#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Comparative Genome Structure, Secondary Metabolite, and Effector Coding Capacity across Pathogens


The genomes of five Cochliobolus heterostrophus strains, two Cochliobolus sativus strains, three additional Cochliobolus species (Cochliobolus victoriae, Cochliobolus carbonum, Cochliobolus miyabeanus), and closely related Setosphaeria turcica were sequenced at the Joint Genome Institute (JGI). The datasets were used to identify SNPs between strains and species, unique genomic regions, core secondary metabolism genes, and small secreted protein (SSP) candidate effector encoding genes with a view towards pinpointing structural elements and gene content associated with specificity of these closely related fungi to different cereal hosts. Whole-genome alignment shows that three to five percent of each genome differs between strains of the same species, while a quarter of each genome differs between species. On average, SNP counts among field isolates of the same C. heterostrophus species are more than 25× higher than those between inbred lines and 50× lower than SNPs between Cochliobolus species. The suites of nonribosomal peptide synthetase (NRPS), polyketide synthase (PKS), and SSP–encoding genes are astoundingly diverse among species but remarkably conserved among isolates of the same species, whether inbred or field strains, except for defining examples that map to unique genomic regions. Functional analysis of several strain-unique PKSs and NRPSs reveal a strong correlation with a role in virulence.


Vyšlo v časopise: Comparative Genome Structure, Secondary Metabolite, and Effector Coding Capacity across Pathogens. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003233
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003233

Souhrn

The genomes of five Cochliobolus heterostrophus strains, two Cochliobolus sativus strains, three additional Cochliobolus species (Cochliobolus victoriae, Cochliobolus carbonum, Cochliobolus miyabeanus), and closely related Setosphaeria turcica were sequenced at the Joint Genome Institute (JGI). The datasets were used to identify SNPs between strains and species, unique genomic regions, core secondary metabolism genes, and small secreted protein (SSP) candidate effector encoding genes with a view towards pinpointing structural elements and gene content associated with specificity of these closely related fungi to different cereal hosts. Whole-genome alignment shows that three to five percent of each genome differs between strains of the same species, while a quarter of each genome differs between species. On average, SNP counts among field isolates of the same C. heterostrophus species are more than 25× higher than those between inbred lines and 50× lower than SNPs between Cochliobolus species. The suites of nonribosomal peptide synthetase (NRPS), polyketide synthase (PKS), and SSP–encoding genes are astoundingly diverse among species but remarkably conserved among isolates of the same species, whether inbred or field strains, except for defining examples that map to unique genomic regions. Functional analysis of several strain-unique PKSs and NRPSs reveal a strong correlation with a role in virulence.


Zdroje

1. OhmR, FeauN, HenrissatB, SchochCL, HorwitzBA, et al. (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen dothideomycetes fungi. PLoS Pathog 8: e1003037 doi:10.1371/journal.ppat.1003037.

2. BerbeeML, PirseyediM, HubbardS (1999) Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia 91: 964–977.

3. KumarJ, SchaferP, HuckelhovenR, LangenG, BaltruschatH, et al. (2002) Bipolaris sorokiniana, a cereal pathogen of global concern: cytological and molecular approaches towards better control. Mol Plant Path 3: 185–195.

4. YoderOC (1980) Toxins in pathogenesis. Ann Rev Phytopathol 18: 103–129.

5. TurgeonBG, BakerSE (2007) Genetic and genomic dissection of the Cochliobolus heterostrophus Tox1 locus controlling biosynthesis of the polyketide virulence factor T-toxin. Adv Genet 57: 219–261.

6. UllstrupAJ (1970) History of Southern Corn Leaf Blight. Plant Dis Reptr 54: 1100–1102.

7. DrechslerC (1925) Leafspot of maize caused by Ophiobolus heterostrophus n. sp., the ascigerous stage of a Helminthosporium exhibiting bipolar germination. J Agr Res 31: 701–726.

