Comparative Genomics of a Plant-Pathogenic Fungus, Pyrenophora tritici-repentis , Reveals Transduplication and the Impact of Repeat Elements on Pathogenicity and Population Divergence

Abstract

Pyrenophora tritici-repentis is a necrotrophic fungus causal to the disease tan spot of wheat, whose contribution to crop loss has increased significantly during the last few decades. Pathogenicity by this fungus is attributed to the production of host-selective toxins (HST), which are recognized by their host in a genotype-specific manner. To better understand the mechanisms that have led to the increase in disease incidence related to this pathogen, we sequenced the genomes of three P. tritici-repentis isolates. A pathogenic isolate that produces two known HSTs was used to assemble a reference nuclear genome of approximately 40 Mb composed of 11 chromosomes that encode 12,141 predicted genes. Comparison of the reference genome with those of a pathogenic isolate that produces a third HST, and a nonpathogenic isolate, showed the nonpathogen genome to be more diverged than those of the two pathogens. Examination of gene-coding regions has provided candidate pathogen-specific proteins and revealed gene families that may play a role in a necrotrophic lifestyle. Analysis of transposable elements suggests that their presence in the genome of pathogenic isolates contributes to the creation of novel genes, effector diversification, possible horizontal gene transfer events, identified copy number variation, and the first example of transduplication by DNA transposable elements in fungi. Overall, comparative analysis of these genomes provides evidence that pathogenicity in this species arose through an influx of transposable elements, which created a genetically flexible landscape that can easily respond to environmental changes.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 190

1. 1.

   Abascal F. Zardoya R. Posada D., 2005 ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105

   Not in our library10.1093/bioinformatics/bti263

2. 2.

   Aboukhaddour R. Cloutier S. Ballance G. M. 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: 201–212

   Not in our library10.1111/j.1364-3703.2008.00520.x

3. 3.

   Aboukhaddour R. Cloutier S. Lamari L. Strelkov S. E., 2011 Simple sequence repeats and diversity of globally distributed populations of Pyrenophora tritici-repentis. Can. J. Plant Pathol. 33: 389–399

   Not in our library

4. 4.

   Aboukhaddour R. Kim Y. M. Strelkov S. E., 2012 RNA-mediated gene silencing of ToxB in Pyrenophora tritici-repentis. Mol. Plant Pathol. 13: 318–326

   Not in our library10.1111/j.1364-3703.2011.00748.x

5. 5.

   Akagi Y. Akamatsu H. Otani H. Kodama M., 2009 Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot. Cell 8: 1732–1738

   Not in our library10.1128/ec.00135-09

6. 6.

   Ali S. Francl L. J., 2002 Race structure of Pyrenophora tritici-repentis isolates obtained from wheat in South America. Plant Prot. Sci. 38: 302–304

   Not in our library

7. 7.

   Ali S. Francl L. J., 2003 Population race structure of Pyrenophora tritici-repentis prevalent on wheat and noncereal grasses in the Great Plains. Plant Dis. 87: 418–422

   Not in our library10.1094/pdis.2003.87.4.418

8. 8.

   Ali S. Gurung S. Adhikari T. B., 2009 Identification and characterization of novel isolates of Pyrenophora tritici-repentis from Arkansas. Plant Dis. 94: 229–235

   Not in our library10.1094/pdis-94-2-0229

9. 9.

   Altschul S. F. Madden T. L. Schaffer A. A. Zhang J. Zhang Z., 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402

   Not in our library10.1093/nar/25.17.3389

10. 10.

    Amaike S. Ozga J. A. Basu U. Strelkov S. E., 2008 Quantification of ToxB gene expression and formation of appressoria by isolates of Pyrenophora tritici-repentis differing in pathogenicity. Plant Pathol. 57: 623–633

    Not in our library

11. 11.
    Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea · 2011

    No notice
12. 12.

    Andrie R. M. Ciuffetti L. M., 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 Interact. 24: 359–367

    Not in our library10.1094/mpmi-06-10-0142

13. 13.

    Andrie R. M. Pandelova I. Ciuffetti L. M., 2007 A combination of phenotypic and genotypic characterization strengthens Pyrenophora tritici-repentis race identification. Phytopathology 97: 694–701

    Not in our library10.1094/phyto-97-6-0694

14. 14.

    Andrie R. M. Schoch C. L. Hedges R. Spatafora J. W. Ciuffetti L. M., 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: 363–377

    Not in our library10.1016/j.fgb.2007.10.014

15. 15.

    Antoni E. A. Rybak K. Tucker M. P. Hane J. K. Solomon P. S., 2009 Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici-repentis. Australas. Plant Pathol. 39: 63–68

    Not in our library

16. 16.

    Apel-Birkhold P. C. Walton J. D., 1996 Cloning, disruption, and expression of two endo-beta 1, 4-xylanase genes, XYL2 and XYL3, from Cochliobolus carbonum. Appl. Environ. Microbiol. 62: 4129–4135

    Not in our library10.1128/aem.62.11.4129-4135.1996

17. 17.

    Aro N. Pakula T. Penttila M., 2005 Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol. Rev. 29: 719–739

    Not in our library10.1016/j.femsre.2004.11.006

18. 18.

    Bailey K. L., 1996 Diseases under conservation tillage systems. Can. J. Plant Sci. 76: 635–639

    Not in our library

19. 19.

