Wild plants and their associated pathogens are involved in ongoing interactions over millennia that have been modified by coevolutionary processes to limit the spatial extent and temporal duration of disease epidemics. These interactions are disrupted by modern agricultural practices and social activities, such as intensified monoculture using superior varieties and international trading of agricultural commodities. These activities, when supplemented with high resource inputs and the broad application of agrochemicals, create conditions uniquely conducive to widespread plant disease epidemics and rapid pathogen evolution. To be effective and durable, sustainable disease management requires a significant shift in emphasis to overtly include ecoevolutionary principles in the design of adaptive management programs aimed at minimizing the evolutionary potential of plant pathogens by reducing their genetic variation, stabilizing their evolutionary dynamics, and preventing dissemination of pathogen variants carrying new infectivity or resistance to agrochemicals.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Abang M, Baum M, Grando S, Ceccarelli S, Linde CC. 1.  et al. 2006. Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 96:1214–22 [Google Scholar]
  2. Abramovitch RB, Anderson JC, Martin GB. 2.  2006. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 7:601–11 [Google Scholar]
  3. Akins RA. 3.  2005. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43:285–18 [Google Scholar]
  4. Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. 4.  2006. Seasonality and the dynamics of infectious diseases. Ecol. Lett. 9:467–84 [Google Scholar]
  5. Anagnostakis S. 5.  1987. Chestnut blight: the classical problem of an introduced pathogen. Mycologia 29:23–37 [Google Scholar]
  6. Andreasen K, Baldwin BG. 6.  2001. Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S–26S rDNA internal and external transcribed spacers. Mol. Biol. Evol. 18:936–44 [Google Scholar]
  7. Angiolella L, Stringaro AR, De Bernardis F, Posteraro B, Bonito M. 7.  et al. 2008. Increase of virulence and its phenotypic traits in drug resistant strains of Candida albicans. Antimicrob. Agents Chemother. 52:927–36 [Google Scholar]
  8. Bailey KL, Duczek LJ. 8.  1996. Managing cereal diseases under reduced tillage. Can. J. Plant Pathol. 18:159–67 [Google Scholar]
  9. Bainbridge A. 9.  1974. Effect of nitrogen nutrition of the host on barley powdery mildew. Plant Pathol. 23:16061 [Google Scholar]
  10. Ballini E, Morel JB, Droc G, Price A, Courtois B. 10.  et al. 2008. A genome-wide meta-analysis of rice blast resistance genes and quantitative trait loci provides new insights into partial and complete resistance. Mol. Plant-Microbe Interact. 21:859–68 [Google Scholar]
  11. Barrett LG, Thrall PH, Burdon JJ, Linde CC. 11.  2008. Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol. Evol. 23:678–85 [Google Scholar]
  12. Bayles RA, Flath K, Hovmoller MS, de Valavieille-Pope C. 12.  2000. Breakdown of the Yr17 resistance to yellow rust of wheat in Northern Europe. Agronomie 20:805–11 [Google Scholar]
  13. Blatter RHE, Brown JKM, Wolfe MS. 13.  1998. Genetic control of the resistance of Erysiphe graminis f.sp. hordei to five triazole fungicides. Plant Pathol. 47:570–79 [Google Scholar]
  14. Bockus WW, Shroyer JP. 14.  1998. The impact of reduced tillage on soilborne pathogens. Annu. Rev. Phytopathol. 36:485–500 [Google Scholar]
  15. Boudreau MA. 15.  2013. Diseases in intercropping systems. Annu. Rev. Phytopathol. 51:499–519 [Google Scholar]
  16. Bousset L, Hovmøller MS, Caffier V, de Vallavieille-Pope C, Østergård H. 16.  2002. Observed and predicted changes over eight years in frequency of barley powdery mildew avirulent to spring barley in France and Denmark. Plant Pathol. 51:33–44 [Google Scholar]
  17. Brasier CM. 17.  2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 57:792–808 [Google Scholar]
  18. Brown JKM, Hovmøller MS. 18.  2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–41 [Google Scholar]
  19. Brown JKM, Rant JC. 19.  2013. Fitness costs and trade-offs of disease resistance and their consequences for breeding arable crops. Plant Pathol. 62:Suppl. 183–95 [Google Scholar]
  20. Brown JKM, Tellier A. 20.  2011. Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu. Rev. Phytopathol. 49:1–23 [Google Scholar]
  21. Brown JKM. 21.  2002. Yield penalties of disease resistance in crops. Curr. Opin. Plant Biol. 5:339–44 [Google Scholar]
  22. Brown SP, Cornforth DM, Mideo N. 22.  2012. Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol. 20:336–42 [Google Scholar]