8. TzengTH, LyngholmLK, FordCF, BronsonCR (1992) A restriction fragment length polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 130: 81–96.

9. KodamaM, RoseMS, YangG, YunSH, YoderOC, et al. (1999) The translocation-associated Tox1 locus of Cochliobolus heterostrophus is two genetic elements on two different chromosomes. Genetics 151: 585–596.

10. HookerA, SmithD, LimS, BeckettJ (1970) Reaction of corn seedlings with male-sterile cytoplasm to Helminthosporium maydis. Plant Dis Reptr 54: 708–712.

11. SmithD, HookerA, LimS (1970) Physiologic races of Helminthosporium maydis. Plant Dis Reptr 54: 819–822.

12. LitzenbergerSC (1949) Nature of susceptibility to Helminthosporium victoriae and resistance to Puccinia coronata in Victoria oats. Phytopathology 39: 300–318.

13. MeehanF, MurphyHC (1947) Differential phytotoxicity of metabolic by-products of Helminthosporium victoriae. Science 106: 270–271.

14. LorangJM, Carkaci-SalliN, WolpertTJ (2004) Identification and characterization of victorin sensitivity in Arabidopsis thaliana. Mol Plant Microbe Interact 17: 577–582.

15. LorangJM, SweatTA, WolpertTJ (2007) Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci U S A 104: 14861–14866.

16. JohalGS, BriggsSP (1992) Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258: 985–987.

17. MultaniDS, MeeleyRB, PatersonAH, GrayJ, BriggsSP, et al. (1998) Plant-pathogen microevolution: Molecular basis for the origin of a fungal disease in maize. Proc Natl Acad Sci USA 95: 1686–1691.

18. WaltonJD (1987) Two enzymes involved in biosynthesis of the host-selective phytotoxin HC-toxin. Proc Natl Acad Sci 84: 8444–8447.

19. WaltonJD (1996) Host-selective toxins: agents of compatibility. Plant Cell 8: 1723–1733.

20. RansomRF, WaltonJD (1997) Histone hyperacetylation in maize in response to treatment with HC-toxin or infection by the filamentous fungus Cochliobolus carbonum. Plant Physiol 115: 1021–1027.

21. WaltonJD (2006) HC-toxin. Phytochemistry 67: 1406–1413.

22. DasguptaMK (1984) The Bengal famine, 1943 and the brown spot of rice–an inquiry into their relations. Hist Agric 2: 1–18.

23. VidhyasekaranP, BorromeoES, MewTW (1992) Helminthosporium oryzae toxin suppresses phenol metabolism in rice plants and aids pathogen colonization. Physiological and Mol Plant Path 41: 307–315.

24. Mathre DE (1997) Compendium of Barley Diseases. 2nd Edition APS Press, St Paul.

25. Weise MV (1987) Compendium of wheat diseases. 2nd Edition APS Press, St Paul.

26. RoaneC (2004) Graminicolous fungi of Virginia: Fungi in collections 1995–2003. Virginia J Sci 55: 139–157.

27. GravertCE, GPM (2002) Fungi and diseases associated with cultivated switchgrass in Iowa. J Iowa Acad Sci 109: 30–34.

28. Valjavec-GratianM, SteffensonB (1997) Pathotypes of Cochliobolus sativus on barley. Plant Dis 81: 1275–1278.

29. Valjavec GratianM, SteffensonBJ (1997) Genetics of virulence in Cochliobolus sativus and resistance in barley. Phytopathology 87: 1140–1143.

30. ZhongS, SteffensonBJ, MartinezJP, CiuffettiLM (2002) A molecular genetic map and electrophoretic karyotype of the plant pathogenic fungus Cochliobolus sativus. MPMI 15: 481–492.

31. SteffensonBJ, HayesPM, KleinhofsA (1996) Genetics of seedling and adult plant resistance to net blotch (Pyrenophora teres f teres) and spot blotch (Cochliobolus sativus) in barley. Theor Appl Genet 92: 552–558.