    Ballance G. M. Lamari L. Bernier C. C., 1989 Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiol. Mol. Plant Pathol. 35: 203–213

    Not in our library

20. 20.

    Bao Z. Eddy S. R., 2002 Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res. 12: 1269–1276

    Not in our library10.1101/gr.88502

21. 21.

    Barrus M. F., 1942 Yellow-spot disease of wheat in New York. Plant Dis. Rep. 26: 246

    Not in our library

22. 22.

    Bennetzen J. L., 2000 Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 42: 251–269

    Not in our library

23. 23.

    Benslimane H. Lamari L. Benbelkacem A. Sayoud R. Bouznad Z., 2011 Distribution of races of Pyrenophora tritici-repentis in Algeria and identification of a new virulence type. Available at: http://www.fupress.net/index.php/pm/article/view/8746. Accessed: November 20, 2012

    Not in our library

24. 24.

    Bockus W. W. Claasen M. M., 1992 Effects of crop rotation and residue management practices on severity of tan spot of winter wheat. Plant Dis. 76: 633–636

    Not in our library

25. 25.

    Bockus W. W. Shroyer J. P., 1998 The impact of reduced tillage on soilborne plant pathogens. Annu. Rev. Phytopathol. 36: 485–500

    Not in our library10.1146/annurev.phyto.36.1.485

26. 26.

    Bok J. W. Chiang Y. M. Szewczyk E. Reyes-Dominguez Y. Davidson A. D., 2009 Chromatin-level regulation of biosynthetic gene clusters. Nat. Chem. Biol. 5: 462–464

    Not in our library10.1038/nchembio.177

27. 27.

    Bouras N. Strelkov S. E., 2010 Influence of carbon source on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat. Can. J. Microbiol. 56: 874–884

    Not in our library10.1139/w10-073

28. 28.

    Bouras N. Kim Y. M. Strelkov S. E., 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: 251–255

    Not in our library10.1016/j.ijfoodmicro.2009.02.001

29. 29.

    Brennan J. P. Murray G. M., 1988 Australian wheat diseases—assessing their economic importance. Agricultural Sci. 1: 26–35

    Not in our library

30. 30.
    Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships · 2010

    No notice
31. 31.

    Cambareri E. B. Jensen B. C. Schabtach E. Selker E. U., 1989 Repeat-induced G-C to A-T mutations in Neurospora. Science 244: 1571–1575

    Not in our library10.1126/science.2544994

32. 32.

    Cantarel B. L. Coutinho P. M. Rancurel C. Bernard T. Lombard V., 2009 The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37: D233–D238

    Not in our library10.1093/nar/gkn663

33. 33.

    Cao T. Kim Y. M. Kav N. N. Strelkov S. E., 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: 1177–1196

    Not in our library10.1002/pmic.200800475

34. 34.

    Carter C. J. Thornburg R. W., 2004 Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol. 134: 460–469

    Not in our library10.1104/pp.103.027482

35. 35.

    Castresana J., 2000 Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17: 540–552

    Not in our library10.1093/oxfordjournals.molbev.a026334

36. 36.

    Cavener D. R., 1992 GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J. Mol. Biol. 223: 811–814

    Not in our library10.1016/0022-2836(92)90992-s

37. 37.

    Ciuffetti L. M. Tuori R. P., 1999 Advances in the characterization of the Pyrenophora tritici-repentis-wheat interaction. Phytopathology 89: 444–449

    Not in our library10.1094/phyto.1999.89.6.444

38. 38.

    Ciuffetti L. M. Tuori R. P. Gaventa J. M., 1997 A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9: 135–144

    Not in our library10.1105/tpc.9.2.135

39. 39.

    Ciuffetti L. M. Francl L. J. Ballance G. M. Bockus W. W. Lamari L., 1998 Standardization of toxin nomenclature in the Pyrenophora tritici-repentis/wheat interaction. Can. J. Plant Pathol. 20: 421–424

    Not in our library

40. 40.

    Ciuffetti L. M. Manning V. A. Pandelova I. Betts M. F. Martinez J. P., 2010 Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol. 187: 911–919

    Not in our library10.1111/j.1469-8137.2010.03362.x

41. 41.

    Clutterbuck A. J., 2011 Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet. Biol. 48: 306–326

    Not in our library10.1016/j.fgb.2010.09.002

42. 42.

    Coghlan A. Eichler E. E. Oliver S. G. Paterson A. H. Stein L., 2005 Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet. 21: 673–682

    Not in our library10.1016/j.tig.2005.09.009

43. 43.
    The Genome of Nectria haematococca: Contribution of Supernumerary Chromosomes to Gene Expansion · 2009

    No notice
44. 44.

    Conesa A. Götz S. García-Gómez J. M. Terol J. Talón M., 2005 Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676

    Not in our library10.1093/bioinformatics/bti610

45. 45.

    Cooper C. R. Vanittanakom N., 2008 Insights into the pathogenicity of Penicillium marneffei. Future Microbiol. 3: 43–55

    Not in our library10.2217/17460913.3.1.43

46. 46.

    Cuomo C. A. Güldener U. Xu J.-R. Trail F. Turgeon B. G., 2007 The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400–1402

    Not in our library10.1126/science.1143708

47. 47.

