Pyrenophora tritici-repentis: A Plant Pathogenic Fungus with Global Impact

  • Lynda M. CiuffettiEmail author
  • Viola A. Manning
  • Iovanna Pandelova
  • Justin D. Faris
  • Timothy L. Friesen
  • Stephen E. Strelkov
  • Genevieve L. Weber
  • Stephen B. Goodwin
  • Thomas J. Wolpert
  • Melania Figueroa


Pyrenophora tritici-repentis (Ptr), causal agent of tan spot of wheat, is a necrotrophic fungus that presents an increasing threat to wheat production due to its rapid, global expansion. Despite its homothallic nature, Ptr populations have high genetic diversity, which positively impacts host range and virulence. Pathogenicity by Ptr is attributable to the production of host-selective toxins (HSTs) and follows an inverse gene-for-gene mechanism, in which HSTs are recognized by unique single dominant genes that confer both toxin-sensitivity and disease susceptibility. Studies addressing the mechanism of action of Ptr HSTs have unveiled both commonalities and complexities of the host response to these toxins. Resistance-like host responses triggered by the HSTs support the emerging hypothesis that necrotrophic pathogens exploit the host defense response as a mechanism to induce host cell death and ensure colonization. Recent advances in sequencing technology have facilitated the comparison of the genetic makeup of pathogenic and nonpathogenic isolates of Ptr. Such comparisons are providing insights into the genetic diversity of the pathogen and the mechanisms that dictate the increase in virulence and incidence of this important pathogen. Comparative genome analysis has also provided evidence that transposable elements (TEs) play a crucial role in genome re-arrangement and expansion, which contributes to the genomic flexibility to create and diversify effectors.


Mitochondrial Genome Reference Genome Pathogenic Race Repeat Induce Point Repeat Induce Point Mutation 
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.



The authors would like to acknowledge the funding agencies that provided generous support for the research of their primary work cited in this chapter. Funding from the National Research Initiative of the USDA Cooperative State Research Education and Extension Service Competitive Grants Program, the Agriculture and Food Research Initiative Competitive Grants Program from the USDA National Institute of Food and Agriculture, and the National Science Foundation to LMC; funding from the USDA Agricultural Research Service and Agriculture and Food Research Initiative Competitive Grants Program from the USDA National Institute of Food and Agriculture to JDF; funding from the Natural Sciences and Engineering Research Council of Canada, and the A.W. Henry Endowment Fund (University of Alberta) to SES; funding from the USDA Agricultural Research Service to SBG; funding from a National Science Foundation Minority Postdoctoral Fellowship to MF. We would like to thank Dr. L.-J. Ma and the Broad Institute and Dr. I. Grigoriev and the US Joint Genome Institute for productive collaborations and sequencing of the Ptr reference genome (isolate Pt-1C-BFP) and Ptr isolates, DW7 and SD20, respectively. We would like to thank Nathan Miller for original artwork included in Fig. 1.1A.


  1. Aboukhaddour R, Cloutier S, Ballance GM, Lamari L (2009) Genome characterization of Pyrenophora tritici-repentis isolates reveals high plasticity and independent chromosomal location of ToxA and ToxB. Mol Plant Pathol 10(2):201–212. [pii]:MPP520, doi: 10.1111/j.1364-3703.2008.00520.x
  2. Aboukhaddour R, Cloutier S, Lamari L, Strelkov SE (2011) Simple sequence repeats and diversity of globally distributed populations of Pyrenophora tritici-repentis. Can J Plant Pathol 33(3):389–399. doi: 10.1080/07060661.2011.590821 Google Scholar
  3. Aboukhaddour R, Kim YM, Strelkov SE (2012) RNA-mediated gene silencing of ToxB in Pyrenophora tritici-repentis. Mol Plant Pathol 13(3):318–326. doi: 10.1111/j.1364-3703.2011.00748.x PubMedGoogle Scholar
  4. Aboukhaddour R, Turkington TK, Strelkov SE (2013) Race structure of Pyrenophora tritici-repentis (tan spot of wheat) in Alberta, Canada. Can J Plant Pathol 35(2):256--268. doi: 10.1080/07060661.2013.782470
  5. Adhikari TB, Bai J, Meinhardt SW, Gurung S, Myrfield M, Patel J, Ali S, Gudmestad NC, Rasmussen JB (2009) Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Mol Plant Microbe In 22(9):1056–1068. doi: 10.1094/MPMI-22-9-1056 Google Scholar
  6. Ali S, Francl L, De Wolf E (1999) First report of Pyrenophora tritici-repentis race 5 from North America. Plant Dis 83(6):591Google Scholar
  7. Ali S, Francl L, Iram S, Ahmad I (2001) First report of tan spot on wheat in Pakistan. Plant Dis 85(9):1031Google Scholar
  8. Ali S, Francl LJ (2003) Population race structure of Pyrenophora tritici-repentis prevalent on wheat and noncereal grasses in the Great Plains. Plant Dis 87(4):418–422Google Scholar
  9. Ali S, Gurung S, Adhikari TB (2010) Identification and characterization of novel isolates of Pyrenophora tritici-repentis from Arkansas. Plant Dis 94(2):229–235Google Scholar
  10. Amaike S, Ozga JA, Basu U, Strelkov SE (2008) Quantification of ToxB gene expression and formation of appressoria by isolates of Pyrenophora tritici-repentis differing in pathogenicity. Plant Pathol 57(4):623–633Google Scholar
  11. Amlacher S, Sarges P, Flemming D, van Noort V, Kunze R, Devos DP, Arumugam M, Bork P, Hurt E (2011) Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146(2):277–289PubMedGoogle Scholar
  12. Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier J-M, Quévillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, Brault B, Chen Z, Choquer M, Collémare J, Cotton P, Danchin EG, Da Silva C, Gautier A, Giraud C, Giraud T, Gonzalez C, Grossetete S, Güldener U, Henrissat B, Howlett BJ, Kodira C, Kretschmer M, Lappartient A, Leroch M, Levis C, Mauceli E, Neuvéglise C, Oeser B, Pearson M, Poulain J, Poussereau N, Quesneville H, Rascle C, Schumacher J, Ségurens B, Sexton A, Silva E, Sirven C, Soanes DM, Talbot NJ, Templeton M, Yandava C, Yarden O, Zeng Q, Rollins JA, Lebrun M-H, Dickman M (2011) Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7(8):e1002230PubMedCentralPubMedGoogle Scholar
  13. Anderson J, Effertz R, Faris J, Francl L, Meinhardt S, Gill B (1999) Genetic analysis of sensitivity to a Pyrenophora tritici-repentis necrosis-inducing toxin in durum and common wheat. Phytopathol 89(4):293–297Google Scholar
  14. Andrie RM, Ciuffetti LM (2011) Pyrenophora bromi, causal agent of brownspot of bromegrass, expresses a gene encoding a protein with homology and similar activity to Ptr ToxB, a host-selective toxin of wheat. Mol Plant Microbe In 24(3):359–367. doi: 10.1094/MPMI-06-10-0142 Google Scholar
  15. Andrie RM, Martinez JP, Ciuffetti LM (2005) Development of ToxA and ToxB promoter-driven fluorescent protein expression vectors for use in filamentous ascomycetes. Mycologia 97(5):1152–1161PubMedGoogle Scholar
  16. Andrie RM, Pandelova I, Ciuffetti LM (2007) A combination of phenotypic and genotypic characterization strengthens Pyrenophora tritici-repentis race identification. Phytopathol 97(6):694–701. doi: 10.1094/PHYTO-97-6-0694 Google Scholar
  17. Andrie RM, Schoch CL, Hedges R, Spatafora JW, Ciuffetti LM (2008) Homologs of ToxB, a host-selective toxin gene from Pyrenophora tritici-repentis, are present in the genome of sister-species Pyrenophora bromi and other members of the Ascomycota. Fungal Genet Biol 45(3):363–377. doi: 10.1016/j.fgb.2007.10.014 PubMedGoogle Scholar
  18. Annone J (1998) Tan spot of wheat in Argentina: importance and disease management strategies. In: Duveiller E, Dubin HJ, Reeves J, McNab A (eds) Helminthosporium blights of wheat: spot blotch and tan spot CIMMYT (International Maize and Wheat Improvement Center), Mexico, pp 339–345Google Scholar
  19. Antoni EA, Rybak K, Tucker MP, Hane JK, Solomon PS, Drenth A, Shankar M, Oliver RP (2010) Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici-repentis. Australasian Plant Pathol 39(1):63–68Google Scholar