32. Gyawali S (2010) Association mapping of resistance to common root rot and spot blotch in barley, and population genetics of Cochliobolus sativus. Thesis NDSU, Fargo, ND.

33. GhazviniH, TekauzA (2007) Virulence diversity in the population of Bipolaris sorokiniana. Plant Dis 91: 814–821.

34. MartinT, BirumaM, FridborgI, OkoriP, DixeliusC (2011) A highly conserved NB-LRR encoding gene cluster effective against Setosphaeria turcica in sorghum. BMC Plant Biol 11: 151.

35. ChungCL, LongfellowJM, WalshEK, KerdiehZ, Van EsbroeckG, et al. (2010) Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize–Setosphaeria turcica pathosystem. BMC Plant Biol 10: 103.

36. LeonardKJ, LevyY, SmithDR (1989) Proposed nomenclature for pathogenic races of Exserohilum turcicum on corn. Plant Dis 73: 776–777.

37. SchneiderDJ, CollmerA (2010) Studying plant-pathogen interactions in the genomics era: beyond molecular Koch's postulates to systems biology. Annu Rev Phytopathol 48: 457–479.

38. CiuffettiLM, ManningVA, PandelovaI, BettsMF, MartinezJP (2010) Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol 187: 911–919.

39. FriesenTL, FarisJD, SolomonPS, OliverRP (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10: 1421–1428.

40. WolpertTJ, DunkleLD, CiuffettiLM (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu Rev Phytopathol 40: 251–285.

41. SweatTA, WolpertTJ (2007) Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis. Plant Cell 19: 673–687.

42. LeachJ, LangBR, YoderOC (1982) Methods for selection of mutants and in vitro culture of Cochliobolus heterostrophus. J Gen Microbiol 128: 1719–1729.

43. Klittich C. (1985) Differences in fitness of strains of Cochliobolus heterostrophus near-isogenic for toxin production. PhD. Thesis, Iowa State Univ.

44. DarlingAE, MauB, PernaNT (2010) ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147 doi:10.1371/journal.pone.0011147.

45. InderbitzinP, AsvarakT, TurgeonBG (2010) Six new genes required for production of T-toxin, a polyketide determinant of high virulence of Cochliobolus heterostrophus to maize. Mol Plant Microbe Interact 23: 458–472.

46. KurtzS, PhillippyA, DelcherAL, SmootM, ShumwayM, et al. (2004) Versatile and open software for comparing large genomes. Genome Biology 5: R12.

47. Yang G (1995) The molecular genetics of T-toxin biosynthesis by Cochliobolus heterostrophus. PhD Thesis, Cornell Univ.

48. YangG, RoseMS, TurgeonBG, YoderOC (1996) A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Plant Cell 11: 2139–2150.

49. ChristiansenSK, WirselS, YoderOC, TurgeonBG (1998) The two Cochliobolus mating type genes are conserved among species but one of them is missing in C. victoriae. Mycol Res 102: 919–929.

50. FinkingR, MarahielMA (2004) Biosynthesis of nonribosomal peptides. Annu Rev Microbiol 58: 453–488.

51. SieberSA, MarahielMA (2003) Learning from nature's drug factories: Nonribosomal synthesis of macrocyclic peptides. J Bacteriol 185: 7036–7043.

52. GrunewaldJ, MarahielMA (2006) Chemoenzymatic and template-directed synthesis of bioactive macrocyclic peptides. Microbiol Mol Biol Rev 70: 121–126.

53. SteinT, VaterJ, KruftV, OttoA, WittmannLieboldB, et al. (1996) The multiple carrier model of nonribosomal peptide biosynthesis at modular multienzymatic templates. J Biol Chem 271: 15428–15435.

54. MootzHD, SchwarzerD, MarahielMA (2002) Ways of assembling complex natural products on modular nonribosomal peptide synthetases. ChemBioChem 3: 490–504.

