Plant disease arises from the interaction of processes occurring at multiple spatial and temporal scales. With new tools such as next-generation sequencing, we are learning about the diversity of microbes circulating within and among plant populations and often coinhabiting host individuals. The proliferation of pathogenic microbes depends on single-species dynamics and multispecies interactions occurring within and among host cells, the spatial organization and genetic landscape of hosts, the frequency and mode of transmission among hosts and host populations, and the abiotic environmental context. Here, we examine empirical evidence from these multiple scales to assess the utility of metacommunity theory, a theoretical framework developed for free-living organisms to further our understanding of and assist in predicting plant-pathogen infection and spread. We suggest that deeper understanding of disease dynamics can arise through the application of this conceptual framework at scales ranging from individual cells to landscapes. In addition, we use this multiscale theoretical perspective to synthesize existing knowledge, generate novel hypotheses, and point toward promising future opportunities for the study of plant pathogens in natural populations.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Abang MM, Baum M, Ceccarelli S, Grando S, Linde CC. 1.  et al. 2006. Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 96:1214–22 [Google Scholar]
  2. Abrahamian P, Sobh H, Seblani R, Abou-Jawdah Y. 2.  2015. Co-infection of two criniviruses and a begomovirus enhances the disease severity in cucumber. Eur. J. Plant Pathol. 142:521–30 [Google Scholar]
  3. Adler FR, Muller-Landau HC. 3.  2005. When do localized natural enemies increase species richness?. Ecol. Lett. 8:438–47 [Google Scholar]
  4. Aflakpui GKS, Gregory PJ, Froud-Williams RJ. 4.  1998. Uptake and partitioning of nitrogen by maize infected with Striga hermonthica. Ann. Bot. 81:287–94 [Google Scholar]
  5. Alexander HM. 5.  2010. Disease in natural plant populations, communities, and ecosystems: insights into ecological and evolutionary processes. Plant Dis. 94:492–503 [Google Scholar]
  6. Alexander HM, Foster BL, Ballantyne F, Collins CD, Antonovics J, Holt RD. 6.  2012. Metapopulations and metacommunities: combining spatial and temporal perspectives in plant ecology. J. Ecol. 100:88–103 [Google Scholar]
  7. Amtmann A, Troufflard S, Armengaud P. 7.  2008. The effect of potassium nutrition on pest and disease resistance in plants. Physiol. Plant. 133:682–91 [Google Scholar]
  8. Anagnostakis SL. 8.  1995. The pathogens and pests of chestnuts. Adv. Bot. Res. 21:125–45 [Google Scholar]
  9. Anderson RM, May RM. 9.  1979. Population biology of infectious diseases. Part 1. Nature 280:361–67 [Google Scholar]
  10. Anderson RM, May RM. 10.  1982. Coevolution of hosts and parasites. Parasitology 85:411–26 [Google Scholar]
  11. Anderson RM, May RM. 11.  1986. The invasion, persistence and spread of infectious diseases within animal and plant communities. Philos. Trans. R. Soc. Lond. B 314:533–70 [Google Scholar]
  12. Antonovics J. 12.  2004. Long-term study of a plant-pathogen metapopulation. Ecology, Genetics, and Evolution of Metapopulations I Hanski, OE Gaggiotti 471–88 Burlington, MA: Elsevier [Google Scholar]
  13. Antonovics J, O’Keefe K, Hood ME. 13.  1998. Theoretical population genetics of mating-type linked haplo-lethal alleles. Int. J. Plant Sci. 159:192–98 [Google Scholar]
  14. Antonovics J, Thrall PH, Jarosz AM. 14.  1997. Genetics and the spatial ecology of species interactions: the Silene-Ustilago system. Spatial Ecology: The Role of Space in Population Dynamics and Interspecific Interactions D Tilman, PM Kareiva 158–80 Princeton, NJ: Princeton Univ. Press [Google Scholar]
