1932

Abstract

This review takes an evolutionary view of breeding crops for durable resistance to disease. An understanding of coevolution between hosts and parasites leads to predictors of potentially durable resistance, such as corresponding virulence having a high fitness cost to the pathogen or resistance being common in natural populations. High partial resistance can also promote durability. Whether or not resistance is actually durable, however, depends on ecological and epidemiological processes that stabilize genetic polymorphism, many of which are absent from intensive agriculture. There continues to be no biological, genetic, or economic model for durable resistance. The analogy between plant breeding and natural selection indicates that the basic requirements are genetic variation in potentially durable resistance, effective and consistent selection for resistance, and an efficient breeding process in which trials of disease resistance are integrated with other traits. Knowledge about genetics and mechanisms can support breeding for durable resistance once these fundamentals are in place.

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2015-08-04
2024-04-18
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Literature Cited

  1. Acevedo-Garcia J, Kusch S, Panstruga R. 1.  2014. Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytol. 204:273–81 [Google Scholar]
  2. Agrawal AA, Heil M. 2.  2012. Synthesizing specificity: multiple approaches to understanding the attack and defense of plants. Trends Plant Sci. 17:239–42 [Google Scholar]
  3. Ali S, Gladieux P, Rahman H, Saqib MS, Fiaz M. 3.  et al. 2014. Inferring the contribution of sexual reproduction, migration and off-season survival to the temporal maintenance of microbial populations: a case study on the wheat fungal pathogen Puccinia striiformis f.sp. tritici. Mol. Ecol. 23:603–17 [Google Scholar]
  4. Andrivon D, Montarry J, Corbiere R, Pasco C, Glais I. 4.  et al. 2013. The hard life of Phytophthora infestans: when trade-offs shape evolution in a biotrophic plant pathogen. Plant Pathol. 62:Suppl. S128–35 [Google Scholar]
  5. Baenziger PS, Russell WK, Graef GL, Campbell BT. 5.  2006. Improving lives: 50 years of crop breeding, genetics, and cytology. Crop Sci. 46:2230–44 [Google Scholar]
  6. Barrett LG, Heil M. 6.  2012. Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci. 17:282–92 [Google Scholar]
  7. Bayles RA, Clarkson JDS, Slater SE. 7.  1997. The UK Cereal Pathogen Virulence Survey. See Ref. 37 103–117
  8. Bennett FGA. 8.  1984. Resistance to powdery mildew in wheat: a review of its use in agriculture and breeding programmes. Plant Pathol. 33:279–300 [Google Scholar]
  9. Bennett FGA, Westcott B. 9.  1982. Field assessment of resistance to powdery mildew in mature wheat plants. Plant Pathol. 31:261–68 [Google Scholar]
  10. Bentley AR, Scutari M, Gosman N, Faure S, Bedford F. 10.  et al. 2014. Applying association mapping and genomic selection to the dissection of key traits in elite European wheat. Theor. Appl. Genet. 127:2619–33 [Google Scholar]
  11. Bergelson J, Purrington CB. 11.  1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:536–58 [Google Scholar]
  12. Bjornstad A, Aastveit K. 12.  1990. Pleiotropic effects of the ml-o mildew resistance gene in barley in different genetic backgrounds. Euphytica 46:217–26 [Google Scholar]
  13. Bomblies K, Weigel D. 13.  2007. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8:382–93 [Google Scholar]
  14. Bonman JM, Khush G, Nelson R. 14.  1992. Breeding rice for resistance to pests. Annu. Rev. Phytopathol. 30:507–28 [Google Scholar]
  15. Bousset L, Chèvre AM. 15.  2013. Stable epidemic control in crops based on evolutionary principles: adjusting the metapopulation concept to agro-ecosystems. Agric. Ecosyst. Environ. 165:118–29 [Google Scholar]
  16. Brown JKM. 16.  1994. Chance and selection in the evolution of barley mildew. Trends Microbiol. 2:470–75 [Google Scholar]
