Plant-parasite coevolution: Bridging the gap between genetics and ecology

Annual Review of Phytopathology

Volumn 49, Issue , 2011, Pages 345-367

  Brown, James K M ^a   Tellier, Aurélien ^b  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Avirulence; Boom and bust cycle; Effector; Frequency dependent selection; Polymorphism; Resistance

Indexed keywords

AGRICULTURE; ANIMAL; BIOLOGICAL MODEL; ENVIRONMENT; EVOLUTION; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOMIC INSTABILITY; HOST PARASITE INTERACTION; PARASITE; PARASITOLOGY; PHYSIOLOGY; PLANT; PLANT IMMUNITY; REVIEW; VIRULENCE;

AGRICULTURE; ANIMALS; BIOLOGICAL EVOLUTION; ENVIRONMENT; GENETIC VARIATION; GENOMIC INSTABILITY; HOST-PARASITE INTERACTIONS; MODELS, GENETIC; PARASITES; PLANT IMMUNITY; PLANTS; POLYMORPHISM, GENETIC; SELECTION, GENETIC; VIRULENCE;

EID: 80051759269     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-072910-095301     Document Type: Review

References (147)

1. Aguileta G, Refregier G, Yockteng R, Fournier E, Giraud T. 2009. Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Inf. Genet. Evol. 9:656-670
2. Allen JC. 1975. Mathematical models of species interactions in time and space. Am. Nat. 109:319-342
3. Allen R L, Bittner-Eddy P D, Grenville-Briggs L J, Meitz J C, Rehmany A P, et al. 2004. Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306:1957-1960 (Pubitemid 39627865)
4. Antonovics J, Thrall PH. 1994. The cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proc. R. Soc. B 257:105-110 (Pubitemid 24274925)
5. Araki H, Tian D C, Goss E M, Jakob K, Halldorsdottir S S, et al. 2006. Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. Proc. Natl. Acad. Sci. USA 103:5887-5892
6. Atwell S, Huang Y S, Vilhjalmsson B J, Willems G, Horton M, et al. 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627-631
7. 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 Evol. Biol. 9:26.
8. Bakker E G, Toomajian C, Kreitman M, Bergelson J. 2006. A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18:1803-1818 (Pubitemid 44260179)
9. Barrett JA. 1980. Pathogen evolution in multilines and variety mixtures. Z. Pflanzenkrankh. Pflanzenschutz 87:383-396
10. Barrett L G, Kniskern J M, Bodenhausen N, Zhang W, Bergelson J. 2009. Continua of specificity and virulence in plant host-pathogen interactions: causes and consequences. New Phytol. 183:513-529
11. Barrett L G, Thrall P H, Dodds P N, van der Merwe M, Linde C C, et al. 2009. Diversity and evolution of effector loci in natural populations of the plant pathogen Melampsora lini. Mol. Biol. Evol. 26:2499-513.
12. Bergelson J, Dwyer G, Emerson JJ. 2001. Models and data on plant-enemy coevolution. Annu. Rev. Genet. 35:469-499 (Pubitemid 34032984)
13. Bergelson J, Kreitman M, Stahl E A, Tian DC. 2001. Evolutionary dynamics of plant R-genes. Science 292:2281-2285 (Pubitemid 32568041)
14. Bergelson J, Purrington CB. 1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:536-558
15. Bomblies K, Weigel D. 2007. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8:382-393 (Pubitemid 46625807)
16. Brockhurst M A, Buckling A, Poullain V, Hochberg ME. 2007. The impact of migration from parasitefree patches on antagonistic host-parasite coevolution. Evolution 61:1238-1243 (Pubitemid 46699452)
17. Brown JKM. 1995. Pathogens' responses to the management of disease resistance genes. In Advances in Plant Pathology, Vol. 11., ed. JH Andrews, IC Tommerup, pp. 75-102. London: Academic.
