The Fusarium graminearum Histone H3 K27 Methyltransferase KMT6 Regulates Development and Expression of Secondary Metabolite Gene Clusters

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Connolly, Lanelle R ^a   Smith, Kristina M ^a   Freitag, Michael ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; LYSINE;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA SEQUENCE; FUNGAL GENE; FUNGAL GENOME; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; FUSARIUM GRAMINEARUM; GENE ACTIVATION; GENE ACTIVITY; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE SILENCING; HIGH THROUGHPUT SEQUENCING; HISTONE MODIFICATION; KMT6 GENE; NONHUMAN; PROTEIN DEPLETION; PROTEIN METHYLATION; PROTEIN SECRETION; TRANSCRIPTION REGULATION; FUSARIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MULTIGENE FAMILY; SECONDARY METABOLISM;

FUSARIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; LYSINE; MULTIGENE FAMILY; SECONDARY METABOLISM;

EID: 84887305892     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003916     Document Type: Article

References (113)

1. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature.
2. Lewis EB, (1978) A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
3. Schwartz YB, Kahn TG, Nix DA, Li XY, Bourgon R, et al. (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38: 700-705.
4. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
5. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
6. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
7. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, et al. (2007) Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1: 286-298.
8. Cavalli G, Paro R, (1999) Epigenetic inheritance of active chromatin after removal of the main transactivator. Science 286: 955-958.
9. Nishioka K, Chuikov S, Sarma K, Erdjument-Bromage H, Allis CD, et al. (2002) Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev 16: 479-489.
10. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, et al. (2005) A high-resolution map of active promoters in the human genome. Nature 436: 876-880.
11. Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE, (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10: R62.
12. Ha M, Ng DW, Li WH, Chen ZJ, (2011) Coordinated histone modifications are associated with gene expression variation within and between species. Genome Res 21: 590-598.
13. Noma K, Allis CD, Grewal SI, (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293: 1150-1155.
14. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, et al. (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411.
15. Schaft D, Roguev A, Kotovic KM, Shevchenko A, Sarov M, et al. (2003) The histone 3 lysine 36 methyltransferase, SET2, is involved in transcriptional elongation. Nucleic Acids Res 31: 2475-2482.
16. Smith KM, Kothe GO, Matsen CB, Khlafallah TK, Adhvaryu KK, et al. (2008) The fungus Neurospora crassa displays telomeric silencing mediated by multiple sirtuins and by methylation of histone H3 lysine 9. Epigenetics Chromatin 1: 5.
17. Jamieson K, Rountree MR, Lewis ZA, Stajich JE, Selker EU, (2013) Regional control of histone H3 lysine 27 methylation in Neurospora. Proc Natl Acad Sci U S A 110: 6027-6032.
18. Shi J, Dawe RK, (2006) Partitioning of the maize epigenome by the number of methyl groups on histone H3 lysines 9 and 27. Genetics 173: 1571-1583.
19. Jin W, Lamb JC, Zhang W, Kolano B, Birchler JA, et al. (2008) Histone modifications associated with both A and B chromosomes of maize. Chromosome Res 16: 1203-1214.
20. Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, et al. (2007) New nomenclature for chromatin-modifying enzymes. Cell 131: 633-636.
21. Shaver S, Casas-Mollano JA, Cerny RL, Cerutti H, (2010) Origin of the polycomb repressive complex 2 and gene silencing by an E(z) homolog in the unicellular alga Chlamydomonas. Epigenetics 5: 301-312.
22. Simon JA, Kingston RE, (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10: 697-708.
23. Margueron R, Reinberg D, (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349.
24. Zhang X, Tamaru H, Khan S, Horton J, Keefe L, et al. (2002) Structure of the Neurospora SET Domain Protein DIM-5, a Histone H3 Lysine Methyltransferase. Cell 111: 117-127.
25. Hobert O, Jallal B, Ullrich A, (1996) Interaction of Vav with ENX-1, a putative transcriptional regulator of homeobox gene expression. Mol Cell Biol 16: 3066-3073.
26. Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, et al. (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400-1402.
27. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373.
28. Gale LR, Bryant JD, Calvo S, Giese H, Katan T, et al. (2005) Chromosome complement of the fungal plant pathogen Fusarium graminearum based on genetic and physical mapping and cytological observations. Genetics 171: 985-1001.
29. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980-986.
30. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, et al. (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4: e1000046.
31. Ryan FJ, Beadle GW, Tatum EL, (1943) The tube method of measuring the growth rate of Neurospora. Am J Botany 30: 784-799.