  17. Brown JKM. 17.  1995. Pathogens' responses to the management of disease resistance genes. Adv. Plant Pathol. 11:75–102 [Google Scholar]
  18. Brown JKM. 18.  1999. The evolution of sex and recombination in fungi. Structure and Dynamics of Fungal Populations JJ Worrall 73–95 Dordrecht, Neth: Kluwer [Google Scholar]
  19. Brown JKM, Chartrain L, Lasserre-Zuber P, Saintenac C. 19.  2015. Genetics of resistance to Zymoseptoria tritici and applications to breeding for resistance. Fungal Genet. Biol. In press. doi: 10.1016/j.fgb.2015.04.017
  20. Brown JKM, Foster EM, O'Hara RB. 20.  1997. Adaptation of powdery mildew populations to cereal varieties in relation to durable and non-durable resistance. See Ref. 37 119–38
  21. Brown JKM, Hovmøller MS. 21.  2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–41 [Google Scholar]
  22. Brown JKM, Hovmøller MS, Wyand RA, Yu DZ. 22.  2002. Oases in the desert: dispersal and host specialization of biotrophic fungal pathogens of plants. Dispersal Ecology JM Bullock, RE Kenward, RS Hails 395–409 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  23. Brown JKM, O'Dell M, Simpson CG, Wolfe MS. 23.  1990. The use of DNA polymorphisms to test hypotheses about a population of Erysiphe graminis f.sp. hordei. Plant Pathol. 39:391–401 [Google Scholar]
  24. Brown JKM, Rant JC. 24.  2013. Fitness costs and trade-offs of disease resistance and their consequences for breeding arable crops. Plant Pathol. 62:Suppl. S183–95 [Google Scholar]
  25. Brown JKM, Simpson CG, Wolfe MS. 25.  1993. Adaptation of barley powdery mildew populations in England to varieties with two resistance genes. Plant Pathol. 42:108–15 [Google Scholar]
  26. Brown JKM, Tellier A. 26.  2011. Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu. Rev. Phytopathol. 49:345–67 [Google Scholar]
  27. Burdon JJ, Barrett LG, Rebetzke G, Thrall PH. 27.  2014. Guiding deployment of resistance in cereals using evolutionary principles. Evol. Appl. 7:609–24 [Google Scholar]
  28. Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M. 28.  et al. 1997. The barley mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705 [Google Scholar]
  29. Caffier V, Didelot F, Pumo B, Causeur D, Dureld CE, Parisi L. 29.  2010. Aggressiveness of eight Venturia inaequalis isolates virulent or avirulent to the major resistance gene Rvi6 on a non-Rvi6 apple cultivar. Plant Pathol. 59:1072–80 [Google Scholar]
  30. Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S. 30.  et al. 2011. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43:956–63 [Google Scholar]
  31. Champouret N, Bouwmeester K, Rietman H, van der Lee T, Maliepaard C. 31.  et al. 2009. Phytophthora infestans isolates lacking Class I ipiO variants are virulent on Rpi-blb1 potato. Mol. Plant-Microbe Interact. 22:1535–45 [Google Scholar]
  32. Chartrain L, Brading PA, Brown JKM. 32.  2005. Presence of the Stb6 gene for resistance to septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat-breeding programmes worldwide. Plant Pathol. 54:134–43 [Google Scholar]
  33. Cook DE, Bayless AM, Wang K, Guo XL, Song QJ. 33.  et al. 2014. Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiol. 165:630–47 [Google Scholar]
  34. Cook DE, Lee TG, Guo XL, Melito S, Wang K. 34.  et al. 2012. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–9 [Google Scholar]
  35. Cook LM, Grant BS, Saccheri IJ, Mallet J. 35.  2012. Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biol. Lett. 8:609–12 [Google Scholar]
  36. Costes E, Lauri PE, Simon S, Andrieu B. 36.  2013. Plant architecture, its diversity and manipulation in agronomic conditions, in relation with pest and pathogen attacks. Eur. J. Plant Pathol. 135:455–70 [Google Scholar]
  37. Crute IR, Holub EB, Burdon JJ. 37.  1997. The Gene-for-Gene Relationship Wallingford, UK: CABI
  38. Damgaard C. 38.  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 [Google Scholar]
  39. Dangl JL, Horvath DM, Staskawicz BJ. 39.  2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–51 [Google Scholar]
  40. Darwin C. 40.  1859. On the Origin of Species by Means of Natural Selection London, UK: John Murray
