De novo assembly of a 40 Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis

PLoS Genetics

Volumn 6, Issue 4, 2010, Pages

  Nowrousian, Minou ^a   Stajich, Jason E ^b   Chu, Meiling ^c   Engh, Ines ^a   Espagne, Eric ^d   Halliday, Karen ^c   Kamerewerd, Jens ^a   Kempken, Frank ^e   Knab, Birgit ^f   Kuo, Hsiao Che ^c,i   Osiewacz, Heinz D ^f   Pöggeler, Stefanie ^g   Read, Nick D ^c   Seiler, Stephan ^g   Smith, Kristina M ^h   Zickler, Denise ^d   Kück, Ulrich ^a   Freitag, Michael ^h  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e UNIVERSITY OF KIEL   (Germany)

^f GOETHE UNIVERSITY   (Germany)

^g UNIVERSITY OF GÖTTINGEN   (Germany)

^h OREGON STATE UNIVERSITY   (United States)

ⁱ NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; POLYKETIDE;

ARTICLE; ASCOMYCETES; CONTROLLED STUDY; DNA SEQUENCE; FRUITING BODY; FUNGAL DEVELOPMENT; FUNGAL GENOME; FUNGAL MORPHOLOGY; FUNGUS; GENE DUPLICATION; GENE REGULATORY NETWORK; HORIZONTAL GENE TRANSFER; MEIOSIS; MOLECULAR PHYLOGENY; NEUROSPORA CRASSA; NONHUMAN; SORDARIA MACROSPORA; SPECIES COMPARISON; SYNTENY; BIOLOGICAL MODEL; GENE EXPRESSION PROFILING; GENETICS; GENOME; GENOMICS; METHODOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SORDARIALES;

EUKARYOTA; FUNGI; NEUROSPORA; NEUROSPORA CRASSA; SORDARIA MACROSPORA;

BASE SEQUENCE; GENE EXPRESSION PROFILING; GENOME; GENOME, FUNGAL; GENOMICS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEUROSPORA CRASSA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SORDARIALES;

EID: 77952337288     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000891     Document Type: Article

References (171)

1. Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105: 1422-1432.
2. Stajich JE, Berbee ML, Blackwell M, Hibbett DS, James TY, et al. (2009) The fungi. Curr Biol 19: R840-R845.
3. Buckley M (2008) The fungal kingdom - diverse and essential roles in earth's ecosystem. Washington DC: American Academy of Microbiology.
4. Smith SE, Read DJ (2000) Mycorrhizal symbiosis. London, San Diego: Academic Press.
5. Archer DB, Connerton IF, MacKenzie DA (2008) Filamentous fungi for production of food additives and processing aids. Adv Biochem Eng Biotechnol 111: 99-147.
6. Hoffmeister D, Keller NP (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24: 393-416.
7. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, et al. (1996) Life with 6000 genes. Science 274: 546-567.
8. Shendure J, Li H (2008) Next-generation DNA sequencing. Nature Biotechnol 26: 1135-1145.
9. Whiteford N, Haslam N, Weber G, Prügel-Bennett A, Essex JW, et al. (2005) An analysis of the feasibility of short read sequencing. Nucl Acids Res 33: e171.
10. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
11. Reinhardt JA, Baltrus DA, Nishimura MT, Jeck WR, Jones CD, et al. (2009) De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Res 19: 294-305.
12. DiGuistini S, Liao N, Platt D, Robertson G, Seidel M, et al. (2009) De novo genome sequence assembly of a filamentous fungus using Sanger, 454 and Illumina sequence data. Genome Biol 10: R94.
13. Li R, Fan W, Tian G, Zhu H, He L, et al. (2009) The sequence and de novo assembly of the giant panda genome. Nature advance online publication: doi:10.1038/nature08696.
14. Kück U, Pöggeler S, Nowrousian M, Nolting N, Engh I (2009) Sordaria macrospora, a model system for fungal development. In: Anke T, Weber D, eds. The Mycota XV, Physiology and Genetics. 1st ed. Berlin, Heidelberg: Springer. pp 17-39.
15. Zickler D (2005) Meiosis in mycelial fungi. In: Kües U, Fischer R, eds. The Mycota I Growth, differentiation and sexuality. Berlin, Heidelberg: Springer. pp 415-438.
16. Zickler D (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115: 158-174.
17. Pöggeler S, Nowrousian M, Kück U (2006) Fruiting-body development in ascomycetes. In: Kües U, Fischer R, eds. The Mycota I. Berlin, Heidelberg: Springer. pp 325-355.
18. Esser K, Straub J (1958) Genetische Untersuchungen an Sordaria macrospora Auersw., Kompensation und Induktion bei genbedingten Entwicklungsdefekten. Z Vererbungsl 98: 729-746.
19. Nowrousian M, Ringelberg C, Dunlap JC, Loros JJ, Kück U (2005) Crossspecies microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol Genet Genomics 273: 137-149.
20. Pöggeler S, Kück U (2006) Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene 378: 1-10.
21. Pöggeler S, Masloff S, Hoff B, Mayrhofer S, Kück U (2003) Versatile EGFP reporter plasmids for cellular localization of recombinant gene products in filamentous fungi. Curr Genet 43: 54-61.
22. Pöggeler S, Nowrousian M, Jacobsen S, Kück U (1997) An efficient procedure to isolate fungal genes from an indexed cosmid library. J Microbiol Meth 29: 49-61.
23. Rech C, Engh I, Kück U (2007) Detection of hyphal fusion in filamentous fungi using differently fluorescene-labeled histones. Curr Genet 52: 259-266.
24. Walz M, Kück U (1995) Transformation of Sordaria macrospora to hygromycin B resistance: characterization of transformants by electrophoretic karyotyping and tetrad analysis. Curr Genet 29: 88-95.
25. Engh I, Würtz C, Witzel-Schlömp K, Zhang HY, Hoff B, et al. (2007) The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies.
26. 6 zinc finger transcription factor required for fruiting body development. Genetics 152: 191-199.
27. Nowrousian M, Frank S, Koers S, Strauch P, Weitner T, et al. (2007) The novel ER membrane protein PRO41 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol Microbiol 64: 923-937.
28. Pöggeler S, Kück U (2004) A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot Cell 3: 232-240.
29. Storlazzi A, Tessé S, Gargano S, James F, Kleckner N, et al. (2003) Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev 17: 2675-2687.
30. Storlazzi A, Tesse S, Ruprich-Robert G, Gargano S, Pöggeler S, et al. (2008) Coupling meiotic chromosome axis integrity to recombination. Genes Dev 22: 796-809.
31. van Heemst D, James F, Pöggeler S, Berteaux-Lecellier V, Zickler D (1999) Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs. Cell 98: 261-271.
32. Nowrousian M, Masloff S, Pöggeler S, Kück U (1999) Cell differentiation during sexual development of the fungus Sordaria macrospora requires ATP citrate lyase activity. Mol Cell Biol 19: 450-460.
33. McClintock B (1945) Neurospora. I. Preliminary observations of the chromosomes of Neurospora crassa. Am J Bot 32: 671-678.
34. Orbach M, Vollrath D, Davis RW, Yanofsky C (1988) An electrophoretic karyotype of Neurospora crassa. Mol Cell Biol 8: 1469-1473.