  23. Brun H, Chevre AM, Fitt BDL, Powers S, Besnard AL. 23.  et al. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185:285–99 [Google Scholar]
  24. Brunner PC, Stefanato FL, McDonald BA. 24.  2008. Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Mol. Plant Pathol. 9:305–16 [Google Scholar]
  25. Burdon JJ, Barrett LG, Rebetzke G, Thrall PH. 25.  2014. Guiding deployment of resistance in cereals using evolutionary principles. Evol. Appl. 7:609–24 [Google Scholar]
  26. Burdon JJ, Thompson JN. 26.  1995. Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. J. Ecol. 83:199–206 [Google Scholar]
  27. Burdon JJ, Thrall PH, Ericson L. 27.  2013. Genes, communities & invasive species: understanding the ecological and evolutionary dynamics of host-pathogen interactions. Curr. Opin. Plant Biol. 16:400–405 [Google Scholar]
  28. Burdon JJ, Thrall PH. 28.  2003. Fitness costs of resistance to pathogens in plants. Genome Biol. 4:227 [Google Scholar]
  29. Burdon JJ, Thrall PH. 29.  2013. What have we learned from studies of wild plant-pathogen associations? The dynamic interplay of time, space and life-history. Eur. J. Plant Pathol. 138:417–29 [Google Scholar]
  30. Burgess T, Wingfield MJ. 30.  2002. Quarantine is important in restricting the spread of exotic seed-borne tree pathogens in the Southern Hemisphere. Int. For. Rev. 4:56–65 [Google Scholar]
  31. Caffier V, Didelot F, Pumo B, Causeur D, Durel CE, Parisi L. 31.  2010. Aggressiveness of eight Venturia inaequalis isolates virulent or avirulent to the major resistance gene Rvi6 on a non-Rvi6 apple cultivar. Plant Pathol. 59:1072–80 [Google Scholar]
  32. Caffier V, Hoffstadt T, Leconte M, de Vallavielle-Pope C. 32.  1996. Seasonal changes in pathotype complexity in French populations of barley powdery mildew. Plant Pathol. 45:454–68 [Google Scholar]
  33. Caffier V, Laurens F. 33.  2005. Breakdown of Pl2, a major gene of resistance to apple powdery mildew, in a French experimental orchard. Plant Pathol. 54:116–24 [Google Scholar]
  34. Chen PR, Bae T, Williams WA, Duguid EM, Rice PA. 34.  et al. 2006. An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus. Nat. Chem. Biol. 2:591–95 [Google Scholar]
  35. Chin KM, Wolfe MS, Minchin PN. 35.  1984. Host-mediated interactions between pathogen genotypes. Plant Pathol. 33:161–71 [Google Scholar]
  36. Cook RJ, Papendick RI. 36.  1972. Influence of water potential of soils and plants on root disease (fungi). Annu. Rev. Phytopathol. 10:349–74 [Google Scholar]
  37. Cowger C, Hoffer ME, Mundt CC. 37.  2000. Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathol. 49:445–51 [Google Scholar]
  38. Cowger C, Mundt CC. 38.  2002. Aggressiveness of Mycosphaerella graminicola isolates from susceptible and partially resistant wheat cultivars. Phytopathology 92:624–30 [Google Scholar]
  39. Dangl JL, Horvath DM, Staskawicz BJ. 39.  2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–51 [Google Scholar]
  40. David M, Swiader J, Williams K, Eastburn D. 40.  2003. Nitrogen nutrition, but not potassium, affects powdery mildew development in Hiemalis begonia. J. Plant Nutr. 26:159–76 [Google Scholar]
  41. Delmotte F, Mestre P, Schneider C, Kassemeyer HH, Kozma P. 41.  et al. 2013. Rapid and multiregional adaptation to host partial resistance in a plant pathogenic oomycete: evidence from European populations of Plasmopara viticola, the causal agent of grapevine downy mildew. Infect. Genet. Evol. 27:500–8 [Google Scholar]
  42. Dileone JA, Mundt CC. 42.  1994. Effect of wheat cultivar mixtures on populations of Puccinia striiformis races. Plant Pathol. 43:917–30 [Google Scholar]
  43. Dinoor A. 43.  1970. Sources of oat crown rust resistance in hexaploid and tetraploid wild oats in Israel. Can. J. Bot. 48:153–63 [Google Scholar]
  44. Doumayrou J, Avellan A, Froissart R, Michalakis Y. 44.  2013. An experimental test of the transmission-virulence trade-off hypothesis in a plant virus. Evolution 67:477–86 [Google Scholar]
  45. Ellstrand NC, Elam DR. 45.  1993. Population genetic consequences of small population size: implications for plant conservation. Annu. Rev. Ecol. Syst. 24:217–42 [Google Scholar]
  46. El-Zik KM. 46.  1985. Integrated control of Verticillium wilt of cotton. Plant Dis. 69:1025–32 [Google Scholar]
  47. Ferreira RC, Briones MRS. 47.  2012. Phylogenetic evidence based on Trypanosoma cruzi nuclear gene sequences and information entropy suggest that inter-strain intragenic recombination is a basic mechanism underlying the allele diversity of hybrid strains. Infect. Genet. Evol. 12:1064–71 [Google Scholar]