  41. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanama P. 41.  et al. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci USA 109:5110–15 [Google Scholar]
  42. Dyck PL, Samborski DJ. 42.  1982. The inheritance of resistance to Puccinia recondita in a group of common wheat cultivars. Can. J. Genet. Cytol. 24:273–83 [Google Scholar]
  43. Ellis JG, Lagudah WS, Spielmeyer W, Dodds PN. 43.  2014. The past, present and future of breeding rust-resistance wheat. Front. Plant Sci. 5:641 [Google Scholar]
  44. Finckh MR, Gacek ES, Goyeau H, Lannou C, Merz U. 44.  2000. Cereal variety and species mixtures in practice, with emphasis on disease resistance. Agronomie 20:813–37 [Google Scholar]
  45. Frank SA. 45.  1992. Models of plant pathogen coevolution. Trends Genet. 8:213–19 [Google Scholar]
  46. Frank SA. 46.  1993. Coevolutionary genetics of plants and pathogens. Evol. Ecol. 7:45–75 [Google Scholar]
  47. Fukuoka S, Yamamoto SI, Mizobuchi R, Yamanouchi U, Ono K. 47.  et al. 2014. Multiple functional polymorphisms in a single disease resistance gene in rice enhance durable resistance to blast. Sci. Rep. 4:4550 [Google Scholar]
  48. Glaszmann JC, Kilian B, Upadhyaya HD, Varshney RK. 48.  2010. Accessing genetic diversity for crop improvement. Curr. Opin. Plant Biol. 13:167–73 [Google Scholar]
  49. Glazebrook J. 49.  2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27 [Google Scholar]
  50. Green GJ. 50.  1975. Virulence changes in Puccinia graminis f. sp. tritici in Canada. Can. J. Bot. 53:1377–86 [Google Scholar]
  51. Hague RE. 51.  1998. Genetics of quantitative resistance to powdery mildew in Fenman winter wheat PhD Thesis, Univ. East Anglia, Norwich, UK
  52. Heil M, Hilpert A, Kaiser W, Linsenmair KE. 52.  2000. Reduced growth and seed set following chemical induction of pathogen defence: Does systemic acquired resistance (SAR) incur allocation costs?. J. Ecol. 88:645–54 [Google Scholar]
  53. 53. HGCA 2014. Barley Disease Management Guide E Boys, J Burgess Kenilworth, UK: HGCA Publ.
  54. 54. HGCA 2012. Wheat Brown Rust Management Topic Sheet 120 Kenilworth, UK: HGCA Publ.
  55. 55. HGCA 2014. Wheat Disease Management Guide E Boys, J Burgess Kenilworth, UK: HGCA Publ.
  56. Holub EB. 56.  2001. The arms race is ancient history in Arabidopsis, the wildflower. Nat. Rev. Genet. 2:516–27 [Google Scholar]
  57. Hovmøller MS, Justesen AF. 57.  2007. Rates of evolution of avirulence phenotypes and DNA markers in a northwest European population of Puccinia striiformis f. sp. tritici. Mol. Ecol. 16:4637–47 [Google Scholar]
  58. Hovmøller MS, Justesen AF, Brown JKM. 58.  2002. Clonality and long-distance migration of Puccinia striiformis f.sp. tritici in north-west Europe. Plant Pathol. 51:24–32 [Google Scholar]
  59. Howles P, Lawrence G, Finnegan J, McFadden H, Ayliffe M. 59.  et al. 2005. Autoactive alleles of the flax L6 rust resistance gene induce non-race-specific rust resistance associated with the hypersensitive response. Mol. Plant-Microbe Interact. 18:570–82 [Google Scholar]
  60. Hu G, Richter TE, Hulbert SH, Pryor T. 60.  1996. Disease lesion mimicry caused by mutations in the rust resistance gene Rp1. Plant Cell 8:1367–76 [Google Scholar]
  61. Huang R, Kranz J, Welz HG. 61.  1994. Selection of pathotypes of Erysiphe graminis f.sp. hordei in pure and mixed stands of spring barley. Plant Pathol. 43:458–70 [Google Scholar]
  62. Huang XH, Han B. 62.  2014. Natural variations and genome-wide association studies in crop plants. Annu. Rev. Plant Biol. 65:531–51 [Google Scholar]
  63. Huang XQ, Wolf M, Ganal MW, Orford S, Koebner RMD, Roder MS. 63.  2007. Did modern plant breeding lead to genetic erosion in European winter wheat varieties?. Crop Sci. 47:343–49 [Google Scholar]
  64. Huang YB, Thomson SJ, Hoffmann WC, Lan YB, Fritz BK. 64.  2013. Development and prospect of unmanned aerial vehicle technologies for agricultural production management. Int. J. Agric. Biol. Eng. 6:1–10 [Google Scholar]