32. Urban M, Mott E, Farley T, Hammond-Kosack K, (2003) The Fusarium graminearum MAP1 gene is essential for pathogenicity and development of perithecia. Mol Plant Pathol 4: 347-359.
33. Cavinder B, Sikhakolli U, Fellows KM, Trail F, (2012) Sexual development and ascospore discharge in Fusarium graminearum. J Vis Exp.
34. Trail F, Xu H, Loranger R, Gadoury D, (2002) Physiological and environmental aspects of ascospore discharge in Gibberella zeae (anamorph Fusarium graminearum). Mycologia 94: 181-189.
35. Hebenstreit D, Gu M, Haider S, Turner DJ, Lio P, et al. (2011) EpiChIP: gene-by-gene quantification of epigenetic modification levels. Nucleic Acids Res 39: e27.
36. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578.
37. Wiemann P, Sieber CM, von Bargen KW, Studt L, Niehaus EM, et al. (2013) Deciphering the Cryptic Genome: Genome-wide Analyses of the Rice Pathogen Fusarium fujikuroi Reveal Complex Regulation of Secondary Metabolism and Novel Metabolites. PLoS Pathog 9: e1003475.
38. Deng J, Carbone I, Dean RA, (2007) The evolutionary history of cytochrome P450 genes in four filamentous Ascomycetes. BMC Evol Biol 7: 30.
39. Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG, (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci U S A 100: 15670-15675.
40. Niehaus EM, Kleigrewe K, Wiemann P, Studt L, Sieber CM, et al. (2013) Genetic Manipulation of the Fusarium fujikuroi Fusarin Gene Cluster Yields Insight into the Complex Regulation and Fusarin Biosynthetic Pathway. Chem Biol 20: 1055-1066.
41. Jin JM, Lee J, Lee YW, (2010) Characterization of carotenoid biosynthetic genes in the ascomycete Gibberella zeae. FEMS Microbiol Lett 302: 197-202.
42. Gaffoor I, Brown DW, Plattner R, Proctor RH, Qi W, et al. (2005) Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot Cell 4: 1926-1933.
43. Morais do Amaral A, Antoniw J, Rudd JJ, Hammond-Kosack KE, (2012) Defining the Predicted Protein Secretome of the Fungal Wheat Leaf Pathogen Mycosphaerella graminicola. PLoS One 7: e49904.
44. Pauler FM, Sloane MA, Huang R, Regha K, Koerner MV, et al. (2009) H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res 19: 221-233.
45. Smith KM, Phatale PA, Sullivan CM, Pomraning KR, Freitag M, (2011) Heterochromatin is required for normal distribution of Neurospora crassa CenH3. Mol Cell Biol 31: 2528-2542.
46. Lewis ZA, Honda S, Khlafallah TK, Jeffress JK, Freitag M, et al. (2009) Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res 19: 427-437.
47. Reyes-Dominguez Y, Bok JW, Berger H, Shwab EK, Basheer A, et al. (2010) Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans. Mol Microbiol 76: 1376-1386.
48. Adhvaryu KK, Morris SA, Strahl BD, Selker EU, (2005) Methylation of Histone H3 Lysine 36 Is Required for Normal Development in Neurospora crassa. Eukaryot Cell 4: 1455-1464.
49. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, et al. (2009) Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 41: 376-381.
50. Li F, Mao G, Tong D, Huang J, Gu L, et al. (2013) The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell 153: 590-600.
51. Roudier F, Ahmed I, Berard C, Sarazin A, Mary-Huard T, et al. (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30: 1928-1938.
52. Park SY, Schwartz YB, Kahn TG, Asker D, Pirrotta V, (2012) Regulation of Polycomb group genes Psc and Su(z)2 in Drosophila melanogaster. Mech Dev 128: 536-547.
53. Ng HH, Robert F, Young RA, Struhl K, (2003) Targeted Recruitment of Set1 Histone Methylase by Elongating Pol II Provides a Localized Mark and Memory of Recent Transcriptional Activity. Mol Cell 11: 709-719.
54. Krogan NJ, Kim M, Tong A, Golshani A, Cagney G, et al. (2003) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 23: 4207-4218.
55. Bok JW, Chiang YM, Szewczyk E, Reyes-Dominguez Y, Davidson AD, et al. (2009) Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol 5: 462-464.
56. Nutzmann HW, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F, et al. (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci U S A 108: 14282-14287.
