Continua of specificity and virulence in plant host-pathogen interactions: Causes and consequences

New Phytologist

Volumn 183, Issue 3, 2009, Pages 513-529

  Barrett, Luke G ^a   Kniskern, Joel M ^a   Bodenhausen, Natacha ^a   Zhang, Wen ^a   Bergelson, Joy ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Coevolution; Community; Disease; Epidemiology; Evolution; Host range; Life history; Parasite

Indexed keywords

ECOLOGICAL MODELING; EPIDEMIOLOGY; FITNESS; HETEROGENEITY; HOST PLANT; HOST RANGE; HOST SPECIFICITY; HOST-PATHOGEN INTERACTION; LIFE HISTORY THEORY; VIRULENCE;

ECOSYSTEM; EVOLUTION; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PLANT; REVIEW; SPECIES DIFFERENCE; VIRULENCE;

ECOSYSTEM; EVOLUTION; HOST-PATHOGEN INTERACTIONS; PLANTS; SPECIES SPECIFICITY; VIRULENCE;

EID: 67650932358     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.02927.x     Document Type: Review

References (190)

1. Abramovitch RB, Martin GB. 2005. AvrPtoB: a bacterial type III effector that both elicits and suppresses programmed cell death associated with plant immunity. FEMS Microbiology Letters 245 : 1 8.
2. 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 : 806 814.
3. Al-Naimi FA, Garrett KA, Bockus WW. 2005. Competition, facilitation, and niche differentiation in two foliar pathogens. Oecologia 143 : 449 457.
4. Ashfield T, Ong LE, Nobuta K, Schneider CM, Innes RW. 2004. Convergent evolution of disease resistance gene specificity in two flowering plant families. Plant Cell 16 : 309 318.
5. Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112 : 369 377.
6. Ayliffe MA, Lagudah ES. 2004. Molecular genetics of disease resistance in cereals. Annals of Botany 94 : 765 773.
7. Barash I, Manulis-Sasson S. 2007. Virulence mechanisms and host specificity of gall-forming Pantoea agglomerans. Trends in Microbiology 15 : 538 545.
8. Barrett LG, Thrall PH, Burdon JJ. 2007. Evolutionary diversification through hybridization in a wild host-pathogen interaction. Evolution 61 : 1613 1621.
9. Barrett LG, Thrall PH, Burdon JJ, Nicotra AB, Linde CC. 2008. Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Molecular Ecology 17 : 3401 3415.
10. Bell T, Freckleton RP, Lewis OT. 2006. Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecology Letters 9 : 569 574.
11. Bent AF, Mackey D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annual Review of Phytopathology 45 : 399 436.
12. Bergelson J, Dwyer G, Emerson JJ. 2001. Models and data on plant-enemy coevolution. Annual Review of Genetics 35 : 469 499.
13. Bergelson J, Purrington CB. 1996. Surveying patterns in the cost of resistance in plants. American Naturalist 148 : 536 558.
14. Biere A, Antonovics J. 1996. Sex-specific costs of resistance to the fungal pathogen Ustilago violaceae (Microbotryum violaceum) in Silene alba. Evolution 50 : 1098 1110.
15. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. Plos Biology 5 : 1962 1972.
16. Bradley DJ, Gilbert GS, Martiny JBH. 2008. Pathogens promote plant diversity through a compensatory response. Ecology Letters 11 : 461 469.
17. Burdon JJ. 1987. Diseases and plant population biology. Cambridge, UK : Cambridge University Press.
18. Burdon JJ. 1991. Fungal pathogens as selective forces in plant populations and communities. Australian Journal of Botany 16 : 423 432.
19. Burdon JJ, Chilvers GA. 1982. Host density as a factor in plant disease ecology. Annual Review of Phytopathology 20 : 143 166.
20. Burdon JJ, Thrall PH. 1999. Spatial and temporal patterns in coevolving plant and pathogen associations. American Naturalist 153 : S15 S33.
21. Caldwell RM, Schafer JF, Compton LE, Patterson FL. 1958. Tolerance to cereal leaf rusts. Science 128 : 714 715.
22. Caraco T, Wang IN. 2008. Free-living pathogens: Life-history constraints and strain competition. Journal of Theoretical Biology 250 : 569 579.
23. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124 : 803 814.
24. Clay K, Kover PX. 1996. The Red Queen Hypothesis and plant/pathogen interactions. Annual Review of Phytopathology 34 : 29 50.
25. Cleaveland S, Laurenson MK, Taylor LH. 2000. Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society of London Series B - Biological Sciences 356 : 991 999.
26. Colhoun J. 1973. Effects of environmental factors on plant disease. Annual Review of Phytopathology 11 : 343 364.
27. Compant S, Duffy B, Nowak J, Clement C, Barka EA. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology 71 : 4951 4959.
28. Connell J. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In : Den Boer P, Gradwell G, eds. Dynamics of populations:Proceedings of the Advanced Study Institute on dynamics of numbers in populations. Oosterbeek, The Netherlands : Pudoc.
29. Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausubel FM. 2005. Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proceedings of the National Academy of Science, USA 102 : 1791 1796.
30. Dobson A, Foufopoulos J. 2001. Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London Series B - Biological Sciences 356 : 1001 1012.
31. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CIA, Ayliffe MA, Kobe B, Ellis JG. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Science, USA 103 : 8888 8893.
32. van der Does HC, Rep M. 2007. Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Molecular Plant-Microbe Interactions 20 : 1175 1182.
33. Douhan GW, Smith ME, Huyrn KL, Westbrook A, Beerli P, Fisher AJ. 2008. Multigene analysis suggests ecological speciation in the fungal pathogen Claviceps purpurea. Molecular Ecology 17 : 2276 2286.
34. Duffy S, Burch CL, Turner PE. 2007. Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution 61 : 2614 2622.
35. Duniway JM. 1979. Water relations of water molds. Annual Review of Phytopathology 17 : 431 460.
36. Dwyer G, Elkinton JS, Buonaccorsi JP. 1997. Host heterogeneity in susceptibility and disease dynamics: tests of a mathematical model. American Naturalist 150 : 685 707.
37. Ellis J, Dodds P, Lawrence G. 2007. Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annual Review of Phytopathology 45 : 289 306.
38. Ellis J, Dodds P, Pryor T. 2000. The generation of plant disease resistance gene specificities. Trends in Plant Science 5 : 373 379. (Pubitemid 30738117)
39. Eriksson J, Henning E. 1896. Die getreideroste. Stockholm, Sweden : Norstedt.
40. Eshed N, Dinoor A. 1980. Genetics of pathogenicity in Puccinia coronata - pathogenic specialization at the host genus level. Phytopathology 70 : 1042 1046.
41. Falconer DS. 1952. The problem of environment and selection. American Naturalist 86 : 293 298.
42. Farr D, Rossman A. 2009. Fungal databases. Systematic Mycology and Microbiology Laboratory. Beltsville, MD: ARS, USDA.
43. Fenton A, Brockhurst MA. 2008. The role of specialist parasites in structuring host communities. Ecological Research 23 : 795 804.
44. Flor HH. 1956. The complementary genic systems in flax and flax rust. Advances in Genetics 8 : 29 54.
45. Fournier E, Giraud T. 2008. Sympatric genetic differentiation of a generalist pathogenic fungus, Botrytis cinerea, on two different host plants, grapevine and bramble. Journal of Evolutionary Biology 21 : 122 132.
46. Frank SA. 1992. Models of plant-pathogen coevolution. Trends in Genetics 8 : 213 219.
47. Frank SA. 1996. Models of parasite virulence. Quarterly Review of Biology 71 : 37 78.
48. Friesen TL, Faris JD, Solomon PS, Oliver RP. 2008. Host-specific toxins: effectors of necrotrophic pathogenicity. Cellular Microbiology 10 : 1421 1428.
49. Friesen TL, Stukenbrock EH, Liu ZH, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics 38 : 953 956.
50. Fry JD. 1996. The evolution of host specialization: are trade-offs overrated? American Naturalist 148 : S84 S107.
51. Futuyma DJ, Moreno G. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19 : 207 233.
52. Gandon S. 2002. Local adaptation and the geometry of host-parasite coevolution. Ecology Letters 5 : 246 256.
53. Gandon S. 2004. Evolution of multihost parasites. Evolution 58 : 455 469.
54. Gandon S. 1998. The curse of the pharaoh hypothesis. Proceedings of the Royal Society of London Series B - Biological Sciences 265 : 1545 1552.
55. Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I. 1996. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London Series B-Biological Sciences 263 : 1003 1009.
56. Garrett KA, Mundt CC. 1999. Epidemiology in mixed host populations. Phytopathology 89 : 984 990.
57. Gaunt RE. 1995. The relationship between plant-disease severity and yield. Annual Review of Phytopathology 33 : 119 144.
58. Gibson CC, Watkinson AR. 1991. Host selectivity and the mediation of competition by the root hemiparasite Rhinanthus minor. Oecologia 86 : 81 87.
59. Gilbert GS. 2002. Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology 40 : 13 43.
60. Gilbert GS. 2005. Dimensions of plant disease in tropical forests. In : Burslem DFRP, Pinard MA, Hartley SE, eds. Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge, UK : Cambridge University Press, 141 164.
61. Gilbert GS, Webb CO. 2007. Phylogenetic signal in plant pathogen-host range. Proceedings of the National Academy of Sciences, USA 104 : 4979 4983.
62. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43 : 205 227.
63. Göhre V, Robatzek S. 2008. Breaking the barriers: Microbial effector molecules subvert plant immunity. Annual Review of Phytopathology 46 : 189 215.
64. Gomez DR, Evans KJ, Baker J, Harvey PR, Scott ES. 2008. Dynamics of introduced populations of Phragmidium violaceum and implications for biological control of European blackberry in Australia. Applied and Environmental Microbiology 74 : 5504 5510.
65. Goss EM, Bergelson J. 2007. Fitness consequences of infection of Arabidopsis thaliana with its natural bacterial pathogen Pseudomonas viridiflava. Oecologia 152 : 71 81.
66. Goss EM, Kreitman M, Bergelson J. 2005. Genetic diversity, recombination and cryptic clades in Pseudomonas viridiflava infecting natural populations of Arabidopsis thaliana. Genetics 169 : 21 35.
67. Govrin EM, Levine A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10 : 751 757.
68. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL. 2006. Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annual Review of Microbiology 60 : 425 449.
69. Greenberg JT, Yao N. 2004. The role and regulation of programmed cell death in plant-pathogen interactions. Cellular Microbiology 6 : 201 211.
70. Greischar MA, Koskella B. 2007. A synthesis of experimental work on parasite local adaptation. Ecology Letters 10 : 418 434.
71. Grewell BJ. 2008. Parasite facilitates plant species coexistence in a coastal wetland. Ecology 89 : 1481 1488.
72. Hamilton WD. 1980. Sex versus nonsex versus parasite. Oikos 35 : 282 290.
73. Hatcher M, Dick J, Dunn A. 2006. How parasites affect interactions between competitors and predators. Ecology Letters 9 : 1253 1271.
74. Heath MC. 2000. Nonhost resistance and nonspecific plant defenses. Current Opinion in Plant Biology 3 : 315 319.
75. Hirano SS, Upper CD. 1990. Population biology and epidemiology of Pseudomonas syringae. Annual Review of Phytopathology 28 : 155 177.
76. Holt RD. 1977. Predation, apparent competition and structure of prey communities. Theoretical Population Biology 12 : 197 229.
77. Hood ME. 2003. Dynamics of multiple infection and within-host competition by the anther-smut pathogen. American Naturalist 162 : 122 133.
78. Hückelhoven R. 2007. Cell wall-associated mechanisms of disease resistance and susceptibility. Annual Review of Phytopathology 45 : 101 127.
79. Hudson P, Greenman J. 1998. Competition mediated by parasites: biological and theoretical progress. Trends in Ecology & Evolution 13 : 387 390.
80. Islam MR, Shepherd KW, Mayo GME. 1989. Effect of genotype and temperature on the expression of L genes in flax conferring resistance to rust. Physiological and Molecular Plant Pathology 35 : 141 150.
81. Iwao K, Rausher MD. 1997. Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. American Naturalist 149 : 316 335.
82. Jaenike J. 1990. Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21 : 243 273.
83. Janzen DH. 1970. Herbivores and number of tree species in tropical forests American Naturalist 104 : 501 528.
84. Jarosz AM, Burdon JJ. 1991. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. II. Local and regional variation in patterns of resistance and racial structure. Evolution 45 : 1618 1627.