  65. 65. Int. At. Energy Agency 2010. Mass Screening Techniques for Selecting Crops Resistant to Diseases. Vienna, Austria: IAEA Publ
  66. Jagger LJ, Newell C, Berry ST, MacCormack R, Boyd LA. 66.  2011. Histopathology provides a phenotype by which to characterize stripe rust resistance genes in wheat. Plant Pathol. 60:640–48 [Google Scholar]
  67. Jeger MJ. 67.  1997. An epidemiological approach to modeling the dynamics of gene-for-gene interactions. See Ref. 37 191–209
  68. Johnson R. 68.  1984. A critical analysis of durable resistance. Annu. Rev. Phytopathol. 22:309–30 [Google Scholar]
  69. Johnson R. 69.  1993. Durability of disease resistance in crops: some closing remarks about the topic and the symposium. Durability of Disease Resistance T Jacobs, JE Parlevliet 283–300 Dordrecht, Neth: Kluwer [Google Scholar]
  70. Jones JDG. 70.  2001. Putting knowledge of plant disease resistance genes to work. Curr. Opin. Plant Biol. 4:281–87 [Google Scholar]
  71. Jones JDG, Dangl JL. 71.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  72. Jørgensen JH. 72.  1992. Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63:141–52 [Google Scholar]
  73. Justesen AF, Ridout CJ, Hovmøller MS. 73.  2002. The recent history of Puccinia striiformis f.sp tritici in Denmark as revealed by disease incidence and AFLP markers. Plant Pathol. 51:13–23 [Google Scholar]
  74. Kjær B, Jensen HP, Jensen J, Jørgensen JH. 74.  1990. Associations between three ml-o powdery mildew resistance genes and agronomic traits in barley. Euphytica 46:185–93 [Google Scholar]
  75. Karasov TL, Horton MW, Bergelson J. 75.  2014. Genomic variability as a driver of plant–pathogen coevolution?. Curr. Opin. Plant Biol. 18:24–30 [Google Scholar]
  76. Karasov TL, Kniskern JM, Gao LP, DeYoung BJ, Ding J. 76.  et al. 2014. The long-term maintenance of a resistance polymorphism through diffuse interactions. Nature 512:436–40 [Google Scholar]
  77. Korves TM, Bergelson J. 77.  2003. A developmental response to pathogen infection in Arabidopsis. Plant Physiol. 133:339–47 [Google Scholar]
  78. Kou YJ, Wang SP. 78.  2010. Broad-spectrum and durability: understanding of quantitative disease resistance. Curr. Opin. Plant Biol. 13:181–85 [Google Scholar]
  79. Krattinger SG, Lagudah ES, Spielmayer W, Singh RP, Huerta-Espino J. 79.  et al. 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–63 [Google Scholar]
  80. Lagudah ES, Krattinger SG, Herrera-Foessel S, Singh RP, Huerta-Espino J. 80.  et al. 2009. Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor. Appl. Genet. 119:889–98 [Google Scholar]
  81. Lanfermeijer FC, Warmink J, Jacques Hille J. 81.  2005. The products of the broken Tm-2 and the durable Tm-22 resistance genes from tomato differ in four amino acids. J. Exp. Bot. 56:2925–33 [Google Scholar]
  82. Laine AL, Barrès B. 82.  2013. Epidemiological and evolutionary consequences of life-history trade-offs in pathogens. Plant Pathol. 62:Suppl. S196–105 [Google Scholar]
  83. Laine AL, Burdon JJ, Nemri A, Thrall PH. 83.  2014. Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation. Proc. R. Soc. B 281:pii:20140522 [Google Scholar]
  84. Lannou C. 84.  2012. Variation and selection of quantitative traits in plant pathogens. Annu. Rev. Phytopathol. 50:319–38 [Google Scholar]
  85. Leach JE, Cruz CMV, Bai JF, Leung H. 85.  2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 39:187–224 [Google Scholar]
  86. Leonard KJ. 86.  1977. Selection pressures and plant pathogens. Ann. N. Y. Acad. Sci. 287:207–22 [Google Scholar]
  87. Li X, Clarke JD, Zhang YL, Dong XN. 87.  2001. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol. Plant-Microbe Interact. 14:1131–39 [Google Scholar]
  88. Li Y, van der Lee TAJ, Evenhuis A, van den Bosch GBM, van Bekkum PJ. 88.  et al. 2012. Population dynamics of Phytophthora infestans in the Netherlands reveals expansion and spread of dominant clonal lineages and virulence in sexual offspring. Genes Genomes Genet. 2:1529–40 [Google Scholar]
