#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The Genome and Development-Dependent Transcriptomes of : A Window into Fungal Evolution


Fungi are a large group of eukaryotes found in nearly all ecosystems. More than 250 fungal genomes have already been sequenced, greatly improving our understanding of fungal evolution, physiology, and development. However, for the Pezizomycetes, an early-diverging lineage of filamentous ascomycetes, there is so far only one genome available, namely that of the black truffle, Tuber melanosporum, a mycorrhizal species with unusual subterranean fruiting bodies. To help close the sequence gap among basal filamentous ascomycetes, and to allow conclusions about the evolution of fungal development, we sequenced the genome and assayed transcriptomes during development of Pyronema confluens, a saprobic Pezizomycete with a typical apothecium as fruiting body. With a size of 50 Mb and ∼13,400 protein-coding genes, the genome is more characteristic of higher filamentous ascomycetes than the large, repeat-rich truffle genome; however, some typical features are different in the P. confluens lineage, e.g. the genomic environment of the mating type genes that is conserved in higher filamentous ascomycetes, but only partly conserved in P. confluens. On the other hand, P. confluens has a full complement of fungal photoreceptors, and expression studies indicate that light perception might be similar to distantly related ascomycetes and, thus, represent a basic feature of filamentous ascomycetes. Analysis of spliced RNA-seq sequence reads allowed the detection of natural antisense transcripts for 281 genes. The P. confluens genome contains an unusually high number of predicted orphan genes, many of which are upregulated during sexual development, consistent with the idea of rapid evolution of sex-associated genes. Comparative transcriptomics identified the transcription factor gene pro44 that is upregulated during development in P. confluens and the Sordariomycete Sordaria macrospora. The P. confluens pro44 gene (PCON_06721) was used to complement the S. macrospora pro44 deletion mutant, showing functional conservation of this developmental regulator.


Vyšlo v časopise: The Genome and Development-Dependent Transcriptomes of : A Window into Fungal Evolution. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003820
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003820

Souhrn

Fungi are a large group of eukaryotes found in nearly all ecosystems. More than 250 fungal genomes have already been sequenced, greatly improving our understanding of fungal evolution, physiology, and development. However, for the Pezizomycetes, an early-diverging lineage of filamentous ascomycetes, there is so far only one genome available, namely that of the black truffle, Tuber melanosporum, a mycorrhizal species with unusual subterranean fruiting bodies. To help close the sequence gap among basal filamentous ascomycetes, and to allow conclusions about the evolution of fungal development, we sequenced the genome and assayed transcriptomes during development of Pyronema confluens, a saprobic Pezizomycete with a typical apothecium as fruiting body. With a size of 50 Mb and ∼13,400 protein-coding genes, the genome is more characteristic of higher filamentous ascomycetes than the large, repeat-rich truffle genome; however, some typical features are different in the P. confluens lineage, e.g. the genomic environment of the mating type genes that is conserved in higher filamentous ascomycetes, but only partly conserved in P. confluens. On the other hand, P. confluens has a full complement of fungal photoreceptors, and expression studies indicate that light perception might be similar to distantly related ascomycetes and, thus, represent a basic feature of filamentous ascomycetes. Analysis of spliced RNA-seq sequence reads allowed the detection of natural antisense transcripts for 281 genes. The P. confluens genome contains an unusually high number of predicted orphan genes, many of which are upregulated during sexual development, consistent with the idea of rapid evolution of sex-associated genes. Comparative transcriptomics identified the transcription factor gene pro44 that is upregulated during development in P. confluens and the Sordariomycete Sordaria macrospora. The P. confluens pro44 gene (PCON_06721) was used to complement the S. macrospora pro44 deletion mutant, showing functional conservation of this developmental regulator.


Zdroje

1. Buckley M (2008) The fungal kingdom - diverse and essential roles in earth's ecosystem. Washington DC: American Academy of Microbiology.

2. HawksworthDL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105: 1422–1432.

3. EbersbergerI, de Matos SimoesR, KupczokA, GubeM, KotheE, et al. (2012) A consistent phylogenetic backbone for the fungi. Mol Biol Evol 29: 1319–1334.

4. HibbettDS, BinderM, BischoffJF, BlackwellM, CannonPF, et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111: 509–547.

5. LiuYJ, HallBD (2004) Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Nat Acad Sci USA 101: 4507–4512.

6. NowrousianM, KückU (2006) Comparative gene expression analysis of fruiting body development in two filamentous fungi. FEMS Microbiol Lett 257: 328–335.