85. Jarosz AM, Davelos AL. 1995. Effects of disease in wild plant-populations and the evolution of pathogen aggressiveness. New Phytologist 129 : 371 387.
86. Kassen B, Bell G. 1998. Experimental evolution in Chlamydomonas. IV. Selection in environments that vary through time at different scales. Heredity 80 : 732 741.
87. Kawecki TJ. 1994. Accumulation of deleterious mutations and the evolutionary cost of being a generalist. American Naturalist 144 : 833 838.
88. Kawecki TJ. 1998. Red Queen meets Santa Rosalia: arms races and the evolution of host specialization in organisms with parasitic lifestyles. American Naturalist 152 : 635 651.
89. Kim YJ, Lin N-C, Martin GB. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109 : 589 598.
90. Kirchner JW, Roy BA. 2002. Evolutionary implications of host-pathogen specificity: fitness consequences of pathogen virulence traits. Evolutionary Ecology Research 4 : 27 48.
91. Kniskern JM, Rausher MD. 2006a. Environmental variation mediates the deleterious effects of Coleosporium ipomoeae on Ipomoea purpurea. Ecology 87 : 675 685.
92. Kniskern JM, Rausher MD. 2006b. Major-gene resistance to the rust pathogen Coleosporium ipomoeae is common in natural populations of Ipomoea purpurea. New Phytologist 171 : 137 144.
93. Kniskern JM, Traw MB, Bergelson J. 2007. Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Molecular Plant-Microbe Interactions 20 : 1512 1522.
94. Korves T, Bergelson J. 2004. A novel cost of R gene resistance in the presence of disease. American Naturalist 163 : 489 504.
95. Kover PX, Schaal BA. 2002. Genetic variation for disease resistance and tolerance among Arabidopsis thaliana accessions. Proceedings of the National Academy of Sciences, USA 99 : 11270 11274.
96. Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS. 2004. Ectoparasitic 'jacks-of-all-trades': Relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. American Naturalist 164 : 506 516. (Pubitemid 39385109)
97. Kunkel BN, Brooks DM. 2002. Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5 : 325 331.
98. Laine A. 2004. Resistance variation within and among host populations in a plant-pathogen metapopulation: implications for regional pathogen dynamics. Journal of Ecology 92 : 990 1000.
99. Laine A. 2006. Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proceedings of the Royal Society of London Series B - Biological Sciences 273 : 267 273.
100. Laine AL. 2008. Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecology Letters 11 : 327 337.
101. Lajeunesse MJ, Forbes MR. 2002. Host range and local parasite adaptation. Proceedings of the Royal Society of London Series B - Biological Sciences 269 : 703 710.
102. Lawton KA, Friedrich L, Hunt M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J. 1996. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant Journal 10 : 71 82.
103. Lenski RE, May RM. 1994. The evolution of virulence in parasites and pathogens - reconciliation between two competing hypotheses. Journal of Theoretical Biology 169 : 253 265.
104. Leonard KJ. 1969. Factors affecting rates of stem rust increase in mixed plantings of susceptible and resistant oat varieties. Phytopathology 59 : 1845 1850.
105. Levins R. 1968. Evolution in changing environments. Princeton NJ, USA : Princeton University Press.
106. Lively CM. 1989. Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43 : 1663 1671.
107. Lively CM. 2006. The ecology of virulence. Ecology Letters 9 : 1089 1095.
108. Loiseau C, Zoorob R, Garnier S, Birard J, Federici P, Julliard R, Sorci G. 2008. Antagonistic effects of a Mhc class I allele on malaria-infected house sparrows. Ecology Letters 11 : 258 265.
109. Lopez-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 : 1710 1715.
110. Lorang JM, Sweat TA, Wolpert TJ. 2007. Plant disease susceptibility conferred by a 'resistance' gene. Proceedings of the National Academy of Sciences, USA 104 : 14861 14866.
111. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112 : 379 389.
112. Mackey D, Holt BF, Wiig A, Dangl JL. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108 : 743 754.
113. Mackinnon MJ, Read AF. 2004. Virulence in malaria: an evolutionary viewpoint. Philosophical Transactions of the Royal Society of London Series B - Biological Sciences 359 : 965 986.