  48. Fisher RA. 48.  1930. The Genetic Theory of Natural Selection. Oxford, UK: Clarendon, 1st ed..
  49. Flor HH. 49.  1955. Host-parasite interactions in flax rust: its genetics and other implications. Phytopathology 45:680–85 [Google Scholar]
  50. Flor HH. 50.  1956. The complementary genic systems in flax and flax rust. Adv. Genet. 8:29–54 [Google Scholar]
  51. Fraaije BA, Cools HJ, Fontaine J, Lovell DJ, Motteram J, West JS. 51.  2005. Role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology 95:933–41 [Google Scholar]
  52. Freinkel S. 52.  2007. American Chestnut: The Life, Death, and Rebirth of a Perfect Tree Oakland, CA: Univ. Calif. Press
  53. Gandon S, Michalakis Y. 53.  2000. Evolution of parasite virulence against qualitative or quantitative host resistance. Proc. R. Soc. Lond. B 267:985–90 [Google Scholar]
  54. Gandon S, Nuismer SL. 54.  2009. Interactions between genetic drift, gene flow, and selection mosaics drive parasite local adaptation. Am. Nat. 173:212–24 [Google Scholar]
  55. Garbelotto M, Svihra P, Rizzo DM. 55.  2001. Sudden oak death syndrome fells 3 oak species. Calif. Agric. 55:9–19 [Google Scholar]
  56. Gent DH, Mahaffee WF, McRoberts N, Pfender WF. 56.  2013. The use and role of predictive systems in disease management. Annu. Rev. Phytopathol. 51:267–89 [Google Scholar]
  57. Gladieux P, Zhang XG, Afoufa-Bastien D, Valdebenito Sanhueza RM, Sbaghi M, Le Cam B. 57.  2008. On the origin and spread of the scab disease of apple: out of central Asia. PLOS ONE 3:e1455 [Google Scholar]
  58. Gomez P, Buckling A. 58.  2011. Bacteria-phage antagonistic coevolution in soil. Science 332:106–9 [Google Scholar]
  59. Gottwald TR, Hughes G, Graham JH, Sun X, Riley T. 59.  2001. The citrus canker epidemic in Florida: the scientific basis of regulatory eradication policy for an invasive species. Phytopathology 91:30–34 [Google Scholar]
  60. Grünwald NJ, Flier WG. 60.  2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171–90 [Google Scholar]
  61. Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S. 61.  2012. Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol. 20:131–38 [Google Scholar]
  62. Gubbins S, Gilligan CA. 62.  1997. Persistence of host-parasite interactions in a disturbed environment. J. Theor. Biol. 188:241–58 [Google Scholar]
  63. Gupta A, Chattoo BB. 63.  2008. Functional analysis of a novel ABC transporter ABC4 from Magnaporthe grisea. FEMS Microbiol. Lett. 278:22–28 [Google Scholar]
  64. Hall AR, Scanlan PD, Morgan AD, Buckling A. 64.  2011. Host-parasite coevolutionary arms races give way to fluctuating selection. Ecol. Lett. 14:635–42 [Google Scholar]
  65. Hamilton WD, Axelrod R, Tanese R. 65.  1990. Sexual reproduction as an adaptation to resist parasites. Proc. Natl. Acad. Sci. USA 87:3566–73 [Google Scholar]
  66. Hamilton WD. 66.  1980. Sex versus non-sex versus parasite. Oikos 35:282–90 [Google Scholar]
  67. Hauggaard-Nielsen H, Jornsgaard B, Kinane J, Jensen ES. 67.  2008. Grain legume-cereal intercropping: the practical application of diversity, competition and facilitation in arable and organic cropping systems. Renew. Agric. Food Syst. 23:3–12 [Google Scholar]
  68. He CQ, Ding NZ, He M, Li SN, Wang XM. 68.  et al. 2010. Intragenic recombination as a mechanism of genetic diversity in bluetongue virus. J. Virol. 84:11487–95 [Google Scholar]
  69. Herrick J. 69.  2011. Genetic variation and DNA replication timing, or why is there late replicating DNA?. Evolution 65:3031–47 [Google Scholar]
  70. Hittalmani S, Parco A, Mew TV, Zeigler RS, Huang N. 70.  2000. Fine mapping and DNA marker-assisted pyramiding of the three major genes for blast resistance in rice. Theor. Appl. Genet. 100:1121–28 [Google Scholar]
  71. Hobbs PR, Sayre K, Gupta R. 71.  2008. The role of conservation agriculture in sustainable agriculture. Philos. Trans. R. Soc. B 363:543–55 [Google Scholar]