35. Pöggeler S, Masloff S, Jacobsen S, Kück U (2000) Karyotype polymorphism correlates with intraspecific infertility in the homothallic ascomycete Sordaria macrospora. J Evol Biol 13: 281-289.
36. Nowrousian M (2009) A novel polyketide biosynthesis gene cluster is involved in fruiting body morphogenesis in the filamentous fungi Sordaria macrospora and Neurospora crassa. Curr Genet 55: 185-198.
37. Nowrousian M, Wü rtz C, Pöggeler S, Kück U (2004) Comparative sequence analysis of Sordaria macrospora and Neurospora crassa as a means to improve genome annotation. Fungal Genet Biol 41: 285-292.
38. Esser K (1982) Cryptogams - Cyanobacteria, Algae, Fungi, Lichens. London: Cambridge University Press.
39. Perkins DD (1992) Neurospora: the organism behind the molecular revolution. Genetics 130: 687-701.
40. Jacobson DJ, Dettman JR, Adams RI, Boesl C, Sultana S, et al. (2006) New findings of Neurospora in Europe and comparisons of diversity in temperate climates on continental scales. Mycologia 98: 550-559.
41. Jacobson DJ, Powell AJ, Dettman JR, Saenz GS, Barton MM, et al. (2004) Neurospora in temperate forests of western North America. Mycologia 96: 66-74.
42. Zerbino DR, Birney E (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
43. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
44. Dewey CN (2007) Aligning multiple whole genomes with Mercator and MAVID. In: Bergman NH, ed. Comparative genomics. Totowa: Humana Press.
45. Liu Q, Mackey AJ, Roos DS, Pereira FCN (2008) Evigan: a hidden variable model for integrating gene evidence for eukaryotic gene predictions. Bioinformatics 24: 597-605.
46. Branscomb E, Predki P (2002) On the high value of low standards. J Bacteriol 194: 6406-6409.
47. Fraser CM, Eisen JA, Nelson KE, Paulsen IT, Salzberg SL (2002) The value of complete microbial genome sequencing (you get what you pay for). J Bacteriol 184: 6403-6405.
48. Kasuga T, Mannhaupt G, Glass NL (2009) Relationship between phylogenetic distribution and genomic features in Neurospora crassa. PLOS ONE 4: e5286. doi:10.1371/journal.pone.0005286.
49. Eddy SR (1998) Profile Hidden Markov Models. Bioinformatics 14: 755-763.
50. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucl Acids Res 36: D281-288.
51. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
52. Zdobnov EM, Apweiler R (2001) InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.
53. Li L, Stoeckert CJJ, Roos DS (2003) OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
54. Jurka J (1998) Repeats in genomic DNA: mining and meaning. Curr Opin Struct Biol 8: 333-337.
55. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
56. Lynch M (2007) The origins of genome architecture. SunderlandMA: Sinauer Assocs. Inc.
57. Kempken F, Kück U (1998) Transposons in filamentous fungi - facts and perspectives. Bioessays 20: 652-659.
58. Braumann I, van den Berg M, Kempken F (2007) Transposons in biotechnologically relevant strains of Aspergillus niger and Penicillium chrysogenum. Fungal Genet Biol 44: 1399-1414.
59. Kapitonov VV, Jurka J (2008) A universal classification of eukaryotic transposable elements in Repbase. Nat Rev Genet 9: 411-412.
60. Kinsey J, Helber J (1989) Isolation of a transposable element from Neurospora crassa. Proc Nat Acad Sci USA 86: 1929-1933.
61. Kempken F, Windhofer F (2001) The hAT family: a versatile transposon group common to plants, fungi, animals, and man. Chromosoma 110: 1-9.
62. Daboussi MJ, Langin t, Brygoo Y (1992) Fot1, a new family of fungal transposable elements. Mol Gen Genet 232: 12-16.
63. Cuomo CA, Güldener 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.
64. 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.
65. Braumann I, van den Berg M, Kempken F (2008) Strain-specific retrotransposon- mediated recombination in a commercially used Aspergillus niger strain. Mol Genet Genomics 280: 319-325.
66. Rasmussen JP, Taylor AH, Ma LJ, Purcell S, Kempken F, et al. (2004) Guest, a transposable element belonging to the Tc1/mariner superfamily is an ancient invader of Neurospora genomes. Fungal Genet Biol 41: 52-61.
67. Graia F, Lespinet O, Rimbault B, Dequard-Chablat M, Coppin E, et al. (2001) Genome quality control: RIP (repeat-induced point mutation) comes to Podospora. Mol Microbiol 40: 586-595.
68. Hamann A, Feller F, Osiewacz HD (2000) The degenerate DNA transposon Pat and repeat-induced point mutation (RIP) in Podospora anserina. Mol Gen Genet 263: 1061-1069.
69. Ikeda K, Nakayashiki H, Kataoka T, Tamba H, Hashimoto Y, et al. (2002) Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context. Mol Microbiol 45: 1355-1364.
70. Idnurm A, Howlett BJ (2003) Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet Biol 39: 31-37.
71. Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20: 417-423.
72. Margolin BS, Garrett-Engele PW, Stevens JN, Fritz DY, Garrett-Engele C, et al. (1998) A methylated Neurospora 5S rRNA pseudogene contains a transposable element inactivated by repeat-induced point mutation. Genetics 149: 1787-1797.
73. Freitag M, Williams RL, Kothe GO, Selker EU (2002) A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Nat Acad Sci USA 99: 8802-8807.
74. Malagnac F, Wendel B, Goyon C, Faugeron G, Zickler D, et al. (1997) A gene essential for de novo methylation and development in Ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell 91: 281-290.
75. Lee DW, Freitag M, Selker EU, Aramayo R (2008) A cytosine methyltransferase homologue is essential for sexual development in Aspergillus nidulans. PLoS ONE 3: e2531. doi:10.1371/journal.pone.0002531.
76. Fulci V, Macino G (2007) Quelling: post-transcriptional gene silencing guided by small RNAs in Neurospora crassa. Curr Opin Microbiol 10: 199-203.
77. Shiu PKT, Raju NB, Zickler D, Metzenberg RL (2001) Meiotic silencing by unpaired DNA. Cell 107: 905-916.
78. Engh I, Nowrousian M, Kück U (2007) Regulation of melain biosynthesis via the dihydroxynaphtalene pathway is dependent on sexual development in the ascomycete Sordaria macrospora. FEMS Microbiol Lett 275: 62-70.
79. Nowrousian M, Piotrowski M, Kück U (2007) Multiple layers of temporal and spatial control regulate accumulation of the fruiting body-specific protein APP in Sordaria macrospora and Neurospora crassa. Fungal Genet Biol 44: 602-614.
80. Kück U (2005) A Sordaria macrospora mutant lacking the leu1 gene shows a developmental arrest during fruiting body formation. Mol Genet Genomics 274: 307-315.
81. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, et al. (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68: 1-108.
82. Zickler D (2009) Observing meiosis in filamentous fungi: Sordaria and Neurospora. Methods Mol Biol 558: 91-114.
83. Nowrousian M, Kück U (2006) Comparative gene expression analysis of fruiting body development in two filamentous fungi. FEMS Microbiol Lett 257: 328-335.
84. Harding RW, Melles S (1983) Genetic analysis of phototropism of Neurospora crassa perithecial beaks using white collar and albino mutants. Plant Physiol 72: 996-1000.
85. Read ND (1983) A scanning electron microscopic study of the external features of perithecium development in Sordaria humana. Can J Bot 61: 3217-3229.
86. Froehlich AC, Liu Y, Loros JJ, Dunlap JC (2002) White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297: 815-819.
87. He Q, Cheng P, Yang Y, Wang L, Gardner K, et al. (2002) White collar-1, a DNA binding transcription factor and a light sensor. Science 297: 840-843.
88. Ballario P, Vittorioso P, Magrelli A, Talora C, Cabibbo A, et al. (1996) White collar-1, a central regulator of blue-light responses in Neurospora, is a zinc finger protein. EMBO J 15: 1650-1657.
89. Purschwitz J, Müller S, Kastner C, Schöser M, Haas H, et al. (2008) Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol 18: 255-259.
90. Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, et al. (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Current Biology 15: 1833-1838.
91. Linden H, Ballario P, Arpaia G, Macino G (1999) Seeing the light: News in Neurospora blue light signal transduction. Adv Genet 41: 35-54.
92. Bieszke JA, Spudich EN, Scott KL, Borkovich KA, Spudich JL (1999) A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. Biochemistry 38: 14138-14145.
93. Griffiths AJ (1992) Fungal senescence. Annu Rev Genet 26: 351-372.
94. Osiewacz HD (1990) Molecular analysis of aging processes in fungi. Mut Res 237: 1-8.
95. Wu M, Xu L-G, Li X, Zhai Z, Shu H-B (2002) AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J Biol Chem 277: 25617-25623.
96. Averbeck NB, Jensen ON, Mann M, Schägger H, Osiewacz HD (2000) Identification and characterization of PaMTH1, a putative O-methyltransferase accumulating during senescence of Podospora anserina cultures. Curr Genet 37: 200-208.
97. Groebe K, Krause F, Kunstmann B, Unterluggauer H, Reifschneider NH, et al. (2007) Differential proteomic profiling of mitochondria from Podospora anserina, rat and human reveals distinct patterns of age-related oxidative changes. Exp Gerontol 42: 887-898.
98. Kunstmann B, Osiewacz HD (2008) Over-expression of an S-adenosylmethionine- dependent methyltransferase leads to an extended lifespan of Podospora anserina without impairments in vital functions. Aging Cell 7: 651-662.
99. Kunstmann B, Osiewacz HD (2009) The S-adenosylmethionine dependent Omethyltransferase PaMTH1: a longevity assurance factor protecting Podospora anserina against oxidative stress. Aging 1: 328-334.
100. Mata J, Lyne R, Burns G, Bähler J (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32: 143-147.