  20. Aung TST (2001) Molecular polymorphism and virulence in Pyrenophora tritici-repentis.
  21. Ballance G, Lamari L, Kowatsch R, Bernier C (1996) Cloning, expression and occurrence of the gene encoding the Ptr necrosis toxin from Pyrenophora tritici-repentis. Mol Plant Pathol.
  22. Ballance GM, Lamari L, Bernier CC (1989) Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiol Mol Plant Pathol 35(3):203–213Google Scholar
  23. Benslimane H, Lamari L, Benbelkacem A, Sayoud R, Bouzand Z (2011) Distribution of races of Pyrenophora tritici-repentis in Algeria and identication of a new virulence type. Phytopathol Mediterr 50(2):203–211Google Scholar
  24. Bergstrom G, Schilder A (1998) Seed pathology of tan spot. In: Duveiller E, Dubin HJ, Reeves J, McNab A (eds) Helminthosporium blights of wheat: spot blotch and tan spot. CIMMYT (International Maize and Wheat Improvement Center), Mexico, pp 364–368Google Scholar
  25. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia E (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33(10):1597-1613 Google Scholar
  26. Bockus WW, Appel JA, Bowden RL, Fritz AK, Gill BS, Martin TJ, Sears RG, Seifers DL, Brown-Guedira GL, Eversmeyer MG (2001) Success stories: breeding for wheat disease resistance in Kansas. Plant Dis 85(5):453–461Google Scholar
  27. Bockus WW, Bowden R, Hunger R, Murray T, Smiley R (2010) Compendium of wheat diseases and pests, vol 3. APS Press, ChicagoGoogle Scholar
  28. Bok JW, Chiang YM, Szewczyk E, Reyes-Dominguez Y, Davidson AD, Sanchez JF, Lo HC, Watanabe K, Strauss J, Oakley BR, Wang CC, Keller NP (2009) Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol 5 (7):462–464. [pii]:nchembio.177, doi: 10.1038/nchembio.177
  29. Bouras N, Kim YM, Strelkov SE (2009) Influence of water activity and temperature on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat. Int J Food Microbiol 131(2–3):251–255. doi: 10.1016/j.ijfoodmicro.2009.02.001
  30. Bouras N, Strelkov SE (2010) Influence of carbon source on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat. Can J Microbiol 56 (10):874–884. doi: 10.1139/w10-073, [pii]:w10-073
  31. Cambareri EB, Jensen BC, Schabtach E, Selker EU (1989) Repeat-induced G-C to A-T mutations in Neurospora. Science 244(4912):1571–1575. doi: 10.1126/science.2544994 PubMedGoogle Scholar
  32. Cao T, Kim YM, Kav NN, Strelkov SE (2009) A proteomic evaluation of Pyrenophora tritici-repentis, causal agent of tan spot of wheat, reveals major differences between virulent and avirulent isolates. Proteomics 9(5):1177–1196. doi: 10.1002/pmic.200800475 PubMedGoogle Scholar
  33. Carter CJ, Thornburg RW (2004) Tobacco Nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol 134(1):460–469. doi: 10.1104/pp.103.027482 PubMedCentralPubMedGoogle Scholar
  34. Catlett NL, Lee B-N, Yoder OC, Turgeon BG (2003) Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Newslett 50:9–11Google Scholar
  35. Cavener DR (1992) GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J Mol Biol 223(3):811–814. doi:0022-2836(92)90992-S [pii]Google Scholar
  36. Chamberlain DW, Allison JL (1945) The brown leafspot on Bromus inermis caused by Pyrenophora bromi. Phytopathol 35:241–248Google Scholar
  37. Cheong J, Wallwork H, Williams K (2004) Identification of a major QTL for yellow leaf spot resistance in the wheat varieties Brookton and Cranbrook. Crop Pasture Sci 55(3):315–319Google Scholar
  38. Chu C-G, Xu S, Faris J, Nevo E, Friesen T (2008a) Seedling resistance to tan spot and Stagonospora nodorum leaf blotch in wild emmer wheat (Triticum dicoccoides). Plant Dis 92(8):1229–1236Google Scholar
  39. Chu CG, Chao S, Friesen TL, Faris JD, Zhong S, Xu SS (2010) Identification of novel tan spot resistance QTLs using an SSR-based linkage map of tetraploid wheat. Mol Breeding 25(2):327–338. doi: 10.1007/s11032-009-9335-2 Google Scholar
  40. Chu CG, Friesen TL, Xu SS, Faris JD (2008b) Identification of novel tan spot resistance loci beyond the known host-selective toxin insensitivity genes in wheat. Theor Appl Genet 117(6):873–881. doi: 10.1007/s00122-008-0826-z PubMedGoogle Scholar
  41. CIMMYT (2012) International maize and Wheat improvement center (CIMMYT), El Batán, Mexico.
  42. Ciuffetti L, Francl L, Ballance G, Bockus W, Lamari L, Meinhardt S, Rasmussen J (1998) Standardization of toxin nomenclature in the Pyrenophora tritici-repentis/wheat interaction. Can J Plant Pathol 20(4):421–424Google Scholar
  43. Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP (2010) Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol 187(4):911–919. doi: 10.1111/j.1469-8137.2010.03362.x, [pii]:NPH3362
  44. Ciuffetti LM, Tuori RP (1999) Advances in the characterization of the Pyrenophora tritici-repentis-wheat interaction. Phytopathol 89(6):444–449Google Scholar
  45. 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(2):135–144. doi: 10.2307/3870536 PubMedCentralPubMedGoogle Scholar
  46. Clutterbuck JA (2011) Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 48(3):306–326. doi:
  47. Condon BJ, Leng Y, Wu D, Bushley KE, Ohm RA, Otillar R, Martin J, Schackwitz W, Grimwood J, Mohdzainudin N, Xue C, Wang R, Manning VA, Dhillon B, Tu ZJ, Steffenson BJ, Salamov A, Sun H, Lowry S, Labutti K, Han J, Copeland A, Lindquist E, Barry K, Schmutz J, Baker SE, Ciuffetti LM, Grigoriev IV, Zhong S, Turgeon BG (2013) Comparative Genome Structure, Secondary Metabolite, and effector Coding Capacity across Cochliobolus Pathogens. PLoS Genet 9(1):e1003233. doi: 10.1371/journal.pgen.1003233, [pii]:PGENETICS-D-12-01094
  48. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676PubMedGoogle Scholar
  49. Conners IL (1937) Diseases of Cereal Crops. . Seventeenth Annual Report of the Canadian Plant Disease Survey 17(5):1–14.
