Identification and Implementation of Resistance: Genomics-Assisted use of Genetic Resources for Breeding Against Powdery Mildew and Stagonospora Nodorum Blotch in Wheat

  • Liselotte L. Selter
  • Margarita Shatalina
  • Jyoti Singla
  • Beat Keller


Wheat belongs to the three most important cereal crops of the world and is grown under a wide variety of climatic and agricultural conditions. Fungal pathogens represent the most relevant biotic stresses for wheat. These include different rust species, powdery mildew, leaf spots, as well as a number of other diseases that result in reduced grain yield and quality. Recently developed genomic tools allow new approaches to improve breeding for resistance to these pathogens based on a more efficient use of genetic resources. In this chapter, we will focus on the powdery mildew and Stagonospora nodorum blotch diseases and discuss the successful identification of wheat genes determining the outcome of pathogen-host interaction and the development of perfect markers for them. Genomic approaches, including gene cloning, allele mining, transcriptomics and comparative genomics have greatly changed and improved our understanding of molecular wheat-powdery mildew interactions. For the necrotrophic pathogen Stagonospora nodorum much of the interaction was found to be based on pathogen toxins and host susceptibility genes. The work on specific gene-for-gene interactions opened new possibilities for more efficient resistance breeding. In addition, the molecular identification of quantitatively acting resistance loci in wheat has made important progress, although only few such genes have been cloned, only one of them each against mildew and Stagonospora nodorum blotch. However, even at this early stage it can be foreseen that the new knowledge might revolutionize breeding for durable resistance in the near future. The progress made towards a whole genome sequence of wheat together with ongoing developments of high throughput techniques provides a completely new perspective on resistance breeding against these two diseases.


Quantitative Trait Locus Powdery Mildew Powdery Mildew Resistance Adult Plant Resistance Powdery Mildew Resistance Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abeysekara NS, Friesen TL, Keller B, Faris JD (2009) Identification and characterization of a novel host-toxin interaction in the wheat-Stagonospora nodorum pathosystem. Theor Appl Genet 120:117–126PubMedCrossRefGoogle Scholar
  2. Anderson PK, Cunningham AA, Patel NG et al (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544PubMedCrossRefGoogle Scholar
  3. Arraiano LS, Balaam N, Fenwick PM et al (2009) Contributions of disease resistance and escape to the control of septoria tritici blotch of wheat. Plant Pathol 58:910–922CrossRefGoogle Scholar
  4. Ayala L, Henry M, van Ginkel M et al (2002) Identification of QTLs for BYDV tolerance in bread wheat. Euphytica 128:249–259CrossRefGoogle Scholar
  5. Balter M (2007) Seeking agriculture’s ancient roots. Science 316:1830–1835PubMedCrossRefGoogle Scholar
  6. Bearchell SJ, Fraaije BA, Shaw MW, Fitt BDL (2005) Wheat archive links long-term fungal pathogen population dynamics to air pollution. Proc Natl Acad Sci 102:5438–5442PubMedCrossRefGoogle Scholar
  7. Berry PM, Dawson TP, Harrison PA, Pearson RG (2002) Modelling potential impacts of climate change on the bioclimatic envelope of species in Britain and Ireland. Global Ecol Biogeogr 11:453–462CrossRefGoogle Scholar
  8. Bhullar NK, Street K, Mackay M et al (2009) Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus. Proc Natl Acad Sci 106:9519–9524PubMedCrossRefGoogle Scholar
  9. Bhullar NK, Zhang ZQ, Wicker T, Keller B (2010) Wheat gene bank accessions as a source of new alleles of the powdery mildew resistance gene Pm3: a large scale allele mining project. BMC Plant Biol 10:88PubMedCentralPubMedCrossRefGoogle Scholar
  10. Bostwick DE, Ohm HW, Shaner G (1993) Inheritance of septoria-glume blotch resistance in wheat. Crop Sci 33:439–443CrossRefGoogle Scholar