7. ZhuangWY, LiuCY (2012) What an rRNA secondary structure tells about phylogeny of fungi in ascomycota with emphasis on evolution of major types of ascus. PLoS One 7: e47546.

8. SpataforaJW, SungG-H, JohnsonD, HesseC, O'RourkeB, et al. (2006) A five-gene phylogeny of Pezizomycotina. Mycologia 98: 1018–1028.

9. MartinF, KohlerA, MuratC, BalestriniR, CoutinhoPM, et al. (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033–1039.

10. YangJ, WangL, JiX, FengY, LiX, et al. (2011) Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathog 7: e1002179.

11. PfisterDH, LiftikME (1995) Two Arthrobotrys anamorphs from Orbilia auricolor. Mycologia 87: 684–688.

12. RaffaeleS, KamounS (2012) Genome evolution in filamentous platn pathogens: why bigger can be better. Nat Rev Microbiol 10: 417–430.

13. ClaussenP (1912) Zur Entwicklungsgeschichte der Ascomyceten. Pyronema confluens. Zeitschr f Bot 4: 1–63.

14. Gwynne-VaughanHCI, WilliamsonHS (1931) Contributions to the study of Pyronema confluens. Ann Bot 45: 355–371.

15. KerlI (1937) Über Regenerationsversuche an Fruchtkörpern und andere entwicklungsphysiologische Untersuchungen bei Pyronema confluens. Zeitschr f Bot 31: 9–174.

16. MooreEJ, KorfRP (1963) The genus Pyronema. Bull Torrey Bot Club 90: 33–42.

17. WilsonIM (1952) The ascogenous hyphae of Pyronema confluens. Ann Bot 56: 321–338.

18. GesingS, SchindlerD, FränzelB, WoltersD, NowrousianM (2012) The histone chaperone ASF1 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol Microbiol 84: 748–765.

19. GesingS, SchindlerD, NowrousianM (2012) Suppression subtractive hybridization and comparative expression analysis to identify developmentally regulated genes in filamentous fungi. J Basic Microbiol doi: 10.1002/jobm.201200223

20. SeaverFJ (1909) Studies in pyrophilous fungi - I. The occurence and cultivation of Pyronema. Mycologia 1: 131–139.

21. RobinsonW (1926) The conditions of growth and development of Pyronema confluens, Tul. (P. omphaloides, (Bull.) Fuckel). Ann Bot 40: 245–272.

22. NowrousianM, StajichJE, ChuM, EnghI, EspagneE, et al. (2010) De novo assembly of a 40 Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet 6: e1000891.

23. The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189–195.

24. TeichertI, WolffG, KückU, NowrousianM (2012) Combining laser microdissection and RNA-seq to chart the transcriptional landscape of fungal development. BMC Genomics 13: 511.

25. CantarelBL, KorfI, RobbSMC, ParraG, RossE, et al. (2008) MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18: 188–196.

26. ParraG, BradnamK, NingZ, KeaneT, KorfI (2009) Assessing the gene space in draft genomes. Nucl Acids Res 37: 289–297.

27. TisserantE, Da SilvaC, KohlerA, MorinE, WinckerP, et al. (2011) Deep RNA sequencing improved the structural annotation of the Tuber melanosporum transcriptome. New Phytol 189: 883–891.

28. WangB, GuoG, WangC, LinY, WangX, et al. (2010) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucl Acids Res 38: 5075–5087.

29. DjebaliS, DavisCA, MerkelA, DobinA, LassmannT, et al. (2012) Landscape of transcription in human cells. Nature 489: 101–108.

30. DonaldsonME, SavilleBJ (2012) Natural antisense transcripts in fungi. Mol Microbiol 83: 405–417.

31. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinf 25: 1105–1111.

32. DelmasS, PullanST, GaddipatiS, KokolskiM, MallaS, et al. (2012) Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 8: e1002875.

33. GowdaM, VenuRC, RaghupathyMB, NobutaK, LiH, et al. (2006) Deep and comparative analysis of the mycelium and appressorium transcriptomes of Magnaporthe grisea using MPSS, RL-SAGE, and oligoarray methods. BMC Genomics 7: 310.

34. SmithCA, RobertsonD, YatesB, NielsenDM, BrownD, et al. (2008) The effect of temperature on natural antisense transcript (NAT) expression in Aspergillus flavus. Curr Genet 54: 241–269.

35. ChengCK, AuCH, WilkeSK, StajichJE, ZolanME, et al. (2013) 5′-Serial analysis of gene expression studies reveal a transcriptomic switch during fruiting body development in Coprinopsis cinerea. BMC Genomics 14: 195.

