The Red Queen Hypothesis and plant/pathogen interactions

Annual Review of Phytopathology

Volumn 34, Issue , 1996, Pages 29-50

  Clay, Keith ^a   Kover, Paula X ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

coevolution; frequency dependent selection; Red Queen hypothesis; resistance; virulence

Indexed keywords

PARASITE; PATHOGEN; PLANT-PATHOGEN INTERACTION; RED QUEEN HYPOTHESIS;

EID: 0029661738     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.phyto.34.1.29     Document Type: Review

References (135)

1. Adams MW, Ellingboe AH, Rossman EC. 1971. Biological uniformity and disease epidemics. Bioscience 21:1067-70
2. Agrios GN. 1988. Plant Pathology. San Diego: Academic
3. Alexander HM. 1992. Evolution of disease resistance in natural plant populations. See Ref. 46a, pp. 326-44
4. Alexander HM, Antonovics J, Kelly AW. 1993. Genotypic variation in plant disease resistance - physiological resistance in relation to field disease transmission. J. Ecol. 81:325-33
5. Alexander HM, Burdon JJ. 1984. The effect of disease induced by Albugo candida (white rust) and Peronospora parasitica (downy mildew) on the survival and reproduction of Capsella bursapastoris (shepherd's purse). Oecologia 64:314-18
6. Augspurger CK. 1983. Seed dispersal of the tropical tree, Platypodium elegans, and the escape of its seedlings from fungal pathogens. J. Ecol. 71:759-71
7. Barrett JA. 1981. The evolutionary consequences of monoculture. In Genetic Consequences of Man-Made Change, ed. JA Bishop, LM Cook, pp. 209-48. London: Academic
8. Barrett J. 1985. The gene-for-gene hypothesis: parable or paradigm. In Ecology and Genetics of Host-Parasite Interactions, ed. D Rollinson, RM Anderson, pp. 215-25. London: Academic
9. Barrett JA. 1988. Frequency-dependent selection in plant-fungal interactions. Phil. Trans. R. Soc. London Ser. B 319:473-83
10. Bell G. 1982. The Masterpiece of Nature. Berkeley: Univ. Calif. Press
11. Bell G, Maynard Smith J. 1987. Short-term selection for recombination among mutually antagonistic species. Nature 328:66-68
12. Bergelson J. 1994. The effects of genotype and the environment on costs of resistance in lettuce. Am. Nat. 143:349-59
13. Bloomberg WJ. 1973. Fusarium root rot of Douglas-fir seedlings. Phytopathology 63.337-41
14. Boyd LA, Smith PH, Brown JKM. 1994. Molecular and cellular expression of quantitative resistance in barley to powdery mildew. Physiol. Mol Plant. Pathol. 45:47-58
15. Bronnimann A. 1968. Zur Kenntnis von Septoria nodorum Berk., dem Erreger der Spelzenbraune und einer Blattdurre des Weizens. Phytopathol. Z. 61:101-46
16. Brooks DH. 1972. Observations on the effects of mildew, Erysiphe graminis, on growth of spring and winter barley. Ann. Appl. Biol. 70:149-56
17. Browning JA, Frey KJ. 1969. Multiline cultivars as a means of disease control. Annu. Rev. Phytopathol. 7:355-82
18. Burdon JJ. 1982. The effect of fungal pathogens on plant communities. In The Plant Community as a Working Mechanism, ed. EI Newman, pp. 99-112. London: Blackwell
19. Burdon JJ. 1987. Diseases and Plant Population Biology. Cambridge: Cambridge Univ. Press
20. Burdon JJ, Chilvers GA. 1976. The effect of clumped planting patterns on epidemics of damping-off disease in cress seedlings. Oecologia 23:17-29
21. Burdon JJ, Chilvers GA. 1977. The effect of barley mildew on barley and wheat competition in mixtures. Aust. J. Biol. Sci. 25:59-65
22. Burdon JJ, Jarosz AM. 1991. Hostpathogen interactions in natural populations of Linum marginale and Melampsora lini: patterns of resistance and racial variation in a large host population. Evolution 45:205-17
23. Burdon JJ, Marshall DR. 1981. Biological control and the reproductive mode of weeds. J. Appl. Ecol. 18:649-58
24. Burdon JJ, Marshall DR. 1981. Inter- and ultra-specific diversity in the disease-response of Glycine species to the leaf-rust fungus Phakopsora pachyrhizi. J. Ecol. 69:381-90