55. LeeBN, KrokenS, ChouDYT, RobbertseB, YoderOC, et al. (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.

56. OideS, MoederW, KrasnoffS, GibsonD, HaasH, et al. (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18: 2836–2853.

57. BushleyKE, TurgeonBG (2010) Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 10: 26.

58. OideS, KrasnoffSB, GibsonDM, TurgeonBG (2007) Intracellular siderophores are essential for ascomycete sexual development in heterothallic Cochliobolus heterostrophus and homothallic Gibberella zeae. Eukaryot Cell 6: 1337–1353.

59. BushleyKE, RipollDR, TurgeonBG (2008) Module evolution and substrate specificity of fungal nonribosomal peptide synthetases involved in siderophore biosynthesis. BMC Evol Biol 8: 328.

60. AhnJH, WaltonJD (1996) Chromosomal organization of TOX2, a complex locus controlling host-selective toxin biosynthesis in Cochliobolus carbonum. Plant Cell 8: 887–897.

61. ManningV, PandelovaI, DhillonB, WilhelmL, GoodwinS, et al. (2012) Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence. G3 In press.

62. Wight WD, Walton JD (2011) Histone deacetylase inhibitor HC-toxin from Alternaria jesenskae. Asilomar, CA. pp. abstract#385, p209.

63. JinJM, LeeS, LeeJ, BaekSR, KimJC, et al. (2010) Functional characterization and manipulation of the apicidin biosynthetic pathway in Fusarium semitectum. Mol Microbiol 76: 456–466.

64. ForsethRR, FoxEM, ChungD, HowlettBJ, KellerNP, et al. (2012) Identification of cryptic products of the gliotoxin gene cluster using NMR-based comparative metabolomics and a model for gliotoxin biosynthesis. J Am Chem Soc 133: 9678–9681.

65. KrokenS, GlassNL, TaylorJW, YoderOC, TurgeonBG (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci U S A 100: 15670–15675.

66. Rose MS, Yoder OC, Turgeon BG. (1996) A decarboxylase required for polyketide toxin production and high virulence by Cochliobolus heterostrophus. 8th Int. Symp. Molec. Plant-Microbe Interact. Knoxville. pp. J-49.

67. BakerSE, KrokenS, InderbitzinP, AsvarakT, LiBY, et al. (2006) Two polyketide synthase-encoding genes are required for biosynthesis of the polyketide virulence factor, T-toxin, by Cochliobolus heterostrophus. Mol Plant Microbe Interact 19: 139–149.

68. DiohW, TharreauD, NotteghemJL, OrbachM, LebrunMH (2000) Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol Plant Microbe Interact 13: 217–227.

69. FarmanML (2007) Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it. FEMS Microbiol Lett 273: 125–132.

70. AkagiY, AkamatsuH, OtaniH, KodamaM (2009) Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8: 1732–1738.

71. KallL, KroghA, SonnhammerEL (2007) Advantages of combined transmembrane topology and signal peptide prediction–the Phobius web server. Nucleic Acids Res 35: W429–432.

72. RouxelT, GrandaubertJ, HaneJK, HoedeC, van de WouwAP, et al. (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun 2: 202.

73. HaneJK, RouxelT, HowlettBJ, KemaGH, GoodwinSB, et al. (2011) A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol 12: R45.

74. GoodwinSB, Ben M'BarekS, DhillonB, WittenbergAHJ, CraneCF, et al. (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7: e1002070 doi:10.1371/journal.pgen.1002070.

75. CuomoCA, GuldenerU, XuJR, TrailF, TurgeonBG, et al. (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400–1402.

76. McCluskeyK, WiestAE, GrigorievIV, LipzenA, MartinJ, et al. (2011) Rediscovery by whole genome sequencing: classical mutations and genome polymorphisms in Neurospora crassa. G3 (Bethesda) 1: 303–316.

