European Journal of Plant Pathology

, Volume 115, Issue 1, pp 35–51

Ecological Genomics and Epidemiology

  • K. A. Garrett
  • S. H. Hulbert
  • J. E. Leach
  • S. E. Travers
Article

Abstract

The huge amount of genomic data now becoming available offers both opportunities and challenges for epidemiologists. In this “preview” of likely developments as the field of ecological genomics evolves and merges with epidemiology, we discuss how epidemiology can use new information about genetic sequences and gene expression to form predictions about epidemic features and outcomes and for understanding host resistance and pathogen evolution. DNA sequencing is now complete for some hosts and several pathogens. Microarrays make it possible to measure gene expression simultaneously for thousands of genes. These tools will contribute to plant disease epidemiology by providing information about which resistance or pathogenicity genes are present in individuals and populations, what genes other than those directly involved in resistance and virulence are important in epidemics, the role of the phenotypic status of hosts and pathogens, and the role of the status of the environmental metagenome. Conversely, models of group dynamics supplied by population biology and ecology may be used to interpret gene expression within individual organisms and in populations of organisms. Genomic tools have great potential for improving understanding of resistance gene evolution and the durability of resistance. For example, DNA sequence analysis can be used to evaluate whether an arms race model of co-evolution is supported. Finally, new genomic tools will make it possible to consider the landscape ecology of epidemics in terms of host resistance both as determined by genotype and as expressed in host phenotypes in response to the biotic and abiotic environment. Host phenotype mixtures can be modeled and evaluated, with epidemiological predictions based on phenotypic characteristics such as physiological age and status in terms of induced systemic resistance or systemic acquired resistance.

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References

  1. Adee, SR, Pfender, WF, Hartnett, DC 1990Competition between Pyrenophora tritici-repentis and Septoria nodorum in the wheat leaf as measured with de Wit replacement seriesPhytopathology8011771182Google Scholar
  2. Alfano, JR, Collmer, A 2004Type III secretion system effector proteins: double agents in bacterial disease and plant defenseAnnual Review of Phytopathology42385414PubMedCrossRefGoogle Scholar
  3. Al-Naimi, FA, Garrett, KA, Bockus, WW 2005Competition, facilitation, and niche differentiation in two foliar pathogensOecologia143449457PubMedCrossRefGoogle Scholar
  4. Antonovics, J 2003Toward community genomics?Ecology84598601Google Scholar
  5. Axtell, MJ, Staskawicz, BJ 2003Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4Cell112369377PubMedCrossRefGoogle Scholar
  6. Bai, J, Pennill, LA, Ning, J, Lee, SW, Ramalingam, J, Webb, CA, Zhao, B, Sun, Q, Nelson, JC, Leach, JE, Hulbert, SH 2002Diversity of nucleotide binding site-leucine-rich repeat genes in cerealsGenome Research1218711884PubMedCrossRefGoogle Scholar
  7. Bergelson, J, Kreitman, M, Stahl, EA, Tian, DC 2001Evolutionary dynamics of plant R-genesScience29222812285PubMedCrossRefGoogle Scholar
  8. Black, WC,IV, Baer, CF, Antolin, MF, DuTeau, NM 2001Population genomics: genome-wide sampling of insect populationsAnnual Review of Entomology46441469PubMedCrossRefGoogle Scholar
  9. Buschges, R, Hollricher, K, Panstruga, R, Simons, G, Wolter, M, Frijters, A, Daelen, R, Lee, T, Diergaarde, P, Groenendijk, J, Topsch, S, Vos, P, Salamini, F, Schulze-Lefert, P 1997The barley Mlo gene: a novel control element of plant pathogen resistanceCell88695705PubMedCrossRefGoogle Scholar