  11. Bougot Y, Lemoine J, Pavoine MT et al (2002) Identification of microsatellite marker associated with Pm3 resistance alleles to powdery in wheat. Plant Breed 121:325–329CrossRefGoogle Scholar
  12. Bougot Y, Lemoine J, Pavoine MT et al (2006) A major QTL effect controlling resistance to powdery mildew in winter wheat at the adult plant stage. Plant Breed 125:550–556CrossRefGoogle Scholar
  13. Brown JKM, Tellier A (2011) Plant-Parasite Coevolution: Bridging the Gap between Genetics and Ecology. Ann Rev Phytopathol 49:345–367CrossRefGoogle Scholar
  14. Brunner S, Hurni S, Streckeisen P et al (2010) Intragenic allele pyramiding combines different specificities of wheat Pm3 resistance alleles. Plant J 64:433–445PubMedCrossRefGoogle Scholar
  15. Brunner S, Hurni S, Herren G et al (2011) Transgenic Pm3b wheat lines show resistance to powdery mildew in the field. Plant Biotech J 9:897–910CrossRefGoogle Scholar
  16. Brunner S, Stirnweis D, Quijano CD et al (2012) Transgenic Pm3 multilines of wheat show increased powdery mildew resistance in the field. Plant Biotech J 10:398–409CrossRefGoogle Scholar
  17. Burger JC, Chapman MA, Burke JM (2008) Molecular insights into the evolution of crop plants. Am J Bot 95:13–122CrossRefGoogle Scholar
  18. Cannon RJC (1998) The implications of predicted climate change for insect pests in the UK, with emphasis on non-indigenous species. Glob Change Biol 4:785–796CrossRefGoogle Scholar
  19. Cao AH, Xing LP, Wang XY et al (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc Natl Acad Sci 108:7727–7732PubMedCrossRefGoogle Scholar
  20. Chakraborty S, Tiedemann AV, Teng PS (2000) Climate change: potential impact on plant diseases. Environ Pollut 108:317–326PubMedCrossRefGoogle Scholar
  21. Chantret N, Mingeot D, Sourdille P et al (2001) A major QTL for powdery mildew resistance is stable over time and at two development stages in winter wheat. Theor Appl Genet 103:962–971CrossRefGoogle Scholar
  22. Charmet G (2011) Wheat domestication: Lessons for the future. C R Biol 334:212–220PubMedCrossRefGoogle Scholar
  23. Ciuffetti LM, Tuori RP, Gaventa JM (1997) A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9:135–144PubMedCentralPubMedGoogle Scholar
  24. Cloutier S, McCallum BD, Loutre C et al (2007) Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol 65:93–106PubMedCrossRefGoogle Scholar
  25. Czembor PC, Arseniuk E, Czaplicki A et al (2003) QTL mapping of partial resistance in winter wheat to Stagonospora nodorum blotch. Genome 46:546–554PubMedCrossRefGoogle Scholar
  26. Dodds PN, Lawrence GJ, Catanzariti AM et al (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci 103:8888–8893PubMedCrossRefGoogle Scholar
  27. Douchkov D, Nowara D, Zierold U, Schweizer P (2005) A high-throughput gene-silencing system for the functional assessment of defense-related genes in barley epidermal cells. Mol Plant Microbe Int 18:755–761CrossRefGoogle Scholar
  28. Du CC, Nelson LR, McDaniel ME (1999) Diallel analysis of gene effects conditioning resistance to Stagonospora nodorum (Berk.) in wheat. Crop Sci 39:686–690CrossRefGoogle Scholar
  29. Duveiller E, Singh RP, Nicol JM (2007) The challenges of maintaining wheat productivity: pests, diseases, and potential epidemics. Euphytica 157:417–430CrossRefGoogle Scholar
  30. Dyck PL (1987) The association of a gene for leaf rust resistance with the chromosome—7d suppressor of stem rust resistance in common wheat. Genome 29:467–469CrossRefGoogle Scholar
  31. Dyck PL (1991) Genetics of adult-plant leaf rust resistance in Chinese Spring and sturdy wheats. Crop Sci 31:309–311CrossRefGoogle Scholar
  32. Dyck PL, Samborskj D, Anderson RG (1966) Inheritance of adult-plant leaf rust resistance derived from common wheat varieties Exchange and Frontana. Can J Genet Cytol 8:665–671Google Scholar