  50. Couturier M, Navarro D, Olivé C, Chevret D, Haon M, Favel A, Lesage-Meessen L, Henrissat B, Coutinho PM, Berrin J-G (2012) Post-genomic analyses of fungal lignocellulosic biomass degradation reveal the unexpected potential of the plant pathogen Ustilago maydis. BMC Genom 13(1):57Google Scholar
  51. Cox DJ, Hosford RJ (1987) Resistant winter wheat compared at different growth stages and leaf positions for tan spot severity. Plant Dis 71:883–886Google Scholar
  52. Custers JH, Harrison SJ, Sela-Buurlage MB, van Deventer E, Lageweg W, Howe PW, van der Meijs PJ, Ponstein AS, Simons BH, Melchers LS, Stuiver MH (2004) Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence. Plant J 39(2):147–160. doi: 10.1111/j.1365-313X.2004.02117.x, [pii]:TPJ2117
  53. da Luz WC, Hosford R Jr (1980) Twelve Pyrenophora trichostoma races for virulence to wheat in the Central Plains of North America. Phytopathol 70:1193–1196Google Scholar
  54. De Wolf E, Effertz R, Ali S, Francl L (1998) Vistas of tan spot research. Can J Plant Pathol 20(4):349–370Google Scholar
  55. Dimalanta ET, Lim A, Runnheim R, Lamers C, Churas C, Forrest DK, de Pablo JJ, Graham MD, Coppersmith SN, Goldstein S, Schwartz DC (2004) A microfluidic system for large DNA molecule arrays. Anal Chem 76(18):5293–5301. doi: 10.1021/ac0496401 PubMedGoogle Scholar
  56. Dittrich H, Kutchan TM (1991) Molecular cloning, expression, and induction of berberine bridge enzyme, an enzyme essential to the formation of benzophenanthridine alkaloids in the response of plants to pathogenic attack. Proc Natl Acad Sci U S A 88(22):9969–9973PubMedCentralPubMedGoogle Scholar
  57. Dreschler C (1923) Some Graminicolous Species of Helminthosporium. J Agric Res 24:0641–0740Google Scholar
  58. Dushnicky L, Ballance G, Sumner M, MacGregor A (1996) Penetration and infection of susceptible and resistant wheat cultivars by a necrosis toxin-producing isolate of Pyrenophora tritici-repentis. Can J Plant Pathol 18(4):392–402Google Scholar
  59. Dushnicky L, Ballance G, Sumner M, MacGregor A (1998a) Detection of infection and host responses in susceptible and resistant wheat cultivars to a toxin-producing isolate of Pyrenophora tritici-repentis. Can J Plant Pathol 20(1):19–27Google Scholar
  60. Dushnicky L, Ballance G, Sumner M, MacGregor A (1998b) The role of lignification as a resistance mechanism in wheat to a toxin-producing isolate of Pyrenophora tritici-repentis. Can J Plant Pathol 20(1):35–47Google Scholar
  61. Duveiller E (2004) Controlling foliar blights of wheat in the rice-wheat systems of Asia. Plant Dis 88(5):552–556Google Scholar
  62. Duveiller E, Singh RP, Nicol JM (2007) The challenges of maintaining wheat productivity: pests, diseases, and potential epidemics. Euphytica 157(3):417–430Google Scholar
  63. Dyrløv Bendtsen J, Nielsen H, von Heijne G, Brunak S (2004) Improved Prediction of Signal Peptides: SignalP 3.0. J Mol Biol 340 (4):783–795Google Scholar
  64. Effertz R, Anderson J, Francl L (2001) Restriction fragment length polymorphism mapping of resistance to two races of Pyrenophora tritici-repentis in adult and seedling wheat. Phytopathol 91(6):572–578Google Scholar
  65. Effertz RJ, Meinhardt SW, Anderson JA, Jordahl JG, Francl LJ (2002) Identification of a chlorosis-inducing toxin from Pyrenophora tritici-repentis and the chromosomal location of an insensitivity locus in wheat. Phytopathol 92(5):527–533. doi: 10.1094/Phyto.2002.92.5.527 Google Scholar
  66. Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol13 (4):472–477Google Scholar
  67. Elias E, Cantrell R, Hosford R (1989) Heritability of resistance to tan spot in durum wheat and its association with other agronomic traits. Crop Sci 29(2):299–304Google Scholar
  68. Ellis MB, Waller JM (1974) C.M.I. Descriptions of pathogenic fungi and bacteria No. 494. Commonwealth Mycological Institute, KewGoogle Scholar
  69. Evans C, Hunger R, Siegerist W (1999) Comparison of greenhouse and field testing to identify wheat resistant to tan spot. Plant Dis 83(3):269–273Google Scholar
  70. Facchini PJ, Penzes C, Johnson AG, Bull D (1996) Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol 112(4):1669–1677. doi: 10.1104/pp.112.4.1669 PubMedCentralPubMedGoogle Scholar
  71. FAOSTAT (2012) Food and Agricultural Organization of the United Nations.
  72. Faris J, Li W, Liu D, Chen P, Gill B (1999) Candidate gene analysis of quantitative disease resistance in wheat. Theor Appl Genet 98(2):219–225Google Scholar
  73. Faris JD, Abeysekara NS, McClean PE, Xu SS, Friesen TL (2012) Tan spot susceptibility governed by the Tsn1 locus and race-nonspecific resistance quantitative trait loci in a population derived from the wheat lines Salamouni and Katepwa. Mol Breeding 30(4):1669–1678. doi: 10.1007/s11032-012-9750-7 Google Scholar
  74. Faris JD, Anderson JA, Francl LJ, Jordahl JG (1996) Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture filtrate from Pyrenophora tritici-repentis. Phytopathol 86(5):459–463. doi: 10.1094/Phyto-86-459 Google Scholar
  75. Faris JD, Anderson JA, Francl LJ, Jordahl JG (1997) RFLP mapping of resistance to chlorosis induction by Pyrenophora tritici-repentis in wheat. Theor Appl Genet 94(1):98–103. doi: 10.1007/s001220050387 PubMedGoogle Scholar
  76. Faris JD, Friesen TL (2005) Identification of quantitative trait loci for race-nonspecific resistance to tan spot in wheat. Theor Appl Genet 111(2):386–392. doi: 10.1007/s00122-005-2033-5 PubMedGoogle Scholar
  77. Faris JD, Liu Z, Xu SS (2013) Genetics of tan spot resistance in wheat. Theor Appl Genet 29:1–21Google Scholar
  78. Faris JD, Zhang Z, Lu H, Lu S, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci U S A 107(30):13544–13549. doi: 10.1073/pnas.1004090107 PubMedCentralPubMedGoogle Scholar
  79. Ferandon C, Xu J, Barroso G (2013) The 135 kbp mitochondrial genome of Agaricus bisporus is the largest known eukaryotic reservoir of group I introns and plasmid-related sequences. Fungal Genet BiolGoogle Scholar
  80. Fernandez MR, Lim S, Dokken-Bouchard FL, Miller SG, Northover PR (2012) Leaf spotting diseases of common and durum wheat in Saskatchewan in 2011. Cereals. Can Plant Dis Surv 92:98http://phytopathca/download/cpds-archive/vol92/cpds_vol_92_2012.pdf
  81. Figueroa Betts M, Manning VA, Cardwell KB, Pandelova I, Ciuffetti LM (2011) The importance of the N-terminus for activity of Ptr ToxB, a chlorosis-inducing host-selective toxin produced by Pyrenophora tritici-repentis. Physiol Mol Plant Pathol 75(4):138–145Google Scholar