18. Brown JKM. 2003. A cost of disease resistance: paradigm or peculiarity? Trends Genet. 19:667-671 (Pubitemid 37464839)
19. Brown JKM. 2003. Little else but parasites. Science 299:1680-1681 (Pubitemid 36337182)
20. Brown JKM. 2007. Fitness costs of plant disease resistance. In Handbook of Plant Science, ed. K Robert, pp. 815-22. Chichester, UK: JohnWiley & Sons.
21. Brown JK M, Handley RJ. 2006. Evolutionary genetics: fight or flinch? Heredity 96:3-4.
22. Brown JK M, Hovmøller MS. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537-541 (Pubitemid 34815327)
23. Burdon J J, Jarosz AM. 1991. Host-pathogen interactions in natural-populations of Linum marginale and Melampsora lini. 1. Patterns of resistance and racial variation in a large host population. Evolution 45:205-217
24. Caicedo A L, Schaal BA. 2004. Heterogeneous evolutionary processes affect R gene diversity in natural populations of Solanum pimpinellifolium. Proc. Natl. Acad. Sci. USA 101:17444-7449 (Pubitemid 39657424)
25. Caldo R A, Nettleton D, Peng J Q, Wise RP. 2006. Stage-specific suppression of basal defense discriminates barley plants containing fast-and delayed-acting Mla powdery mildew resistance alleles. Mol. Plant-Microbe Interact. 19:939-947 (Pubitemid 44260236)
26. Campbell C L, Madden LV. 1990. Introduction to Plant Disease Epidemiology. New York: Wiley Interscience.
27. Clarke B. 1964. Frequency-dependent selection for dominance of rare polymorphic genes. Evolution 18:364-369
28. Clarke B. 1976. The ecological genetics of host-parasite relationships. In Genetic Aspects of Host-Parasite Relationships, ed. AER Taylor, R Muller, pp. 97-103. Oxford, UK: Blackwell.
29. Damgaard C. 1999. Coevolution of a plant host-pathogen gene-for-gene system in a metapopulation model without cost of resistance or cost of virulence. J. Theor. Biol. 201:1-12. (Pubitemid 29531308)
30. de Meaux J, Cattan-Toupance I, Lavigne C, Langin T, Neema C. 2003. Polymorphism of a complex resistance gene candidate family in wild populations of common bean (Phaseolus vulgaris) in Argentina: comparison with phenotypic resistance polymorphism. Mol. Ecol. 12:263-273 (Pubitemid 36108122)
31. Decaestecker E, Gaba S, Raeymaekers JA M, Stoks R, Van Kerckhoven L, et al. 2007. Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature 450:870-873 (Pubitemid 350231319)
32. Dodds P N, Lawrence G J, Catanzariti A M, Teh T, Wang CI A, et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA 103:8888-8893 (Pubitemid 43878113)
33. Dodds P N, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-548
34. Dunning F M, Sun W, Jansen K L, Helft L, Bent AF. 2007. Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception. Plant Cell 19:3297-313. (Pubitemid 350276726)
35. Fenton A, Antonovics J, Brockhurst MA. 2009. Inverse-gene-for-gene infection genetics and coevolutionary dynamics. Am. Nat. 174:E230-242
36. Fleming RA. 1980. Selection pressures and plant-pathogens-robustness of the model. Phytopathology 70:175-178
37. Flor HH. 1971. Current status of gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296
38. Frank SA. 1992. Models of plant pathogen coevolution. Trends Genet. 8:213-219
39. Frank SA. 1993. Coevolutionary genetics of plants and pathogens. Evol. Ecol. 7:45-75. (Pubitemid 24406979)
40. Frank SA. 1994. Coevolutionary genetics of hosts and parasites with quantitative inheritance. Evol. Ecol. 8:74-94. (Pubitemid 2036745)
41. Gandon S, Buckling A, Decaestecker E, Day T. 2008. Host-parasite coevolution and patterns of adaptation across time and space. J. Evol. Biol. 21:1861-1866
42. Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I. 1996. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc. R. Soc. Lond. B 263:1003-9.