  33. Endresen DTF, Street K, Mackay M et al (2011) Predictive association between biotic stress traits and eco-geographic data for wheat and barley landraces. Crop Sci 51:2036–2055CrossRefGoogle Scholar
  34. Faris JD, Friesen TL (2009) Reevaluation of a tetraploid wheat population indicates that the Tsn1-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility. Phytopathol 99:906–912CrossRefGoogle Scholar
  35. Faris JD, Zhang Z, Lu H et al (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci 107:13544–13549PubMedCrossRefGoogle Scholar
  36. Feuillet C, Travella S, Stein N et al (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci 100:15253–15258PubMedCrossRefGoogle Scholar
  37. Flor HH (1955) Host-parasite interaction in flax rust—its genetics and other implications. Phytopathol 45:680–685Google Scholar
  38. Francki MG, Shankar M, Walker E et al (2011) New quantitative trait loci in wheat for flag leaf resistance to Stagonospora nodorum blotch. Phytopathol 101:1278–1284CrossRefGoogle Scholar
  39. Fried PM, Meister E (1987) Inheritance of leaf and head resistance of winter-wheat to Septoria-nodorum in a diallel cross. Phytopathol 77:1371–1375CrossRefGoogle Scholar
  40. Friesen TL, Stukenbrock EH, Liu Z et al (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genet 38:953–956PubMedCrossRefGoogle Scholar
  41. Friesen TL, Meinhardt SW, Faris JD (2007) The Stagonospora nodorum-wheat pathosystem involves multiple proteinaceous host-selective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner. Plant J 51:681–692PubMedCrossRefGoogle Scholar
  42. Fu DL, Uauy C, Distelfeld A et al (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–1360PubMedCrossRefGoogle Scholar
  43. Ge YF, Johnson JW, Roberts JJ, Rajaram S (1998) Temperature and resistance gene interactions in the expression of resistance to Blumeria graminis f. sp. tritici. Euphytica 99:103–109CrossRefGoogle Scholar
  44. Griffey CA, Das MK (1994) Inheritance of adult-plant resistance to powdery mildew in Knox—62 and Massey winter wheats. Crop Sci 34:641–646CrossRefGoogle Scholar
  45. Hane JK, Lowe RGT, Solomon PS et al (2007) Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19:3347–3368PubMedCentralPubMedCrossRefGoogle Scholar
  46. Hartl L, Weiss H, Zeller FJ et al (1993) Use of RFLP markers for the identification of alleles of the Pm3 locus conferring powdery mildew resistance in wheat (Triticum aestivum L.). Theor Appl Genet 86:959–963PubMedCrossRefGoogle Scholar
  47. He R, Chang Z, Yang Z et al (2009) Inheritance and mapping of powdery mildew resistance gene Pm43 introgressed from Thinopyrum intermedium into wheat. Theor Appl Genet 118:1173–1180PubMedCrossRefGoogle Scholar
  48. Heun M, Friebe B, Bushuk W (1990) Chromosomal location of the powdery mildew resistance gene of Amigo wheat. Phytopathol 80:1129–1133CrossRefGoogle Scholar
  49. Horbach R, Navarro-Quesada AR, Knogge W, Deising HB (2011) When and how to kill a plant cell: Infection strategies of plant pathogenic fungi. J Plant Physiol 168:51–62PubMedCrossRefGoogle Scholar
  50. Hua W, Liu Z, Zhu J et al (2009) Identification and genetic mapping of Pm42, a new recessive wheat powdery mildew resistance gene derived from wild emmer (Triticum turgidum var. dicoccoides). Theor Appl Genet 119:223–230PubMedCrossRefGoogle Scholar
  51. Huang L, Brooks SA, Li WL et al (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics 164:655–664PubMedGoogle Scholar
  52. Huang J, Zhao Z, Song F, Wang X et al (2012) Molecular detection of a gene effective against powdery mildew in the wheat cultivar Liangxing 66. Mol Breeding 30:1737–1745Google Scholar
  53. Kaur N, Street K, Mackay M et al (2008) Molecular approaches for characterization and use of natural disease resistance in wheat. Europ J Plant Pathol 121:387–397CrossRefGoogle Scholar
  54. Keller M, Keller B, Schachermayr G et al (1999) Quantitative trait loci for resistance against powdery mildew in a segregating wheat x spelt population. Theor Appl Genet 98:903–912CrossRefGoogle Scholar