  10. Caicedo, AL, Schaal, BA, Kunkel, BN 1999Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thalianaProceedings of the National Academy of Sciences of the United States of America96302306PubMedCrossRefGoogle Scholar
  11. Calonnec, A, Goyeau, H, Vallavielle-Pope, C 1996Effects of induced resistance on infection efficiency and sporulation of Puccinia striiformis on seedlings in varietal mixtures and on field epidemics in pure standsEuropean Journal of Plant Pathology102733741CrossRefGoogle Scholar
  12. Chain, PSG, Carniel, E, Larimer, FW, Lamerdin, J, Stoutland, PO, Regala, WM, Georgescu, AM, Vergez, LM, Land, ML, Motin, VL, Brubaker, RR, Fowler, J, Hinnebusch, J, Marceau, M, Medigue, C, Simonet, M, Chenal-Francisque, V, Souza, B, Dacheux, D, Elliott, JM, Derbise, A, Hauser, LJ, Garcia, E 2004Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosisProceedings of the National Academy of Sciences of the United States of America1011382613831PubMedCrossRefGoogle Scholar
  13. Chang, JH, Urbach, JM, Law, TF, Arnold, LW, Hu, A, Gombar, S, Grant, SR, Ausubel, FM, Dangl, JL 2005A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringaeProceedings of the National Academy of Sciences of the United States of America10225492554PubMedCrossRefGoogle Scholar
  14. Chen, W, Provart, NJ, Glazebrook, J, Katagiri, F, Chang, HS, Eulgem, T, Mauch, F, Luan, S, Zou, G, Whitham, SA, Budworth, PR, Tao, Y, Xie, Z, Chen, X, Lam, S, Kreps, JA, Harper, JF, Si-Ammour, A, Mauch-Mani, B, Heinlein, M, Kobayashi, K, Hohn, T, Dangl, JL, Wang, X, Zhu, T 2002Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stressesThe Plant Cell14559574PubMedCrossRefGoogle Scholar
  15. Collmer, A, Lindeberg, M, Petnicki-Ocwieja, T, Schneider, DJ, Alfano, JR 2002Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectorsTrends in Microbiology10462469PubMedCrossRefGoogle Scholar
  16. Cortesi, P, Fischer, M, Milgroom, MG 2000Identification and spread of Fomitiporia punctata associated with wood decay of grapevine showing symptoms of EscaPhytopathology90967972PubMedGoogle Scholar
  17. Cortesi, P, Milgroom, MG 2001Outcrossing and diversity of vegetative compatibility types in populations of Eutypa lata from grapevinesJournal of Plant Pathology837986Google Scholar
  18. Cowger, C, Wallace, LD, Mundt, CC 2005Velocity of spread of wheat stripe rust epidemicsPhytopathology95972982PubMedGoogle Scholar
  19. Cox, CM, Garrett, KA, Bowden, RL, Fritz, AK, Dendy, SP, Heer, WF 2004Cultivar mixtures for the simultaneous management of multiple diseases: Tan spot and leaf rust of wheatPhytopathology94961969PubMedGoogle Scholar
  20. Cui, J, Bahrami, AK, Pringle, EG, Hernandez-Guzman, G, Bender, CL, Pierce, NE, Ausubel, FM 2005Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivoresProceedings of the National Academy of Sciences of the United States of America10217911796PubMedCrossRefGoogle Scholar
  21. Deslandes, L, Olivier, J, Peeters, N, Feng, DX, Khounlotham, M, Boucher, C, Somssich, I, Genin, S, Marco, Y 2003Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleusProceedings of the National Academy of Sciences of the United States of America10080248029PubMedCrossRefGoogle Scholar
  22. Durrant, WE, Dong, X 2004Systemic acquired resistanceAnnual Review of Phytopathology42185209PubMedCrossRefGoogle Scholar
  23. Ellis, JG, Lawrence, GJ, Luck, JE, Dodds, PN 1999Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificityThe Plant Cell11495506PubMedCrossRefGoogle Scholar
  24. Escriu, F, Fraile, A, Garcia-Arenal, F 2000aEvolution of virulence in natural populations of the satellite RNA of Cucumber mosaic virusPhytopathology90480485Google Scholar