  82. Finking R, Marahiel MA (2004) Biosynthesis of nonribosomal peptides. Annu Rev Microbiol 58(1):453–488. doi: 10.1146/annurev.micro.58.030603.123615
  83. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38(suppl 1):D211–D222. doi: 10.1093/nar/gkp985 PubMedCentralPubMedGoogle Scholar
  84. Flor H (1956) The complementary genic systems in flax and flax rust. Adv Genet 8:29–54Google Scholar
  85. Friesen TL, Ali S, Kianian S, Francl LJ, Rasmussen JB (2003) Role of host sensitivity to Ptr ToxA in development of tan spot of wheat. Phytopathol 93(4):397–401. doi: 10.1094/PHYTO.2003.93.4.397 Google Scholar
  86. Friesen TL, Ali S, Klein KK, Rasmussen JB (2005) Population genetic analysis of a global collection of Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Phytopathol 95(10):1144–1150. doi: 10.1094/PHYTO-95-1144 Google Scholar
  87. Friesen TL, Faris JD (2004) Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor Appl Genet 109(3):464–471. doi: 10.1007/s00122-004-1678-9 PubMedGoogle Scholar
  88. Friesen TL, Faris JD, Solomon PS, Oliver RP (2008) Host‐specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10 (7):1421–1428Google Scholar
  89. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38(8):953–956PubMedGoogle Scholar
  90. Fujii I, Yoshida N, Shimomaki S, Oikawa H, Ebizuka Y (2005) An iterative type I polyketide synthase PKSN catalyzes synthesis of the decaketide alternapyrone with regio-specific octa-methylation. Chem Biol 12(12):1301–1309PubMedGoogle Scholar
  91. Fukuhara H, Sor F, Drissi R, Dinouel N, Miyakawa I, Rousset S, Viola A (1993) Linear mitochondrial DNAs of yeasts: frequency of occurrence and general features. Mol Cell Biol 13(4):2309–2314PubMedCentralPubMedGoogle Scholar
  92. Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20(9):417–423. doi:
  93. Gamba FM, Lamari L (1998) Mendelian inheritance of resistance to tan spot [Pyrenophora tritici-repentis] in selected genotypes of durum wheat (Triticum turgidum). Can J Plant Pathol-Revue Canadienne De Phytopathologie 20(4):408–414Google Scholar
  94. Gamba FM, Strelkov SE, Lamari L (2012) Virulence of Pyrenophora tritici-repentis in the Southern Cone Region of South America. Can J Plant Pathol 34(4):545–550Google Scholar
  95. Gardiner DM, Cozijnsen AJ, Wilson LM, Pedras MS, Howlett BJ (2004) The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol Microbiol 53 (5):1307-1318. doi: 10.1111/j.1365-2958.2004.04215.x, [pii]:MMI4215
  96. Gilchrist SL, Fuentes SF, Isla de Bauer ML (1984) Determinacion de fuentes de resistencia contra Helminthosporium tritici-repentis bajo condiciones de campo e invernadero. Agrociencia 56:95–105Google Scholar
  97. Glazebrook J, Ton J (2007) Biotic interactions: recurring themes and expanding scales. Curr Opin Plant Biol 10(4):331–334Google Scholar
  98. Griffiths A (1995) Natural plasmids of filamentous fungi. Microbiol Rev 59(4):673–685PubMedCentralPubMedGoogle Scholar
  99. Gurung S, Short D, Adhikari T (2013) Global population structure and migration patterns suggest significant population differentiation among isolates of Pyrenophora tritici-repentis. Fungal Genet Biol 52:32–41PubMedGoogle Scholar
  100. Hanada K, Vallejo V, Nobuta K, Slotkin RK, Lisch D, Meyers BC, Shiu SH, Jiang N (2009) The functional role of pack-MULEs in rice inferred from purifying selection and expression profile. Plant Cell 21(1):25–38. doi: 10.1105/tpc.108.063206, [pii]:tpc.108.063206
  101. Hane JK, Lowe RG, Solomon PS, Tan K-C, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE (2007) Dothideomycete–plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell Online 19(11):3347–3368Google Scholar
  102. Harrison MJ, Baldwin I (2004) Biotic interactions: ploy and counter-ploy in the biotic interactions of plants. Curr Opin Plant Biol 7:353–355Google Scholar
  103. Hoen DR, Park KC, Elrouby N, Yu Z, Mohabir N, Cowan RK, Bureau TE (2006) Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol Biol Evol 23(6):1254–1268. doi: 10.1093/molbev/msk015, [pii]:msk015
  104. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35(suppl 2):W585–W587. doi: 10.1093/nar/gkm259 PubMedCentralPubMedGoogle Scholar
  105. Hosford R Jr (1971) A form of Pyrenophora trichostoma pathogenic to wheat and other grasses. Phytopathol 61:28–32Google Scholar
  106. Hosford RM, Jr. (1982) Tan spot-developing knowledge 1902–1981, virulent races and wheat differentials, methodology, rating systems, other leaf diseases, literature. In: Tan Spot of Wheat and Related Diseases Workshop, Fargo, North Dakota, Agricultural Experimental Station, North Dakota State University, pp 1–24 Google Scholar
  107. Jaffe DB, Butler J, Gnerre S, Mauceli E, Lindblad-Toh K, Mesirov JP, Zody MC, Lander ES (2003) Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res 13(1):91–96. doi: 10.1101/gr.828403 PubMedCentralPubMedGoogle Scholar
  108. Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431 (7008):569-573. doi: 10.1038/nature02953, [pii]:nature02953
  109. Jin J-M, Lee S, Lee J, Baek S-R, Kim J-C, Yun S-H, Park S-Y, Kang S, Lee Y-W (2010) Functional characterization and manipulation of the apicidin biosynthetic pathway in Fusarium semitectum. Mol Microbiol 76(2):456–466. doi: 10.1111/j.1365-2958.2010.07109.x PubMedGoogle Scholar
  110. Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, Kohmoto K (2000) Cloning and Characterization of a Cyclic Peptide Synthetase Gene from Alternaria alternata Apple Pathotype Whose Product Is Involved in AM-Toxin Synthesis and Pathogenicity. Mol Plant Microbe In 13 (7):742–753. doi: 10.1094/mpmi.2000.13.7.742
  111. Jorgensen L, Olsen L (2007) Control of tan spot (Drechslera tritici-repentis) using cultivar resistance, tillage methods and fungicides. Crop Prot 26(11):1606–1616Google Scholar
  112. Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE (2005) The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15(9):1292–1297. doi: 10.1101/gr.4064205, [pii]:15/9/1292
  113. Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism—from biochemistry to genomics. Nat Rev Microbiol 3(12):937–947PubMedGoogle Scholar
  114. Keren N, Ohkawa H, Welsh EA, Liberton M, Pakrasi HB (2005) Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell Online 17(10):2768–2781Google Scholar
  115. Kihara J, Moriwaki A, Tanaka N, Tanaka C, Ueno M, Arase S (2008) Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol Lett 281(2):221–227. doi: 10.1111/j.1574-6968.2008.01101.x PubMedGoogle Scholar
  116. Kim YM, Bouras N, Kav NN, Strelkov SE (2010) Inhibition of photosynthesis and modification of the wheat leaf proteome by Ptr ToxB: a host-specific toxin from the fungal pathogen Pyrenophora tritici-repentis. Proteomics 10(16):2911–2926PubMedGoogle Scholar