101. Schlecht U, Primig M (2003) Mining meiosis and gametogenesis with DNA microarrays. Reproduction 225: 447-456.
102. Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, et al. (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9: R77.
103. Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525-558.
104. Malik SB, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JMJ (2008) An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLOS ONE 3: e2879. doi:10.1371/journal.pone.0002879.
105. Hunter N (2006) Meiotic recombination. In: Aguilera A, Rothstein R, eds. Molecular genetics of recombination. Berlin, Heidelberg: Springer. pp 381-443.
106. O'Gorman CM, Fuller HT, Dyer PS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457: 471-475.
107. Pöggeler S (2002) Genomic evidence for mating abilities in the asexual pathogen Aspergillus fumigatus. Curr Genet 42: 153-160.
108. Read ND, Fleissner A, Roca MG, Glass NL (2010) Hyphal fusion. In: Borkovich KA, Ebbole D, eds. Molecular biology of filamentous fungi Am. Soc. Microbiol. pp 260-273.
109. Saupe S (2000) Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 64: 489-502.
110. Micali OC, Smith ML (2006) A nonself recognition gene complex in Neurospora crassa. Genetics 173: 1991-2004.
111. Cortesi P, McCulloch CE, Song H, Lin H, Milgroom MG (2001) Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics 159: 107-118.
112. Debets A, Griffiths AJ (1998) Poymorphism of het genes prevents resource plundering in Neurospora crassa. Mycol Res 102: 1343-1349.
113. Debets F, Yang X, Griffiths AJ (1994) Vegetative incompatibility in Neurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Curr Genet 26: 113-119.
114. van Diepeningen AD, Debets AJ, Hoekstra RF (1997) Heterokaryon incompatibility blocks virus transfer among natural isolates of black Aspergilli. Curr Genet 32: 209-217.
115. Glass NL, Kaneko I (2003) Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2: 1-8.
116. Smith ML, Micali OC, Hubbard SP, Mir-Rashed N, Jacobson DJ, et al. (2000) Vegetative incompatibility in the het-6 region of Neurospora crassa is mediated by two linked genes. Genetics 155: 1095-1104.
117. Paoletti M, Saupe SJ, Clavé C (2007) Genesis of a fungal non-self recognition repertoire. PLoS ONE 2: e283. doi:10.1371/journal.pone.0000283.
118. Beadle GW, Coonradt VL (1944) Heterocaryosis in Neurospora crassa. Genetics 29: 291-308.
119. Espagne E, Balhadère P, Penin ML, Barreau C, Turcq B (2002) HET-E and HET-D belong to a new subfamily of WD40 proteins involved in vegetative incompatibility specificity in the fungus Podospora anserina. Genetics 161: 71-81.
120. Shiu PK, Glass NL (1999) Molecular characterization of tol, a mediator of mating-type-associated vegetative incompatibility in Neurospora crassa. Genetics 151: 545-555.
121. Fedorova N, Badger J, Robson G, Wortman J, Nierman W (2005) Comparative analysis of programmed cell death pathways in filamentous fungi. BMC Genomics 6: 177.
122. Kaneko I, Dementhon K, Xiang Q, Glass NL (2006) Nonallelic interactions between het-c and a polymorphic locus, pin-c, are essential for nonself recognition and programmed cell death in Neurospora crassa. Genetics 172: 1545-1555.
123. Sarkar S, Iyer G, Wu J, Glass NL (2002) Nonself recognition is mediated by HET-C heterocomplex formation during vegetative incompatibility. EMBO J 21: 4841-4850.
124. Jacobson DJ, Beurkens K, Klomarens KL (1998) Microscopic and ultrastructural examination of vegetative incompatibility in partial diploids heterozygous at het loci in Neurospora crassa. Fungal Genet Biol 23: 45-56.
125. Mylek OM (1975) Heterokaryon incompatibility genes in Neurospora crassa detected using duplication-producing chromosome rearrangements. Genetics 80: 107-124.
126. Perkins DD (1975) The use of duplication-generating rearrangements for studying heterokaryon incompatibility genes in Neurospora. Genetics 80: 87-105.
127. Wu J, Glass NL (2001) Identification of specificity determinants and generation of alleles with novel specificity at the het-c heterokaryon incompatibility locus of Neurospora crassa. Mol Cell Biol 21: 1045-1057.
128. Pöggeler S, Risch S, Kück U, Osiewacz HD (1997) Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 147: 567-580.
129. Jacobson DJ (1992) Control of mating type heterokaryon incompatibility by the tol gene in Neurospora crassa and N. tetrasperma. Genome 35: 347-353.
130. Mir-Rashed N, Jacobson DJ, Dehghany MR, Micali OC, Smith ML (2000) Molecular and functional analyses of incompatibility genes at het-6 in a population of Neurospora crassa. Fungal Genet Biol 30: 197-205.
131. Powell AJ, Jacobson DJ, Natvig DO (2007) Ancestral polymorphism and linkage disequilibrium at the het-6 region in pseudohomothallic Neurospora tetrasperma. Fungal Genet Biol 44: 896-904.