  25. Escriu, F, Fraile, A, Garcia-Arenal, F 2003The evolution of virulence in a plant virusEvolution57755765PubMedGoogle Scholar
  26. Escriu, F, Perry, KL, Garcia-Arenal, F 2000bTransmissibility of Cucumber mosaic virus by Aphis gossypii correlates with viral accumulation and is affected by the presence of its satellite RNAPhytopathology9010681072Google Scholar
  27. Feder, ME, Mitchell-Olds, T 2003Evolutionary and ecological functional genomicsNature Reviews Genetics4651665PubMedCrossRefGoogle Scholar
  28. Frick, UB, Schaller, A 2002cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plantsPlanta2168394PubMedCrossRefGoogle Scholar
  29. Garrett, KA, Bowden, RL 2002An Allee effect reduces the invasive potential of Tilletia indicaPhytopathology9211521159PubMedGoogle Scholar
  30. Garrett, KA, Mundt, CC 1999Epidemiology in mixed host populationsPhytopathology89984990PubMedGoogle Scholar
  31. Gilbert, GS 2002Evolutionary ecology of plant diseases in␣natural ecosystemsAnnual Review of Phytopathology401343PubMedCrossRefGoogle Scholar
  32. Glazebrook, J, Chen, W, Estes, B, Chang, HS, Nawrath, C, Métraux, JP, Zhu, T, Katagiri, F 2003Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotypingThe Plant Journal34217228PubMedCrossRefGoogle Scholar
  33. Hughes, G 1996Incorporating spatial pattern of harmful organisms into crop loss modelsCrop Protection15407421CrossRefGoogle Scholar
  34. Hulbert, S 1998Arming plants against pathogens-recombination in resistance lociTrends in Plant Science3121122CrossRefGoogle Scholar
  35. Hulbert, SH, Webb, CA, Smith, SM, Sun, Q 2001Resistance gene complexes: evolution and utilizationAnnual Review of Phytopathology39285312PubMedCrossRefGoogle Scholar
  36. Iavicoli, A, Boutet, E, Buchala, A, Métraux, JP 2003Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0Molecular Plant–Microbe Interactions16851858PubMedGoogle Scholar
  37. Jeger, MJ 2004Analysis of disease progress as a basis for evaluating disease management practicesAnnual Review of Phytopathology426182PubMedCrossRefGoogle Scholar
  38. Jia, Y, Bryan, GT, Farrall, L, Valent, B 2003Natural variation at the Pi-ta rice blast resistance locusPhytopathology9314521459PubMedGoogle Scholar
  39. Jia, Y, McAdams, SA, Bryan, GT, Hershey, HP, Valent, B 2000Direct interaction of resistance gene and avirulence gene products confers rice blast resistanceThe European Molecular Biology Organization Journal1940044014Google Scholar
  40. Johnson, R 1981Durable resistance: definition of, genetic control, and attainment in plant breedingPhytopathology71567568Google Scholar
  41. Jones, PG, Allaway, D, Gilmour, DM, Harris, C, Rankin, D, Retzel, ER, Jones, CA 2002Gene discovery and microarray analysis of cacao (Theobroma cacao L.) varietiesPlanta216255264PubMedCrossRefGoogle Scholar
  42. Kerk, NM, Ceserani, T, Tausta, SL, Sussex, IM, Nelson, TM 2003Laser capture microdissection of cells from plant tissuesPlant Physiology1322735PubMedCrossRefGoogle Scholar
  43. Kleczkowski, A, Gilligan, CA, Bailey, DJ 1997Scaling and spatial dynamics in plant–pathogen systems: from individuals to populationsProceedings of the Royal Society of London B264979984CrossRefGoogle Scholar
  44. Kranz J, (2002) Comparative Epidemiology of Plant Diseases. SpringerGoogle Scholar
  45. Lannou, C, Vallavieille-Pope, C, Biass, C, Goyeau, H 1994The efficacy of mixtures of susceptible and resistant hosts to two wheat rusts of different lesion size: controlled condition experiments and computerized simulationsJournal of Phytopathology140227237Google Scholar
  46. Leach, JE, Vera Cruz, CM, Bai, J, Leung, H 2001Pathogen fitness penalty as a predictor of durability of disease resistance genesAnnual Review of Phytopathology39187224PubMedCrossRefGoogle Scholar