    Custers J. H. Harrison S. J. Sela-Buurlage M. B. Van Deventer E. Lageweg W., 2004 Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence. Plant J. 39: 147–160

    Not in our library10.1111/j.1365-313x.2004.02117.x

48. 48.

    Daboussi M. J., 1997 Fungal transposable elements and genome evolution. Genetica 100: 253–260

    Not in our library

49. 49.

    Daboussi M. J. Capy P., 2003 Transposable elements in filamentous fungi. Annu. Rev. Microbiol. 57: 275–299

    Not in our library10.1146/annurev.micro.57.030502.091029

50. 50.
    progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement · 2010

    No notice
51. 51.

    De Vries R. P. Visser J., 2001 Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol. Mol. Biol. Rev. 65: 497–522

    Not in our library10.1128/mmbr.65.4.497-522.2001

52. 52.

    De Wolf E. D. Effertz R. J. Ali S. Francl L. J., 1998 Vistas of tan spot research. Can. J. Plant Pathol. 20: 349–444

    Not in our library

53. 53.

    Dean R. A. Talbot N. J. Ebbole D. J. Farman M. L. Mitchell T. K., 2005 The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980–986

    Not in our library10.1038/nature03449

54. 54.

    Delneri D. Colson I. Grammenoudi S. Roberts I. N. Louis E. J., 2003 Engineering evolution to study speciation in yeasts. Nature 422: 68–72

    Not in our library10.1038/nature01418

55. 55.

    Dimalanta E. T. Lim A. Runnheim R. Lamers C. Churas C., 2004 A microfluidic system for large DNA molecule arrays. Anal. Chem. 76: 5293–5301

    Not in our library10.1021/ac0496401

56. 56.

    Dittrich H. Kutchan T. M., 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. USA 88: 9969–9973

    Not in our library10.1073/pnas.88.22.9969

57. 57.

    Duplessis S. Cuomo C. A. Lin Y.-C. Aerts A. Tisserant E., 2011 Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl. Acad. Sci. USA 108: 9166–9171

    Not in our library10.1073/pnas.1019315108

58. 58.

    Dushnicky L. G. Ballance G. M. Sumner M. J. Macgregor A. W., 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: 19–27

    Not in our library

59. 59.

    Dushnicky L. G. Ballance G. M. Sumner M. J. Macgregor A. W., 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: 35–47

    Not in our library

60. 60.

    Dyrløv Bendtsen J. Nielsen H. Von Heijne G. Brunak S., 2004 Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340: 783–795

    Not in our library10.1016/j.jmb.2004.05.028

61. 61.

    Edgar R. C., 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797

    Not in our library10.1093/nar/gkh340

62. 62.

    Effertz R. J. Meinhardt S. W. Anderson J. A. Jordahl J. G. Francl L. J., 2002 Identification of a chlorosis-inducing toxin from Pyrenophora tritici-repentis and the chromosomal location of an insensitivity locus in wheat. Phytopathology 92: 527–533

    Not in our library10.1094/phyto.2002.92.5.527

63. 63.

    Ellwood S. R. Liu Z. Syme R. A. Lai Z. Hane J. K., 2010 A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres. Genome Biol. 11: R109

    Not in our library10.1186/gb-2010-11-11-r109

64. 64.

    Enright A. J. Van Dongen S. Ouzounis C. A., 2002 An efficient algorithm for large-scale protein families. Nucleic Acids Res. 30: 1575–1584

    Not in our library10.1093/nar/30.7.1575

65. 65.

    Facchini P. J. Penzes C. Johnson A. G. Bull D., 1996 Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol. 112: 1669–1677

    Not in our library10.1104/pp.112.4.1669

66. 66.

    Faris J. D. Zhang Z. Lu H. Lu S. Reddy L., 2010 A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl. Acad. Sci. USA 107: 13544–13549

    Not in our library10.1073/pnas.1004090107

67. 67.

    Figueroa Betts M. Manning V. A. Cardwell K. B. Pandelova I. Ciuffetti L. M., 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: 138–145

    Not in our library

68. 68.

    Finn R. D. Mistry J. Tate J. Coggill P. Heger A., 2010 The Pfam protein families database. Nucleic Acids Res. 38: D211–D222

    Not in our library10.1093/nar/gkp985

69. 69.

    Finn R. D. Clements J. Eddy S. R., 2011 HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39: W29–W37

    Not in our library10.1093/nar/gkr367

70. 70.

    Freitag M. Williams R. L. Kothe G. O. Selker E. U., 2002 A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc. Natl. Acad. Sci. USA 99: 8802–8807

    Not in our library10.1073/pnas.132212899

71. 71.

    Friesen T. L. Faris J. D., 2004 Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor. Appl. Genet. 109: 464–471

    Not in our library10.1007/s00122-004-1678-9

72. 72.

    Friesen T. L. Faris J. D., 2010 Characterization of the wheat-Stagonospora nodorum disease system: what is the molecular basis of this quantitative necrotrophic disease interaction. Can. J. Plant Pathol. 32: 20–28

    Not in our library

73. 73.

    Friesen T. L. Ali S. Klein K. K. Rasmussen J. B., 2005 Population genetic analysis of a global collection of Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Phytopathology 95: 1144–1150

    Not in our library10.1094/phyto-95-1144

74. 74.

    Friesen T. L. Stukenbrock E. H. Liu Z. Meinhardt S. Ling H., 2006 Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38: 953–956

    Not in our library10.1038/ng1839

75. 75.

