What have we learned from studies of wild plant-pathogen associations?-the dynamic interplay of time, space and life-history

European Journal of Plant Pathology

Volumn 138, Issue 3, 2014, Pages 417-429

  Burdon, J J ^a   Thrall, P H ^a  

^a CSIRO   (Australia)

Author keywords

Asynchrony; Epidemiology; Evolution; Fungal pathogen; Host pathogen interactions; Metapopulation; Time series

Indexed keywords

COEVOLUTION; COMPLEXITY; EPIDEMIOLOGY; FUNGAL DISEASE; FUNGUS; HOST-PATHOGEN INTERACTION; LIFE HISTORY TRAIT; METAPOPULATION; RECOLONIZATION; TIME SERIES; WILD POPULATION;

EID: 84894273935     PISSN: 09291873     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10658-013-0265-9     Document Type: Article

References (102)

1. Alexander, H. M., Thrall, P. H., Antonovics, J., Jarosz, A. M., & Oudemans, P. V. (1996). Population dynamics and genetics of plant disease: a case study of anther-smut disease. Ecology, 77, 990-996.
2. Alexander, H. M., Mauck, K. E., Whitfield, A. E., Garrett, K. A., Malmstrom, C. M. (2013). Plant-virus interactions and the agro-ecological interface. European Journal of Plant Pathology, in press.
3. Allan, E., van Ruijen, J., Crawley, M. J. (2010). Foliar fungal pathogens and grassland biodiversity. Ecology, 2572-2582.
4. Anderson, R. M., & May, R. M. (1991). Infectious diseases of humans: Dynamics and control. New York: Oxford University Press.
5. Antonovics, J. (2004). Long-term study of a plant-pathogen metapopulation. In I. Hanski & O. E. Gaggiotti (Eds.), Metapopulation ecology, genetics, and evolution (pp. 471-488). San Diego: Elsevier Academic Press.
6. 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 Phytologist, 183, 513-529.
7. Barrett, L. G., Thrall, P. H., Burdon, J. J., & Linde, C. C. (2008). Life-history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology and Evolution, 23, 678-685.
8. Barton, J., Fowler, S. V., Gianotti, A. F., Winks, C. J., de Beurs, M., Arnold, G. C., et al. (2007). Successful biological control of mist flower (Ageratina riparia) in New Zealand: agent establishment, impact and benefits to the native flora. Biological Control, 40, 370-385.
9. Bishop, C. L., Wardell-Johnson, G. W., & Williams, M. R. (2010). Community-level changes in Banksia woodland following plant pathogen invasion in the Southwest Australian floristic region. Journal of Vegetation Science, 21, 888-898.
10. Borer, E. T., Hosseini, P. R., Seabloom, E. W., & Dobson, A. P. (2007). Pathogen-induced reversal of native dominance in a grassland community. PNAS, 104, 5473-5478.
11. Bradley, D. J., Gilbert, G. S., & Martiny, J. B. H. (2008). Pathogens promote plant diversity through a compensatory response. Ecology Letters, 111, 461-469.
12. Brooks, C. P., Antonovics, J., & Keitt, T. H. (2008). Spatial and temporal heterogeneity explain disease dynamics in a spatially explicit network. American Naturalist, 172, 149-159.
13. Burdon, J. J. (1993). The role of parasites in plant populations and communities. In E.-D. Schulze & H. A. Mooney (Eds.), Biodiversity and ecosystem function (pp. 165-179). Berlin: Springer.
14. Burdon, J. J., Ericson, L., & Müller, W. J. (1995). Temporal and spatial relationships in a metapopulation of the rust pathogen Triphragmium ulmariae and its host, Filipendula ulmaria. Journal of Ecology, 82, 979-989.
15. Burdon, J. J., Oates, J. D., & Marshall, D. R. (1983). Interactions between Avena and Puccinia species. I. The wild hosts: Avena barbata Pott ex Link, A. fatua L. and A. ludoviciana Durieu. Journal of Applied Ecology, 20, 571-585.
16. Burdon, J. J., & Thrall, P. H. (2008). Pathogen evolution across the agro-ecological interface: implications for management. Evolutionary Applications, 1, 57-65.