  117. Kim YM, Strelkov S (2007) Heterologous expression and activity of Ptr ToxB from virulent and avirulent isolates of Pyrenophora tritici-repentis. Can J Plant Pathol 29(3):232–242Google Scholar
  118. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BP, Chen Z, Henrissat B, Lee YH, Park J, Garcia-Pedrajas MD, Barbara DJ, Anchieta A, de Jonge R, Santhanam P, Maruthachalam K, Atallah Z, Amyotte SG, Paz Z, Inderbitzin P, Hayes RJ, Heiman DI, Young S, Zeng Q, Engels R, Galagan J, Cuomo CA, Dobinson KF, Ma LJ (2011) Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 7(7):e1002137. doi: 10.1371/journal.ppat.1002137, [pii]:PPATHOGENS-D-10-00156
  119. Krupinksy JM (1986) Pyrenophora tritici-repentis, P. bromi, and Leptosphaeria nodorum on Bromus inermis in the Northern Great Plains. Plant Dis 70:61–64Google Scholar
  120. Krupinsky JM (1992a) Grass Hosts of Pyrenophora tritici-repentis. Plant Dis 76:92–95Google Scholar
  121. Krupinsky JM (1992b) Collection of conidia and ascospores of Pyrenophora tritici-repentis from wheat straw. In: Advances in Tan Spot Research. Proceedings of the Second International Wheat Tan Spot and Spot Blotch Workshop, Fargo, North Dakota, Agricultural Experiment Station, North Dakota State University, pp 91-95Google Scholar
  122. Kwon C, Rasmussen J, Meinhardt S (1998) Activity of Ptr ToxA from Pyrenophora tritici-repentis requires host metabolism. Physiol Mol Plant Pathol 52(3):201–212Google Scholar
  123. Lamari L, Bernier C (1989a) Evaluation of wheat lines and cultivars to tan spot (Pyrenophora tritici-repentis) based on lesion type. Can J Plant Pathol 11(1):49–56Google Scholar
  124. Lamari L, Bernier CC (1989b) Virulence of isolates of Pyrenophora tritici-repentis on 11 wheat cultivars and cytology of the differential host reactions. Can J Plant Pathol 11(3):284–290Google Scholar
  125. Lamari L, Bernier CC (1991) Genetics of tan necrosis and extensive chlorosis in tan spot of wheat caused by Pyrenophora tritici-repentis. Phytopathol 91:1092–1095Google Scholar
  126. Lamari L, Gilbert J, Tekauz A (1998) Race differentiation in Pyrenophora tritici-repentis and survey of physiologic variation in western Canada. Can J Plant Pathol-Revue Canadienne De Phytopathologie 20(4):396–400Google Scholar
  127. Lamari L, Sayoud R, Boulif M, Bernier CC (1995) Identification of a new race in Pyrenophora tritici-repentis: Implications for the current pathotype classification system. Can J Plant Pathol-Revue Canadienne De Phytopathologie 17(4):312–318Google Scholar
  128. Lamari L, Strelkov S, Yahyaoui A, Amedov M, Saidov M, Djunusova M, Koichibayev M (2005) Virulence of Pyrenophora tritici-repentis in the countries of the Silk Road. Can J Plant Pathol 27(3):383–388Google Scholar
  129. Lamari L, Strelkov S, Yahyaoui A, Orabi J, Smith R (2003) The identification of two new races of Pyrenophora tritici-repentis from the host center of diversity confirms a one-to-one relationship in tan spot of wheat. Phytopathol 93(4):391–396Google Scholar
  130. Lamari L, Strelkov SE (2010) The wheat/Pyrenophora tritici-repentis interaction: progress towards an understanding of tan spot disease. Can J Plant Pathol-Revue Canadienne De Phytopathologie 32(1):4–10. doi: 10.1080/07060661003594117, [pii]:920007044
  131. Lamey HA, McMullen MP (2011) Crop rotations for managing plant disease.
  132. Larez C, Hosford R Jr, Freeman T (1986) Infection of wheat and oats by Pyrenophora tritici-repentis and initial characterization of resistance. Phytopathol 76(9):931–938Google Scholar
  133. Leisova-Svobodova L, Hanzalova A, Kucera L (2010) The variability of a Pyrenophora tritici-repentis population as revealed by inter-retrotransposon amplified polymorphism with regard to the Ptr ToxA gene. Czech Mycol 61(2):125–128Google Scholar
  134. Lepoint P, Renard M-E, Legreve A, Duveiller E, Maraite H (2010) Genetic diversity of the mating type and toxin production genes in Pyrenophora tritici-repentis. Phytopathol 100:474–483Google Scholar
  135. Li H, Ruan J, Durbin R (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18(11):1851–1858. doi:gr.078212.108 [pii]/gr.078212.108Google Scholar
  136. Li HB, Yan W, Liu GR, Wen SM, Liu CJ (2011) Identification and validation of quantitative trait loci conferring tan spot resistance in the bread wheat variety Ernie. Theor Appl Genet 122(2):395–403. doi: 10.1007/s00122-010-1455-x PubMedGoogle Scholar
  137. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25(15):1966–1967. doi: 10.1093/bioinformatics/btp336, [pii]:btp336 [pii]
  138. Lichter A, Gaventa JM, Ciuffetti LM (2002) Chromosome-based molecular characterization of pathogenic and non-pathogenic wheat isolates of Pyrenophora tritici-repentis. Fungal Genet Biol 37(2):180–189. doi:S1087184502005005 [pii]Google Scholar
  139. Lin J, Qi R, Aston C, Jing J, Anantharaman TS, Mishra B, White O, Daly MJ, Minton KW, Venter JC, Schwartz DC (1999) Whole-genome shotgun optical mapping of Deinococcus radiodurans. Science 285 (5433):1558–1562. doi:7810 [pii]Google Scholar
  140. Lisch D (2005) Pack-MULEs: theft on a massive scale. BioEssays 27(4):353–355. doi: 10.1002/bies.20219 PubMedGoogle Scholar
  141. Liu Z, Ellwood SR, Oliver RP, Friesen TL (2011) Pyrenophora teres: profile of an increasingly damaging barley pathogen. Mol Plant Pathol 12(1):1–19. doi: 10.1111/j.1364-3703.2010.00649.x PubMedGoogle Scholar
  142. Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M, Tzeng SC, Maier CS, Wolpert TJ (2012) Tricking the guard: exploiting plant defense for disease susceptibility. Science 338(6107):659–662. doi: 10.1126/science.1226743 PubMedCentralPubMedGoogle Scholar
  143. Lorang JM, Tuori RP, Martinez JP, Sawyer TL, Redman RS, Rollins JA, Wolpert TJ, Johnson KB, Rodriguez RJ, Dickman MB, Ciuffetti LM (2001) Green fluorescent protein is lighting up fungal biology. Appl Environ Microbiol 67(5):1987–1994. doi: 10.1128/AEM.67.5.1987-1994.2001 PubMedCentralPubMedGoogle Scholar
  144. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25(5):0955–0964Google Scholar
  145. Luck J, Spackman M, Freeman A, Griffiths W, Finlay K, Chakraborty S (2011) Climate change and diseases of food crops. Plant Pathol 60(1):113–121Google Scholar
  146. Lysoe E, Bone KR, Klemsdal SS (2009) Real-time quantitative expression studies of the zearalenone biosynthetic gene cluster in Fusarium graminearum. Phytopathol 99(2):176–184. doi: 10.1094/PHYTO-99-2-0176,  10.1094/PHYTO-99-2-0176 [pii]