  55. Kleijer G, Bronnimann A, Fossati A (1977) Chromosomal location of a dominant gene for resistance at seedling stage to Septoria-nodorum berk in wheat variety Atlas—66. J Plant Breed 78:170–173Google Scholar
  56. Koltin Y, Kenneth R (1970) Role of sexual stage in over-summering of Erysiphe-graminis dc fsp hordei marchal under semi-arid conditions. Ann Appl Biol 65:263–268CrossRefGoogle Scholar
  57. Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185PubMedCrossRefGoogle Scholar
  58. Krattinger SG, Lagudah ES, Spielmeyer W et al (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363PubMedCrossRefGoogle Scholar
  59. Kumar GR, Sakthivel K, Sundaram RM et al (2010) Allele mining in crops: Prospects and potentials. Biotech Adv 28:451–461CrossRefGoogle Scholar
  60. Lan C, Liang S, Wang Z et al (2009) Quantitative trait loci mapping for adult-plant resistance to powdery mildew in Chinese wheat cultivar Bainong 64. Phytopathol 99:1121–1126CrossRefGoogle Scholar
  61. Liang SS, Suenaga K, He ZH et al (2006) Quantitative trait loci mapping for adult-plant resistance to powdery mildew in bread wheat. Phytopathol 96:784–789CrossRefGoogle Scholar
  62. Lillemo M, Singh RP, Huerta-Espino J et al (2007) Leaf rust resistance gene LR34 is involved in powdery mildew resistance of CIMMYT bread wheat line Saar. Wheat Production in Stressed Environments 12:97–102CrossRefGoogle Scholar
  63. Lillemo M, Asalf B, Singh RP et al (2008) The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theor Appl Genet 116:1155–1166PubMedCrossRefGoogle Scholar
  64. Liu Z, Friesen TL, Ling H et al (2006) The Tsn1-ToxA interaction in the wheat-Stagonospora nodorum pathosystem parallels that of the wheat-tan spot system. Genome 49:1265–1273PubMedCrossRefGoogle Scholar
  65. Liu Z, Zhang Z, Faris JD et al (2012) The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathog 8:e1002467PubMedCentralPubMedCrossRefGoogle Scholar
  66. Liu ZH, Faris JD, Meinhardt SW et al (2004a) Genetic and physical mapping of a gene conditioning sensitivity in wheat to a partially purified host-selective toxin produced by Stagonospora nodorum. Phytopathol 94:1056–1060CrossRefGoogle Scholar
  67. Liu ZH, Friesen TL, Rasmussen JB et al (2004b) Quantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat. Phytopathol 94:1061–1067CrossRefGoogle Scholar
  68. Lorang JM, Sweat TA, Wolpert TJ (2007) Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci 104:14861–14866PubMedCrossRefGoogle Scholar
  69. Luck J, Spackman M, Freeman A et al (2011) Climate change and diseases of food crops. Plant Pathol 60:113–121CrossRefGoogle Scholar
  70. Luo PG, Luo HY, Chang ZJ et al (2009) Characterization and chromosomal location of Pm40 in common wheat: a new gene for resistance to powdery mildew derived from Elytrigia intermedium. Theor Appl Genet 118:1059–1064PubMedCrossRefGoogle Scholar
  71. Ma H, Hughes GR (1995) Genetic-control and chromosomal location of Triticum timopheevii-derived resistance to Septoria nodorum blotch in durum-wheat. Genome 38:332–338PubMedCrossRefGoogle Scholar
  72. Ma ZQ, Sorrells ME, Tanksley SD (1994) RFLP markers linked to powdery mildew resistance gene Pm1, Pm2, Pm3 and Pm4 in wheat. Genome 37:871–875PubMedCrossRefGoogle Scholar
  73. McCouch SR, Sweeney M, Li JM et al (2007) Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa. Euphytica 154:317–339CrossRefGoogle Scholar
  74. McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA (2013) Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol doi: 10.1111/nph.12257Google Scholar
  75. McIntosh RA (1992) Close genetic-linkage of genes conferring adult-plant resistance to leaf rust and stripe rust in wheat. Plant Pathol 41:523–527CrossRefGoogle Scholar
  76. Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 7:352–356PubMedCrossRefGoogle Scholar
  77. Mengiste T (2012) Plant immunity to necrotrophs. Ann Rev Phytopathol 50:267–294CrossRefGoogle Scholar