25. Burdon JJ, Shattock RC. 1980. Disease in plant communities. Ann. Appl. Biol. 5:145-219
26. Burdon JJ, Thompson JN. 1995. Changed patteras of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. J. Ecol. 83:199-206
27. Burt A, Bell G. 1991. Seed reproduction is associated with a transient escape from parasite damage in American beech. Oikos 61:145-48
28. Camargo LEA, Williams PH, Osborn TC. 1995. Mapping of quantitative trait loci controlling resistance of Brassica oleracea to Xanthomonas campestris pv. campestris in the field and greenhouse. Phytopathology 85:1296-300
29. Catherall PL. 1966. Effects of barley yellow dwarf virus on the growth and yield of single plants and simulated swards of perennial ryegrass. Ann. Appl. Biol. 57:155-62
30. Chaboudez P, Burdon JJ. 1995. Frequency-dependent selection in a wild plant-pathogen system. Oecologia 102:490-93
31. Christ BJ, Person CO, Pope DD. 1987. The genetic determination of variation in pathogenicity. See Ref. 126a, pp. 7-19
32. Clarke B. 1976. The evolution of genetic diversity. Proc. Roy. Soc. London Ser. B 205:453-74
33. Clay K. 1989. The impact of parasitic and mutualistic fungi on competitive interactions among plants. In Perspectives on Plant Competition, ed. J Grace, D Tilman, pp. 391-412. London: Academic
34. Clay K. 1990. Comparative demography of three graminoids infected by systemic, clavicipitaceous fungi. Ecology 71:558-70
35. Clay K. 1994. Hereditary symbiosis in the grass genus Danthonia. New Phytol. 126:223-31
36. Clay K, Kover P. 1996. Evolution and stasis in plant/pathogen associations. Ecology 77:997-1003
37. Crute IR, Holub EB, Tor M, Brose E, Beynon JL. 1993. The identification and mapping of loci in Arabidopsis thaliana for recognition of the fungal pathogens: Peronospora parasitica (downy mildew) and Albugo Candida (white blister). In Advances in Molecular Genetics of Plant-Microbe Interactions, ed. EW Nester, DPS Verma, pp. 437-44. The Netherlands: Kluwer
38. Culver JN, Dawson WD. 1991. Tobacco mosaic virus elicitor coat protein genes produce a hypersensitive phenotype in transgenic Nicotiana sylvestris plants. Mol. Plant-Microb. Interact 4:458-63
39. Day PR. 1974. Genetics of Host-Parasite Interaction. San Francisco, CA: Freeman
40. de Nooij MP, van der Aa HA. 1987. Phomopsis subordinaria and related stalk disease in natural populations of Plantago lanceolata L. Can. J. Bot. 65:2318-25
41. Doling DA. 1964. The influence of seedling competition on the amount of loose smut (Ustilago nuda (Jens.) Rostr.) appearing in barley crops. Ann. Appl. Biol. 54:91-98
42. Dybdahl MF, Lively CM. 1995. Hostparasite interactions: infection of common clones in natural populations of a freshwater snail (Potamopyrgus antipodarum). Proc. R. Soc. London Ser. B 260:99-103
43. Ellingboe AH. 1982. Host resistance and host-parasite interactions: a perspective. In Phytopathogenic Prokaryotes, ed. MS Mount, GH Lacey, pp. 103-17. New York: Academic
44. Eskes A. 1982. Expression of incomplete resistance to pathogens. In Durable Resistance in Crops, ed. F Lambert, JM Waller, NA van der Graaf, pp. 169-98. New York: Plenum
45. Fischer GW, Holton CS. 1957. Biology and Control of the Smut Fungi. New York: Ronald Press
46. Flor HH. 1956. The complementary genic systems in flax and flax rust. Adv. Genet. 8:29-54
47. Frank SA. 1991. Spatial variation in coevolutionary dynamics. Evol. Ecol. 5:193-217
48. Frank SA. 1993. Coevolutionary genetics of plants and pathogens. Evol. Ecol. 7:45-75
49. Frank SA. 1994. Recognition and polymorphism in host-parasite genetics. Phil. Trans. R. Soc. London Ser. B 346:283-93
50. Fritz RS, Simms EL, eds. 1992. Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. Chicago: Univ. Chicago Press
51. Giese H. 1981. Powdery mildew resistance genes in the Ml-a and Ml-k regions on barley chromosome 5. Hereditas 95:51-62
52. Glesner RR, Tilman D. 1978. Sexuality and the components of environmental uncertainty: clues from geographical parthenogenesis in terrestrial animals. Am. Nat. 112:659-73