36. DoyleEE, DonaldsonME, MorrisonEN, SavilleBJ (2011) Ustilago maydis transcript features identified through full-length cDNA analysis. Mol Genet Genomics 286: 143–159.

37. OhmRA, de JongJF, LugonesLG, AertsA, KotheE, et al. (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotech 28: 957–963.

38. ManningVA, PandelovaI, DhillonB, WilhelmLJ, GoodwinSB, et al. (2013) Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence. G3 (Bethesda) 3: 41–63.

39. MaL-J, van der DoesHC, BorkovichKA, ColemanJJ, DaboussiM-J, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367–373.

40. ColemanJJ, RounsleySD, Rodriguez-CarresM, KuoA, WasmannCC, et al. (2009) The genome of Nectria haematococca: Contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5: e1000618.

41. FreitagM, WilliamsRL, KotheGO, SelkerEU (2002) A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Nat Acad Sci USA 99: 8802–8807.

42. SelkerEU, CambareriEB, JensenBC, HaackKR (1987) Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51: 741–752.

43. CambareriEB, BryanJC, SchabtachE, SelkerEU (1989) Repeat-induced point mutations. Science 244: 1571–1575.

44. GalaganJE, SelkerEU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20: 417–423.

45. StajichJE, DietrichFS, RoySW (2007) Comparative genomic analysis of fungal genomes reveals intron-rich ancestors. Genome Biol 8: R223.

46. HebenstreitD, FangM, GuM, CharoensawanV, van OudenaardenA, et al. (2011) RNA sequencing reveals two major classes of gene expression levels in metazoan cells. Mol Syst Biol 7: 497.

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

48. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

49. SandersonMJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinf 19: 301–302.

50. BonitoG, SmithME, NowakM, HealyRA, GuevaraG, et al. (2013) Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage. PLoS One 8: e52765.

51. TurgeonG, YoderOC (2000) Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol 31: 1–5.

52. PöggelerS (2001) Mating-type genes for classical strain improvements of ascomycetes. Appl Microbiol Biotechnol 56: 589–601.

53. PöggelerS, RischS, KückU, OsiewaczHD (1997) Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 147: 567–580.

54. PöggelerS, O'GormanCM, HoffB, KückU (2011) Molecular organization of the mating-type loci in the homothallic ascomycete Eupenicillium crustaceum. Fungal Biol 115: 615–624.

55. Debuchy R, Berteaux-Leceleir V, Silar P (2010) Mating systems and sexual morphogenesis in ascomycetes. In: Borkovich KA, Ebbole DJ, editors. Cellular and molecular biology of filamentous fungi. Washington, DC: ASM Press. pp. 501–535.

56. PaolettiM, SeymourFA, AlcocerMJC, KaurN, CalvoAM, et al. (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol 17: 1384–1389.

57. RydholmC, DyerPS, LutzoniF (2007) DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri. Eukaryot Cell 6: 868–874.

58. RubiniA, BelfioriB, RiccioniC, TisserantE, ArcioniS, et al. (2011) Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytol 183: 710–722.

59. Debuchy R, Turgeon BG (2006) Mating-type structure, evolution, and function in Euascomycetes. In: Kües U, Fischer R, editors. The Mycota I: Growth, differentiation and sexuality. Berlin, Heidelberg: Springer-Verlag. pp. 293–323.

60. ButlerG, KennyC, FaganA, KurischkoC, GaillardinC, et al. (2004) Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc Nat Acad Sci USA 101: 1632–1637.

61. Dyer PS (2007) Sexual reproduction and significance of MAT in the Aspergilli. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA, editors. Sex in fungi. Washington, DC: ASM Press. pp. 123–142.

62. HoffB, PöggelerS, KückU (2008) Eighty years after its discovery, Fleming's Penicillium strain discloses the secret of its sex. Eukaryot Cell 7: 465–470.

63. LeeSC, NiM, LiW, ShertzC, HeitmanJ (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74: 298–340.

64. SwansonWJ, VacquierVD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3: 137–144.

65. ClarkNL, AagarardJE, SwansonWJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131: 11–22.

66. BrawandD, SoumillonM, NecsuleaA, JulienP, CsardiG, et al. (2011) The evolution of gene expression levels in mammalian organs. Nature 478: 343–348.

67. ButlerG, RasmussenMD, LinMF, SantosMAS, SakthikumarS, et al. (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657–662.