17. Burdon, J. J., Thrall, P. H., & Brown, A. H. D. (1999). Resistance and virulence structure in two Linum marginale-Melampsora lini host-pathogen metapopulations with different mating systems. Evolution, 53, 704-716.
18. Burdon, J. J., Thrall, P. H., Ericson, L. (2013). Genes, communities & invasive species: understanding the ecological and evolutionary dynamics of host-pathogen interactions. Current Opinion in Plant Biology, in press.
19. Burdon, J. J., Thrall, P. H., Nemri, A. (2012). Approaches to understanding the impact of life-history features on plant-pathogen co-evolutionary dynamics. In R. A. Sniezko, A. D. Yanchuk, J. T. Kliejunas, K. M. Palmieri, J. M. Alexander, S. J. (Tech. coords.), Interactions in forestry: Disease and insect resistance in forest trees (pp. 104-111). Proc. 4th International Workshop on the Genetics of Host-Parasite. Gen. Tech. Rep. PSW-GTR-240. Albany, CA: Pacific Southwest Research Station, Forest Service, U. S. Department of Agriculture.
20. Burdon, J. J., Wennström, A., Elmqvist, T., & Kirby, G. C. (1996). The role of race specific resistance in natural plant populations. Oikos, 76, 411-416.
21. Cai, G., Gale, L. R., Schneider, R. W., Kistler, H. C., Davis, R. M., Elias, K. S., et al. (2003). Origin of race 3 of Fusarium oxysporum f. sp. lycopersici at a single site in California. Phytopathology, 93, 1014-1022.
22. Carlsson-Graner, U. (1997). Anther-smut disease in Silene dioica: variation in susceptibility among genotypes and populations and patterns of disease within populations. Evolution, 51, 1416-1426.
23. Carlsson-Graner, U. (2006). Disease dynamics, host specificity and pathogen persistence in isolated host populations. Oikos, 112, 174-184.
24. Carlsson-Graner, U., & Thrall, P. H. (2002). The spatial distribution of plant populations, disease dynamics and evolution of resistance. Oikos, 97, 97-110.
25. Carlsson, U., & Elmqvist, T. (1992). Epidemiology of anther-smut disease (Microbotryum violaceum) and numeric regulation of populations of Silene dioica. Oecologia, 90, 509-517.
26. Carlsson, U., Elmqvist, T., Wennstrom, A., & Ericson, L. (1990). Infection by pathogens and population age of host plants. Journal of Ecology, 78, 1094-1105.
27. Chappell, T. M., & Rausher, M. D. (2011). Genetics of resistance to the rust fungus Coleosporium ipomoeae in three species of Morning Glory (Ipomoea). PLoS ONE, 6, e28875. doi: 10. 1371/journal. pone. 0028875.
28. Cullen, J. M. (2012). Skeleton weed. In M. H. Julien, R. E. C. McFayden, & J. M. Cullen (Eds.), Biological control of weeds in Australia (pp. 150-161). Melbourne: CSIRO Publishing.
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. Journal of Theoretical Biology, 201, 1-12.
30. Dobson, A. P., & Crawley, M. (1994). Pathogens and the structure of plant communities. TREE, 9, 393-398.
31. Ericson, L., Burdon, J. J., & Müller, W. J. (1999). Spatial and temporal dynamics of epidemics of the rust fungus Uromyces valerianae on populations of its host, Valeriana salina. Journal of Ecology, 87, 649-658.
32. Flor, H. H. (1956). The complementary genic systems in flax and flax rust. Advances in Genetics, 8, 29-54.
33. Fontaine, M. C., Gladieux, P., Hood, M. E., & Giraud, T. (2013). History of the invasion of the anther smut pathogen on Silene latifolia in North America. New Phytologist, 198, 946-956.
34. Friesen, T. L., Stukenbrock, E. H., Liu, Z., Meinhardt, S., Ling, H., Faris, J. D., et al. (2006). Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics, 38, 953-956.
35. Garcia-Guzman, G., Burdon, J. J., Ash, J. E., & Cunningham, R. B. (1996). Regional and local patterns in the spatial distribution of the flower-infecting smut fungus Sporisorium amphilophis in natural populations of its host Bothrichloa macra. New Phytologist, 132, 459-469.