53. Govinthasamy T, Cavers PB. 1995. The effects of smut (Ustilago destruens) on seed production, dormancy, and viability in fall panicum (Panicum dichotomiflorum). Can. J. Bot. 73:1628-34
54. Gray AJ, Drury M, Raybould AF. 1990. Spartina and the ergot fungus Claviceps purpurea - a singular contest? In Pests, Pathogens and Plant Communities, ed. JJ Burdon, SR Leather, pp. 63-79. Oxford: Blackwell Sci.
55. Groth JV, Roelfs AP. 1982. Effects of sexual and asexual reproduction on race abundance in cereal rust fungus populations. Phytopathology 72:1503-7
56. Haldane JBS. 1949. Disease and evolution. La Ric. Sci. Suppl. 19:68-76
57. Hamilton WD. 1980. Sex versus non-sex parasite. Oikos 35:282-90
58. Hamilton WD, Axelrod R, Tanese R. 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl. Acad. Sci. USA 87:3566-73
59. Harry IB, Clarke DD. 1987. The genetics of race-specific resistance in groundsel Senecio vulgaris L. to the powdery mildew fungus Erysiphe fischeri Blumer. New Phytol. 107:715-23
60. Hart H. 1929. Relation of stomatal behaviour to stem rust resistance in wheat. J. Agric. Res. 39:929-48
61. Heath MC. 1992. Evolution of resistance to fungal parasitism in natural ecosystems New Phytol. 119:331-43
62. Hermann RK, Chilcote WW. 1965. Effect of seed beds on germination and survival of Douglas-fir. Oregon For. Res. Lab. 4:1-28
63. Innes RW. 1995. Plant-parasite interactions: Has the gene-for-gene model become outdated? Trends Microb. 3:483-85
64. Jaenike J. 1978. An hypothesis to account for the maintenance of sex within populations. Evol. Theory 3:191-94
65. Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104:501-28
66. Jarosz AM, Burdon JJ. 1990. Predominance of a single major gene for resistance to Pkakopsora pachyrhizi in a population of Glycine argyrea. Heredity 64:347-53
67. Jarosz AM, Burdon JJ. 1991. Hostpathogen interactions in natural populations of Linum marginale and Melampspora lini: II. Local and regional variation in patterns of resistance and racial structure. Evolution 45:1618-27
68. Jayakar SD. 1970. A mathematical model for interaction of gene frequencies in a parasite and its host. Theor. Pop. Biol. 1:140-64
69. Johnson R. 1987. Selected examples of relationships between pathogenicity in cereal rusts and resistance in their hosts. See Ref. 126a, pp. 181-92
70. Kearny B, Staskawicz BJ. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346:385-87
71. Keen NT. 1990. Gene-for gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447-63
72. Kelley. 1994. Viral pathogens and the advantage of sex in the perennial grass Anthoxanthum odoratum. Phil. Trans. R. Soc. London Ser. B 346:295-302
73. Kelley SE, Clay K. 1987. Interspecific competitive interactions and the maintenance of genotypic variation within the populations of two perennial grasses. Evolution 41:92-103
74. Kolmer JA. 1995. Selection of Puccinia recondita f.sp. tritici virulence phenotypes in three multilines of Thatcher wheat lines near isogenic for leaf rust resistance genes. Can. J. Bot. 73:1081-88
75. Kuc J. 1983. Induced systemic resistance in plants to diseases caused by fungi and bacteria. In The Dynamics of Host Defense, ed. JA Bailey, JB Deverall, pp. 191-221. New York: Academic
76. Laviolette FA, Athow KL. 1971. Relationship of age of soybean seedlings and inoculum to infection by Pythium ultimatum. Phytopathology 61:439-40
77. Lawrence GJ, Mayo GME, Shepard KW. 1981. Interaction between genes controlling pathogenicity in the flax rust fungus. Phytopathology 71:12-19
78. Leach LD. 1947. Growth rates of host and pathogen as factors determining the seventy of preemergence damping-off. J. Agric. Res. 75:161-79
79. Lee JC, Yang X, Schwartz M, Strobel G, Clardy J. 1995. The relationship between an endangered North American tree and an endophytic fungus. Chem. Biol. 2:721-27
80. Leonard KJ. 1977. Selection pressures and plant pathogens. Ann. NY Acad. Sci. 287:207-22