  72. Hohl HR, Iselin K. 72.  1984. Strains of Phytophthora infestans from Switzerland with A2 mating type behaviour. Trans. Brit. Mycol. Soc. 83:529–30 [Google Scholar]
  73. Horns F, Hood ME. 73.  2012. The evolution of disease resistance and tolerance in spatially structured populations. Ecol. Evol. 2:1705–11 [Google Scholar]
  74. Hovmøller MS, Caffier V, Jalli M. 74.  2000. The European barley powdery mildew virulence survey and disease nursery 1993–1999. Agronomie 20:729–43 [Google Scholar]
  75. Hurst LD, Peck JR. 75.  1996. Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol. Evol. 11:46–52 [Google Scholar]
  76. Innocenti P, Morrow EH, Dowling DK. 76.  2011. Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science 332:845–48 [Google Scholar]
  77. Inukai T, Nelson RJ, Zeigler RS, Sarkarung S, Mackill DJ. 77.  et al. 1994. Allelism of blast resistance genes in near-isogenic lines of rice. Phytopathology 84:1278–83 [Google Scholar]
  78. Jaramillo N, Domingo E, Munoz-Egea MC, Tabares E, Gadea I. 78.  2013. Evidence of Muller's ratchet in herpes simplex virus type 1. J. Gen. Virol. 94:366–75 [Google Scholar]
  79. Jefferson PG. 79.  2002. Irrigation increases Verticillium wilt incidence in a susceptible alfalfa cultivar. Plant Dis. 86:588–92 [Google Scholar]
  80. Jenner CE, Wang X, Ponz F, Walsh JA. 80.  2002. A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Res. 86:1–6 [Google Scholar]
  81. Johnson T. 81.  1961. Man-guided evolution in plant rusts. Science 133:357–62 [Google Scholar]
  82. Judelson HS, Blanco FA. 82.  2005. The spores of Phytophthora: weapons of the plant destroyer. Nat. Microbiol. Rev. 3:47–58 [Google Scholar]
  83. Keller M, Rogiers SY, Schultz HR. 83.  2003. Nitrogen and ultraviolet radiation modify grapevines' susceptibility to powdery mildew. Vitis 42:87–94 [Google Scholar]
  84. Kinkel LL, Bakker MG, Schlatter DC. 84.  2011. A coevolutionary framework for managing disease-suppressive soils. Annu. Rev. Phytopathol. 49:47–67 [Google Scholar]
  85. Kinloch BB Jr. 85.  2003. White pine blister rust in North America: past and prognosis. Phytopathology 93:1044–47 [Google Scholar]
  86. Kondrashov A. 86.  1988. Deleterious mutation and the evolution of sexual reproduction. Nature 336:435–40 [Google Scholar]
  87. Koskella B, Giraud T, Hood ME. 87.  2006. Pathogen relatedness affects the prevalence of within-host competition. Am. Nat. 168:121–26 [Google Scholar]
  88. Krenz JE, Sackett KE, Mundt CC. 88.  2008. Specificity of incomplete resistance to Mycosphaerella graminicola in wheat. Phytopathology 98:555–61 [Google Scholar]
  89. Laine AL, Burdon JJ, Dodds PN, Thrall PH. 89.  2011. Spatial variation in disease resistance: from molecules to metapopulations. J. Ecol. 99:96–112 [Google Scholar]
  90. Lande R, Barrowclough GF. 90.  1987. Effective population size, genetic variation, and their use in population management. Viable Populations for Conservation ME Soule 87–123 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  91. Lanier GN, Schubert DC, Manion PD. 91.  1988. Dutch elm disease and elm yellows in central New York. Out of the frying pan into the fire. Plant Dis. 72:189–94 [Google Scholar]
  92. Lannou C, Mundt CC. 92.  1997. Evolution of a pathogen population in host mixtures: rate of emergence of complex races. Theor. Appl. Genet. 94:991–99 [Google Scholar]
  93. Lenski RE, May RM. 93.  1994. The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J. Theor. Biol. 169:253–65 [Google Scholar]
  94. Liu YC, Milgroom MG. 94.  2007. High diversity of vegetative compatibility types in Cryphonectria parasitica in Japan and China. Mycologia 99:279–84 [Google Scholar]