  47. Leung, H, Zhu, Y, Revilla-Molina, I, Fan, JX, Chen, H, Pangga, I, Vera Cruz, C, Mew, TW 2003Using genetic diversity to achieve sustainable rice disease managementPlant Disease8711561169Google Scholar
  48. Liu, B, Zhang, SH, Zhu, XY, Yang, Q, Wu, S, Mei, M, Mauleon, R, Leach, J, Mew, T, Leung, H 2004Candidate defense genes as predictors of quantitative blast resistance in riceMolecular Plant–Microbe Interactions1711461152PubMedGoogle Scholar
  49. Luck, JE, Lawrence, GL, Dodds, PN, Shepherd, KW, Ellis, JG 2000Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determinationThe Plant Cell1213671377PubMedCrossRefGoogle Scholar
  50. Mackey, D, Belkhadir, Y, Alonso, JM, Ecker, JR, Dangl, JL 2003Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistanceCell112379389PubMedCrossRefGoogle Scholar
  51. Madden, LV, Hughes, G, Irwin, ME 2000Coupling disease-progress-curve and time-of-infection functions for predicting yield loss of cropsPhytopathology90788800PubMedGoogle Scholar
  52. Maleck, K, Levine, A, Eulgem, T, Morgan, A, Schmid, J, Lawton, KA, Dangl, JL, Dietrich, RA 2000The transcriptome of Arabidopsis thaliana during systemic acquired resistanceNature Genetics26403410PubMedCrossRefGoogle Scholar
  53. Mauricio, R 2005Can ecology help genomics: the genome as ecosystem?Genetica123205209PubMedCrossRefGoogle Scholar
  54. Meyers, BC, Kozik, A, Griego, A, Kuang, H, Michelmore, RW 2003Genome-wide analysis of NBS-LRR-encoding genes in ArabidopsisThe Plant Cell15809834PubMedCrossRefGoogle Scholar
  55. Milgroom, MG, Peever, TL 2003Population biology of plant pathogens: the synthesis of plant disease epidemiology and population geneticsPlant Disease87608617Google Scholar
  56. Mitchell, CE, Tilman, D, Groth, JV 2002Effects of grassland plant species diversity, abundance, and composition on foliar fungal diseaseEcology8317131726CrossRefGoogle Scholar
  57. Mundt, CC, Brophy, LS, Schmitt, MS 1995Disease severity and yield of pure-line wheat cultivars and mixtures in the presence of eyespot, yellow rust, and their combinationPlant Pathology44173182Google Scholar
  58. Mundt, CC, Leonard, KJ 1986Effect of host genotype unit area on development of focal epidemics of bean rust and common maize rust in mixtures of resistant and susceptible plantsPhytopathology76895900CrossRefGoogle Scholar
  59. Mundt, CC 2002Use of multiline cultivars and cultivar mixtures for disease managementAnnual Review of Phytopathology40381410PubMedCrossRefGoogle Scholar
  60. Mysore, KS, D’Ascenzo, MD, He, X, Martin, GB 2003Overexpression of the disease resistance gene Pto in tomato induces gene expression changes similar to immune responses in human and fruitflyPlant Physiology13219011912PubMedCrossRefGoogle Scholar
  61. Nakazono, M, Qiu, F, Borsuk, LA, Schnable, PS 2003Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maizeThe Plant Cell15583596PubMedCrossRefGoogle Scholar
  62. Newcombe, G, Bradshaw, HD 1996Quantitative trait loci conferring resistance in hybrid poplar to Septoria populicola, the cause of leaf spotCanadian Journal of Forest Research2619431950Google Scholar
  63. Ngugi, HK, King, SB, Holt, J, Julian, AM 2001Simultaneous temporal progress of sorghum anthracnose and leaf blight in crop mixtures with disparate patternsPhytopathology91720729PubMedGoogle Scholar
  64. Otten, W, Filipe, JAN, Bailey, DJ, Gilligan, CA 2003Quantification and analysis of transmission rates for soil-borne epidemicsEcology8432323239Google Scholar
  65. Parniske, M, Hammond-Kosack, KE, Golstein, C, Thomas, CM, Jones, DA, Harrison, K, Wulff, BBH, Jones, JDG 1997Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomatoCell91821832PubMedCrossRefGoogle Scholar