36. Garcia-Guzman, G., & Morales, E. (2007). Life-history strategies of plant pathogens: distribution patterns and phylogenetic analysis. Ecology, 88, 589-596.
37. Gilbert, G. S., & Webb, C. O. (2007). Phylogenetic signal in plant pathogen-host range. Proceedings of the National Academy of Sciences of the United States of America, 104, 4979-4983.
38. Goss, E. M., Carbone, I., & Grünwald, N. J. (2009). Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Molecular Ecology, 18, 1161-1174.
39. Haldane, J. B. S. (1949). Disease and evolution. Ricerca Scientifica, 19, 68-76.
40. Hamilton, M. G., Williams, D. R., Tilyard, P. A., Pinkard, E. A., Wardlaw, T. J., Glen, M., et al. (2012). A latitudinal cline in disease resistance of a host tree. Heredity, 110, 372-379.
41. Hansen, E. M., & Goheen, E. M. (2000). Phellinus weirii and other native root pathogens as determinants of forest structure and process in western North America. Annual Review of Phytopathology, 38, 515-539.
42. Hanski, I. (1991). Metapopulation dynamics-brief-history and conceptual domain. Biological Journal of the Linnean Society, 42, 3-16.
43. Hanski, I. (1999). Metapopulation ecology. Oxford: Oxford University Press.
44. Holah, J. C., Wilson, M. V., & Hansen, E. M. (1997). Impacts of a native root-rotting pathogen on successional development of old-growth Douglas fir forests. Oecologia, 111, 429-433.
45. Jansky, S. H., Simon, R., & Spooner, D. M. (2008). A test of taxonomic predictivity: resistance to early blight in wild relatives of cultivated potato. Phytopathology, 98, 680-687.
46. Kaltz, O., & Shykoff, J. A. (1998). Local adaptation in host-parasite systems. Heredity, 81, 361-370.
47. Katan, T., Katan, J., Gordon, T. R., & Pozniak, D. (1994). Physiologic races and vegetative compatibility groups of Fusarium oxysporum f. sp. melonis in Israel. Phytopathology, 84, 153-157.
48. Knops, J. M. H., Tilman, D., Haddad, N. M., Naeem, S., Mitchell, C. E., Haarstad, J., et al. (1999). Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecology Letters, 2, 286-293.
49. Koslow, J. M., & Clay, K. (2007). The mixed mating system of Impatiens capensis and infection by a foliar rust pathogen: patterns of resistance and fitness consequences. Evolution, 61, 2643-2654.
50. Lafferty, K. D., & Kuris, A. M. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology & Evolution, 17, 507-513.
51. Laine, A.-L. (2007). Detecting local adaptation in a natural plant-pathogen metapopulation: a laboratory vs. field transplant approach. Journal of Evolutionary Biology, 11, 327-337.
52. Laine, A.-L., & Hanski, I. (2006). Large-scale spatial dynamics of a specialist plant pathogen in a fragmented landscape. Journal of Ecology, 94, 217-226.
53. Laine, A.-L., Burdon, J. J., Dodds, P. N., & Thrall, P. H. (2011). Spatial variation in disease resistance: from molecules to metapopulations. Journal of Ecology, 99, 96-112.
54. Lebeda, A., Petrzelova, I., & Maryska, Z. (2008). Structure and variation in the wild-plant pathosystem: Lactuca serriola-Bremia lactucae. European Journal of Plant Pathology, 122, 127-146.
55. Levins, R. (1970). Extinction. Lecture Notes in Mathematics, 2, 75-107.
56. Lockhart, A. B., Thrall, P. H., & Antonovics, J. (1996). Sexually transmitted diseases in animals: ecological and evolutionary implications. Biological Reviews of the Cambridge Philosophical Society, 71, 415-471.
57. Lyimo, H. J. F., Pratt, R. C., & Mnyuku, R. S. (2012). An effective integrated crop management strategy for enhanced maize production in tropical agroecosystems prone to gray leaf spot. Crop Protection, 41, 57-63.
58. McDonald, B. A., & Linde, C. (2002a). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349-379.
59. McDonald, B. A., & Linde, C. (2002b). The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica, 124, 163-180.