  95. López-Villavicencio M, Courjol F, Gibson AK, Hood ME, Jonot O. 95.  et al. 2011. Competition, cooperation among kin, and virulence in multiple infections. Evolution 65:1357–66 [Google Scholar]
  96. López-Villavicencio M, Jonot O, Coantic A, Hood ME, Enjalbert J, Giraud T. 96.  2007. Multiple infections by the anther smut pathogen are frequent and involve related strains. PLOS Pathog. 3:e176 [Google Scholar]
  97. Marcel TC, Gorguet B, Ta MT, Kohutova Z, Vels A, Niks RE. 97.  2008. Isolate specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping populations and near-isogenic lines. New Phytol. 177:743–55 [Google Scholar]
  98. Marcroft SJ, Van de Wouw AP, Salisbury PA, Potter TD, Howlett BJ. 98.  2012. Rotation of canola (Brassica napus) cultivars with different complements of blackleg resistance genes decreases disease severity. Plant Pathol. 61:934–44 [Google Scholar]
  99. Marshall B, Newton AC, Zhan J. 99.  2009. Evolution of pathogen aggressiveness under cultivar mixtures. Plant Pathol. 58:378–88 [Google Scholar]
  100. Martin AP, Palumbi SR. 100.  1993. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl. Acad. Sci. USA 90:4087–91 [Google Scholar]
  101. Mazzola M. 101.  2004. Assessment and management of soil community structure for disease suppression. Annu. Rev. Phytopathol. 42:35–59 [Google Scholar]
  102. McDonald BA, Linde CC. 102.  2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349–79 [Google Scholar]
  103. McDonald BA, Zhan J, Burdon JJ. 103.  1999. Genetic structure of Rhynchosporium secalis in Australia. Phytopathology 89:639–45 [Google Scholar]
  104. Messinger SM, Ostling A. 104.  2009. The consequences of spatial structure for the evolution of pathogen transmission rate and virulence. Am. Nat. 174:441–54 [Google Scholar]
  105. Meyer SE, Nelson DL, Clement S, Ramakrishnan A. 105.  2010. Ecological genetics of the Bromus tectorum (Poaceae)–Ustilago bullata (Ustilaginaceae) pathosystem: a role for frequency-dependent selection?. Am. J. Bot. 97:1304–12 [Google Scholar]
  106. Michelmore RW, Christopoulou M, Caldwell KS. 106.  2013. Impacts of resistance gene genetics, function, and evolution on a durable future. Annu. Rev. Phytopathol. 51:291–319 [Google Scholar]
  107. Mikonranta L, Friman V-P, Laakso J. 107.  2012. Life history trade-offs and relaxed selection can decrease bacterial virulence in environmental reservoirs. PLOS ONE 7:8e43801 [Google Scholar]
  108. Mitchell-Olds T, Bradley D. 108.  1996. Genetics of Brassica rapa. 3. Costs of disease resistance to three fungal pathogens. Evolution 50:1859–65 [Google Scholar]
  109. Montarry J, Cartier E, Jacquemond M, Palloix A, Moury B. 109.  2012. Virus adaptation to quantitative plant resistance: erosion or breakdown?. J. Evol. Biol. 25:2242–52 [Google Scholar]
  110. Morgounov A, Tufan HA, Sharma R, Akin B, Bagci A. 110.  et al. 2012. Global incidence of wheat rusts and powdery mildew during 1969–2010 and durability of resistance of winter wheat variety Bezostaya 1. Eur. J. Plant Pathol. 132:323–40 [Google Scholar]
  111. Morrow MR, Krieg DR. 111.  1990. Cotton management strategies for a short growing season environment: water-nitrogen considerations. Agron. J. 82:52–56 [Google Scholar]
  112. Mundt CC. 112.  2002. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40:381–410 [Google Scholar]
  113. Mykytowycz R. 113.  1953. An attenuated strain of the myxomatosis virus recovered from the field. Nature 172:448–49 [Google Scholar]
  114. Nancy AM. 114.  1996. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93:2873–78 [Google Scholar]
  115. Nunney L. 115.  1995. Measuring the ratio of effective population size and adult numbers using genetic and ecological data. Evolution 49:389–92 [Google Scholar]
  116. Nunney L. 116.  1999. The effective size of a hierarchically structured population. Evolution 53:1–10 [Google Scholar]