  66. Pieterse, CMJ, Loon, LC 1999Salicylic acid-independent plant defence pathwaysTrends in Plant Science45258PubMedCrossRefGoogle Scholar
  67. Ponciano, G, Ishihara, H, Tsuyumu, S, Leach, JE 2003Bacterial effectors in plant disease and defense: keys to durable resistance?Plant Disease8712721282Google Scholar
  68. Ponciano, G, Webb, K, Bai, J, Vera Cruz, C, Leach, JE 2004Molecular characterization of the avrXa7 locus from Xanthomonas oryzae pv. oryzae field isolatesPhysiological and Molecular Plant Pathology64145153CrossRefGoogle Scholar
  69. Robinson, RA 1976Plant Pathosystems.Springer-VerlagNew YorkGoogle Scholar
  70. Rohmer, L, Guttman, DS, Dangl, JL 2004Diverse evolutionary mechanisms shape the type iii effector virulence factor repertoire in the plant pathogen Pseudomonas syringaeGenetics16713411360PubMedCrossRefGoogle Scholar
  71. Rondon, MR, August, PR, Bettermann, AD, Brady, SF, Grossman, TH, Liles, MR, Loiacono, KA, Lynch, BA, MacNeil, IA, Minor, C, Tiong, CL, Gilman, M, Osburne, MS, Clardy, J, Handelsman, J, Goodman, RM 2000Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganismsApplied and Environmental Microbiology6625412547PubMedCrossRefGoogle Scholar
  72. Ryals, JA, Neuenschwander, UH, Willits, MG, Molina, A, Steiner, H-Y, Hunt, MD 1996Systemic acquired resistanceThe Plant Cell818091819PubMedCrossRefGoogle Scholar
  73. Schenk, PM, Kazan, K, Manners, JM, Anderson, JP, Simpson, RS, Wilson, IW, Somerville, SC, Maclean, DJ 2003Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicolaPlant Physiology1329991010PubMedCrossRefGoogle Scholar
  74. Scherm, H 1996On the velocity of epidemic waves in model plant disease epidemicsEcological Modelling87217222CrossRefGoogle Scholar
  75. Scofield, SR, Tobias, CM, Rathjen, JP, Chang, JH, Lavelle, DT, Michelmore, RW, Staskawicz, BJ 1996Molecular basis of gene-for-gene specificity in bacterial speck disease of tomatoScience27420632065PubMedCrossRefGoogle Scholar
  76. Smith, KP, Goodman, RM 1999Host variation for interactions with beneficial plant-associated microbesAnnual Review of Phytopathology37473491PubMedCrossRefGoogle Scholar
  77. Smith, SM, Pryor, AJ, Hulbert, SH 2004Allelic and haplotypic diversity at the Rp1 rust resistance locus of maizeGenetics16719391947PubMedCrossRefGoogle Scholar
  78. Spoel, SH, Koornneef, A, Claessens, SMC, Korzelius, JP, Pelt, JA, Mueller, MJ, Buchala, AJ, Métraux, JP, Brown, R, Kazan, K, Loon, LC, Dong, X, Pieterse, CMJ 2003NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosolThe Plant Cell15760770PubMedCrossRefGoogle Scholar
  79. Tang, X, Frederick, RD, Zhou, J, Halterman, DA, Jia, Y, Martin, GB 1996Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinaseScience27420602063PubMedCrossRefGoogle Scholar
  80. Thomma, BPHJ, Eggermont, K, Penninckx, IAWA, Mauch-Mani, B, Vogelsang, R, Cammue, BPA, Brroekaert, WF 1998Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogensProceedings of the National Academy of Sciences of the United States of America951510715111CrossRefPubMedGoogle Scholar
  81. Tian, D, Araki, H, Stahl, E, Bergelson, J, Kreitman, M 2002Signature of balancing selection in ArabidopsisProceedings of the National Academy of Sciences of the United States of America991152511530PubMedCrossRefGoogle Scholar
  82. Sluys, MA, Monteiro-Vitorello, CB, Camargo, LEA, Menck, CFM, Silva, ACR, Ferro, JA, Oliveira, MC, Setubal, JC, Kitajima, JP, Simpson, AJ 2002Comparative genomic analysis of plant-associated bacteriaAnnual Review of Phytopathology40169189PubMedCrossRefGoogle Scholar
  83. van Wees SCM, de Swart EAM, van Pelt JA, van Loon LC and Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proceedings of the National Academy of Science of the United States of America 97: 8711–8716Google Scholar