  147. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, Rep M (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464(7287):367–373. doi: 10.1038/nature08850, [pii]:nature08850
  148. Maloney AP, VanEtten HD (1994) A gene from the fungal plant pathogen Nectria haematococca that encodes the phytoalexin-detoxifying enzyme pisatin demethylase defines a new cytochrome P450 family. Mol Gen Genet MGG 243(5):506–514. doi: 10.1007/bf00284198 Google Scholar
  149. Mamluk O (1993) Durum wheat diseases in West Asia and North Africa (WANA). In: The adoption of agricultural technology: a guide for survey design 9:89--107Google Scholar
  150. Manning VA, Andrie RM, Trippe AF, Ciuffetti LM (2004) Ptr ToxA requires multiple motifs for complete activity. Mol Plant Microbe In 17(5):491–501Google Scholar
  151. Manning VA, Chu AL, Scofield SR, Ciuffetti LM (2010) Intracellular expression of a host-selective toxin, ToxA, in diverse plants phenocopies silencing of a ToxA-interacting protein, ToxABP1. New Phytol 187(4):1034–1047PubMedGoogle Scholar
  152. Manning VA, Chu AL, Steeves JE, Wolpert TJ, Ciuffetti LM (2009) A host-selective toxin of Pyrenophora tritici-repentis, Ptr ToxA, induces photosystem changes and reactive oxygen species accumulation in sensitive wheat. Mol Plant Microbe In 22(6):665–676Google Scholar
  153. Manning VA, Ciuffetti LM (2005) Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17(11):3203–3212. doi: 10.1105/tpc.105.035063 PubMedCentralPubMedGoogle Scholar
  154. Manning VA, Hamilton SM, Karplus PA, Ciuffetti LM (2008) The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization. Mol Plant Microbe In 21(3):315–325Google Scholar
  155. Manning VA, Hardison LK, Ciuffetti LM (2007) Ptr ToxA interacts with a chloroplast-localized protein. Mol Plant Microbe In 20(2):168–177Google Scholar
  156. Manning VA, Pandelova I, Dhillon B, Wilhelm LJ, Goodwin SB, Berlin AM, Figueroa M, Freitag M, Hane JK, Henrissat B, Holman WH, Kodira CD, Martin J, Oliver RP, Robbertse B, Schackwitz W, Schwartz DC, Spatafora JW, Turgeon BG, Yandava C, Young S, Zhou S, Zeng Q, Grigoriev IV, Ma LJ, Ciuffetti LM (2013) Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence. G3 (Bethesda) 3(1):41–63. doi: 10.1534/g3.112.004044, [pii]:GGG_004044
  157. Martinez JP, Oesch NW, Ciuffetti LM (2004) Characterization of the multiple-copy host-selective toxin gene, ToxB, in pathogenic and nonpathogenic isolates of Pyrenophora tritici-repentis. Mol Plant Microbe In 17(5):467–474. doi: 10.1094/MPMI.2004.17.5.467 Google Scholar
  158. Martinez JP, Ottum SA, Ali S, Francl LJ, Ciuffetti LM (2001) Characterization of the ToxB gene from Pyrenophora tritici-repentis. Mol Plant Microbe In 14(5):675–677Google Scholar
  159. McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Somers DJ, Appels R, Devos KM (2008) Catalogue of gene symbols for wheat. In: MacGene 2008Google Scholar
  160. Meinhardt S, Ali S, Ling H, Francl L, Rasmussen J, Friesen T (2003) A new race of Pyrenophora tritici-repentis that produces a putative host-selective toxin. In: Proceedings of fourth international wheat tan spot and spot blotch workshop, Bemidji, Minnesota, USA. Agricultural Experiment Station, North Dakota State University, pp 117–121 21–24 July, 2002, 2003Google Scholar
  161. Meinhardt SW, Cheng W, Kwon CY, Donohue CM, Rasmussen JB (2002) Role of the arginyl-glycyl-aspartic motif in the action of Ptr ToxA produced by Pyrenophora tritici-repentis. Plant Physiol 130(3):1545–1551PubMedCentralPubMedGoogle Scholar
  162. Misra A, Singh R (1972) Pathogenic differences among three isolates of Helminthosporium tritici-repentis and the performance of wheat varieties against them. Indian Phytopathol 25:350–353Google Scholar
  163. Mitra M (1934) A new leaf spot disease of wheat caused by Helminthosporium tritici repentis Died. Indian J Agric Sci 4:692–700Google Scholar
  164. Moreno M, Perello A (2010) Occurrence of Pyrenophora tritici-repentis causing tan spot in Argentina. In:A Arya, AE Perelló (eds.), Management of Fungal Pathogens: Current Trends and Progress. CABI Publishers doi: 10.1079/9781845936037.0275
  165. Moreno M, Stenglein S, Perelló A (2012) Pyrenophora tritici-repentis, Causal agent of tan spot: a review of intraspecific genetic diversity. In: Caliskan M (ed) The molecular basis of plant genetic diversity. ISBN: 978-953-51-0157-4, InTech, DOI:  10.5772/33516,
  166. Mullineux S-T, Costa M, Bassi GS, Michel F, Hausner G (2010) A group II intron encodes a functional LAGLIDADG homing endonuclease and self-splices under moderate temperature and ionic conditions. RNA 16(9):1818–1831PubMedCentralPubMedGoogle Scholar
  167. Murray GM, Brennan JP (2009) The current and potential costs from diseases of wheat in Australia. Grains Research and Development CorporationGoogle Scholar
  168. Nagle B, Frohberg R, Hosford R Jr (1982) Inheritance of resistance to tan spot of wheat. In: Tan spot of wheat and related diseases workshop, North Dakota State University, Fargo, pp 40–45Google Scholar
  169. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kosti I, LaButti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GH, Lawrence C, Scott JA, Spatafora JW, Turgeon BG, de Wit PJ, Zhong S, Goodwin SB, Grigoriev IV (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 8(12):e1003037. doi: 10.1371/journal.ppat.1003037, [pii]:PPATHOGENS-D-12-00952
  170. Oliver R, Lord M, Rybak K, Faris J, Solomon P (2008) Emergence of tan spot disease caused by toxigenic Pyrenophora tritici-repentis in Australia is not associated with increased deployment of toxin-sensitive cultivars. Phytopathol 98(5):488–491Google Scholar
  171. Orolaza N, Lamari L, Ballance G (1995) Evidence of a host-specific chlorosis toxin from Pyrenophora tritici-repentis, the causal agent of tan spot of wheat. Phytopathol 85(10):1282Google Scholar
  172. Pandelova I, Betts MF, Manning VA, Wilhelm LJ, Mockler TC, Ciuffetti LM (2009) Analysis of transcriptome changes induced by Ptr ToxA in wheat provides insights into the mechanisms of plant susceptibility. Mol Plant 2(5):1067–1083. doi: 10.1093/Mp/Ssp045 PubMedGoogle Scholar
  173. Pandelova I, Figueroa M, Wilhelm LJ, Manning VA, Mankaney AN, Mockler TC, Ciuffetti LM (2012) Host-selective toxins of Pyrenophora tritici-repentis induce common responses associated with host susceptibility. Plos One 7(7). doi:ARTN e40240 DOI  10.1371/journal.pone.0040240
  174. Postnikova E, Khasanov B (1998) Tan spot in central Asia. In: Helminthosporium blights of wheat: spot blotch and tan spot. El Batan, Mexico, pp 107–113Google Scholar