  89. Li ZF, Lan CX, He ZH, Singh RP, Rosewarne GM. 89.  et al. 2014. Overview and application of QTL for adult plant resistance to leaf rust and powdery mildew in wheat. Crop Sci. 54:1907–25 [Google Scholar]
  90. Li ZK, Sanchez A, Angeles E, Singh S, Domingo J. 90.  et al. 2001. Are the dominant and recessive plant disease resistance genes similar? A case study of rice R genes and Xanthomonas oryzae pv. oryzae races. Genetics 159:757–65 [Google Scholar]
  91. Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M. 91.  et al. 2012. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:659–62 [Google Scholar]
  92. Markell SG, Milus EA. 92.  2008. Emergence of a novel population of Puccinia striiformis f.sp. tritici in eastern United States. Phytopathology 98:632–39 [Google Scholar]
  93. McDonald BA, Linde C. 93.  2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349–79 [Google Scholar]
  94. McGrann GRD, Stavrinides A, Russell J, Corbitt MM, Booth A. 94.  et al. 2014. A trade-off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot. J. Exp. Bot. 65:1025–37 [Google Scholar]
  95. McGrann GRD, Steed A, Burt C, Nicholson P, Brown JKM. 95.  2015. Differential effects of lesion mimic mutants in barley on disease development by facultative pathogens. J. Exp. Bot. In press. doi: 10.1093/jxb/erv154
  96. Michelmore RW, Christopoulou M, Caldwell KS. 96.  2013. Impacts of resistance gene genetics, function, and evolution on a durable future. Annu. Rev. Phytopathol. 51:291–319 [Google Scholar]
  97. Montarry J, Hamelin FM, Glais I, Corbière R, Andrivon D. 97.  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 [Google Scholar]
  98. Mundt CC. 98.  1990. Probability of mutation to multiple virulence and durability of resistance gene pyramids. Phytopathology 80:221–23 [Google Scholar]
  99. Mundt CC. 99.  1991. Probability of mutation to multiple virulence and durability of resistance gene pyramids: further comments. Phytopathology 81:240–42 [Google Scholar]
  100. Mundt CC. 100.  2002. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40:381–410 [Google Scholar]
  101. Mundt CC. 101.  2014. Durable resistance: a key to sustainable management of pathogens and pests. Infect. Genet. Evol. 27:446–55 [Google Scholar]
  102. Negassa M. 102.  1985. Geographic distribution and genotypic diversity of resistance to powdery mildew of barley in Ethiopia. Hereditas 102:113–21 [Google Scholar]
  103. Niks RE, Qi X, Marcel TC. 103.  2015. Quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions and mechanisms. Annu. Rev. Phytopathol. 53445–70
  104. Oliver RP, Friesen TL, Faris JD, Solomon PS. 104.  2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annu. Rev. Phytopathol. 50:23–43 [Google Scholar]
  105. Palloix A, Ayme V, Moury B. 105.  2009. Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol. 183:190–99 [Google Scholar]
  106. Pariaud Ravigné V, Halkett F, Goyeau H, Carlier J, Lannou C. 106.  2009. Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathol. 58:409–24 [Google Scholar]
  107. Park RF. 107.  2008. Breeding cereals for rust resistance in Australia. Plant Pathol. 57:591–602 [Google Scholar]
  108. Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D'Hont A. 108.  et al. 2004. A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430:887–91 [Google Scholar]
  109. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. 109.  2008. Shades of gray: the world of quantitative disease resistance. Trends Plant Sci. 14:21–29 [Google Scholar]
  110. Quenouille J, Montarry J, Palloix A, Moury B. 110.  2013. Farther, slower, stronger: how the plant genetic background protects a major resistance gene from breakdown. Mol. Plant Pathol. 14:109–18 [Google Scholar]
  111. Rajaram S, Singh RP, Torres E. 111.  1988. Current CIMMYT approaches in breeding wheat for rust resistance. Breeding Strategies for Resistance to the Rusts of Wheat NW Simmonds, S Rajaram 101–18 Mexico City, Mex: CIMMYT [Google Scholar]
  112. Risk JM, Selter LL, Chauhan H, Krattinger SG, Kumlehn J. 112.  et al. 2013. The wheat Lr34 gene provides resistance against multiple fungal pathogens in barley. Plant Biotechnol. J. 11:847–54 [Google Scholar]