    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: 1301–1309

    Not in our library10.1016/j.chembiol.2005.09.015

76. 76.

    Gamba F. M. Lamari L. Brule-Babel A. L., 1998 Inheritance of race-specific necrotic and chlorotic reactions induced by Pyrenophora tritici-repentis in hexaploid wheats. Can. J. Plant Pathol. 20: 401–407

    Not in our library

77. 77.

    Gange A. C. Gange E. G. Mohammad A. B. Boddy L., 2011 Host shifts in fungi caused by climate change? Fungal Ecol. 4: 184–190

    Not in our library

78. 78.

    Gardiner D. M. Cozijnsen A. J. Wilson L. M. Pedras M. S. Howlett B. J., 2004 The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol. Microbiol. 53: 1307–1318

    Not in our library10.1111/j.1365-2958.2004.04215.x

79. 79.

    Gielkens M. M. Dekkers E. Visser J. De Graaff L. H., 1999 Two cellobiohydrolase-encoding genes from Aspergillus niger require D-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl. Environ. Microbiol. 65: 4340–4345

    Not in our library10.1128/aem.65.10.4340-4345.1999

80. 80.
    Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis · 2011

    No notice
81. 81.

    Gruber S. Seidl-Seiboth V., 2012 Self vs. non-self: fungal cell wall degradation in Trichoderma. Microbiology 158: 26–34

    Not in our library10.1099/mic.0.052613-0

82. 82.

    Gruber S. Kubicek C. P. Seidl-Seiboth V., 2011 Differential regulation of orthologous chitinase genes in mycoparasitic Trichoderma species. Appl. Environ. Microbiol. 77: 7217–7226

    Not in our library10.1128/aem.06027-11

83. 83.

    Haas B. J. Kamoun S. Zody M. C. Jiang R. H. Handsaker R. E., 2009 Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398

    Not in our library10.1038/nature08358

84. 84.

    Hanada K. Vallejo V. Nobuta K. Slotkin R. K. Lisch D., 2009 The functional role of pack-MULEs in rice inferred from purifying selection and expression profile. Plant Cell 21: 25–38

    Not in our library10.1105/tpc.108.063206

85. 85.
    RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences · 2008

    No notice
86. 86.

    Hane J. K. Lowe R. G. Solomon P. S. Tan K. C. Schoch C. L., 2007 Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19: 3347–3368

    Not in our library10.1105/tpc.107.052829

87. 87.

    Harimoto Y. Tanaka T. Kodama M. Yamamoto M. Otani H., 2008 Multiple copies of AMT2 are prerequisite for the apple pathotype of Alternaria alternata to produce enough AM-toxin for expressing pathogenicity. J. of Genl. Plant Pathol. 74: 222–229

    Not in our library

88. 88.

    Hartl L. Zach S. Seidl-Seiboth V., 2012 Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl. Microbiol. Biotechnol. 93: 533–543

    Not in our library10.1007/s00253-011-3723-3

89. 89.

    Hays S. M. Swanson J. Selker E. U., 2002 Identification and characterization of the genes encoding the core histones and histone variants of Neurospora crassa. Genetics 160: 961–973

    Not in our library10.1093/genetics/160.3.961

90. 90.

    Hoen D. R. Park K. C. Elrouby N. Yu Z. Mohabir N., 2006 Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol. Biol. Evol. 23: 1254–1268

    Not in our library10.1093/molbev/msk015

91. 91.

    Horton P. Park K.-J. Obayashi T. Fujita N. Harada H., 2007 WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35: W585–W587

    Not in our library10.1093/nar/gkm259

92. 92.

    Imperato F. Pandalai S. G., 2006 Phytochemistry: Advances in Research: 2006. Research Signpost, Kerala, India

    Not in our library

93. 93.

    Jaffe D. B. Butler J. Gnerre S. Mauceli E. Lindblad-Toh K., 2003 Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res. 13: 91–96

    Not in our library10.1101/gr.828403

94. 94.

    Jiang N. Bao Z. Zhang X. Eddy S. R. Wessler S. R., 2004 Pack-MULE transposable elements mediate gene evolution in plants. Nature 431: 569–573

    Not in our library10.1038/nature02953

95. 95.

    Jiang R. H. Y. Weide R. Van De Vondervoort P. J. I. Govers F., 2006 Amplification generates modular diversity at an avirulence locus in the pathogen Phytophthora. Genome Res. 16: 827–840

    Not in our library10.1101/gr.5193806

96. 96.

    Jin J.-M. Lee S. Lee J. Baek S.-R. Kim J.-C., 2010 Functional characterization and manipulation of the apicidin biosynthetic pathway in Fusarium semitectum. Mol. Microbiol. 76: 456–466

    Not in our library10.1111/j.1365-2958.2010.07109.x

97. 97.

    Johnson R. D. Johnson L. Itoh Y. Kodama M. Otani H., 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 Interact. 13: 742–753

    Not in our library10.1094/mpmi.2000.13.7.742

98. 98.

    Juretic N. Hoen D. R. Huynh M. L. Harrison P. M. Bureau T. E., 2005 The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res. 15: 1292–1297

    Not in our library10.1101/gr.4064205

99. 99.