  78. Mingeot D, Chantret N, Baret PV et al (2002) Mapping QTL involved in adult plant resistance to powdery mildew in the winter wheat line RE714 in two susceptible genetic backgrounds. Plant Breed 121:133–140CrossRefGoogle Scholar
  79. Mundt CC (2002) Use of multiline cultivars and cultivar mixtures for disease management. Ann Rev Phytopathol 40:381–410CrossRefGoogle Scholar
  80. Murphy NEA, Loughman R, Wilson R et al (2000) Resistance to septoria nodorum blotch in the Aegilops tauschii accession RL5271 is controlled by a single gene. Euphytica 113:227–233CrossRefGoogle Scholar
  81. Nagy ED, Lee T-C, Ramakrishna W et al (2007) Fine mapping of the Pc locus of Sorghum bicolor, a gene controlling the reaction to a fungal pathogen and its host-selective toxin. Theor Appl Genet 114:961–970PubMedCrossRefGoogle Scholar
  82. Newton AC, Johnson SN, Gregory PJ (2011) Implications of climate change for diseases, crop yields and food security. Euphytica 179:3–18CrossRefGoogle Scholar
  83. Oberhaensli S, Parlange F, Buchmann JP et al (2011) Comparative sequence analysis of wheat and barley powdery mildew fungi reveals gene colinearity, dates divergence and indicates host-pathogen co-evolution. Fung Genet Biol 48:327–334CrossRefGoogle Scholar
  84. Oerke EC, Dehne HW, Schoenbeck F, Weber A (1994) Crop production and crop protection: Estimated losses in major food and cash crops. Elsevier Science Publishers, AmsterdamGoogle Scholar
  85. Olesen JE, Mortensen JV, Jorgensen LN, Andersen MN (2000) Irrigation strategy, nitrogen application and fungicide control in winter wheat on a sandy soil. I. Yield, yield components and nitrogen uptake. J Agricult Sci 134:1–11CrossRefGoogle Scholar
  86. Oliver RP, Solomon PS (2010) New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol 13:415–419PubMedCrossRefGoogle Scholar
  87. Oliver RP, Friesen TL, Faris JD, Solomon PS (2012) Stagonospora nodorum: From Pathology to Genomics and Host Resistance. Ann Rev Phytopathol 50:23–43CrossRefGoogle Scholar
  88. Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6:320–326PubMedCrossRefGoogle Scholar
  89. Peng JH, Sun D, Nevo E (2011) Domestication evolution, genetics and genomics in wheat. Molecular Breed 28:281–301CrossRefGoogle Scholar
  90. Perfect SE, Green JR (2001) Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2:101–108PubMedCrossRefGoogle Scholar
  91. Pimentel D, McNair S, Janecka J et al (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agr Ecosyst Environ 84:1–20CrossRefGoogle Scholar
  92. Qiu JW, Schurch AC, Yahiaoui N et al (2007) Physical mapping and identification of a candidate for the leaf rust resistance gene Lr1 of wheat. Theor Appl Genet 115:159–168PubMedCrossRefGoogle Scholar
  93. Schnurbusch T, Paillard S, Fossati D et al (2003) Detection of QTLs for Stagonospora glume blotch resistance in Swiss winter wheat. Theor App Genet 107:1226–1234CrossRefGoogle Scholar
  94. Schweizer P, Pokorny J, Abderhalden O, Dudler R (1999) A transient assay system for the functional assessment of defense-related genes in wheat. Mol Plant Microbe Int 12:647–654CrossRefGoogle Scholar
  95. Scott PR, Benedikz PW, Cox CJ (1982) A genetic-study of the relationship between height, time of ear emergence and resistance to Septoria-nodorum in wheat. Plant Pathol 31:45–60CrossRefGoogle Scholar
  96. Shaner G (1973) Evaluation of slow-mildewing resistance of Knox wheat in field. Phytopathol 63:867–872CrossRefGoogle Scholar
  97. Sharma AK, Sharma RK, Babu KS (2004) Effect of planting options and irrigation schedules on development of powdery mildew and yield of wheat in the North Western plains of India. Crop Prot 23:249–253CrossRefGoogle Scholar
  98. Sharma S, Khan TA, Ashraf MS (2011) Studies on powdery mildew disease of mulberry (Morus alba): a new report from Uttar Pradesh, India. Archives of Phytopathology and Plant Protection 44:105–112Google Scholar
  99. Shaw MW, Bearchell SJ, Fitt BDL, Fraaije BA (2008) Long-term relationships between environment and abundance in wheat of Phaeosphaeria nodorum and Mycosphaerella graminicola. New Phytol 177:229–238PubMedGoogle Scholar