  15. Aylor DE. 15.  1990. The role of intermittent wind in the dispersal of fungal pathogens. Annu. Rev. Phytopathol. 28:73–92 [Google Scholar]
  16. Barrett LG, Bell T, Dwyer G, Bergelson J. 16.  2011. Cheating, trade-offs and the evolution of aggressiveness in a natural pathogen population. Ecol. Lett. 14:1149–57 [Google Scholar]
  17. Bawden F, Kassanis B. 17.  1950. Some effects of host-plant nutrition on the multiplication of viruses. Ann. Appl. Biol. 37:215–28 [Google Scholar]
  18. Bolker BM, Pacala SW. 18.  1999. Spatial moment equations for plant competition: understanding spatial strategies and the advantages of short dispersal. Am. Nat. 153:575–602 [Google Scholar]
  19. Borer ET, Adams VT, Engler GA, Adams AL, Schumann CB, Seabloom EW. 19.  2009. Aphid fecundity and grassland invasion: Invader life history is the key. Ecol. Appl. 19:1187–96 [Google Scholar]
  20. Borer ET, Antonovics J, Kinkel LL, Hudson PJ, Daszak P. 20.  et al. 2012. Bridging taxonomic and disciplinary divides in infectious disease. EcoHealth 8:261–67 [Google Scholar]
  21. Borer ET, Kinkel LL, May G, Seabloom EW. 21.  2013. The world within: quantifying the determinants and outcomes of a host's microbiome. Basic Appl. Ecol. 14:533–39 [Google Scholar]
  22. Borer ET, Mitchell CE, Power AG, Seabloom EW. 22.  2009. Consumers indirectly increase infection risk in grassland food webs. PNAS 106:503–6 [Google Scholar]
  23. Borer ET, Seabloom EW, Mitchell CE, Power AG. 23.  2010. Local context drives infection of grasses by vector-borne generalist viruses. Ecol. Lett. 13:810–18 [Google Scholar]
  24. Burdon JJ. 24.  1980. Variation in disease-resistance within a population of Trifolium repens. J. Ecol. 68:737–44 [Google Scholar]
  25. Burdon JJ, Chilvers GA. 25.  1982. Host density as a factor in plant-disease ecology. Annu. Rev. Phytopathol. 20:143–66 [Google Scholar]
  26. Burdon JJ, Thrall PH. 26.  2000. Coevolution at multiple spatial scales: Linum marginaleMelampsora lini—from the individual to the species. Evol. Ecol. 14:261–81 [Google Scholar]
  27. Burdon JJ, Thrall PH. 27.  2014. What have we learned from studies of wild plant-pathogen associations? The dynamic interplay of time, space and life-history. Eur. J. Plant Pathol. 138:417–29 [Google Scholar]
  28. Burr TJ, Otten L. 28.  1999. Crown gall of grape: biology and disease management. Annu. Rev. Phytopathol. 37:53–80 [Google Scholar]
  29. Busby PE, Peay KG, Newcombe G. 29.  2015. Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol. doi:10.1111/nph.13742
  30. Carlsson U, Elmqvist T. 30.  1992. Epidemiology of anther-smut disease (Microbotryum violaceum) and numeric regulation of populations of Silene dioica. Oecologia 90:509–17 [Google Scholar]
  31. Carlsson-Graner U, Thrall PH. 31.  2006. The impact of host longevity on disease transmission: host-pathogen dynamics and the evolution of resistance. Evol. Ecol. Res. 8:659–75 [Google Scholar]
  32. Carrington JC, Kasschau KD, Mahajan SK, Schaad MC. 32.  1996. Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8:1669–81 [Google Scholar]
  33. Carter W. 33.  1962. Insects in Relation to Plant Disease New York: Interscience
  34. Chen YG, Olson DM, Ruberson JR. 34.  2010. Effects of nitrogen fertilization on tritrophic interactions. Arthropod-Plant Interact. 4:81–94 [Google Scholar]
  35. Christian N, Whitaker BK, Clay K. 35.  2015. Microbiomes: unifying animal and plant systems through the lens of community ecology theory. Front. Microbiol. 6:00869 [Google Scholar]
  36. Crawley MJ, Johnston AE, Silvertown J, Dodd M, de Mazancourt C. 36.  et al. 2005. Determinants of species richness in the park grass experiment. Am. Nat. 165:179–92 [Google Scholar]