  84. Venter, JC, Remington, K, Heidelberg, JF, Halpern, AL, Rusch, D, Eisen, JA, Wu, D, Paulsen, I, Nelson, KE, Nelson, W, Fouts, DE, Levy, S, Knap, AH, Lomas, MW, Nealson, K, White, O, Peterson, J, Hoffman, J, Parsons, R, Baden-Tillson, H, Pfannkoch, C, Rogers, YH, Smith, HO 2004Environmental genome shotgun sequencing of the Sargasso SeaScience3046674PubMedCrossRefGoogle Scholar
  85. Vera Cruz, CM, Bai, J, Oña, I, Leung, H, Nelson, RJ, Mew, TW, Leach, JE 2000Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutationProceedings of the National Academy of Sciences of the United States of America971350013505PubMedCrossRefGoogle Scholar
  86. Bodman, SB, Bauer, WD, Coplin, DL 2003Quorum sensing in plant-pathogenic bacteriaAnnual Review of Phytopathology41455482CrossRefGoogle Scholar
  87. Waggoner, PE, Aylor, DE 2000Epidemiology: a science of patternsAnnual Review of Phytopathology387194PubMedCrossRefGoogle Scholar
  88. Wan, J, Dunning, MF, Bent, AF 2002Probing plant–pathogen interactions and downstream defense signaling using DNA microarraysFunctional and Integrative Genomics2259273PubMedCrossRefGoogle Scholar
  89. Welch, SM, Roe, JL, Das, S, Dong, Z, He, R, Kirkham, MB 2005Merging genomic control networks and soil-plant-atmosphere-continuum modelsAgricultural Systems86243274CrossRefGoogle Scholar
  90. Welch, SM, Roe, JL, Dong, Z 2003A Genetic neural network model of flowering time control in Arabidopsis thalianaAgronomy Journal957181CrossRefGoogle Scholar
  91. Weller, DM, Raaijmakers, JM, McSpadden-Gardener, BB, Thomashow, LS 2002Microbial populations responsible for specific soil suppressiveness to plant pathogensAnnual Review of Phytopathology40309348PubMedCrossRefGoogle Scholar
  92. Whitham, SA, Quan, S, Chang, HS, Cooper, B, Estes, B, Zhu, T, Wang, X, Hou, YM 2003aDiverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsisthaliana plantsThe Plant Journal33271283CrossRefGoogle Scholar
  93. Whitham, TG, Martinsen, GD,  Floate, KD, Dungey, HS, Potts, BM, Keim, P 1999Plant hybrid zones affect biodiversity: tools for a genetic-based understanding of community structureEcology80416428CrossRefGoogle Scholar
  94. Whitham, TG, Young, WP, Martinsen, GD, Gehring, CA, Schweitzer, JA, Shuster, SM, Wimp, GM, Fischer, DG, Bailey, JK, Lindroth, RL, Woolbright, S, Kuske, CR 2003bCommunity genetics: a consequence of the extended phenotypeEcology84559573Google Scholar
  95. With, KA 2002The landscape ecology of invasive spreadConservation Biology1611921203CrossRefGoogle Scholar
  96. Wolter, M, Hollricher, K, Salamini, F, Schulze-Lefert, P 1993The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defense mimic phenotypeMolecular and General Genetics239122128PubMedGoogle Scholar
  97. Zadoks, JC, Vandenbosch, F 1994On the spread of plant disease – a theory on fociAnnual Review of Phytopathology32503521CrossRefPubMedGoogle Scholar
  98. Zhu, Y, Chen, H, Fan, J, Wang, Y, Li, Y, Chen, J, Fan, J, Yang, S, Hu, L, Leaung, H, Mew, CW, Teng, PS, Wang, Z, Mundt, CC 2000Genetic diversity and disease control in riceNature406718722PubMedCrossRefGoogle Scholar
  99. Zwankhuizen, MJ, Govers, F, Zadoks, JC 1998Development of potato late blight epidemics: disease foci, disease gradients, and infection sourcesPhytopathology88754763PubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • K. A. Garrett
    • 1
  • S. H. Hulbert
    • 1
  • J. E. Leach
    • 2
  • S. E. Travers
    • 1
  1. 1.Department of Plant PathologyKansas State UniversityManhattanUSA
  2. 2.Department of Bioagricultural Sciences and Pest ManagementColorado State UniversityFt. CollinsUSA

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