114. Malmstrom CM, Hughes CC, Newton LA, Stoner CJ. 2005a. Virus infection in remnant native bunchgrasses from invaded California grasslands. New Phytologist 168 : 217 230.
115. Malmstrom CM, McCullough AJ, Johnson HA, Newton LA, Borer ET. 2005b. Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145 : 153 164.
116. Malmstrom CM, Stoner CJ, Brandenburg S, Newton LA. 2006. Virus infection and grazing exert counteracting influences on survivorship of native bunchgrass seedlings competing with invasive exotics. Journal of Ecology 94 : 264 275.
117. Malpica J, Sacristan S, Fraile A, Garcia-Arenal F. 2006. Association and host selectivity in multi-host pathogens. PLoS ONE 1 : e41.
118. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu TY, Earle ED, Tanksley SD. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262 : 1432 1436.
119. Maurhofer M, Keel C, Schnider U, Voisard C, Haas D, Defago G. 1992. Influence of enhanced antibiotic production in Pseudomonas fluorescens strain-Cha0 on its disease suppressive capacity. Phytopathology 82 : 190 195.
120. May RM, Anderson RM. 1983. Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London Series B - Biological Sciences 219 : 281 313.
121. Melotto M, Underwood W, He SY. 2008. Role of stomata in plant innate immunity and foliar bacterial diseases. Annual Review of Phytopathology 46 : 101 122.
122. 2, nitrogen deposition, and decreased species diversity on foliar fungal plant disease. Global Change Biology 9 : 438 451.
123. Mitchell CE, Tilman D, Groth JV. 2002. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83 : 1713 1726.
124. Mundt CC. 2002. Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology 40 : 381 410.
125. Mysore KS, Ryu CM. 2004. Nonhost resistance: how much do we know? Trends in Plant Science 9 : 97 104.
126. Nürnberger T, Lipka V. 2005. Nonhost resistance in plants: new insights into an old phenomenon. Molecular Plant Pathology 6 : 335 345.
127. Packer A, Clay K. 2000. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404 : 278 281.
128. Palaima A. 2007. The fitness cost of generalization: present limitations and future possible solutions. Biological Journal of the Linnean Society 90 : 583 590.
129. Pan JJ, Clay K. 2002. Infection by the systemic fungus Epichloe glyceriae and clonal growth of its host grass Glyceria striata. Oikos 98 : 37 46.
130. Pan JJ, Clay K. 2003. Infection by the systemic fungus Epichloe glyceriae alters clonal growth of its grass host, Glyceria striata. Proceedings of the Royal Society of London Series B - Biological Sciences 270 : 1585 1591.
131. Parker IM, Gilbert GS. 2004. The evolutionary ecology of novel plant-pathogen interactions. Annual Review of Ecology Evolution and Systematics 35 : 675 700.
132. Parker MA. 1985. Local population differentiation for compatibility in an annual legume and its host specific fungal pathogen. Evolution 39 : 713 723.
133. Parker MA. 1991. Nonadaptive evolution and disease resistance in an annual legume. Evolution 45 : 1209 1217.
134. Paul ND, Laxmi KA, Ayres PG. 1990. Responses of rust (Puccinia lagenophorae) to nutrient supply in groundsel (Senecio vulgaris) and effects of infection on host nutrient relations. New Phytologist 115 : 99 106.
135. Poulin R, Mouillot D. 2005. Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91 : 511 514.
136. Power AG, Mitchell CE. 2004. Pathogen spillover in disease epidemics. American Naturalist 164 : S79 S89.
137. Price PW. 1980. Evolutionary biology of parasites. Princeton, NJ, USA : Princeton University Press.
138. Read AF. 1994. The evolution of virulence. Trends in Microbiology 2 : 73 76.
139. Read AF, Taylor LH. 2001. The ecology of genetically diverse infections. Science 292 : 1099 1102.
140. Reboud X, Bell G. 1997. Experimental evolution in Chlamydomonas. 3. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78 : 507 514.
141. Redman RS, Dunigan DD, Rodriguez RJ. 2001. Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytologist 151 : 705 716.