  37. Crawley MJ, Ross GJS. 37.  1990. The population dynamics of plants [and discussion]. Philos. Trans. R. Soc. Lond. B 330:125–40 [Google Scholar]
  38. Cronin JP, Welsh ME, Dekkers MG, Abercrombie ST, Mitchell CE. 38.  2010. Host physiological phenotype explains pathogen reservoir potential. Ecol. Lett. 13:1221–32 [Google Scholar]
  39. Cubero J, Lastra B, Salcedo CI, Piquer J, López MM. 39.  2006. Systemic movement of Agrobacterium tumefaciens in several plant species. J. Appl. Microbiol. 101:412–21 [Google Scholar]
  40. Diamond JM. 40.  1975. Assembly of species communities. Ecology and Evolution of Communities ML Cody, JM Diamond 342–444 Cambridge, MA: Belknap Press [Google Scholar]
  41. Fatima U, Senthil-Kumar M. 41.  2015. Plant and pathogen nutrient acquisition strategies. Front. Plant Sci. 6:750 [Google Scholar]
  42. Feau N, Lauron-Moreau A, Piou D, Marcais B, Dutech C, Desprez-Loustau ML. 42.  2012. Niche partitioning of the genetic lineages of the oak powdery mildew complex. Fungal Ecol. 5:154–62 [Google Scholar]
  43. Fitt BDL, Huang YJ, van den Bosch F, West JS. 43.  2006. Coexistence of related pathogen species on arable crops in space and time. Annu. Rev. Phytopathol. 44:163–82 [Google Scholar]
  44. Froissart R, Doumayrou J, Vuillaume F, Alizon S, Michalakis Y. 44.  2010. The virulence-transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies. Philos. Trans. R. Soc. B 365:1907–18 [Google Scholar]
  45. Garrett KA, Mundt CC. 45.  1999. Epidemiology in mixed host populations. Phytopathology 89:984–90 [Google Scholar]
  46. Gilbert GS. 46.  2002. Evolutionary ecology of plant diseases in natural ecosystems. Annu. Rev. Phytopathol. 40:13–43 [Google Scholar]
  47. Gray SM, Banerjee N. 47.  1999. Mechanisms of arthropod transmission of plant and animal viruses. Microbiol. Mol. Biol. Rev. 63:128–48 [Google Scholar]
  48. Grenfell B, Harwood J. 48.  1997. (Meta)population dynamics of infectious diseases. Trends Ecol. Evol. 12:395–99 [Google Scholar]
  49. Gustafson EJ, Gardner RH. 49.  1996. The effect of landscape heterogeneity on the probability of patch colonization. Ecology 77:94–107 [Google Scholar]
  50. Guttman DS, McHardy AC, Schulze-Lefert P. 50.  2014. Microbial genome-enabled insights into plant-microorganism interactions. Nat. Rev. Genet. 15:797–813 [Google Scholar]
  51. Hall SR, Knight CJ, Becker CR, Duffy MA, Tessier AJ, Caceres CE. 51.  2009. Quality matters: resource quality for hosts and the timing of epidemics. Ecol. Lett. 12:118–28 [Google Scholar]
  52. Hanski I. 52.  1999. Metapopulation Ecology Oxford: Oxford Univ. Press
  53. Harris KF, Maramorosch K. 53.  1980. Vectors of Plant Pathogens New York: Academic
  54. Hastings A. 54.  1980. Disturbance, coexistence, history, and competition for space. Theor. Popul. Biol. 18:363–73 [Google Scholar]
  55. Hess G. 55.  1996. Disease in metapopulation models: implications for conservation. Ecology 77:1617–32 [Google Scholar]
  56. Hipper C, Brault V, Ziegler-Graff V, Revers F. 56.  2013. Viral and cellular factors involved in phloem transport of plant viruses. Front. Plant Sci. 4:154 [Google Scholar]
  57. Holmes F. 57.  1929. Local lesions in tobacco mosaic. Bot. Gaz. 87:39–55 [Google Scholar]
  58. Holyoak M, Leibold MA, Holt RD. 58.  2005. Metacommunities: Spatial Dynamics and Ecological Communities. Chicago: Univ. Chicago Press
  59. Hood ME. 59.  2003. Dynamics of multiple infection and within-host competition by the anther-smut pathogen. Am. Nat. 162:122–33 [Google Scholar]
  60. Hubbell SP. 60.  2001. The Unified Neutral Theory of Biodiversity and Biogeography Princeton: Princeton Univ. Press
  61. Huber DM, Watson RD. 61.  1974. Nitrogen form and plant disease. Annu. Rev. Phytopathol. 12:139–65 [Google Scholar]