    Jurka J., 2000 Repbase update: a database and an electronic journal of repetitive elements. Trends Genet. 16: 418–420

    Not in our library10.1016/s0168-9525(00)02093-x

100. 100.

     Keeling P. J. Palmer J. D., 2008 Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9: 605–618

     Not in our library10.1038/nrg2386

101. 101.

     Kent W. J., 2002 BLAT—the BLAST-like alignment tool. Genome Res. 12: 656–664

     Not in our library10.1101/gr.229202

102. 102.

     Kihara J. Moriwaki A. Tanaka N. Tanaka C. Ueno M., 2008 Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol. Lett. 281: 221–227

     Not in our library10.1111/j.1574-6968.2008.01101.x

103. 103.

     Kim H. Ahn J. H. Gorlach J. M. Caprari C. Scott-Craig J. S., 2001 Mutational analysis of beta-glucanase genes from the plant-pathogenic fungus Cochliobolus carbonum. Mol. Plant Microbe Interact. 14: 1436–1443

     Not in our library10.1094/mpmi.2001.14.12.1436

104. 104.
     Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens · 2011

     No notice
105. 105.

     Kohli M. Mehta Y. Ackermann M., 1992 Spread of tan spot in the Southern Cone Region of South America, pp. 86–90 in Second International Tan Spot Workshop, edited by Francl L. J. Krupinsky J. McMullen M. North Dakota State University, Fargo, ND

     Not in our library

106. 106.

     Krupinsky J. M., 1982 Observations on the host range of isolates of Pyrenophora trichostoma. Can. J. Plant Pathol. 4: 42–46

     Not in our library

107. 107.
     A new method to compute K-mer frequencies and its application to annotate large repetitive plant genomes · 2008

     No notice
108. 108.

     Kwon C. Y. Rasmussen J. B. Meinhardt S. W., 1998 Activity of Ptr ToxA from Pyrenophora tritici-repentis requires host metabolism. Physiol. Mol. Plant Pathol. 52: 201–212

     Not in our library

109. 109.

     Lamari L. Bernier C. C., 1991 Genetics of tan necrosis and extensive chlorosis in tan spot of wheat caused by Pyrenophora tritici-repentis. Phytopathology 91: 1092–1095

     Not in our library

110. 110.

     Lamari L. Strelkov S. E., 2010 The wheat/Pyrenophora tritici-repentis interaction: progress towards an understanding of tan spot disease. Can. J. Plant Pathol. 32: 4–10

     Not in our library

111. 111.

     Lamari L. Strelkov S. E. Yahyaoui A. Orabi J. Smith R. B., 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. Phytopathology 93: 391–396

     Not in our library10.1094/phyto.2003.93.4.391

112. 112.

     Lamari L. Strelkov S. E. Yahyaoui A. Amedov M. Saidov M., 2005 Virulence of Pyrenophora tritici-repentis in the countries of the Silk Road. Can. J. Plant Pathol. 27: 383–388

     Not in our library

113. 113.

     Lee B.-N. Kroken S. Chou D. Y. T. Robbertse B. Yoder O. C., 2005 Functional analysis of all nonribosomal peptide synthetases in Cochliobolus heterostrophus reveals a factor, NPS6, involved in virulence and resistance to oxidative stress. Eukaryot. Cell 4: 545–555

     Not in our library10.1128/ec.4.3.545-555.2005

114. 114.

     Leisova L. Hanzalova A. Kucera L., 2008 Genetic diversity of Pyrenophora tritici-repentis isolates as revealed by AFLP analysis. J. Plant Pathol. 90: 233–245

     Not in our library

115. 115.

     Leisova-Svobodova L. Hanzalova A. Kucera L., 2010a Expansion and variability of the Ptr ToxA gene in populations of Pyrenophora tritici-repentis and Pyrenophora teres. J. Plant Pathol. 92: 729–735

     Not in our library

116. 116.

     Leisova-Svobodova L. Hanzalova A. Kucera L., 2010b 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: 125–128

     Not in our library

117. 117.

     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. Phytopathology 100: 474–483

     Not in our library10.1094/phyto-100-5-0474

118. 118.

     Li H. Ruan J. Durbin R., 2008 Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18: 1851–1858

     Not in our library10.1101/gr.078212.108

119. 119.

     Li R. Yu C. Li Y. Lam T. W. Yiu S. M., 2009 SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966–1967

     Not in our library10.1093/bioinformatics/btp336

120. 120.

     Lichter A. Gaventa J. M. Ciuffetti L. M., 2002 Chromosome-based molecular characterization of pathogenic and non-pathogenic wheat isolates of Pyrenophora tritici-repentis. Fungal Genet. Biol. 37: 180–189

     Not in our library10.1016/s1087-1845(02)00500-5

121. 121.

     Lin J. Qi R. Aston C. Jing J. Anantharaman T. S., 1999 Whole-genome shotgun optical mapping of Deinococcus radiodurans. Science 285: 1558–1562

     Not in our library10.1126/science.285.5433.1558

122. 122.

     Liu Z. Ellwood S. R. Oliver R. P. Friesen T. L., 2011 Pyrenophora teres: profile of an increasingly damaging barley pathogen. Mol. Plant Pathol. 12: 1–19

     Not in our library10.1111/j.1364-3703.2010.00649.x

123. 123.