  117. O'Brien L, Brown JS, Young RM, Pascoe I. 117.  1980. Occurrence and distribution of wheat stripe rust in Victoria and susceptibility of commercial wheat cultivars. Australas. Plant Pathol. 9:14 [Google Scholar]
  118. O'Hara RB, Brown JKM. 118.  1996. Immigration of the barley mildew pathogen into field plots of barley. Plant Pathol. 45:1071–76 [Google Scholar]
  119. Papaïx J, Burdon JJ, Lannou C, Thrall PH. 119.  2014. Evolution of pathogen specialisation in a host metapopulation: joint effects of host and pathogen dispersal. PLOS Comput. Biol. 10:5e1003633 [Google Scholar]
  120. Papaïx J, Monod H, Goyeau H, du Cheyron P, Lannou C. 120.  2011. Influence of cultivated landscape composition on variety resistance: an assessment based on wheat leaf rust epidemics. New Phytol. 191:1095–107 [Google Scholar]
  121. Pariaud B, Ravigné V, Halkett F, Goyeau H, Carlier J, Lannou C. 121.  2009. Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathol. 58:409–24 [Google Scholar]
  122. Pariaud B, Robert C, Goyeau H, Lannou C. 122.  2009. Aggressiveness components and adaptation to a host cultivar in wheat leaf rust. Phytopathology 99:869–78 [Google Scholar]
  123. Pedersen WL, Leath S. 123.  1988. Pyramiding major genes for resistance to maintain residual effects. Annu. Rev. Phytopathol. 26:369–78 [Google Scholar]
  124. Peressotti E, Wiedemann-Merdinoglu S, Delmotte F, Bellin D, Di Gaspero G. 124.  et al. 2010. Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety. BMC Plant Biol. 10:147 [Google Scholar]
  125. Pink DAC. 125.  2002. Strategies using genes for non-durable disease resistance. Euphytica 124:227–36 [Google Scholar]
  126. Platz GJ, Sheppard JA. 126.  2007. Sustained genetic control of wheat rust diseases in north-eastern Australia. Aust. J. Agric. Res. 58:854–57 [Google Scholar]
  127. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. 127.  2009. Shades of gray: the world of quantitative disease resistance. Trends Plant Sci. 14:21–29 [Google Scholar]
  128. Purdy LH, Krupa SV, Dean JL. 128.  1985. Introduction of sugarcane rust into the Americas and its spread to Florida. Plant Dis. 69:689–93 [Google Scholar]
  129. Rauscher G, Simko I, Mayton H, Bonierbale M, Smart CD. 129.  et al. 2010. Quantitative resistance to late blight from Solanum berthaultii cosegregates with RPi-ber: insights in stability through isolates and environment. Theor. Appl. Genet. 121:1553–67 [Google Scholar]
  130. Roelfs AP. 130.  1982. Effects of barberry eradication on stem rust in the United States. Plant Dis. 66:177–81 [Google Scholar]
  131. Sabat AJ, Wladyka B, Kosowska-Shick K, Grundmann H, van Dijl JM. 131.  et al. 2008. Polymorphism, genetic exchange and intragenic recombination of the aureolysin gene among Staphylococcus aureus strains. BMC Microbiol. 8:129 [Google Scholar]
  132. Salamati S, Zhan J, Burdon JJ, McDonald BA. 132.  2000. The genetic structure of field populations of Rhynchosporium secalis from three continents suggests moderate gene flow and regular sexual reproduction. Phytopathology 90:901–8 [Google Scholar]
  133. Sapoukhina N, Durel CE, Le Cam B. 133.  2009. Spatial deployment of gene-for-gene resistance governs evolution and spread of pathogen populations. Theor. Ecol. 2:229–38 [Google Scholar]
  134. Schoeny A, Lemarchand E, Tivoli B, Jumel S, Rouault F. 134.  2010. Effect and underlying mechanism of pea-cereal intercropping on the epidemic development of Ascochyta blight. Eur. J. Plant Pathol. 126:317–31 [Google Scholar]
  135. Schornack S, Moscou MJ, Ward ER, Horvath DM. 135.  2013. Engineering plant disease resistance based on TAL effectors. Annu. Rev. Phytopathol. 51:383–406 [Google Scholar]
  136. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S. 136.  et al. 2011. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 49:465–81 [Google Scholar]