43. Gandon S, Nuismer SL. 2009. Interactions between genetic drift, gene flow, and selection mosaics drive parasite local adaptation. Am. Nat. 173:212-224
44. Gandon S, van Baalen M, Jansen VAA. 2002. The evolution of parasite virulence, superinfection, and host resistance. Am. Nat. 159:658-669 (Pubitemid 34598381)
45. Gavrilets S, Michalakis Y. 2008. Effects of environmental heterogeneity on victim-exploiter coevolution. Evolution 62:3100-3116
46. Gilligan CA. 1983. Modeling of soilborne pathogens. Annu. Rev. Phytopathol. 21:45-64.
47. Giraud T, Gladieux P, Gavrilets S. 2010. Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol. Evol. 25:387-395
48. Guo M, Tian F, Wamboldt Y, Alfano JR. 2009. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol. Plant-Microbe Interact. 22:1069-80.
49. Haas B J, Kamoun S, Zody M C, Jiang RH Y, Handsaker R E, et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393-398
50. Haldane JBS. 1949. Disease and evolution. Ric. Sci. 19:68-76.
51. Hamilton WD. 1980. Sex versus non-sex versus parasite. Oikos 35:282-290
52. Holub EB. 2001. The arms race is ancient history in Arabidopsis, the wildflower. Nat. Rev. Genet. 2:516-527
53. Jeger MJ. 1997. An epidemiological approach to modeling the dynamics of gene-for-gene interactions. In The Gene-for-Gene Relationship, ed. IR Crute, EB Holub, JJ Burdon, pp. 191-209. Wallingford, UK: CABI.
54. Johnson R. 1984. A critical analysis of durable resistance. Annu. Rev. Phytopathol. 22:309-330
55. Jones JD G, Dangl JL. 2006. The plant immune system. Nature 444:323-329 (Pubitemid 44764102)
56. Jordan T, Seeholzer S, Schwizer S, Keller B. 2011. The wheat Mla homolog TmMla1 exhibits an evolutionary conserved function against powdery mildew in both wheat and barley. Plant J. 65:610-21.
57. Karlin S, McGregor J. 1972. Polymorphisms for genetic and ecological systems with weak coupling. Theor. Pop. Biol. 3:210-238
58. Katagiri F, Tsuda K. 2010. Understanding the plant immune system. Mol. Plant-Microbe Interact. 23:1531-1536
59. Kawecki T J, Ebert D. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7:1225-1241 (Pubitemid 39588356)
60. Kesinger J C, Allen LJS. 2002. Genetic models for plant pathosystems. Math. Biosci. 177:247-269 (Pubitemid 34457393)
61. Kesinger J C, Allen LJ S, Strauss RE. 2001. Discrete-time models for gene frequencies and population densities in plant pathosystems. Nonlinear Anal.-Theory Methods Appl. 47:1489-500. (Pubitemid 32733042)
62. Kirby G C, Burdon JJ. 1997. Effects of mutation and random drift on Leonard's gene-for-gene coevolution model. Phytopathology 87:488-493
63. Korves T, Bergelson J. 2004. A novel cost of R gene resistance in the presence of disease. Am. Nat. 163:489-504. (Pubitemid 38630543)
64. Laine AL. 2004. Resistance variation within and among host populations in a plant-pathogen metapopulation: implications for regional pathogen dynamics. J. Ecol. 92:990-1000.