77. LangfelderK, StreibelM, JahnB, HaaseG, BrakhageAA (2003) Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet Biol 38: 143–158.

78. TsaiHF, WheelerMH, ChangYC, Kwon-ChungKJ (1999) A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 181: 6469–6477.

79. PihetM, VandeputteP, TronchinG, RenierG, SaulnierP, et al. (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9: 177.

80. OliverRP, SolomonPS (2010) New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol 13: 415–9.

81. MehrabiR, BahkaliAH, Abd-ElsalamKA, MoslemM, Ben M'barekS, et al. (2011) Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev 35: 542–554.

82. KhaldiN, CollemareJ, LebrunMH, WolfeKH (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9: R18.

83. Turgeon BG, Lu S-W (2000) Evolution of host specific virulence in Cochliobolus heterostrophus. In Fungal Pathology, Ed Kronstad, JW; Kluwer, Dordrecht, The Netherlands: 93–126.

84. Wolpert TJ, Navarre DA, Lorang JM (1998) Victorin-induced oat cell death. In: Kohmoto K, Yoder OC, editors. Molecular Genetics of Host-Specific Toxins in Plant Disease. Dordrecht: Kluwer. pp. 105–114.

85. CiuffettiLM, TuoriRP, GaventaJM (1997) A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9: 135–144.

86. YunSH, TurgeonBG, YoderOC (1998) REMI-induced mutants of Mycosphaerella zeae-maydis lacking the polyketide PM-toxin are deficient in pathogenesis to corn. Physiol Mol Plant Pathol 52: 53–66.

87. Yun SH (1998) Molecular genetics and manipulation of pathogenicity and mating determinants in Cochliobolus heterostrophus and Mycosphaerella zeae-maydis. PhD Thesis, Cornell University.

88. PanaccioneDG, Scott-CraigJS, PocardJA, WaltonJD (1992) A cyclic peptide synthetase gene required for pathogenicity of the fungus Cochliobolus carbonum on maize. Proc Natl Acad Sci USA 89: 6590–6594.

89. AhnJH, ChengYQ, WaltonJD (2002) An extended physical map of the TOX2 locus of Cochliobolus carbonum required for biosynthesis of HC-toxin. Fungal Genet Biol 35: 31–38.

90. JinJM, LeeS, LeeJ, BaekSR, KimJC, et al. (2010) Functional characterization and manipulation of the apicidin biosynthetic pathway in Fusarium semitectum. Mol Microbiol 76: 456–466.

91. SindhuA, ChintamananiS, BrandtAS, ZanisM, ScofieldSR, et al. (2008) A guardian of grasses: specific origin and conservation of a unique disease-resistance gene in the grass lineage. Proc Natl Acad Sci U S A 105: 1762–1767.

92. LengYQ, ZhongSB (2012) Sfp-type 4 ′-phosphopantetheinyl transferase is required for lysine synthesis, tolerance to oxidative stress and virulence in the plant pathogenic fungus Cochliobolus sativus. Mol Plant Path 13: 375–387.

93. GardinerDM, CozijnsenAJ, WilsonLM, PedrasMS, HowlettBJ (2004) The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol Microbiol 53: 1307–1318.

94. ScharfDH, HeinekampT, RemmeN, HortschanskyP, BrakhageAA, et al. (2011) Biosynthesis and function of gliotoxin in Aspergillus fumigatus. Appl Microbiol Biotechnol 93: 467–472.

95. SweatTA, LorangJM, BakkerEG, WolpertTJ (2008) Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis. Mol Plant Microbe Interact 21: 7–19.

96. FarisJD, ZhangZ, LuH, LuS, ReddyL, et al. (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci U S A 107: 13544–13549.

97. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.

98. GnerreS, MaccallumI, PrzybylskiD, RibeiroFJ, BurtonJN, et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A 108: 1513–1518.