  137. Slatkin M, Voelm L. 137.  1991. FST in a hierarchical island model. Genetics 127:627–29 [Google Scholar]
  138. Sommerhalder RJ, McDonald BA, Mascher F, Zhan J. 138.  2011. Effect of hosts on competition among clones and evidence of differential selection between pathogenic and saprophytic phases in experimental populations of the wheat pathogen Phaeosphaeria nodorum. BMC Evol. Biol 11:188 [Google Scholar]
  139. St. Clair DA. 139.  2010. Quantitative disease resistance and quantitative resistance loci in breeding.. Annu. Rev. Phytopathol. 48:247–68 [Google Scholar]
  140. Staub JE, Grumet R. 140.  1993. Selection for multiple disease resistance reduces cucumber yield potential. Euphytica 67:205–13 [Google Scholar]
  141. Subramanian S. 141.  2013. Significance of population size on the fixation of nonsynonymous mutations in genes under varying levels of selection pressure. Genetics 193:995–1002 [Google Scholar]
  142. Sun CB, Suresh A, Deng YZ, Naqvi NI. 142.  2006. A multidrug resistance transporter in Magnaporthe is required for host penetration and for survival during oxidative stress. Plant Cell 18:3686–705 [Google Scholar]
  143. Susi H, Barrès B, Vale PF, Laine A-L.143.  2015. Co-infection alters population dynamics of infectious disease. Nat. Commun. 6:5975
  144. Tatum LA. 144.  1971. The southern corn leaf blight epidemic. Science 171:1113–16 [Google Scholar]
  145. Thomas JA, Welch JJ, Lanfear R, Bromham L. 145.  2010. A generation time effect on the rate of molecular evolution in invertebrates. Mol. Biol. Evol. 27:1173–80 [Google Scholar]
  146. Thrall PH, Burdon JJ. 146.  2000. Effect of resistance variation in a natural plant host-pathogen metapopulation on disease dynamics. Plant Pathol. 49:767–73 [Google Scholar]
  147. Thrall PH, Burdon JJ. 147.  2002. Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathol. 51:169–84 [Google Scholar]
  148. Thrall PH, Burdon JJ. 148.  2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735–37 [Google Scholar]
  149. Thrall PH, Laine AL, Ravensdale M, Nemri A, Dodds PN. 149.  et al. 2012. Rapid antagonistic coevolution in a natural host-pathogen metapopulation. Ecol. Lett. 15:425–35 [Google Scholar]
  150. Thrall PH, Oakeshott JG, Fitt G, Southerton S, Burdon JJ. 150.  et al. 2011. Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agroecosystems. Evol. Appl. 4:200–15 [Google Scholar]
  151. Thurston HD. 151.  1990. Plant disease management practices of traditional farmers. Plant Dis. 74:96–101 [Google Scholar]
  152. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J. 152.  2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–76 [Google Scholar]
  153. Truong-Bolduc QC, Dunman PM, Strahilevitz J, Projan SJ, Hooper DC. 153.  2005. MgrA is a multiple regulator of two new efflux pumps in Staphylococcus aureus. J. Bacteriol. 187:2395–405 [Google Scholar]
  154. Turkington TK, Xi K, Tewari JP, Lee HK, Clayton GW, Harker KN. 154.  2005. Cultivar rotation as a strategy to reduce leaf diseases under barley monoculture. Can. J. Plant Pathol. 27:283–90 [Google Scholar]
  155. Ullstrup AJ. 155.  1972. The impacts of the southern leaf corn blight epidemics of 1970–1971. Annu. Rev. Phytopathol. 10:37–50 [Google Scholar]
  156. Urban M, Bhargava T, Hamer JE. 156.  1999. An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J. 18:512–21 [Google Scholar]
  157. Van Elsas JD, Speksnijder AJ, van Overbeek LS. 157.  2008. A procedure for the metagenomics exploration of disease-suppressive soils. J. Microbiol. Methods 75:515–22 [Google Scholar]
  158. Waage JK, Mumford JD. 158.  2008. Agricultural biosecurity. Philos. Trans. R. Soc. B 363:863–76 [Google Scholar]
  159. Watson IA, de Sousa CNA. 159.  1983. Long distance transport of spores of Puccinia graminis tritici in the Southern Hemisphere. Proc. Linn. Soc. N.S.W. 106:311–21 [Google Scholar]
