999. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667-671.
82. Tack, A. J. M., P. H. Thrall, L. G. Barrett, J. J. Burdon, and A.-L. Laine. 2012. Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences. J. Evol. Biol. 25:1918-1936.
83. Tellier, A., and J. Brown. 2007. Stability of genetic polymorphism in hostparasite interactions. Proc. R. Soc. Lond. B 274:809-817.
84. Thompson, J., and J. J. Burdon. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360:121-125.
85. Thrall, P. H., and J. J. Burdon. 2002. Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathol. 51:169-184.
86. Thrall, P. H., and J. J. Burdon. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735-1737.
87. Thrall, P. H., J. J. Burdon, and J. Bever. 2002. Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56:1340-1351.
88. Thrall, P. H., A.-L. Laine, M. Ravensdale, A. Nemri, P. N. Dodds, L. G. Barrett, and J. J. Burdon. 2012. Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol. Lett. 15:425-435.
89. Van der Plank, J. E. 1968. Disease resistance in plants. Academic Press, London, U.K.
90. Vera Cruz, C. M., J. Bai, I. Ona, H. Leung, R. J. Nelson, T.W. Mew, and J. E. Leach. 2000. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc. Natl. Acad. Sci. USA 97:13500-13505.
91. Villaréal, L. M., and C. Lannou. 2000. Selection for increased spore efficacy by host genetic background in a wheat powdery mildew population. Phytopathology 90:1300-1306.
92. Woolhouse, M. E. J., J. P. Webster, E. Domingo, B. Charlesworth, and B. R. Levin. 2002. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32:569-577.
93. Zhan, J., and B. A. McDonald. 2013. Experimental measures of pathogen competition and relative fitness. Annu. Rev. Phytopathol. 51:2.1-2.23.
94. Zhan, J., L. Yang, W. Zhu, L. Shang, and A. C. Newton. 2012. Pathogen populations evolve to greater race complexity in agricultural systems-evidence from analysis of Rhynchosporium secalis virulence data. PLoS One 7:e38611.