99. MarguliesM, EgholmM, AltmanWE, AttiyaS, BaderJS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376–380.

100. Smit A, Hubley R, Green PRO-, (1996–2010) RepeatMasker Open-3.0.

101. JurkaJ, KapitonovVV, PavlicekA, KlonowskiP, KohanyO, et al. (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogen and Genome Res 110: 462–467.

102. PriceAL, JonesNC, PevznerPA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21: I351–I358.

103. SalamovAA, SolovyevVV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10: 516–522.

104. BirneyE, DurbinR (2000) Using GeneWise in the Drosophila annotation experiment. Genome Res 10: 547–548.

105. IsonoK, McIninchJD, BorodovskyM (1994) Characteristic features of the nucleotide sequences of yeast mitochondrial ribosomal protein genes as analyzed by computer program GeneMark. DNA Res 1: 263–269.

106. KentWJ (2002) BLAT–the BLAST-like alignment tool. Genome Res 12: 656–664.

107. GrigorievIV, NordbergH, ShabalovI, AertsA, CantorM, et al. (2011) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26–32.

108. StankeM, SchoffmannO, MorgensternB, WaackS (2006) Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7: 62.

109. ZhongSB, YangBJ, AlfenasAC (2008) Development of microsatellite markers for the guava rust fungus, Puccinia psidii. Molec Ecol Res 8: 348–350.

110. LanderES, GreenP, AbrahamsonJ, BarlowA, DalyMJ, et al. (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174–181.

111. BirneyE, ClampM, DurbinR (2004) GeneWise and genomewise. Genome Res 14: 988–995.

112. StajichJE, BlockD, BoulezK, BrennerSE, ChervitzSA, et al. (2002) The bioperl toolkit: Perl modules for the life sciences. Genome Res 12: 1611–1618.

113. FinnRD, ClementsJ, EddySR (2011) HMMER web server: interactive sequence similarity searching. Nucl Acids Res 39: W29–W37.

114. AbascalF, ZardoyaR, PosadaD (2005) ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.

115. StamatakisA (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

116. StamatakisA, HooverP, RougemontJ (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57: 758–771.

117. TinlineR, StaufferJ, DicksonJ (1960) Cochliobolus sativus III Effect of ultraviolet radiation. Can J Bot 38: 275–282.

118. FetchTG, SteffensonBJ (1999) Rating scales for assessing infection responses of barley infected with Cochliobolus sativus. Plant Disease 83: 213–217.

119. WuDL, OideS, ZhangN, ChoiMY, TurgeonBG (2012) ChLae1 and ChVel1 regulate T-toxin production, virulence, oxidative stress response, and development of the maize pathogen Cochliobolus heterostrophus. PLoS Pathog 8: e1002542 doi:10.1371/journal.ppat.1002542.

120. LengY, WuC, LiuZ, FriesenTL, RasmussenJ, ZhongS (2011) Development of transformation and RNA-mediated gene silencing systems for functional genomics of Cochliobolus sativus. Mol Plant Pathol 12: 289–298.

121. CatlettN, LeeB-N, YoderO, TurgeonB (2003) Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Newsl 50: 9–11.

122. AhnJH, ChengYQ, WaltonJD (2002) An extended physical map of the TOX2 locus of Cochliobolus carbonum required for biosynthesis of HC-toxin. Fungal Genet Biol 35: 31–38.

123. WirselS, HorwitzB, YamaguchiK, YoderOC, TurgeonBG (1998) Single mating type-specific genes and their 3′ UTRs control mating and fertility in Cochliobolus heterostrophus. Mol Gen Genet 259: 272–281.

124. Turgeon B, Debuchy R, editors (2007) Cochliobolus and Podospora: Mechanisms of sex determination and the evolution of reproductive lifestyle. Washington, DC: ASM. p93–121 p.

125. Debuchy R, Turgeon BG (2006) Mating-type structure, evolution and function in Euascomycetes. In: Kües U, Fischer R, editors. The Mycota. Berlin, Heidelberg: Springer-Verlag. pp. 293–324.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#