  62. Hudson PJ, Dobson AP, Lafferty KD. 62.  2006. Is a healthy ecosystem one that is rich in parasites?. Trends Ecol. Evol. 21:381–85 [Google Scholar]
  63. Jeger MJ, Salama NKG, Shaw MW, van den Berg F, van den Bosch F. 63.  2014. Effects of plant pathogens on population dynamics and community composition in grassland ecosystems: two case studies. Eur. J. Plant Pathol. 138:513–27 [Google Scholar]
  64. Jenkyn JF, Bainbridge A. 64.  1978. Biology and pathology of cereal powdery mildews. Powdery Mildews DM Spencer 284–321 London: Academic [Google Scholar]
  65. Johnson PTJ, Hartson RB, Larson DJ, Sutherland DR. 65.  2008. Diversity and disease: Community structure drives parasite transmission and host fitness. Ecol. Lett. 11:1017–26 [Google Scholar]
  66. Johnson PTJ, Townsend AR, Cleveland CC, Glibert PM, Howarth RW. 66.  et al. 2010. Linking environmental nutrient enrichment and disease emergence in humans and wildlife. Ecol. Appl. 20:16–29 [Google Scholar]
  67. Johnston-Monje D, Mousa WK, Lazarovits G, Raizada MN. 67.  2014. Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol. 14:233 [Google Scholar]
  68. Jousimo J, Tack AJM, Ovaskainen O, Mononen T, Susi H. 68.  et al. 2014. Ecological and evolutionary effects of fragmentation on infectious disease dynamics. Science 344:1289–93 [Google Scholar]
  69. Karnosky DF. 69.  1979. Dutch elm disease: a review of the history, environmental implications, control, and research needs. Environ. Conserv. 6:311–22 [Google Scholar]
  70. Keeling MJ, Rohani P. 70.  2008. Modeling Infectious Diseases in Humans and Animals Princeton: Princeton Univ. Press
  71. Keesing F, Holt RD, Ostfeld RS. 71.  2006. Effects of species diversity on disease risk. Ecol. Lett. 9:485–98 [Google Scholar]
  72. Knops JMH, Tilman D, Haddad NM, Naeem S, Mitchell CE. 72.  et al. 1999. Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol. Lett. 2:286–93 [Google Scholar]
  73. Kuris AM, Blaustein AR, Alio JJ. 73.  1980. Hosts as islands. Am. Nat. 116:570–86 [Google Scholar]
  74. Lacroix C, Seabloom EW, Borer ET. 74.  2014. Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses. New Phytol. 204:424–33 [Google Scholar]
  75. Laine AL, Burdon JJ, Dodds PN, Thrall PH. 75.  2011. Spatial variation in disease resistance: from molecules to metapopulations. J. Ecol. 99:96–112 [Google Scholar]
  76. Lamichhane JR, Venturi V. 76.  2015. Synergisms between microbial pathogens in plant disease complexes: a growing trend. Front. Plant Sci. 6:385 [Google Scholar]
  77. Leibold MA. 77.  1998. Similarity and local co-existence of species in regional biotas. Evol. Ecol. 12:95–110 [Google Scholar]
  78. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM. 78.  et al. 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7:601–13 [Google Scholar]
  79. Leibold MA, Miller TE. 79.  2004. From metapopulations to metacommunities. Ecology, Genetics and Evolution of Metapopulations IHE Gaggiotti 133–50 Burlington, MA: Academic [Google Scholar]
  80. Lemoine R, Camera SL, Atanassova R, Dédaldéchamp F, Allario T. 80.  et al. 2013. Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci. 4:272 [Google Scholar]
  81. Levins R. 81.  1969. Some demographic and genetic consequences of environmental heterogeneity for biological control. Entomol. Soc. Am. 15:237–40 [Google Scholar]
  82. López-Villavicencio M, Jonot O, Coantic A, Hood ME, Enjalbert J, Giraud T. 82.  2007. Multiple infections by the anther smut pathogen are frequent and involve related strains. PLOS Pathog. 3:e176 [Google Scholar]
  83. May RM, Anderson RM. 83.  1979. Population biology of infectious diseases. Part 2. Nature 280:455–61 [Google Scholar]