  175. Pramateftaki PV, Kouvelis VN, Lanaridis P, Typas MA (2006) The mitochondrial genome of the wine yeast Hanseniaspora uvarum: a unique genome organization among yeast/fungal counterparts. FEMS Yeast Res 6(1):77–90PubMedGoogle Scholar
  176. Raffaele S, Win J, Cano LM, Kamoun S (2010) Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. BMC Genomics 11:637. doi: 10.1186/1471-2164-11-637, [pii]:1471-2164-11-637
  177. Rasmussen JB, Kwon CY, Meinhardt SW (2004) Requirement of host signaling mechanisms for the action of Ptr ToxA in wheat. Eur J Plant Pathol 110(3):333–335Google Scholar
  178. Rees R, Platz G, Mayer R (1988) Susceptibility of Australian wheats to Pyrenophora tritici-repentis. Crop Pasture Sci 39(2):141–151Google Scholar
  179. Reeves CD, Hu Z, Reid R, Kealey JT (2008) Genes for the biosynthesis of the fungal polyketides hypothemycin from Hypomyces subiculosus and radicicol from Pochonia chlamydosporia. Appl Environ Microbiol 74 (16):5121–5129. doi:10.1128/AEM.00478-08, [pii]Google Scholar
  180. Rep M (2005) Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol Lett 253 (1):19-27. doi: 10.1016/j.femsle.2005.09.014, [pii]:S0378-1097(05)00648-8
  181. Richards TA, Leonard G, Soanes DM, Talbot NJ (2011) Gene transfer into the fungi. Fungal Biol Rev 25(2):98–110Google Scholar
  182. Rosenzweig C, Iglesias A, Yang X, Epstein PR, Chivian E (2000) Climate change and US agriculture: the impacts of warming and extreme weather events on productivity, plant diseases, and pests. Center for Health and the Global Environment, Harvard Medical School, HarvardGoogle Scholar
  183. Rosenzweig C, Iglesias A, Yang X, Epstein PR, Chivian E (2001) Climate change and extreme weather events; implications for food production, plant diseases, and pests. Global Change Hum Health 2(2):90–104Google Scholar
  184. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen AJ, Ciuffetti LM, Degrave A, Dilmaghani A, Duret L, Fudal I, Goodwin SB, Gout L, Glaser N, Linglin J, Kema GH, Lapalu N, Lawrence CB, May K, Meyer M, Ollivier B, Poulain J, Schoch CL, Simon A, Spatafora JW, Stachowiak A, Turgeon BG, Tyler BM, Vincent D, Weissenbach J, Amselem J, Quesneville H, Oliver RP, Wincker P, Balesdent MH, Howlett BJ (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun 2:202. doi: 10.1038/ncomms1189, [pii]:ncomms1189
  185. Sarma GN, Manning VA, Ciuffetti LM, Karplus PA (2005) Structure of Ptr ToxA: An RGD-containing host-selective toxin from Pyrenophora tritici-repentis. Plant Cell Online 17(11):3190–3202Google Scholar
  186. Schilder A, Bergstrom G (1990) Variation in virulence within the population of Pyrenophora tritici-repentis in New York. Phytopathol 80(1):84–90Google Scholar
  187. Schilder A, Bergstrom G (1992) The dispersal of conidia and ascospores of Pyrenophora tritici-repentis. In: Advances in Tan Spot Research. Proceedings of the Second International Wheat Tan Spot and Spot Blotch Workshop, Fargo, North Dakota, Agricultural Experiment Station, North Dakota State University, pp 96-99 Google Scholar
  188. Schilder A, Bergstrom G (1995) Seed transmission of Pyrenophora tritici-repentis, causal fungus of tan spot of wheat. Eur J Plant Pathol 101(1):81–91Google Scholar
  189. Schoch C, Crous PW, Groenewald JZ, Boehm E, Burgess TI, De Gruyter J, De Hoog G, Dixon L, Grube M, Gueidan C (2009) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64(1):1-15-S10Google Scholar
  190. Selker EU, Cambareri EB, Jensen BC, Haack KR (1987) Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51(5):741–752PubMedGoogle Scholar
  191. Sharma R, Duveiller E, Ahmed F, Arun B, Bhandari D, Bhatta M, Chand R, Chaurasiya P, Gharti D, Hossain M (2004) Helminthosporium leaf blight resistance and agronomic performance of wheat genotypes across warm regions of South Asia. Plant Breeding 123(6):520–524Google Scholar
  192. Sharma R, Duveiller E, Rasmussen J, Friesen T, Ali S (2003) Effect of stress on Helminthosporium leaf blight in wheat. In: Proceedings of Fourth International Wheat Tan Spot and Spot Blotch Workshop, Bemidji, Minnesota, USA. Agricultural Experiment Station, North Dakota State University, 21–24 July 2002, 2003, pp 140–144Google Scholar
  193. Sierotzki H, Parisi S, Steinfeld U, Tenzer I, Poirey S, Gisi U (2000) Mode of resistance to respiration inhibitors at the cytochrome bc1 enzyme complex of Mycosphaerella fijiensis field isolates. Pest Manag Sci 56(10):833–841Google Scholar
  194. Singh D (2007) First report of tan spot of wheat caused by Pyrenophora tritici-repentis in the Northern Hills and Northwestern Plains Zones of India. Plant Dis 91(4):460Google Scholar
  195. Singh P, Mergoum M, Gonzalez-Hernandez J, Ali S, Adhikari T, Kianian S, Elias E, Hughes G (2008) Genetics and molecular mapping of resistance to necrosis inducing race 5 of Pyrenophora tritici-repentis in tetraploid wheat. Mol Breeding 21(3):293–304Google Scholar
  196. Singh PK, Duveiller E, Singh RP (2012) Resistance breeding for tan spot (Pyrenophora tritici-repentis) In: Sharma I (ed) Disease Resistance in Wheat, pp 136Google Scholar
  197. Singh PK, Hughes GR (2006) Inheritance of resistance to the chlorosis component of tan spot of wheat caused by Pyrenophora tritici-repentis, races 1 and 3. Euphytica 152(3):413–420. doi: 10.1007/s10681-006-9229-x Google Scholar
  198. Singh PK, Mergoum M, Hughes GR (2007) Variation in virulence to wheat in Pyrenophora tritici-repentis population from Saskatchewan, Canada, from 2000 to 2002. Can J Plant Pathol-Revue Canadienne De Phytopathologie 29(2):166–171Google Scholar
  199. Stergiopoulos I, de Wit PJGM (2009) Fungal effector proteins. Ann Rev Phytopathol 47:233–263Google Scholar
  200. Strelkov S, Kowatsch R, Ballance G, Lamari L (2006) Characterization of the ToxB gene from North African and Canadian isolates of Pyrenophora tritici-repentis. Physiol Mol Plant Pathol 67(3):164–170Google Scholar
  201. Strelkov S, Lamari L (2003) Host parasite interactions in tan spot [Pyrenophora tritici-repentis] of wheat. Can J Plant Pathol 25(4):339–349Google Scholar
  202. Strelkov S, Lamari L, Ballance G (1998) Induced chlorophyll degradation by a chlorosis toxin from Pyrenophora tritici-repentis. Can J Plant Pathol 20(4):428–435Google Scholar
  203. Strelkov SE, Lamari L, Ballance GM (1999) Characterization of a host-specific protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Mol Plant Microbe In 12(8):728–732Google Scholar
  204. Strelkov SE, Lamari L, Sayoud R, Smith RB (2002) Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis. Can J Plant Pathol 24:29–35Google Scholar