132. Cox RJ (2007) Polyketides, proteins and genes in fungi: programmed nanomachines begin to reveal their secrets. Org Biomol Chem 5: 2010-2026.
133. Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303: 1805-1810.
134. Keller NP, Hohn TM (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21: 17-29.
135. Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG (2003) Phylogenomic analyis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Nat Acad Sci USA 100: 15670-15675.
136. Hane JK, Lowe RGT, Solomon PS, Tan K-C, Schoch CL, et al. (2007) Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19: 3347-3368.
137. Rosewich UL, Kistler HC (2000) Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38: 326-363.
138. Khaldi N, Wolfe KH (2008) Elusive origins of the extra genes in Aspergillus oryzae. PLOS ONE 3: e3036. doi:10.1371/journal.pone.0003036.
139. Patron NJ, Waller RF, Cozijnsen AJ, Straney DC, Gardiner DM, et al. (2007) Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol Biol 7: 174.
140. Khaldi N, Collemare J, Lebrun M-H, Wolfe KH (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9: R18.
141. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, et al. (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38: 953-956.
142. 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. doi:10.1371/journal.pgen.1000046.
143. Garcia-Vallvé S, Romeu A, Palau J (2000) Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol 17: 352-361.
144. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, et al. (2009) The genome of Nectria haematococca: Contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5: e1000618. doi:10.1371/ journal.pgen.1000618.
145. Hoge JHC, Springer J, Zantinge B, Wessels JGH (1982) Absence of differences in polysomal RNAs from vegetative monokaryotic and dikaryotic cells of the fungus Schizophyllum commune. Exp Mycol 6: 225-232.
146. Pomraning KR, Smith KM, Freitag M (2009) Genome-wide high throughput analysis of DNA methylation in eukaryotes. Methods 47: 142-150.
147. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
148. Engels R, Yu T, Burge C, Mesirov JP, DeCaprio D, et al. (2006) Combo: a whole genome comparative browser. Bioinformatics 22: 1782-1783.
149. Korf I (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59.
150. Stanke M, Schöffmann O, Morgenstern B, Waack S (2006) Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7: 62.
151. Stanke M, Waack S (2003) Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19(suppl. 2): ii215-225.
152. Besemer J, Borodovsky M (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucl Acids Res 33: W451-454.
153. Birney E, Clamp M, Durbin R (2004) GeneWise and Genomewise. Genome Res 14: 988-955.
154. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, et al. (2002) The Bioperl Toolkit: Perl modules for the life sciences. Genome Res 12: 1611-1618.
155. Horton P, Park KJ, Obayashi T, Nakai K (2006) Protein subcellular localization prediction with WoLF PSORT. Proceedings of the 4th Annual Asia Pacific Bioinformatics Conference APBC06, Taipei, Taiwan. pp 39-48.
156. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
157. Tusnady GE, Simon I (1998) Principles governing amino acid composition of integral membrane proteins: Applications to topology prediction. J Mol Biol 283: 489-506.
158. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 305: 567-580.
159. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 25: 955-964.
160. Nawrocki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335-1337.
161. Taquist H, Cui Y, Ardell DH (2007) TFAM 1.0: an online tRNA function classifier. Nucl Acids Res 35: W350-353.
162. Nowrousian M, Cebula P (2005) The gene for a lectin-like protein is transcriptionally activated during sexual development, but is not essential for fruiting body formation in the filamentous fungus Sordaria macrospora. BMC Microbiol 5: 64.
163. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24: 4876-4882.
164. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
165. Huelsenbeck JP, Ronquist F (2001) Bayesian inference of phylogeny. Bioinformatics 17: 754-755.
166. Ronquist F, Huelsenbeck JP (2003) Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
167. Hall BG (2004) Phylogenetic trees made easy. Sunderland: Sinauer Associates.
168. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, et al. (2007) Dendroscope - An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8: 460.
169. Page R (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Appl Biosci 12: 357-358.
170. Dementhon K, Iyer G, Glass NL (2006) VIB-1 Is required for expression of genes necessary for programmed cell death in Neurospora crassa. Eukaryot Cell 5: 2161-2173.
171. Liu YJ, Hall BD (2004) Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Nat Acad Sci USA 101: 4507-4512.