  113. Robert-Seilaniantz A, Grant M, Jones JDG. 113.  2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49:317–43 [Google Scholar]
  114. Ruiz-Lozano JM, Gianinazzi S, Gianinazzi-Pearson V. 114.  1999. Genes involved in resistance to powdery mildew in barley differentially modulate root colonization by the mycorrhizal fungus Glomus mossae. Mycorrhiza 9:237–40 [Google Scholar]
  115. 115. St. Clair DA 2010. Quantitative disease resistance and quantitative resistance loci in breeding. Annu. Rev. Phytopathol. 48:247–68 [Google Scholar]
  116. Saville RJ, Gosman N, Burt CJ, Makepeace J, Steed A. 116.  et al. 2012. The “Green Revolution” dwarfing genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare. J. Exp. Bot. 63:1271–83 [Google Scholar]
  117. Schafer JF, Roelfs AP. 117.  1985. Estimated relation between numbers of urediniospores of Puccinia graminis f.sp. tritici and rates of occurrence of virulence. Phytopathology 75:749–50 [Google Scholar]
  118. Schwarzbach E. 118.  1979. Response to selection for virulence against the ml-o based mildew resistance in barley, not fitting the gene-for-gene hypothesis. Barley Genet. Newsl. 9:85–88 [Google Scholar]
  119. Schwarzbach E, Slater SE, Clarkson JDS. 119.  2002. Occurrence of partially mlo-virulent isolates of barley powdery mildew in agricultural environments in Europe. Cereal Rusts Powdery Mildews Bull., Eur. Mediterr. Cereal Rusts Found., Neth. http://www.crpmb.org/2002/0208schwarzbach/
  120. Scott PR, Benedikz PW. 120.  1977. Field techniques for assessing reaction of winter wheat cultivars to Septoria nodorum. Ann. Appl. Biol. 85:345–58 [Google Scholar]
  121. Simmonds NW. 121.  1988. Synthesis: the strategy of rust resistance breeding. Breeding Strategies for Resistance to the Rusts of Wheat NW Simmonds, S Rajaram 119–36 Mexico City, Mex.: CIMMYT [Google Scholar]
  122. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S. 122.  et al. 2011. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 49:465–81 [Google Scholar]
  123. Smithson JB, Lenne JM. 123.  1996. Varietal mixtures: a viable strategy for sustainable productivity in subsistence agriculture. Ann. Appl. Biol. 128:127–58 [Google Scholar]
  124. Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM. 124.  et al. 2003. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl. Acad Sci. USA 100:9128–33 [Google Scholar]
  125. Stukenbrock EH, McDonald BA. 125.  2008. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46:75–100 [Google Scholar]
  126. Stuthman DD, Leonard KJ, Miller-Garvin J. 126.  2007. Breeding crops for durable resistance to disease. Adv. Agron. 95:319–67 [Google Scholar]
  127. Summers RW, Brown JKM. 127.  2013. Constraints on breeding for disease resistance in commercially competitive wheat cultivars. Plant Pathol. 62:Suppl. S1115–21 [Google Scholar]
  128. Tack AJM, Thrall PH, Barrett LG, Burdon JJ, Laine AL. 128.  2012. Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences. J. Evol. Biol. 25:1918–36 [Google Scholar]
  129. Tellier A, Brown JKM. 129.  2007. Polymorphism in multilocus host-parasite coevolutionary interactions. Genetics 177:1777–90 [Google Scholar]
  130. Tellier A, Brown JKM. 130.  2007. Stability of genetic polymorphism in host-parasite interactions. Proc. R. Soc. B 274:809–17 [Google Scholar]
  131. Tellier A, Brown JKM. 131.  2008. The relationship of host-mediated induced resistance to polymorphism in gene-for-gene relationships. Phytopathology 98:128–36 [Google Scholar]
  132. Tellier A, Brown JKM. 132.  2009. The influence of perenniality and seed banks on polymorphism in plant-parasite interactions. Am. Nat. 174:769–79 [Google Scholar]
  133. Tellier A, Brown JKM. 133.  2011. Spatial heterogeneity, frequency-dependent selection and polymorphism in host-parasite interactions. BMC Evol. Biol. 11:319 [Google Scholar]
  134. Tellier A, Moreno-Gamez S, Stephan W. 134.  2014. Speed of adaptation and genomic footprints of host-parasite coevolution under arms race and trench warfare dynamics. Evolution 68:2211–24 [Google Scholar]