65. Laine AL. 2006. Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proc. R. Soc. B 273:267-273
66. Laine AL. 2008. Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecol. Lett. 11:327-337
67. Laine AL. 2009. Role of coevolution in generating biological diversity: spatially divergent selection trajectories. J. Exp. Bot. 60:2957-2970
68. Laine A L, Tellier A. 2008. Heterogeneous selection promotes maintenance of polymorphism in hostparasite interactions. Oikos 117:1281-1288
69. Leach J E, Cruz CM V, Bai J F, Leung H. 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 39:187-224. (Pubitemid 32965184)
70. Leonard KJ. 1969. Genetic equilibria in host-pathogen systems. Phytopathology 59:1858-1863
71. Leonard KJ. 1977. Selection pressures and plant pathogens. Ann. N. Y. Acad. Sci. 287:207-222 (Pubitemid 8059130)
72. Leonard KJ. 1994. Stability of equilibria in a gene-for-gene coevolution model of host-parasite interactions. Phytopathology 84:70-77. (Pubitemid 2043975)
73. LeonardK J, CzochorRJ. 1978. Response to selection pressures and plant pathogens stability of equilibria. Phytopathology 68:971-973
74. Leonard K J, Czochor RJ. 1980. Theory of genetic interactions among populations of plants and their pathogens. Annu. Rev. Phytopathol. 18:237-258
75. LeveneH. 1953. Genetic equilibrium when more than one ecological niche is available. Am.Nat. 87:331-33.
76. Lewontin R. 1958. A general method for investigating the equilibrium of gene frequency in a population. Genetics 43:419-434
77. Li J, Ding J, Zhang W, Zhang Y L, Tang P, et al. 2010. Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Mol. Genet. Genomics 283:427-438
78. Little T J, Watt K, Ebert D. 2006. Parasite-host specificity: experimental studies on the basis of parasite adaptation. Evolution 60:31-38. (Pubitemid 44795597)
79. May RM. 1972. Limit cycles in predator-prey communities. Science 177:900-902
80. Meyers B C, Chin D B, Shen K A, Sivaramakrishnan S, Lavelle D O, et al. 1998. The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817-1832
81. Michelmore R W, Meyers BC. 1998. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8:1113-1130 (Pubitemid 29027217)
82. Mode CJ. 1958. Amathematical model for the co-evolution of obligate parasites and their hosts. Evolution 12:158-165
83. Montarry J, Hamelin F M, Glais I, Corbìere 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 Evol. Biol. 10:283.
84. Morgan A D, Gandon S, Buckling A. 2005. The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253-256 (Pubitemid 41294487)
85. Mundt CC. 2002. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40:381-410. (Pubitemid 35235586)
86. Nemri A, Atwell S, Tarone A M, Huang Y S, Zhao K, et al. 2010. Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping. Proc. Natl. Acad. Sci. USA 107:10302-7.
87. Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, et al. 2010. HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130-3141
88. Nuismer SL. 2006. Parasite local adaptation in a geographic mosaic. Evolution 60:24-30. (Pubitemid 44795596)
89. Nuismer S L, Gandon S. 2008. Moving beyond common-garden and transplant designs: insight into the causes of local adaptation in species interactions. Am. Nat. 171:658-668 (Pubitemid 351589848)
90. OldroydGE D, Staskawicz BJ. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl. Acad. Sci. USA 95:10300-5. (Pubitemid 28415336)
91. Parker I M, Gilbert GS. 2004. The evolutionary ecology of novel plant-pathogen interactions. Annu. Rev. Ecol. Evol. Syst. 35:675-700. (Pubitemid 40059735)
92. Person C. 1966. Genetic polymorphism in parasitic systems. Nature 212:266-267
93. Ridout C J, Skamnioti P, Porritt O, Sacristan S, Jones JD G, Brown JKM. 2006. Multiple avirulence paralogues in cereal powdery mildew fungimay contribute to parasite fitness and defeat of plant resistance. Plant Cell 18:2402-2414 (Pubitemid 44484734)
94. Rose L E, Langley C H, Bernal A J, Michelmore RW. 2005. Natural variation in the Pto pathogen resistance gene within species of wild tomato (Lycopersicon). I. Functional analysis of Pto alleles. Genetics 171:345-357 (Pubitemid 41437563)
95. Rose L E, Michelmore R W, Langley CH. 2007. Natural variation in the Pto pathogen resistance gene within species of wild tomato (Lycopersicon). II. Population genetics of Pto. Genetics 175:1307-1319 (Pubitemid 46798232)
96. Roux F, Gao L P, Bergelson J. 2010. Impact of initial pathogen density on resistance and tolerance in a polymorphic disease resistance gene system in Arabidopsis thaliana. Genetics 185:283-291
97. Sacristan S, Garcia-Arenal F. 2008. The evolution of virulence and pathogenicity in plant pathogen populations. Mol. Plant Pathol. 9:369-384 (Pubitemid 351550678)
98. Sacristan S, Vigouroux M, Pedersen C, Skamnioti P, Thordal-Christensen H, et al. 2009. Coevolution between a family of parasite virulence effectors and a class of LINE-1 retrotransposons. PLoS ONE 4:e7463.