  84. May RM, Nowak MA. 84.  1994. Superinfection, metapopulation dynamics, and the evolution of diversity. J. Theor. Biol. 170:95–114 [Google Scholar]
  85. Mihaljevic JR. 85.  2012. Linking metacommunity theory and symbiont evolutionary ecology. Trends Ecol. Evol. 27:323–29 [Google Scholar]
  86. Miller ZJ. 86.  2012. Fungal pathogen species richness: Why do some plant species have more pathogens than others?. Am. Nat. 179:282–92 [Google Scholar]
  87. Mitchell CE, Blumenthal D, Jarosik V, Puckett EE, Pysek P. 87.  2010. Controls on pathogen species richness in plants’ introduced and native ranges: roles of residence time, range size and host traits. Ecol. Lett. 13:1525–35 [Google Scholar]
  88. Mitchell CE, Tilman D, Groth JV. 88.  2002. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83:1713–26 [Google Scholar]
  89. Moore S, Manore C, Bokil V, Borer E, Hosseini P. 89.  2011. Spatiotemporal model of barley and cereal yellow dwarf virus transmission dynamics with seasonality and plant competition. Bull. Math. Biol. 73:2707–30 [Google Scholar]
  90. Moore SM, Borer ET. 90.  2012. The influence of host diversity and composition on epidemiological patterns at multiple spatial scales. Ecology 93:1095–105 [Google Scholar]
  91. Mundt CC, Sackett KE, Wallace LD. 91.  2011. Landscape heterogeneity and disease spread: experimental approaches with a plant pathogen. Ecol. Appl. 21:321–28 [Google Scholar]
  92. Nadarasah G, Stavrinides J. 92.  2011. Insects as alternative hosts for phytopathogenic bacteria. FEMS Microbiol. Rev. 35:555–75 [Google Scholar]
  93. Nee S, May RM. 93.  1992. Dynamics of metapopulations: habitat destruction and competitive coexistence. J. Anim. Ecol. 61:37–40 [Google Scholar]
  94. Noble AE, Temme NM, Fagan WF, Keitt TH. 94.  2011. A sampling theory for asymmetric communities. J. Theor. Biol. 273:1–14 [Google Scholar]
  95. Olesinski AA, Almon E, Navot N, Perl A, Galun E. 95.  et al. 1996. Tissue-specific expression of the tobacco mosaic virus movement protein in transgenic potato plants alters plasmodesmal function and carbohydrate partitioning. Plant Physiol. 111:541–50 [Google Scholar]
  96. Ovaskainen O, Laine AL. 96.  2006. Inferring evolutionary signals from ecological data in a plant-pathogen metapopulation. Ecology 87:880–91 [Google Scholar]
  97. Papaix J, Burdon JJ, Lannou C, Thrall PH. 97.  2014. Evolution of pathogen specialisation in a host metapopulation: joint effects of host and pathogen dispersal. PLOS Comput. Biol. 10:e1003633 [Google Scholar]
  98. Perez G, Slippers B, Wingfield BD, Hunter GC, Wingfield MJ. 98.  2010. Micro- and macrospatial scale analyses illustrates mixed mating strategies and extensive geneflow in populations of an invasive haploid pathogen. Mol. Ecol. 19:1801–13 [Google Scholar]
  99. Pierik M, van Ruijven J, Bezemer TM, Geerts R, Berendse F. 99.  2011. Recovery of plant species richness during long-term fertilization of a species-rich grassland. Ecology 92:1393–98 [Google Scholar]
  100. Power AG, Mitchell CE. 100.  2004. Pathogen spillover in disease epidemics. Am. Nat. 164:S79–89 [Google Scholar]
  101. Purcell AH, Almeida RPP. 101.  2005. Insects as vectors of disease agents. Encyclopedia of Plant and Crop Science RM Goodman 5 Boca Raton, FL: CRC Press [Google Scholar]
  102. Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL. 102.  2008. Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecol. Lett. 11:793–801 [Google Scholar]
  103. Rhee Y, Tzfira T, Chen MH, Waigmann E, Citovsky V. 103.  2000. Cell-to-cell movement of tobacco mosaic virus: enigmas and explanations. Mol. Plant Pathol. 1:33–39 [Google Scholar]
  104. Rizzo DM, Garbelotto M. 104.  2003. Sudden oak death: endangering California and Oregon forest ecosystems. Front. Ecol. Environ. 1:197–204 [Google Scholar]