  160. Watson IA. 160.  1981. Wheat and its rust parasites in Australia. Wheat Science: Today and Tomorrow LT Evans, WJ Peacock 129–47 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  161. Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS. 161.  2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309–48 [Google Scholar]
  162. Wellings CR. 162.  2007. Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979–2006. Aust. J. Agric. Res. 58:567–75 [Google Scholar]
  163. Wellings CR. 163.  2011. Global status of stripe rust: a review of historical and current threats. Euphytica 179:129–41 [Google Scholar]
  164. Wolfe MS. 164.  1985. The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Annu. Rev. Phytopathol. 23:251–73 [Google Scholar]
  165. Wright S. 165.  1931. Evolution in Mendelian populations. Genetics 16:97–159 [Google Scholar]
  166. Wright S. 166.  1938. Size of population and breeding structure in relation to evolution. Science 87:430–31 [Google Scholar]
  167. Wright S. 167.  1943. Isolation by distance. Genetics 28:114–38 [Google Scholar]
  168. Yang L, Gao F, Shang L, Zhan J, McDonald BA. 168.  2013. Association between virulence and triazole resistance in pathogenic fungus Mycosphaerella graminicola. PLOS ONE 8:e59568 [Google Scholar]
  169. Zeller SL, Kalinina O, Schmid B. 169.  2013. Costs of resistance to fungal pathogens in genetically modified wheat. J. Plant Ecol. 6:92–100 [Google Scholar]
  170. Zhan J, McDonald BA. 170.  2013. Experimental measures of pathogen competition and relative fitness. Annu. Rev. Phytopathol. 51:131–53 [Google Scholar]
  171. Zhan J, Mundt CC, Hoffer MH, McDonald BA. 171.  2002. Local adaptation and effect of host genotype on the evolution of pathogen: an experimental test in a plant pathosystem. J. Evol. Biol. 15:634–47 [Google Scholar]
  172. Zhan J, Mundt CC, McDonald BA. 172.  2001. Using RFLPs to assess temporal variation and estimate the number of ascospores that initiate epidemics in field populations of Mycosphaerella graminicola. Phytopathology 91:1011–17 [Google Scholar]
  173. Zhan J, Mundt CC, McDonald BA. 173.  2007. Sexual reproduction facilitates the adaptation of parasites to antagonistic host environment: evidence from field experiment with wheat–Mycosphaerella graminicola system. Int. J. Parasitol. 37:861–70 [Google Scholar]
  174. Zhan J, Pettway RE, McDonald BA. 174.  2003. The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genet. Biol. 38:286–97 [Google Scholar]
  175. Zhan J, Stefanato F, McDonald BA. 175.  2006. Selection for increased cyproconazole tolerance in Mycosphaerella graminicola through local adaptation and in response to host resistance. Mol. Plant Pathol. 7:259–68 [Google Scholar]
  176. Zhan J, Thrall PH, Burdon JJ. 176.  2014. Achieving sustainable plant disease management through evolutionary principles. Trends Plant Sci. 19:570–75 [Google Scholar]
  177. Zhan J, Yang L, Zhu W, Shang L, Newton AC. 177.  2012. Pathogen populations evolve to greater race complexity in agricultural systems: evidence from analysis of Rhynchosporium secalis virulence data. PLOS ONE 7:e38611 [Google Scholar]
  178. Zhang H, Wang C, Cheng Y, Chen X, Han Q. 178.  et al. 2012. Histological and cytological characterization of adult plant resistance to wheat stripe rust. Plant Cell Rep. 31:2121–37 [Google Scholar]
  179. Zhong BJ, Fong R, Collins LJ, McLenachan PA, Penny D. 179.  2014. Two new fern chloroplasts and decelerated evolution linked to the long generation time in tree ferns. Genome Biol. Evol. 6:1166–73 [Google Scholar]
  180. Zhu Y, Chen H, Fan J, Wang Y, Li Y. 180.  et al. 2000. Genetic diversity and disease control in rice. Nature 406:718–22 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error