60. Meyer, J.-Y., Taputuarai, R., Killgore, E. (2008). Dissemination and impacts of the fungal pathogen, Colletotrichum gloeosporioides f. sp. miconiae, on the invasive alien tree, Miconia calvescens, in Tahiti (South Pacific) (pp. 594-600). XII Intern. Symp. Biological Control of Weeds: CAB International.
61. Meyer, S. E., Nelson, D. L., & Clement, S. (2001). Evidence for resistance polymorphism in the Bromus tectorum-Ustilago bullata pathosystem: implications for biocontrol. Canadian Journal of Plant Pathology, 23, 19-27.
62. Mitchell, C. E., Tilman, D., & Groth, J. V. (2002). Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology, 83, 1713-1726.
63. Mundt, C. C. (2002). Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology, 40, 381-410.
64. Mundt, C. C., Sackett, K. E., & Wallace, L. D. (2011). Landscape heterogeneity and disease spread: experimental approaches with a plant pathogen. Ecological Applications, 21, 321-328.
65. Oates, J. D., Burdon, J. J., & Brouwer, J. B. (1983). Interactions between Avena and Puccinia species. II. The pathogens: Puccinia coronata Cda and P. graminis Pers. f. sp. avenae Eriks. and Henn. Journal of Applied Ecology, 20, 585-596.
66. Oliver, R. P., & Ipcho, S. V. S. (2004). Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Molecular Plant Pathology, 5, 347-352.
67. Packer, A., & Clay, K. (2000). Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature, 404, 278-281.
68. Papaix, J., Goyeau, H., Du Cheyron, P., Monod, H., & Lannou, C. (2011). Influence of cultivated landscape composition on variety resistance: an assessment based on wheat leaf rust epidemics. New Phytologist, 191, 1095-1107.
69. Parker, M. A. (1991). Nonadaptive evolution of disease resistance in an annual legume. Evolution, 45, 1209-1217.
70. Petrzelova, I., & Lebeda, A. (2004). Occurrence of Bremia lactucae in natural populations of Lactuca serriola. Journal of Phytopathology, 152, 391-398.
71. Petrzelova, I., & Lebeda, A. (2011). Distribution of race-specific resistance against Bremia lactucae in natural populations of Lactuca serriola. European Journal of Plant Pathology, 129, 233-253.
72. Philibert, A., Desprez-Loustau, M.-L., Fabre, B., Frey, P., Halkett, F., Husson, C., et al. (2011). Predicting invasion success of forest pathogenic fungi from species traits. Journal of Applied Ecology, 48, 1381-1390.
73. Plantegenest, M., Le May, C., & Fabre, F. (2007). Landscape epidemiology of plant diseases. Journal of the Royal Society, Interface, 4, 963-972.
74. Power, A. G., & Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. American Naturalist, 164, S79-S89.
75. Roslin, T., Laine, A.-L., & Gripenberg, S. (2007). Spatial population structure in an obligate plant pathogen colonizing oak Quercus robur. Functional Ecology, 21, 1168-1177.
76. Santini, A., Ghelardini, L., De Pace, C., Desprez-Loustau, M. L., Capretti, P., Chandelier, A., et al. (2013). Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytologist, 197, 238-250.
77. Seabloom, E. W., Borer, E. T., Lacroix, C., Mitchell, C. E., & Power, A. G. (2013). Richness and composition of niche-assembled viral pathogen communities. PLoS ONE, 8, e55675. doi: 10. 1371/journal. pone. 0055675.
78. Smith, D. L., Ericson, L., & Burdon, J. J. (2011). Co-evolutionary hot and cold spots of selective pressure move in space and time. Journal of Ecology, 99, 634-641.
79. Soubeyrand, S., Laine, A.-L., Hanski, I., & Penttinen, A. (2009). Spatiotemporal structure of host-pathogen interactions in a metapopulation. American Naturalist, 174, 308-320.
80. Springer, Y. P. (2007). Clinal resistance structure and pathogen local adaptation in a serpentine flax-flax rust interaction. Evolution, 61, 1812-1822.