     Loftus B. Anderson I. Davies R. Alsmark U. C. M. Samuelson J., 2005 The genome of the protist parasite Entamoeba histolytica. Nature 433: 865–868

     Not in our library10.1038/nature03291

124. 124.

     Lönneborg A. Sharma P. Stougaard P., 1995 Construction of subtractive cDNA library using magnetic beads and PCR. PCR Methods Appl. 4: 168–176

     Not in our library10.1101/gr.4.4.s168

125. 125.

     Lorang J. M. Tuori R. P. Martinez J. P. Sawyer T. L. Redman R. S., 2001 Green fluorescent protein is lighting up fungal biology. Appl. Environ. Microbiol. 67: 1987–1994

     Not in our library10.1128/aem.67.5.1987-1994.2001

126. 126.

     Lysoe E. Bone K. R. Klemsdal S. S., 2009 Real-time quantitative expression studies of the zearalenone biosynthetic gene cluster in Fusarium graminearum. Phytopathology 99: 176–184

     Not in our library10.1094/phyto-99-2-0176

127. 127.

     Ma L. J. Van Der Does H. C. Borkovich K. A. Coleman J. J. Daboussi M. J., 2010 Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367–373

     Not in our library10.1038/nature08850

128. 128.

     Maloney A. P. VanEtten H. D., 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. 243: 506–514

     Not in our library10.1007/bf00284198

129. 129.

     Manning V. A. Ciuffetti L. M., 2005 Localization of Ptr ToxA Produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17: 3203–3212

     Not in our library10.1105/tpc.105.035063

130. 130.

     Manning V. A. Hamilton S. M. Karplus P. A. Ciuffetti L. M., 2008 The Arg-Gly-Asp−containing, solvent-exposed loop of Ptr ToxA is required for internalization. Mol. Plant Microbe Interact. 21: 315–325

     Not in our library10.1094/mpmi-21-3-0315

131. 131.

     Manning V. A. Chu A. L. Steeves J. E. Wolpert T. J. Ciuffetti L. M., 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 Interact. 22: 665–676

     Not in our library10.1094/mpmi-22-6-0665

132. 132.

     Markham J. E. Hille J., 2001 Host-selective toxins as agents of cell death in plant-fungus interactions. Mol. Plant Pathol. 2: 229–239

     Not in our library10.1046/j.1464-6722.2001.00066.x

133. 133.
     Characterization of the ToxB Gene from Pyrenophora tritici-repentis · 2001

     Not checked
134. 134.

     Martinez J. P. Oesch N. W. Ciuffetti L. M., 2004 Characterization of the multiple-copy host-selective toxin gene, ToxB, in pathogenic and nonpathogenic isolates of Pyrenophora tritici-repentis. Mol. Plant Microbe Interact. 17: 467–474

     Not in our library10.1094/mpmi.2004.17.5.467

135. 135.

     McCallum B. D. Bernier C. C. Lamari L., 1994 Generation and utilization of chemical-resistant mutants in Pyrenophora tritici-repentis, the causal agent of tan spot of wheat. Can. J. Bot. 72: 100–105

     Not in our library

136. 136.

     Medd R. W. Murray G. M. Pickering D. I., 2003 Review of the epidemiology and economic importance of Pyrenophora semeniperda. Australas. Plant Pathol. 32: 539–550

     Not in our library

137. 137.

     Moreno M. V. Stenglein S. A. Balatti P. A. Perello A. E., 2008 Pathogenic and molecular variability among isolates of Pyrenophora tritici-repentis, causal agent of tan spot of wheat in Argentina. Eur. J. Plant Pathol. 122: 239–252

     Not in our library

138. 138.

     Murray G. M. Brennan J. P., 2009 Estimating disease losses to the Australian wheat industry. Australas. Plant Pathol. 38: 558–570

     Not in our library

139. 139.

     Needleman S. B. Wunsch C. D., 1970 A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48: 443–453

     Not in our library10.1016/0022-2836(70)90057-4

140. 140.

     Oliver R. P. Solomon P. S., 2010 New developments in pathogenicity and virulence of necrotrophs. Curr. Opin. Plant Biol. 13: 415–419

     Not in our library

141. 141.

     Pandelova I. Betts M. F. Manning V. A. Wilhelm L. J. Mockler T. C., 2009 Analysis of transcriptome changes induced by Ptr ToxA in wheat provides insights into the mechanisms of plant susceptibility. Molec. Plant 2: 1067–1083

     Not in our library10.1093/mp/ssp045

142. 142.

     Pandelova I. Figueroa M. Wilhelm L. J. Manning V. A. Mankaney A. N., 2012 Host-selective toxins of Pyrenophora tritici-repentis induce common responses associated with host susceptibility. PLoS ONE 7: e40240

     Not in our library10.1371/journal.pone.0040240

143. 143.

     Pautasso M. Döring T. Garbelotto M. Pellis L. Jeger M., 2012 Impacts of climate change on plant diseases—opinions and trends. Eur. J. Plant Pathol. 133: 1–19

     Not in our library

144. 144.

     Postnikova E. N. Khasanov B. A., 1998 Tan spot in Central Asia, pp. 107–113 in Helminthosporium Blights of Wheat: Spot Blotch and Tan Spot, El Batan, Mexico, edited by E. Duveiller, H. J. Dubin, J. Reeves, A. McNab. CIMMYT (International Maize and Wheat Improvement Center), Mexico, D.F., Mexico

     Not in our library

145. 145.