142. Ronald PC, Salmeron JM, Carland FM, Staskawicz BJ. 1992. The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. Journal of Bacteriology 174 : 1604 1611.
143. Rouhier N, Jacquot J. 2008. Getting sick may help plants overcome abiotic stress. New Phytologist 180 : 738 741.
144. Sacristan S, Garcia-Arenal F. 2008. The evolution of virulence and pathogenicity in plant pathogen populations. Molecular Plant Pathology 9 : 369 384.
145. Salathé M, Scherer A, Bonhoeffer S. 2005. Neutral drift and polymorphism in gene-for-gene systems. Ecology Letters 8 : 925 932.
146. Salvaudon L, Giraud T, Shykoff JA. 2008a. Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Current Opinion in Plant Biology 11 : 135 143.
147. Salvaudon L, Heraudet V, Shykoff JA. 2005. Parasite-host fitness trade-offs change with parasite identity: Genotype-specific interactions in a plant-pathogen system. Evolution 59 : 2518 2524.
148. Salvaudon L, Heraudet V, Shykoff JA. 2008b. Arabidopsis thaliana and the Robin Hood parasite: a chivalrous oomycete that steals fitness from fecund hosts and benefits the poorest one? Biology Letters 4 : 526 529.
149. Sarkar SF, Gordon JS, Martin GB, Guttman DS. 2006. Comparative genomics of host-specific virulence in Pseudomonas syringae. Genetics 174 : 1041 1056.
150. Sarkar SF, Guttman DS. 2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Applied and Environmental Microbiology 70 : 1999 2012.
151. Schnathorst W. 1965. Environmental relationships in powdery mildews. Annual Review of Phytopathology 3 : 343 &.
152. Schurch S, Roy BA. 2004. Comparing single- vs. mixed-genotype infections of Mycosphaerella graminicola on wheat: effects on pathogen virulence and host tolerance. Evolutionary Ecology 18 : 1 14.
153. Seabloom EW, Hosseini PR, Power AG, Borer ET. 2009. Diversity and composition of viral communities: Coinfection of barley and cereal yellow dwarf viruses in California grasslands. American Naturalist 173 : E79 E98.
154. Seiwa K, Miwa Y, Sahashi N, Kanno H, Tomita M, Ueno N, Yamazaki M. 2008. Pathogen attack and spatial patterns of juvenile mortality and growth in a temperate tree, Prunus grayana. Canadian Journal of Forest Research 38 : 2445 2454.
155. Shearer BL, Crane CE, Barrett S, Cochrane A. 2007. Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Australian Journal of Botany 55 : 225 238.
156. Shykoff JA, Meyhofer A, Bucheli E. 1999. Genetic isolation among host races of the anther smut fungus Microbotryum violaceum on three host plant species. International Journal of Plant Sciences 160 : 907 916.
157. Simms EL, Triplett J. 1994. Costs and benefits of plant-responses to disease - resistance and tolerance. Evolution 48 : 1973 1985.
158. Sloan DB, Giraud T, Hood ME. 2008. Maximized virulence in a sterilizing pathogen: the anther-smut fungus and its co-evolved hosts. Journal of Evolutionary Biology 21 : 1544 1554.
159. Smith DM. 2000. American chestnut: Ill-fated monarch of the eastern hardwood forest. Journal of Forestry 98 : 12 15.
160. Smith KP, Handelsman J, Goodman RM. 1999. Genetic basis in plants for interactions with disease-suppressive bacteria. Proceedings of the National Academy of Sciences, USA 96 : 4786 4790.
161. Spoel SH, Johnson JS, Dong X. 2007. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences, USA 104 : 18842 18847.
162. Springer YP, Hardcastle BA, Gilbert GS. 2007. Soil calcium and plant disease in serpentine ecosystems: a test of the pathogen refuge hypothesis. Oecologia 151 : 10 21.
163. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J. 1999. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400 : 667 671.
164. Sticher L, Mauch-Mani B, Metraux JP. 1997. Systemic acquired resistance. Annual Review of Phytopathology 35 : 235 270.
165. Sweat TA, Lorang JM, Bakker EG, Wolpert TJ. 2008. Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis. Molecular Plant-Microbe Interactions 21 : 7 19.