  100. Singh RP (1992) Association between gene Lr34 for leaf rust resistance and leaf tip necrosis in wheat. Crop Sci 32:874–878CrossRefGoogle Scholar
  101. Spanu PD, Abbott JC, Amselem J et al (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–1546PubMedCrossRefGoogle Scholar
  102. Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005) Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theor Appl Genet 111:731–735PubMedCrossRefGoogle Scholar
  103. Srichumpa P, Brunner S, Keller B, Yahiaoui N (2005) Allelic series of four powdery mildew resistance genes at the Pm3 locus in hexaploid bread wheat. Plant Physiol 139:885–895PubMedCentralPubMedCrossRefGoogle Scholar
  104. Stukenbrock EH, McDonald BA (2007) Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Mol Plant Pathol 8:321–332PubMedCrossRefGoogle Scholar
  105. Stukenbrock EH, Banke S, McDonald BA (2006) Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Mol Ecol 15:2895–2904PubMedCrossRefGoogle Scholar
  106. Tan K-C, Ferguson-Hunt M, Rybak K et al (2012) Quantitative variation in effector activity of ToxA isoforms from Stagonospora nodorum and Pyrenophora tritici-repentis. Mol Plant Microbe Int 25:515–522CrossRefGoogle Scholar
  107. Tommasini L, Yahiaoui N, Srichumpa P, Keller B (2006) Development of functional markers specific for seven Pm3 resistance alleles and their validation in the bread wheat gene pool. Theor Appl Genet 114:165–175Google Scholar
  108. Tucker DM, Griffey CA, Liu S et al (2007) Confirmation of three quantitative trait loci conferring adult plant resistance to powdery mildew in two winter wheat populations. Euphytica 155:1–13CrossRefGoogle Scholar
  109. Varshney RK, Nayak SN, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530PubMedCrossRefGoogle Scholar
  110. Waters ODC, Lichtenzveig J, Rybak K et al (2011) Prevalence and importance of sensitivity to the Stagonospora nodorum necrotrophic effector SnTox3 in current Western Australian wheat cultivars. Crop Pasture Science 62:556–562CrossRefGoogle Scholar
  111. Wicker T, Oberhaensli S, Parlange F et al (2013) The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat Genet 45:1092–1096Google Scholar
  112. Wicker T, Yahiaoui N, Keller B (2007) Contrasting rates of evolution in Pm3 loci from three wheat species and rice. Genetics 177:1207–1216PubMedCrossRefGoogle Scholar
  113. Wolfe MS (1984) Trying to understand and control powdery mildew. Plant Pathol (Oxford) 33:451–466Google Scholar
  114. Xu W, Li C, Hu L, Wang H et al (2011) Identification and molecular mapping of PmHNK54: a novel powdery mildew resistance gene in common wheat. Plant Breed 130:603–607CrossRefGoogle Scholar
  115. Xu XY, Bai GH, Carver BF et al (2006) Molecular characterization of a powdery mildew resistance gene in wheat cultivar Suwon 92. Phytopathol 96:496–500CrossRefGoogle Scholar
  116. Yahiaoui N, Brunner S, Keller B (2006) Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J 47:85–98PubMedCrossRefGoogle Scholar
  117. Yahiaoui N, Kaur N, Keller B (2009) Independent evolution of functional Pm3 resistance genes in wild tetraploid wheat and domesticated bread wheat. Plant J 57:846–856PubMedCrossRefGoogle Scholar
  118. Yahiaoui N, Srichumpa P, Dudler R, Keller B (2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J 37:528–538PubMedCrossRefGoogle Scholar
  119. Zeller FJ, Lutz J, Stephan U (1993) Chromosome location of genes for resistance to powdery mildew in common wheat (Triticum aestivum L.) 1. Mlk and other alleles at the Pm3 locus. Euphytica 68:223–229CrossRefGoogle Scholar
  120. Zhu YY, Chen HR, Fan JH et al (2000) Genetic diversity and disease control in rice. Nature 406:718–722PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Liselotte L. Selter
    • 1
  • Margarita Shatalina
    • 1
  • Jyoti Singla
    • 1
  • Beat Keller
    • 1
  1. 1.Institute of Plant BiologyUniversity of ZurichZurichSwitzerland

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