     Pujol Vieira Dos Santos A. M. Santos Matsumura A. T. Van Der Sand S. T., 2002 Intraspecific genetic diversity of Drechslera tritici-repentis as detected by a random amplified polymorphic DNA analysis. Genet. Mol. Biol. 25: 243–250

     Not in our library

146. 146.
     Copy Number Variation and Transcriptional Polymorphisms of Phytophthora sojae RXLR Effector Genes Avr1a and Avr3a · 2009

     Corrected
147. 147.

     Raffaele S. Kamoun S., 2012 Genome evolution in filamentous plant pathogens: why bigger can be better. Nat. Rev. Microbiol. 10: 417–430

     Not in our library10.1038/nrmicro2790

148. 148.
     Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans · 2010

     No notice
149. 149.

     Rasmussen J. B. Kwon C. Y. Meinhardt S. W., 2004 Requirement of host signaling mechanisms for the action of Ptr ToxA in wheat. Eur. J. Plant Pathol. 110: 333–335

     Not in our library

150. 150.

     Rees R. G. Platz G. J., 1983 Effects of yellow spot on wheat: comparison of epidemics at different stages of crop development. Aust. J. Agric. Res. 31: 259–267

     Not in our library

151. 151.

     Rees R. G. Platz G. J., 1992 Tan spot and its control—some Australian experiences. pp. 1–9 in Second International Tan Spot Workshop, edited by Francl L. J. Krupinsky J. McMullen M. North Dakota State University, Fargo, ND

     Not in our library

152. 152.

     Reeves C. D. Hu Z. Reid R. Kealey J. T., 2008 Genes for the biosynthesis of the fungal polyketides hypothemycin from Hypomyces subiculosus and radicicol from Pochonia chlamydosporia. Appl. Environ. Microbiol. 74: 5121–5129

     Not in our library10.1128/aem.00478-08

153. 153.

     Rep M., 2005 Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol. Lett. 253: 19–27

     Not in our library10.1016/j.femsle.2005.09.014

154. 154.

     Rice P. Longden I. Bleasby A., 2000 EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16: 76–77

     Not in our library10.1016/s0168-9525(00)02024-2

155. 155.

     Robbertse B. Reeves J. B. Schoch C. L. Spatafora J. W., 2006 A phylogenomic analysis of the Ascomycota. Fungal Genet. Biol. 43: 715–725

     Not in our library10.1016/j.fgb.2006.05.001

156. 156.

     Robbertse B. Yoder R. J. Boyd A. Reeves J. Spatafora J. W., 2011 Hal: an automated pipeline for phylogenetic analyses of genomic data. PLoS Curr. 3: RRN1213

     Not in our library10.1371/currents.rrn1213

157. 157.

     Rouxel T. Grandaubert J. Hane J. K. Hoede C. Van De Wouw A. P., 2011 Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat. Commun. 2: 202

     Not in our library10.1038/ncomms1189

158. 158.

     Sarma G. N. Manning V. A. Ciuffetti L. M. Karplus P. A., 2005 Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. Plant Cell 17: 3190–3202

     Not in our library10.1105/tpc.105.034918

159. 159.

     Schoch C. L. Shoemaker R. A. Seifert K. A. Hambleton S. Spatafora J. W., 2006 A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 98: 1041–1052

     Not in our library10.3852/mycologia.98.6.1041

160. 160.

     Schoch C. L. Crous P. W. Groenewald J. Z. Boehm E. W. A. Burgess T. I., 2009a A class-wide phylogenetic assessment of Dothideomycetes. Studies Mycol. 64: 1–15S10

     Not in our library10.3114/sim.2009.64.01

161. 161.

     Schoch C. L. Sung G. H. Lopez-Giraldez F. Townsend J. P. Miadlikowska J., 2009b The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst. Biol. 58: 224–239

     Not in our library10.1093/sysbio/syp020

162. 162.

     Schwarzer D. Marahiel M. A., 2001 Multimodular biocatalysts for natural product assembly. Naturwissenschaften 88: 93–101

     Not in our library10.1007/s001140100211

163. 163.

     Selker E. U. Cambareri E. B. Jensen B. C. Haack K. R., 1987 Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51: 741–752

     Not in our library10.1016/0092-8674(87)90097-3

164. 164.

     Shaukat A. Francl L. J., 2002 Race structure of Pyrenophora tritici-repentis isolates obtained from wheat in South America. Plant Prot. Sci. 38: 302–304

     Not in our library

165. 165.

     Singh P. K. Hughes G. R., 2006 Genetic similarity among isolates of Pyrenophora tritici-repentis, causal agent of tan spot of wheat. J. Phytopathol. 154: 178–184

     Not in our library

166. 166.

     Spanu P. D. Abbott J. C. Amselem J. Burgis T. A. Soanes D. M., 2010 Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543–1546

     Not in our library10.1126/science.1194573

167. 167.

     Spatafora J. W. Sung G. H. Johnson D. Hesse C. O’rourke B., 2006 A five-gene phylogeny of Pezizomycotina. Mycologia 98: 1018–1028

     Not in our library10.3852/mycologia.98.6.1018

168. 168.