57. Malz S, Grell MN, Thrane C, Maier FJ, Rosager P, et al. (2005) Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet Biol 42: 420-433.
58. Bergmann S, Schumann J, Scherlach K, Lange C, Brakhage AA, et al. (2007) Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat Chem Biol 3: 213-217.
59. Chiang YM, Szewczyk E, Davidson AD, Keller N, Oakley BR, et al. (2009) A gene cluster containing two fungal polyketide synthases encodes the biosynthetic pathway for a polyketide, asperfuranone, in Aspergillus nidulans. J Am Chem Soc 131: 2965-2970.
60. Bromann K, Toivari M, Viljanen K, Vuoristo A, Ruohonen L, et al. (2012) Identification and characterization of a novel diterpene gene cluster in Aspergillus nidulans. PLoS One 7: e35450.
61. Maiya S, Grundmann A, Li SM, Turner G, (2009) Improved tryprostatin B production by heterologous gene expression in Aspergillus nidulans. Fungal Genet Biol 46: 436-440.
62. Itoh T, Tokunaga K, Matsuda Y, Fujii I, Abe I, et al. (2010) Reconstitution of a fungal meroterpenoid biosynthesis reveals the involvement of a novel family of terpene cyclases. Nat Chem 2: 858-864.
63. Sakai K, Kinoshita H, Nihira T, (2012) Heterologous expression system in Aspergillus oryzae for fungal biosynthetic gene clusters of secondary metabolites. Appl Microbiol Biotechnol 93: 2011-2022.
64. Williams RB, Henrikson JC, Hoover AR, Lee AE, Cichewicz RH, (2008) Epigenetic remodeling of the fungal secondary metabolome. Org Biomol Chem 6: 1895-1897.
65. Henrikson JC, Hoover AR, Joyner PM, Cichewicz RH, (2009) A chemical epigenetics approach for engineering the in situ biosynthesis of a cryptic natural product from Aspergillus niger. Org Biomol Chem 7: 435-438.
66. Schroeckh V, Scherlach K, Nutzmann HW, Shelest E, Schmidt-Heck W, et al. (2009) Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106: 14558-14563.
67. Shwab EK, Bok JW, Tribus M, Galehr J, Graessle S, et al. (2007) Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot Cell 6: 1656-1664.
68. Giles SS, Soukup AA, Lauer C, Shaaban M, Lin A, et al. (2011) Cryptic Aspergillus nidulans antimicrobials. Appl Environ Microbiol 77: 3669-3675.
69. Soukup AA, Chiang YM, Bok JW, Reyes-Dominguez Y, Oakley BR, et al. (2012) Overexpression of the Aspergillus nidulans histone 4 acetyltransferase EsaA increases activation of secondary metabolite production. Mol Microbiol 86: 314-330.
70. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, et al. (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320: 1504-1506.
71. Myung K, Li S, Butchko RA, Busman M, Proctor RH, et al. (2009) FvVE1 regulates biosynthesis of the mycotoxins fumonisins and fusarins in Fusarium verticillioides. J Agric Food Chem 57: 5089-5094.
72. Wiemann P, Brown DW, Kleigrewe K, Bok JW, Keller NP, et al. (2010) FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol 77: 972-994.
73. Jiang J, Liu X, Yin Y, Ma Z, (2011) Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PLoS One 6: e28291.
74. Merhej J, Urban M, Dufresne M, Hammond-Kosack KE, Richard-Forget F, et al. (2011) The velvet gene, FgVe1, affects fungal development and positively regulates trichothecene biosynthesis and pathogenicity in Fusarium graminearum. Mol Plant Pathol.
75. Bok JW, Keller NP, (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3: 527-535.
76. Perrin RM, Fedorova ND, Bok JW, Cramer RA, Wortman JR, et al. (2007) Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathog 3: e50.
77. Sarikaya Bayram O, Bayram O, Valerius O, Park HS, Irniger S, et al. (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6: e1001226.
78. Shaaban M, Palmer JM, El-Naggar WA, El-Sokkary MA, Habib el SE, et al. (2010) Involvement of transposon-like elements in penicillin gene cluster regulation. Fungal Genet Biol 47: 423-432.
79. Palmer JM, Perrin RM, Dagenais TR, Keller NP, (2008) H3K9 methylation regulates growth and development in Aspergillus fumigatus. Eukaryot Cell 7: 2052-2060.