99. Salathe M, Scherer A, Bonhoeffer S. 2005. Neutral drift and polymorphism in gene-for-gene systems. Ecol. Lett. 8:925-932 (Pubitemid 41247268)
100. Salvaudon L, Giraud T, Shykoff JA. 2008. Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Curr. Opin. Plant Biol. 11:1-9.
101. Sasaki A. 2000. Host-parasite coevolution in amultilocus gene-for-gene system. Proc. R. Soc. B 267:2183-88.
102. Sasaki A, Hamilton W D, Ubeda F. 2002. Clone mixtures and a pacemaker: new facets of Red-Queen theory and ecology. Proc. R. Soc. Lond. B 269:761-772 (Pubitemid 34478347)
103. Schornack S, vanDamme M, BozkurtT O, Cano L M, Smoker M, et al. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. Proc. Natl. Acad. Sci. USA 107:17421-7426
104. Schwessinger B, Zipfel C. 2008. News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11:389-395
105. Sedcole JR. 1978. Selection pressures and plant pathogens-stability of equilibria. Phytopathology 68:967-70.
106. Seeholzer S, Tsuchimatsu T, Jordan T, Bieri S, Pajonk S, et al. 2010. Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Mol. Plant-Microbe Interact. 23:497-509.
107. Segarra J. 2005. Stable polymorphisms in a two-locus gene-for-gene system. Phytopathology 95:728-736 (Pubitemid 40856524)
108. Seger J. 1988. Dynamics of some simple host-parasitemodels with more than 2 genotypes in each species. Philos. Trans. R. Soc. B 319:541-555
109. Shoresh M, Harman G E, Mastouri F. 2010. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 48:21-43.
110. Soubeyrand S, Laine A L, Hanski I, Penttinen A. 2009. Spatiotemporal structure of host-pathogen interactions in a metapopulation. Am. Nat. 174:308-320
111. Spanu P D, Abbott J C, Amselem J, Burgis T A, Soanes D M, et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal functional tradeoffs in parasitism. Science 330:1543-1546
112. St. Clair DA. 2010. Quantitative disease resistance and quantitative resistance loci in breeding. Annu. Rev. Phytopathol. 48:247-268
113. Stahl E A, Dwyer G, Mauricio R, Kreitman M, Bergelson J. 1999. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667-671
114. Stukenbrock E H, McDonald BA. 2007. Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Mol. Plant Pathol. 8:321-332 (Pubitemid 46640487)
115. Stukenbrock E H, McDonald BA. 2008. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46:75-100.
116. Stukenbrock E H, McDonald BA. 2009. Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Mol. Plant-Microbe Interact. 22:371-380
117. Sun P, Yang XB. 1998. Stability of a gene-for-gene coevolution system under constant perturbations. Phytopathology 88:592-597 (Pubitemid 28456088)
118. Sun P, Yang XB. 1999. Two properties of a gene-for-gene coevolution system under human perturbations. Phytopathology 89:811-816 (Pubitemid 29407540)
119. Tellier A, Brown JKM. 2007. Polymorphism in multilocus host-parasite coevolutionary interactions. Genetics 177:1777-1790 (Pubitemid 350277070)
120. Tellier A, Brown JKM. 2007. Stability of genetic polymorphism in host-parasite interactions. Proc. R. Soc. B 274:809-817 (Pubitemid 47056760)
121. Tellier A, Brown JKM. 2008. The relationship of host-mediated induced resistance to polymorphism in gene-for-gene relationships. Phytopathology 98:128-136
122. Tellier A, Brown JKM. 2009. The influence of perenniality and seed banks on polymorphism in plantparasite interactions. Am. Nat. 174:769-779