  105. Rodrigo G, Zwart MP, Elena SF. 105.  2014. Onset of virus systemic infection in plants is determined by speed of cell-to-cell movement and number of primary infection foci. J. R. Soc. Interface 11:20140555 [Google Scholar]
  106. Rodriguez RJ, White JF, Arnold AE, Redman RS. 106.  2009. Fungal endophytes: diversity and functional roles. New Phytol. 182:314–30 [Google Scholar]
  107. Rosskopf EN, Charudattan R, DeValerio JT, Stall WM. 107.  2000. Field evaluation of Phomopsis amaranthicola, a biological control agent of Amaranthus spp. Plant Dis. 84:1225–30 [Google Scholar]
  108. Rottstock T, Joshi J, Kummer V, Fischer M. 108.  2014. Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95:1907–17 [Google Scholar]
  109. Sanderfoot AA, Lazarowitz SG. 109.  1996. Getting it together in plant virus movement: cooperative interactions between bipartite geminivirus movement proteins. Trends Cell Biol. 6:353–58 [Google Scholar]
  110. Schulz B, Boyle C. 110.  2005. The endophytic continuum. Mycol. Res. 109:661–86 [Google Scholar]
  111. Seabloom EW, Bjornstad ON, Bolker BM, Reichman OJ. 111.  2005. Spatial signature of environmental heterogeneity, dispersal, and competition in successional grasslands. Ecol. Monogr. 75:199–214 [Google Scholar]
  112. Seabloom EW, Borer ET, Gross K, Kendig AE, Lacroix C. 112.  et al. 2015. The community ecology of pathogens: coinfection, coexistence and community composition. Ecol. Lett. 18:401–15 [Google Scholar]
  113. Seabloom EW, Borer ET, Lacroix C, Mitchell CE, Power AG. 113.  2013. Richness and composition of niche-assembled viral pathogen communities. PLOS ONE 8:e55675 [Google Scholar]
  114. Seabloom EW, Borer ET, Mitchell CE, Power AG. 114.  2010. Viral diversity and prevalence gradients in North American Pacific Coast grasslands. Ecology 91:721–32 [Google Scholar]
  115. Seabloom EW, Hosseini PR, Power AG, Borer ET. 115.  2009. Diversity and composition of viral communities: coinfection of barley and cereal yellow dwarf viruses in California grasslands. Am. Nat. 173:E79–98 [Google Scholar]
  116. Skelsey P, With KA, Garrett KA. 116.  2013. Why dispersal should be maximized at intermediate scales of heterogeneity. Theor. Ecol. 6:203–11 [Google Scholar]
  117. Smith DL, Ericson L, Burdon JJ. 117.  2011. Co-evolutionary hot and cold spots of selective pressure move in space and time. J. Ecol. 99:634–41 [Google Scholar]
  118. Smith V. 118.  2002. Effects of resource supplies on the structure and function of microbial communities. Antonie van Leeuwenhoek 81:99–106 [Google Scholar]
  119. Smith VH, Holt RD. 119.  1996. Resource competition and within-host disease dynamics. Trends Ecol. Evol. 11:386–89 [Google Scholar]
  120. Sommerhalder RJ, McDonald BA, Mascher F, Zhan J. 120.  2011. Effect of hosts on competition among clones and evidence of differential selection between pathogenic and saprophytic phases in experimental populations of the wheat pathogen Phaeosphaeria nodorum. BMC Evol. Biol. 11:188 [Google Scholar]
  121. Springer YP. 121.  2009. Edaphic quality and plant-pathogen interactions: effects of soil calcium on fungal infection of a serpentine flax. Ecology 90:1852–62 [Google Scholar]
  122. Stevens CJ, Dise NB, Mountford JO, Gowing DJ. 122.  2004. Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–79 [Google Scholar]
  123. Strengbom J, Nordin A, Nasholm T, Ericson L. 123.  2002. Parasitic fungus mediates change in nitrogen-exposed boreal forest vegetation. J. Ecol. 90:61–67 [Google Scholar]
  124. Strong DR, Levin DA. 124.  1975. Species richness of parasitic fungi of British trees. PNAS 72:2116–19 [Google Scholar]