81. Leonard KJ. 1987. The host population as a selective factor (including stabilizing selection). See Ref. 126a, pp. 163-78
82. Leonard KJ, Czochor RJ. 1980. Theory of genetic interactions among populations of plants and their pathogens. Annu. Rev. Phytopathol. 18:237-58
83. Levin DA. 1975. Pest pressure and recombination systems in plants. Am. Nat. 109:437-51
84. Lively CM. 1987. Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328:519-21
85. Lively CM, Apanius V. 1995. Genetic diversity in host-parasite interactions. In Ecology of Infectious Diseases in Natural Populations, ed. BT Grenfall, AP Dobson, pp. 421-49. Cambridge: Cambridge Univ. Press
86. Lively CM, Craddock C, Vrijenhoek RC. 1990. Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344:864-66
87. Lively CM, Howard RS. 1994. Selection by parasites for clonal diversity and mixed mating. Phil. Trans. R. Soc. London Ser. B 346:271-81
88. Lively CM, Johnson SG, Delph LF, Clay K. 1995. Rust infection affects growth of Impatiens capensis only under high density. Ecology 76:1859-62
89. Lively CM, Lloyd DG. 1990. The cost of biparental sex under individual selection. Am. Nat. 135:489-500
90. Luig NH. 1983. A survey of virulence genes in wheat stem rust, Puccinia graminis f.sp. trizici. Adv. Plant Breed. 11:1-98
91. Maroof MAS, Webster RK, Allard RW. 1983. Evolution of resistance to scald. powdery mildew, and net blotch in barley composite cross II populations. Theor. Appl. Genet. 66:279-83
92. Marshall DR, Pryor AJ. 1979. Multiline varieties and disease control. II. The "dirty crop" approach with components carrying two or more genes for resistance. Euphytica 28:145-59
93. Maynard Smith J. 1978. The Evolution of Sex. Cambridge: Cambridge Univ. Press
94. McDonald BA, Allard RW, Webster RK. 1988. Responses of two-, three-, and four-component barley mixtures to a variable pathogen population. Crop Sci. 28:447-52
95. McDonald BA, McDermott JM. 1993. Population genetics of plant pathogenic fungi. Bioscience 43:311-19
96. McDonald BA, McDermott JM, Allard RW, Webster RK. 1989. Coevolution of host and pathogen populations in the Hordeum vulgare-Rhynchosporium secalis pathosystem. Proc. Natl. Acad. Sci. USA 86:3924-27
97. Mode CJ. 1958. A mathematical model for the co-evolution of obligate parasites and their hosts. Evolution 12:158-65
98. Moritz C, McCallum H, Donnellan S, Roberts JD. 1991. Parasite loads in parthenogenic and sexual lizards (Heteronotia binoei): support for the Red Queen hypothesis. Proc. R. Soc. London Ser. B 244:145-49
99. Mundt CC, Leonard KJ. 1985. Effect of host genotype unit area on epidemic development of crown rust following focal and general inoculations of mixtures of immune and susceptible oat plants. Phytopathology 75:1141-45
100. Muona O, Allard RW, Webster RK. 1982. Evolution of resistance to Rhynchosporium secalis (Oud.) Davis in barley composite cross II. Theor. Appl. Genet. 61:209-14
101. Neergaard P. 1977. Seed Pathology. New York: Wiley
102. de Nooij MP, van Damme JMM. 1988. Variation in host susceptibility among and within populations of Plantago lanceolata L. infected by the fungus Phomopsis subordinaria (Desm.) Trav. Oecologia 75:535-38
103. Oates JD, Burdon JJ, Brouwer JB. 1983. Interactions between Avena and Puccinia species. II. The pathogens: Puccinia coronata Cda and P. graminis f. sp. avenae Eriks. and Henn. J. Appl. Ecol. 20:585-96
104. Parker MA. 1985. Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution 39:713-23
105. Parker MA. 1986. Individual variation in pathogen attack and reproductive success in the annual legume Amphicarpaea bracteata. Oecologia 69:253-59
106. Parker MA. 1987. Pathogen impact on sexual vs. asexual reproductive success in Arisaema triphyllum. Am. J. Bot. 74:1758-63
107. Parker MA. 1988. Genetic uniformity and disease resistance in a clonal plant. Am. Nat. 132:538-49