  205. Sun XC, Bockus W, Bai G (2010) Quantitative trait loci for resistance to Pyrenophora tritici-repentis race 1 in a Chinese wheat. Phytopathol 100(5):468–473. doi: 10.1094/PHYTO-100-5-0468 Google Scholar
  206. Sygmund C, Klausberger M, Felice AK, Ludwig R (2011) Reduction of quinones and phenoxy radicals by extracellular glucose dehydrogenase from Glomerella cingulata suggests a role in plant pathogenicity. Microbiol 157(11):3203–3212. doi: 10.1099/mic.0.051904-0 Google Scholar
  207. Tadesse W, Hsam SLK, Wenzel G, Zeller FJ (2006a) Identification and monosomic analysis of tan spot resistance genes in synthetic wheat lines (Triticum turgidum L. × Aegilops tauschii Coss.). Crop Sci 46(3):1212–1217. doi: 10.2135/cropsci2005.10-0396 Google Scholar
  208. Tadesse W, Hsam SLK, Zeller FJ (2006b) Evaluation of common wheat cultivars for tan spot resistance and chromosomal location of a resistance gene in the cultivar ‘Salamouni’. Plant Breeding 125(4):318–322. doi: 10.1111/j.1439-0523.2006.01243.x Google Scholar
  209. Tadesse W, Reents HJ, Hsam SLK, Zeller FJ (2010) Monosomic analysis of tan spot resistance gene in the winter wheat cultivar ‘Arina’. Plant Breeding 129(5):477–479. doi: 10.1111/j.1439-0523.2009.01729.x Google Scholar
  210. Tadesse W, Schmolke M, Hsam SL, Mohler V, Wenzel G, Zeller F (2007) Molecular mapping of resistance genes to tan spot [Pyrenophora tritici-repentis race 1] in synthetic wheat lines. TAG Theor Appl Genet 114(5):855–862Google Scholar
  211. Tai Y-S, Bragg J (2007) Dual applications of a virus vector for studies of wheat–fungal interactions. Biotechnol 6(2):288–291Google Scholar
  212. Tai Y-S, Bragg J, Meinhardt SW (2007) Functional characterization of ToxA and molecular identification of its intracellular targeting protein in wheat. Am J Plant Physiol 2:76–89Google Scholar
  213. Tekauz A, Mueller E, Beyene M, Stulzer M, Schultz D (2004) Leaf spot diseases of winter wheat in Manitoba in 2003. Can Plant Dis Surv 83:73–74Google Scholar
  214. Todorova M (2006) First report of tan spot caused by Pyrenophora tritici-repentis (anamorph Drechslera tritici-repentis) in Bulgaria. Plant Pathol 55(2):305Google Scholar
  215. Tomas A, Bockus WW (1987) Cultivar-specific toxicity of the culture filtrates of Pyrenophora tritici-repentis. Phytopathol 77(9):1337–1340Google Scholar
  216. Tomas A, Feng GH, Reeck GR, Bockus WW, Leach JE (1990) Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Mol Plant-Microbe In 3:221–224Google Scholar
  217. Torriani SF, Brunner PC, McDonald BA, Sierotzki H (2009) QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag Sci 65(2):155–162PubMedGoogle Scholar
  218. Torriani SF, Goodwin SB, Kema GH, Pangilinan JL, McDonald BA (2008) Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 45(5):628–637PubMedGoogle Scholar
  219. Tuori RP, Wolpert TJ, Ciuffetti LM (1995) Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Mol Plant Microbe In 8(1):41–48Google Scholar
  220. Tuori RP, Wolpert TJ, Ciuffetti LM (2000) Heterologous expression of functional Ptr ToxA. Mol Plant Microbe In 13(4):456–464Google Scholar
  221. USDA_ERS (2012) United States Department of Agriculture Economic Research Center: Wheat Data.
  222. Vincent D, Du Fall LA, Livk A, Mathesius U, Lipscombe RJ, Oliver RP, Friesen TL, Solomon PS (2012) A functional genomics approach to dissect the mode of action of the Stagonospora nodorum effector protein SnToxA in wheat. Mol Plant Pathol 13(5):467–482. doi: 10.1111/j.1364-3703.2011.00763.x PubMedGoogle Scholar
  223. Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11 (3):301–307. doi: 10.1016/j.pbi.2008.03.002, [pii]:S1369-5266(08)00042-3
  224. Walton JD (1996) Host-selective toxins: agents of compatibility. Plant Cell 8(10):1723PubMedCentralPubMedGoogle Scholar
  225. Walton JD (2006) HC-toxin. Phytochemistry 67(14):1406–1413Google Scholar
  226. Wegulo SN, Breathnach JA, Baenziger PS (2009) Effect of growth stage on the relationship between tan spot and spot blotch severity and yield in winter wheat. Crop Prot 28(8):696–702Google Scholar
  227. Wi SJ, Jang SJ, Park KY (2010) Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum. Mol Cells 30(1):37–49PubMedGoogle Scholar
  228. Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285. doi: 10.1146/annurev.phyto.40.011402.114210, [pii]:011402.114210
  229. Yoder O, Macko V, Wolpert T, Turgeon B (1997) Cochliobolus spp. and their host-specific toxins. Mycota 5(Part A):145–166Google Scholar
  230. Zeiders KE, Sherwood RT, Berg CC (1986) Reactions of smooth bromegrass accessions to brown leaf spot caused by Pyrenophora bromi. Plant Dis 70(4):324–326Google Scholar
  231. Zerbino DR, Birney E (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Gen Res 18(5):821–829. doi: 10.1101/gr.074492.107 Google Scholar
  232. Zhang GJ, Berbee ML (2001) Pyrenophora phylogenetics inferred from ITS and glyceradehyde-3-phosphate dehydrogenase gene sequences. Mycologia 93(6):1048–1063. doi: 10.2307/3761667 Google Scholar
  233. Zhang H-F, Francl LJ, Jordahl JG, Meinhardt SW (1997) Structural and physical properties of a necrosis-inducing toxin from Pyrenophora tritici-repentis. Phytopathol 87(2):154–160Google Scholar
  234. Zhou S, Herschleb J, Schwartz DC (2007) A single molecule system for whole genome analysis. Elsevier, AmsterdamGoogle Scholar
  235. Zhou S, Wei F, Nguyen J, Bechner M, Potamousis K, Goldstein S, Pape L, Mehan MR, Churas C, Pasternak S, Forrest DK, Wise R, Ware D, Wing RA, Waterman MS, Livny M, Schwartz DC (2009) A single molecule scaffold for the maize genome. PLoS Genet 5(11):e1000711. doi: 10.1371/journal.pgen.1000711 PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Lynda M. Ciuffetti
    • 1
    Email author
  • Viola A. Manning
    • 2
  • Iovanna Pandelova
    • 2
  • Justin D. Faris
    • 3
  • Timothy L. Friesen
    • 3
  • Stephen E. Strelkov
    • 4
  • Genevieve L. Weber
    • 2
  • Stephen B. Goodwin
    • 5
  • Thomas J. Wolpert
    • 1
  • Melania Figueroa
    • 6
  1. 1.Department of Botany and Plant Pathology and Center for Genome Research and BiocomputingOregon State UniversityCorvallisUSA
  2. 2.Department of Botany and Plant PathologyOregon State UniversityCorvallisUSA
  3. 3.Cereals Crop Research Unit, Agricultural Research ServiceU.S Department of AgricultureFargoUSA
  4. 4.Department of Agricultural, Food and Nutritional ScienceUniversity of AlbertaEdmontonCanada
  5. 5.Crop Production and Pest Control Research Unit, Agricultural Research ServiceU.S Department of AgricultureWest LafayetteUSA
  6. 6.Department of Plant PathologyUniversity of MinnesotaSt. PaulUSA

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