  135. Thrall PH, Burdon JJ. 135.  2002. Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathol. 51:169–84 [Google Scholar]
  136. Thrall PH, Burdon JJ. 136.  2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735–37 [Google Scholar]
  137. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J. 137.  2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77 [Google Scholar]
  138. Torriani SFF, Melichar JPE, Mills C, Pain N, Sierotzki H, Courbot M. 138.  2015. Zymoseptoria tritici: a major threat to wheat production, integrated approaches to control. Fung. Genet. Biol. In press. doi: 10.1016/j.fgb.2015.04.010
  139. van der Vossen E, Sikkema A, te Lintel Hekkert B, Gros J, Stevens P. 139.  et al. 2003. An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 36:867–82 [Google Scholar]
  140. van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J. 140.  2006. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 103:5602–7 [Google Scholar]
  141. Vera Cruz CM, Bai JF, Ona I, Leung H, Nelson RJ. 141.  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 [Google Scholar]
  142. Visser B, Herselman L, Park RF, Karaoglu H, Bender CM, Pretorius ZA. 142.  2011. Characterization of two new Puccinia graminis f.sp. tritici races within the Ug99 lineage in South Africa. Euphytica 179:119–27 [Google Scholar]
  143. Vleeshouwers VGAA, Oliver RP. 143.  2014. Effectors as tools in disease resistance breeding. Mol. Plant-Microbe Interact. 27:196–206 [Google Scholar]
  144. Vleeshouwers VGAA, Raffaele S, Vossen J, Champouret N, Oliva R. 144.  et al. 2011. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49:507–31 [Google Scholar]
  145. Vos IA, Pieterse CMJ, van Wees. 145.  2013. Costs and benefits of hormone- regulated plant defences. Plant Pathol. 62:Suppl. S143–55 [Google Scholar]
  146. Wang Q, Liu YQ, He J, Zheng XM, Hu JL. 146.  2014. STV11 encodes a sulphotransferase and confers durable resistance to rice stripe virus. Nat. Commun. 5:4768 [Google Scholar]
  147. Wang YP, Cheng X, Shan QW, Zhang Y, Liu JX. 147.  et al. 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32:947–51 [Google Scholar]
  148. Webb KM, Oña I, Bai J, Garrett KA, Mew T. 148.  2010. A benefit of high temperature: increased effectiveness of a rice bacterial blight disease resistance gene. New Phytol. 185:568–76 [Google Scholar]
  149. Wichmann G, Bergelson J. 149.  2004. Effector genes of Xanthamonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genetics 166:693–706 [Google Scholar]
  150. Wilson AD. 150.  2013. Diverse applications of electronic nose technologies in agriculture and forestry. Sensors 13:2295–348 [Google Scholar]
  151. Wingen LU, Shaw MW, Brown JKM. 151.  2013. Long-distance dispersal and its influence on adaptation to host resistance in a heterogeneous landscape. Plant Pathol. 62:9–20 [Google Scholar]
  152. Wolfe MS. 152.  1984. Trying to understand and control powdery mildew. Plant Pathol. 33:451–66 [Google Scholar]
  153. Wolfe MS. 153.  1985. The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Annu. Rev. Phytopathol. 23:251–73 [Google Scholar]
  154. Wulff BBH, Horvath DM, Ward ER. 154.  2011. Improving immunity in crops: new tactics in an old game. Curr. Opin. Plant Biol. 14:468–76 [Google Scholar]
  155. Wulff BBH, Kruijt M, Collins PL, Thomas CM, Ludwig AA. 155.  et al. 2004. Gene shuffling–generated and natural variants of the tomato resistance gene Cf-9 exhibit different auto-necrosis-inducing activities in Nicotiana species. Plant J. 40:942–56 [Google Scholar]
  156. Yang B, Sugio A, White FF. 156.  2005. Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a Type III effector of Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 18:142–49 [Google Scholar]
  157. Yu DZ, Yang XJ, Yang LJ, Jeger MJ, Brown JKM. 157.  2001. Assessment of partial resistance to powdery mildew in Chinese wheat varieties. Plant Breed. 120:279–84 [Google Scholar]
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