108. Parker MA. 1988. Polymorphism for disease resistance in the annual legume Amphicarpaea bracteata. Heredity 60:27-31
109. Parker MA. 1994. Pathogens and sex in plants. Evol. Ecol. 8:560-84
110. Paul ND, Ayres PG. 1986. The effects of infection by rust (Puccinia lagenophorae Cooke) on the growth of groundsel (Senecio vulgaris L.) cultivated under a range of nutrient concentrations. Ann. Bot. 58:321-31
111. Paul ND, Ayres PG. 1987. Survival, growth, and reproduction of groundsel (Senecio vulgaris L.) infected by rust (Puccinia lagenopkorae) in the field during summer. J. Ecol. 75:61-71
112. Rice WR. 1983. Sexual reproduction: an adaptation reducing parent-offspring contagion. Evolution 37:1317-20
113. Richter TE, Pryor TJ, Bennetzen JL, Hulbert SH. 1995. New rust resistance specificities associated with recombination in the Rd1 complex in maize. Genetics 141:373-81
114. Roy BA. 1993. Patterns of rust infection as a function of host genetic diversity and host density in natural populations of the apomictic crucifer Arabis holboellii. Evolution 47:111-24
115. Savile DBO. 1987. Use of rust fungi (Uredinales) in determining ages and relationships in Poaceae. In Grass Systematics and Evolution, ed. TR Soderstrom, KW Hilu, C Campbell, ME Barkworth, pp. 168-78. Washington, DC: Smithsonian Inst. Press
116. Schmid B. 1994. Effects of genetic diversity in experimental stands of Solidago altissima - evidence for the potential role of pathogens as selective agents in plant populations. J. Ecol. 82:165-76
117. Scott SW, Griffiths E. 1980. Effect of controlled epidemics of powdery mildew on grain yield of spring barley Ann. Appl. Biol. 94:19-31
118. Seger J, Hamilton WD. 1988. Parasites and sex. In The Evolution of Sex, ed. RE Michod, BR Levin, pp. 176-93. Sunderland: Sinauer
119. Simms EL. 1992. Costs of plant resistance to herbivory. See Ref. 46a, pp. 392-425
120. Simms EL. 1993. Genetic variation for pathogen resistance in tall morningglory. Plant Dis. 77:901-44
121. Simms EL, Vision TJ. 1995. Pathogen-induced systemic resistance in Ipomoea purpurea. Oecologia 102:494-500
122. Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG. 1995. Molecular genetics of plant disease resistance. Science 268:661-67
123. Stevens NE. 1948. Disease damage in clonal and self-pollinated crops. J. Am. Soc. Agron. 40:841-44
124. Stockwell D, Hanchey P. 1983. The role of the cuticle in resistance of beans to Rhizoctonia solani. Phytopathology 73:1640-42
125. Strauss SY, Karban R. 1994. The significance of outcrossing in an intimate plant-herbivore relationship. I. Does outcrossing provide an escape from herbivores adapted to the parent plant? Evolution 48:454-64
126. Thompson JN, Burdon JJ. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360:121-25
127. Thrall PH, Biere A, Antonovics J. 1993. Plant-life history and disease susceptibility - the occurrence of Ustilago violacea on different species within the Caryophyllaceae. J. Ecol. 81:489-98
128. Thrall PH, Jarosz AM. 1994. Hostpathogen dynamics in experimental populations of Silene alba and Ustilago violacea. II. Experimental tests of theoretical models. J. Ecol. 82:561-70
129. Ullstrup AJ. 1972. The impacts of the southern corn leaf blight epidemics of 1970-1971. Annu. Rev. Phytopathol. 10:37-50
130. Vanderplank JE. 1984. Disease Resistance in Plants. London: Academic
131. Watson IA. 1970. Changes in virulence and population shifts in plant pathogens. Annu. Rev. Phytopathol. 8:209-30
132. Williams GC. 1975. Sex and Evolution. Princeton: Princeton Univ. Press
133. Wolfe MS, Barrett JA. 1985. The current status and prospects in multiline cultivars and variety mixtures for disease resistance. Annu. Rev. Phytopathol. 23:251-73
134. Wolfe MS, Caten CE, eds. 1987. Populations of Plant Pathogens: Their Dynamics and Genetics. Oxford: Blackwell Sci.
135. Yahara T, Oyama K. 1993. Effects of virus infection on demographic traits of an agamospermous population of Eupatorium chinense (Asteraceae). Oecologia 96:310-15