81. Sullivan, L. L., Johnson, B. L., Brudvig, L. A., & Haddad, N. M. (2011). Can dispersal mode predict corridor effects on plant parasites? Ecology, 92, 1559-1564.
82. Tack, A. J. M., Thrall, P. H., Barrett, L. G., Burdon, J. J., & Laine, A.-L. (2012). Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems-causes and consequences. Journal of Evolutionary Biology, 25, 1918-1936.
83. Thompson, J. N. (1994). The coevolutionary process. Chicago: University of Chicago Press.
84. Thompson, J. N. (2005). The geographic mosaic of coevolution. Chicago: University of Chicago Press.
85. Thrall, P. H., & Antonovics, J. (1995). Theoretical and empirical studies of metapopulations-population and genetic dynamics of the Silene-Ustilago system. Canadian Journal of Botany, 73, S1249-S1258.
86. Thrall, P. H., & Burdon, J. J. (1997). Host-pathogen dynamics in a metapopulation context: the ecological and evolutionary consequences of being spatial. Journal of Ecology, 85, 743-753.
87. Thrall, P. H., & Burdon, J. J. (1999). The spatial scale of pathogen dispersal: consequences for disease dynamics and persistence. Evolutionary Ecology Research, 1, 681-701.
88. Thrall, P. H., & Burdon, J. J. (2002). Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathology, 51, 169-184.
89. Thrall, P. H., & Burdon, J. J. (2004). Host-pathogen life-history interactions affect biological control success. Weed Technology, 18, 1269-1274.
90. Thrall, P. H., Burdon, J. J., & Bever, J. D. (2002). Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution, 56, 1340-1351.
91. Thrall, P. H., Burdon, J. J., & Bock, C. H. (2001). Short-term epidemic dynamics in the Cakile maritima-Alternaria brassicicola host-pathogen metapopulation association. Journal of Ecology, 89, 723-735.
92. Thrall, P. H., Burdon, J. J., & Godfree, R. (2003). The influence of spatial structure on pathogen colonization and extinction: a test using an experimental metapopulation. Plant Pathology, 52, 350-361.
93. Thrall, P. H., & Jarosz, A. M. (1994). Host-pathogen dynamics in experimental populations of Silene alba and Ustilago violacea. II. Experimental tests of theoretical models. Journal of Ecology, 82, 561-570.
94. Thrall, P. H., Laine, A.-L., Ravensdale, M., Nemri, A., Dodds, P. N., Barrett, L. G., et al. (2012). Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecology Letters, 15, 425-435.
95. van der Plank, J. E. (1963). Plant diseases: Epidemics and control. New York: Academic.
96. van Der Putten, W. H., van Dijk, C., & Peters, B. A. M. (1993). Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature, 362, 53-56.
97. Vogler, W., & Lindsay, A. (2002). The impact of the rust fungus Maravalia cryptostegiae on three rubber vine (Cryptostegia grandiflora) populations in tropical Queensland. In H. S. Jacob, J. Dodd, J. H. Moore (Eds.), Proc. 13th Australian Weeds Conf. Weeds 'threats now and forever' (pp. 180-182). Plant Protection Soc. WA.
98. Wahl, I. (1970). Prevalence and geographic distribution of resistance to crown rust in Avena sterilis. Phytopathology, 60, 746-749.
99. Wang, B., Brubaker, C. L., Tate, W., Woods, M. J., & Burdon, J. J. (2008). Evolution of virulence in Fusarium oxysporum f. sp. vasinfectum using serial passage assays through susceptible cotton. Phytopathology, 98, 296-303.
100. Wang, B., Brubaker, C. L., Summerell, B. A., Thrall, P. H., & Burdon, J. J. (2010). Local origin of two vegetative compatibility groups of Fusarium oxysporum f. sp. vasinfectum in Australia. Evolutionary Applications, 3, 505-524.
101. Wolfe, M. S. (1985). The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Annual Review of Phytopathology, 23, 251-273.
102. Wood, A. R., & Morris, M. J. (2007). Impact of the gall-forming rust fungus Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa: 15 years of monitoring. Biological Control, 41, 68-77.