     Sposato P. Ahn J. H. Walton J. D., 1995 Characterization and disruption of a gene in the maize pathogen Cochliobolus carbonum encoding a cellulase lacking a cellulose binding domain and hinge region. Mol. Plant Microbe Interact. 8: 602–609

     Not in our library10.1094/mpmi-8-0602

169. 169.

     Stamatakis A., 2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690

     Not in our library10.1093/bioinformatics/btl446

170. 170.

     Stergiopoulos I. De Wit P. J. G. M., 2009 Fungal effector proteins. Annu. Rev. Phytopathol. 47: 233–263

     Not in our library10.1146/annurev.phyto.112408.132637

171. 171.

     Strelkov S. E. Lamari L., 2003 Host–parasite interactions in tan spot [Pyrenophora tritici-repentis] of wheat. Can. J. Plant Pathol. 25: 339–349

     Not in our library

172. 172.

     Strelkov S. E. Lamari L. Ballance G. M., 1999 Characterization of a host-specific protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Mol. Plant Microbe Interact. 12: 728–732

     Not in our library

173. 173.

     Strelkov S. E. Lamari L. Sayoud R. Smith R. B., 2002 Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis. Can. J. Plant Pathol. 24: 29–35

     Not in our library

174. 174.

     Stukenbrock E. H. McDonald B. A., 2007 Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Mol. Plant Pathol. 8: 321–332

     Not in our library10.1111/j.1364-3703.2007.00396.x

175. 175.

     Stukenbrock E. H. McDonald B. A., 2008 The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46: 75–100

     Not in our library10.1146/annurev.phyto.010708.154114

176. 176.

     Summerall B. A. Klein T. A. Burgess L. W., 1988 Influence of stubble-management on yellow spot of wheat. Plant Prot. Q. 3: 12–13

     Not in our library

177. 177.

     Sutton J. C. Vyn T. J., 1990 Crop sequences and tillage practices in relation to diseases of winter wheat in Ontario. Can. J. Plant Pathol. 12: 358–368

     Not in our library

178. 178.

     Sygmund C. Klausberger M. Felice A. K. Ludwig R., 2011 Reduction of quinones and phenoxy radicals by extracellular glucose dehydrogenase from Glomerella cingulata suggests a role in plant pathogenicity. Microbiology 157: 3203–3212

     Not in our library10.1099/mic.0.051904-0

179. 179.

     Tan K. C. Oliver R. P. Solomon P. S. Moffat C. S., 2010 Proteinaceous necrotrophic effectors in fungal virulence. Funct. Plant Biol. 37: 907–912

     Not in our library

180. 180.

     Tomas A. Bockus W. W., 1987 Cultivar-specific toxicity of the culture filtrates of Pyrenophora tritici-repentis. Phytopathology 77: 1337–1340

     Not in our library

181. 181.

     Tomas A. Feng G. H. Reeck G. R. Bockus W. W. Leach J. E., 1990 Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Mol. Plant Microbe Interact. 3: 221–224

     Not in our library

182. 182.

     Tuori R. P. Wolpert T. J. Ciuffetti L. M., 1995 Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Mol. Plant Microbe Interact. 8: 41–48

     Not in our library10.1094/mpmi-8-0041

183. 183.

     Turgeon B. G. Oide S. Bushley K., 2008 Creating and screening Cochliobolus heterostrophus non-ribosomal peptide synthetase mutants. Mycol. Res. 112: 200–206

     Not in our library10.1016/j.mycres.2007.10.012

184. 184.

     Vincent D. Du Fall L. A. Livk A. Mathesius U. Lipscombe R. J., 2011 A functional genomics approach to dissect the mode of action of the Stagonospora nodorum effector protein SnToxA in wheat. Mol. Plant Pathol. 13: 467–482

     Not in our library10.1111/j.1364-3703.2011.00763.x

185. 185.

     Vogel J., 2008 Unique aspects of the grass cell wall. Curr. Opin. Plant Biol. 11: 301–307

     Not in our library10.1016/j.pbi.2008.03.002

186. 186.

     Walton J. D., 2006 HC-toxin. Phytochemistry 67: 1406–1413

     Not in our library10.1016/j.phytochem.2006.05.033

187. 187.

     Wolpert T. J. Dunkle L. D. Ciuffetti L. M., 2002 Host-selective toxins and avirulence determinants: what’s in a name? Annu. Rev. Phytopathol. 40: 251–285

     Not in our library10.1146/annurev.phyto.40.011402.114210

188. 188.

     Zerbino D. R. Birney E., 2008 Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18: 821–829

     Not in our library10.1101/gr.074492.107

189. 189.

     Zhou S. Herschleb J. Schwartz D. C., 2007 A Single Molecule System for Whole Genome Analysis. Elsevier, Amsterdam

     Not in our library

190. 190.

     Zhou S. G. Wei F. S. Nguyen J. Bechner M. Potamousis K., 2009 A single molecule scaffold for the maize genome. PLoS Genet. 5: e1000711

     Not in our library10.1371/journal.pgen.1000711

Cited by papers we hold 6

• Prediction of effector protein structures from fungal phytopathogens enables evolutionary analyses · 2023
  No notice
• Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen · 2018
  No notice
• Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum · 2014
  No notice
• Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens · 2014
  No notice
• Comparative Genome Structure, Secondary Metabolite, and Effector Coding Capacity across Cochliobolus Pathogens · 2013
  No notice
• Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi · 2012
  Corrected

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.