166. Tewksbury JJ, Reagan KM, Machnicki NJ, Carlo TA, Haak DC, Penaloza ALC, Levey DJ. 2008. Evolutionary ecology of pungency in wild chilies. Proceedings of the National Academy of Sciences, USA 105 : 11808 11811.
167. Thompson JN. 1994. The coevolutionary process. Chicago, IL, USA : University of Chicago Press.
168. Thompson JN, Burdon JJ. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360 : 121 125.
169. Thrall PH, Barrett LG, Burdon JJ, Alexander HM. 2005. Variation in pathogen aggressiveness within a metapopulation of the Cakile maritima-Alternaria brassicicola host-pathogen association. Plant Pathology 54 : 265 274.
170. Thrall PH, Burdon JJ. 1999. The spatial scale of pathogen dispersal: consequences for disease dynamics and persistence. Evolutionary Ecology Research 1 : 681 701.
171. Thrall PH, Burdon JJ. 2000. Effect of resistance variation in a natural plant host-pathogen metapopulation on disease dynamics. Plant Pathology 49 : 767 773.
172. Thrall PH, Burdon JJ. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299 : 1735 1737.
173. Thrall PH, Hochberg ME, Burdon JJ, Bever JD. 2007. Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology & Evolution 22 : 120 126.
174. Thrall PH, Jarosz AM. 1994. Host-pathogen dynamics in experimental populations of Silena alba and Ustilago violacea. 1. Ecological and genetic determinants of disease spread. Journal of Ecology 82 : 549 559.
175. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J. 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423 : 74 77.
176. Tian DC, Araki H, Stahl E, Bergelson J, Kreitman M. 2002. Signature of balancing selection in Arabidopsis. Proceedings of the National Academy of Sciences, USA 99 : 11525 11530.
177. Traw MB, Kim J, Enright S, Cipollini DF, Bergelson J. 2003. Negative cross-talk between salicylate- and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Molecular Ecology 12 : 1125 1135.
178. Traw MB, Kniskern JM, Bergelson J. 2007. Sar increases fitness of Arabidopsis thaliana in the presence of natural bacterial pathogens. Evolution 61 : 2444 2449.
179. Uauy C, Brevis JC, Chen XM, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J. 2005. High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Theoretical and Applied Genetics 112 : 97 105.
180. Uknes S, Mauchmani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J. 1992. Acquired-resistance in Arabidopsis. Plant Cell 4 : 645 656.
181. Van der Hoorn RAL, De Wit P, Joosten M. 2002. Balancing selection favors guarding resistance proteins. Trends in Plant Science 7 : 67 71.
182. Van Oosten VR, Bodenhausen N, Reymond P, Van Pelt JA, Van Loon LC, Dicke M, Pieterse CM. 2008. Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Molecular Plant-Microbe Interactions 21 : 919 930.
183. Van Wees SCM, Van der Ent S, Pieterse CMJ. 2008. Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology 11 : 443 448.
184. Vazquez DP, Poulin R, Krasnov BR, Shenbrot GI. 2005. Species abundance and the distribution of specialization in host-parasite interaction networks. Journal of Animal Ecology 74 : 946 955.
185. Wallis CM, Stone AL, Sherman DJ, Damsteegt VD, Gildow FE, Schneider WL. 2007. Adaptation of plum pox virus to a herbaceous host (Pisum sativum) following serial passages. Journal of General Virology 88 : 2839 2845.
186. Walsh UF, Morrissey JP, O'Gara F. 2001. Pseudomonas for biocontrol of phytopathogens: from functional genomics to commercial exploitation. Current Opinion in Biotechnology 12 : 289 295.
187. Whitlock MC. 1996. The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. American Naturalist 148 : S65 S77.
188. Williamson B, Tudzynsk B, Tudzynski P, van Kan JAL. 2007. Botrytis cinerea: the cause of grey mould disease. Molecular Plant Pathology 8 : 561 580.
189. Woolhouse MEJ, Taylor LH, Haydon DT. 2001. Population biology of multihost pathogens. Science 292 : 1109 1112.
190. Wylie SJ, Jones RAC. 2009. Role of recombination in the evolution of host specialization within bean yellow mosaic virus. Phytopathology 99 : 512 518.