123. Thompson JN. 1999. Specific hypotheses on the geographicmosaic of coevolution. Am.Nat. 153:S1-S14.
124. Thompson JN. 2005. The Geographic Mosaic of Coevolution. Chicago, IL: Univ. Chicago Press.
125. Thompson J N, Burdon JJ. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360:121-125
126. Thrall P H, Burdon JJ. 2002. Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathol. 51:169-184 (Pubitemid 34432051)
127. Thrall P H, Burdon JJ. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735-1737 (Pubitemid 36337200)
128. Thrall P H, Burdon J J, Bever JD. 2002. Local adaptation in the Linum marginale-Melampsora lini hostpathogen interaction. Evolution 56:1340-1351 (Pubitemid 34881588)
129. Thrall P H, Burdon J J, Bock CH. 2001. Short-term epidemic dynamics in the Cakile maritima-Alternaria brassicicola host-pathogen association. J. Ecol. 89:723-735 (Pubitemid 32972500)
130. Thrall P H, HochbergM E, Burdon J J, Bever JD. 2007. Coevolution of symbioticmutualists and parasites in a community context. Trends Ecol. Evol. 22:120-126 (Pubitemid 46273827)
131. Tian D, Traw M B, Chen J Q, Kreitman M, Bergelson J. 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74-77. (Pubitemid 36569584)
132. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 2009. Network properties of robust immunity in plants. PLoS Genet. 5:e1000772.
133. van der Biezen E A, Jones JDG. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454-456 (Pubitemid 29002901)
134. van der Hoorn RA L, DeWit P, JoostenM. 2002. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7:67-71. (Pubitemid 36726075)
135. van der Merwe M M, Kinnear M W, Barrett L G, Dodds P N, Ericson L, et al. 2009. Positive selection in AvrP4 avirulence gene homologues across the genus Melampsora. Proc. Roy. Soc. B 276:2913-2922
136. van der Meijden E, Wijn M, Verkaar HJ. 1988. Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355-363 (Pubitemid 19318515)
137. Vanderplank JE. 1968. Disease Resistance in Plants. New York: Academic 206 pp.
138. Vera Cruz C M, Bai J F, Ona I, Leung H, Nelson R J, 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. Proc. Natl. Acad. Sci. USA 97:13500-5.
139. Vlot A C, Dempsey DM A, Klessig DF. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177-206.
140. Wei F S, Wong R A, Wise RP. 2002. Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14:1903-1917 (Pubitemid 35008255)
141. Wichmann G, Bergelson J. 2004. Effector genes of Xanthamonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genetics 166:693-706. (Pubitemid 38391735)
142. Wilfert L, Jiggins FM. 2010. Host-parasite coevolution: genetic variation in a virus population and the interaction with a host gene. J. Evol. Biol. 23:1447-1455
143. WoolhouseME J, Webster J P, Domingo E, Charlesworth B, Levin BR. 2002. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32:569-577 (Pubitemid 35435167)
144. Yahiaoui N, Brunner S, Keller B. 2006. Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J. 47:85-98. (Pubitemid 43883016)
145. Yahiaoui N, Kaur N, Keller B. 2009. Independent evolution of functional Pm3 resistance genes in wild tetraploid wheat and domesticated bread wheat. Plant J. 57:846-856
146. Ye T Z, Yang R C, Yeh FC. 2003. Coevolution in natural pathosystems: effects of dominance on hostpathogen interactions. Phytopathology 93:633-639 (Pubitemid 36516869)
147. Zipfel C. 2008. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20:10-16