  125. Strong DR, Levin DA. 125.  1979. Species richness of plant parasites and growth form of their hosts. Am. Nat. 114:1–22 [Google Scholar]
  126. Sun L, Qiu FB, Zhang XX, Dai X, Dong XZ, Song W. 126.  2008. Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microb. Ecol. 55:415–24 [Google Scholar]
  127. Susi H, Barrès B, Vale PF, Laine A-L. 127.  2015. Co-infection alters population dynamics of infectious disease. Nat. Commun. 6:5975 [Google Scholar]
  128. Susi H, Vale PF, Laine AL. 128.  2015. Host genotype and coinfection modify the relationship of within and between host transmission. Am. Nat. 186:252–63 [Google Scholar]
  129. Suzán G, García-Peña GE, Castro-Arellano I, Rico O, Rubio AV. 129.  et al. 2015. Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space. Ecol. Evol. 5:865–73 [Google Scholar]
  130. Swope SM, Stein IR. 130.  2012. Soil type mediates indirect interactions between Centaurea solstitialis and its biocontrol agents. Biol. Invasions 14:1697–710 [Google Scholar]
  131. Syller J. 131.  2012. Facilitative and antagonistic interactions between plant viruses in mixed infections. Mol. Plant Pathol. 13:204–16 [Google Scholar]
  132. Tack AJM, Hakala J, Petaja T, Kulmala M, Laine AL. 132.  2014. Genotype and spatial structure shape pathogen dispersal and disease dynamics at small spatial scales. Ecology 95:703–14 [Google Scholar]
  133. Tilman D, May RM, Lehman CL, Nowak MA. 133.  1994. Habitat destruction and the extinction debt. Nature 371:65–66 [Google Scholar]
  134. Tooley PW, Kyde KL. 134.  2007. Susceptibility of some Eastern forest species to Phytophthora ramorum. Plant Dis. 91:435–38 [Google Scholar]
  135. Tromas N, Zwart MP, Lafforgue G, Elena SF. 135.  2014. Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLOS Genet. 10:e1004186 [Google Scholar]
  136. Vasco DA, Wearing HJ, Rohani P. 136.  2007. Tracking the dynamics of pathogen interactions: modeling ecological and immune-mediated processes in a two-pathogen single-host system. J. Theor. Biol. 245:9–25 [Google Scholar]
  137. Whitfield AE, Falk BW, Rotenberg D. 137.  2015. Insect vector-mediated transmission of plant viruses. Virology 479:278–89 [Google Scholar]
  138. Wille P, Boller T, Kaltz O. 138.  2002. Mixed inoculation alters infection success of strains of the endophyte Epichloë bromicola on its grass host Bromus erectus. Proc. R. Soc. B 269:397–402 [Google Scholar]
  139. Wilson CL. 139.  1969. Use of plant pathogens in weed control. Annu. Rev. Phytopathol. 7:411–34 [Google Scholar]
  140. Wilson EB, Worcester J. 140.  1945. The spread of an epidemic. PNAS 31:327–33 [Google Scholar]
  141. Wilson M, Lindow SE. 141.  1994. Coexistence among epiphytic bacterial-populations mediated through nutritional resource partitioning. Appl. Environ. Microb. 60:4468–77 [Google Scholar]
  142. Wintermantel WM, Cortez AA, Anchieta AG, Gulati-Sakhuja A, Hladky LL. 142.  2008. Co-infection by two criniviruses alters accumulation of each virus in a host-specific manner and influences efficiency of virus transmission. Phytopathology 98:1340–45 [Google Scholar]
  143. Yadeta K, Thomma B. 143.  2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Front. Plant Sci. 4:97 [Google Scholar]
  144. Yang X, Tang ZY, Ji CJ, Liu HY, Ma WH. 144.  et al. 2014. Scaling of nitrogen and phosphorus across plant organs in shrubland biomes across Northern China. Sci. Rep. 4:5448 [Google Scholar]
  145. Zhu YY, Chen HR, Fan JH, Wang YY, Li Y. 145.  et al. 2000. Genetic diversity and disease control in rice. Nature 406:718–22 [Google Scholar]
  146. Zwart MP, Daros JA, Elena SF. 146.  2012. Effects of potyvirus effective population size in inoculated leaves on viral accumulation and the onset of symptoms. J. Virol. 86:9737–47 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error