80. Palmer JM, Theisen JM, Duran RM, Grayburn WS, Calvo AM, et al. (2013) Secondary metabolism and development is mediated by LlmF control of VeA subcellular localization in Aspergillus nidulans. PLoS Genet 9: e1003193.
81. Palmer JM, Mallaredy S, Perry DW, Sanchez JF, Theisen JM, et al. (2010) Telomere position effect is regulated by heterochromatin-associated proteins and NkuA in Aspergillus nidulans. Microbiology 156: 3522-3531.
82. Palmer JM, Keller NP, (2010) Secondary metabolism in fungi: does chromosomal location matter? Curr Opin Microbiol 13: 431-436.
83. Farman ML, Kim YS, (2005) Telomere hypervariability in Magnaporthe oryzae. Mol Plant Pathol 6: 287-298.
84. Farman ML, (2007) Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it. FEMS Microbiol Lett 273: 125-132.
85. Cubillos FA, Billi E, Zorgo E, Parts L, Fargier P, et al. (2011) Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol 20: 1401-1413.
86. Parts L, Cubillos FA, Warringer J, Jain K, Salinas F, et al. (2011) Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res 21: 1131-1138.
87. Walton JD, (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30: 167-171.
88. Selker EU, Tountas NA, Cross SH, Margolin BS, Murphy JG, et al. (2003) The methylated component of the Neurospora crassa genome. Nature 422: 893-897.
89. Cappellini RA, Peterson JL, (1965) Macroconidium formation in submerged cultures by a non-sporulating strain of Gibberella zeae. Mycologia 57: 962-966.
90. Leslie JF, Summerell BA (2006) The fusarium laboratory manual. Ames, Iowa: Blackwell Pub. xii, 388 p. p.
91. Geissman TA, Verbiscar AJ, Phinney BO, Cragg G, (1966) Studies on the biosynthesis of gibberellins from (-)-kaurenoic acid in cultures of Gibberella fujikuroi. Phytochem 5: 933-947.
92. Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, et al. (2006) Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1: 3111-3120.
93. Powell WA, Kistler HC, (1990) In vivo rearrangement of foreign DNA by Fusarium oxysporum produces linear self-replicating plasmids. J Bacteriol 172: 3163-3171.
94. Alting-Mees MA, Short JM, (1989) pBluescript II: gene mapping vectors. Nucleic Acids Res 17: 9494.
95. Tuori RP, Wolpert TJ, Ciuffetti LM, (2000) Heterologous expression of functional Ptr ToxA. Mol Plant Microbe Interact 13: 456-464.
96. Klittich C, Leslie JF, (1988) Nitrate reduction mutants of fusarium moniliforme (gibberella fujikuroi). Genetics 118: 417-423.
97. Pomraning KR, Smith KM, Freitag M, (2009) Genome-wide high throughput analysis of DNA methylation in eukaryotes. Methods 47: 142-150.
98. Miao VP, Freitag M, Selker EU, (2000) Short TpA-rich segments of the zeta-eta region induce DNA methylation in Neurospora crassa. J Mol Biol 300: 249-273.
99. Honda S, Selker EU, (2008) Direct interaction between DNA methyltransferase DIM-2 and HP1 is required for DNA methylation in Neurospora crassa. Mol Cell Biol 28: 6044-6055.
100. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
101. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, et al. (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34: 75-79.
102. Pomraning KR, Smith KM, Bredeweg EL, Connolly LR, Phatale PA, et al. (2012) Library preparation and data analysis packages for rapid genome sequencing. Methods Mol Biol 944: 1-22.
103. Li H, Ruan J, Durbin R, (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851-1858.
104. Luo Z, Freitag M, Sachs MS, (1995) Translational regulation in response to changes in amino acid availability in Neurospora crassa. Mol Cell Biol 15: 5235-5245.
105. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
106. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
107. Stein LD, Mungall C, Shu S, Caudy M, Mangone M, et al. (2002) The generic genome browser: a building block for a model organism system database. Genome Res 12: 1599-1610.
108. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
109. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
110. Hartigan JAaW, M.A., (1979) A K-means clustering algorithm. Applied Statistics 28: 100-108.
111. Tobiasen C, Aahman J, Ravnholt KS, Bjerrum MJ, Grell MN, et al. (2007) Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr Genet 51: 43-58.
112. Brown DW, Butchko RA, Baker SE, Proctor RH, (2012) Phylogenomic and functional domain analysis of polyketide synthases in Fusarium. Fungal Biol 116: 318-331.
113. Son H, Seo YS, Min K, Park AR, Lee J, et al. (2011) A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7: e1002310.