68. PöggelerS (1999) Phylogenetic relationships between mating-type sequences from homothallic and heterothallic ascomycetes. Curr Genet 36: 222–231.

69. KarlssonM, NygrenK, JohannessonH (2008) The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic Neurospora. Mol Biol Evol 25: 168–178.

70. NygrenK, WallbergA, SamilsN, StajichJE, TownsendJP, et al. (2012) Analyses of expressed sequence tags in Neurospora reveal rapid evolution of genes associated with the early stages of sexual reproduction in fungi. BMC Evol Biol 12: 229.

71. LipmanDJ, SouvorovA, KooninEV, PanchenkoAR, TatusovaTA (2002) The relationship of protein conservation and sequence length. BMC Evol Biol 2: 20.

72. PálC, PappB, HurstLD (2001) Highly expressed genes in yeast evolve slowly. Genetics 158: 927–931.

73. SubramanianS, KumarS (2004) Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168: 373–381.

74. CaiJJ, WooPCY, LauSKP, SmithDK, YuenKY (2006) Accelerated evoutionary rate may be responsible for the emergence of lineage-specific genes in ascomycota. J Mol Evol 63: 1–11.

75. CarvunisA-R, RollandT, WapinskiI, CalderwoodMA, YildirimMA, et al. (2012) Proto-genes and de novo gene birth. Nature 487: 370–374.

76. TautzD, Domazet-LošoT (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12: 692–702.

77. KasugaT, GlassNL (2008) Dissecting colony development of Neurospora crassa using mRNA profiling and comparative genomics approaches. Eukaryot Cell 7: 1549–1564.

78. Rodriguez-RomeroJ, HedtkeM, KastnerC, MüllerS, FischerR (2010) Fungi, hidden in soil or up in the air: light makes a difference. Annu Rev Microbiol 64: 585–610.

79. SeidlV, SeibelC, KubicekCP, SchmollM (2009) Sexual development in the industrial workhorse Trichoderma reesei. Proc Nat Acad Sci USA 106: 13909–13914.

80. ChenCL, KuoHC, TungSY, HsuPWC, WangCL, et al. (2012) Blue light acts as a s double-edged sword in regulating sexual development in Hypocrea jecorina (Trichoderma reesei). PLoS One 7: e44969.

81. PerkinsJH (1969) Morphogenesis in Schizophyllum commune. I. Effects of white light. Plant Physiol 44: 1706–1711.

82. KüesU (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64: 316–353.

83. PerkinsJH, GordonSA (1969) Morphogenesis in Schizophyllum commune. II. Effects of monochromatic light. Plant Physiol 44: 1712–1716.

84. FroehlichAC, LiuY, LorosJJ, DunlapJC (2002) White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297: 815–819.

85. BallarioP, VittoriosoP, MagrelliA, TaloraC, CabibboA, 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.

86. CrosthwaiteSC, DunlapJC, LorosJJ (1997) Neurospora wc-1 and wc-2: Transcription, photoresponses, and the origins of circadian rhythmicity. Science 276: 763–769.

87. LindenH, MacinoG (1997) White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J 16: 98–109.

88. TaloraC, FranchiL, LindenH, BallarioP, MacinoG (1999) Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J 18: 4961–4968.

89. HeintzenC, LorosJJ, DunlapJC (2001) The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104: 453–464.

90. SchwerdtfegerC, LindenH (2003) VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J 22: 4846–4855.

91. BlumensteinA, VienkenK, TaslerR, PurschwitzJ, VeithD, et al. (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr Biol 15: 1833–1838.

92. BieszkeJA, SpudichEN, ScottKL, BorkovichKA, SpudichJL (1999) A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. Biochemistry 38: 14138–14145.

93. BieszkeJA, BraunEL, BeanLE, KangS, NatvigDO, et al. (1999) The nop-1 gene of Neurospora crassa encodes a seven transmembrane helix retinal-binding protein homologous to archaeal rhodopsins. Proc Nat Acad Sci USA 96: 8034–8039.

94. BrownLS (2004) Fungal rhodopsins and opsin-related proteins: eukaryotic homologues of bacteriorhodopsin with unknown functions. Photochem Photobiol Sci 3: 555–565.

95. DunlapJC, LorosJJ (2006) How fungi keep time: circadian system in Neurospora and other fungi. Curr Opin Microbiol 9: 579–587.

96. SalichosL, RokasA (2010) The diversity and evolution of circadian clock proteins in fungi. Mycologia 102: 269–278.

97. CrosthwaiteSC, LorosJJ, DunlapJC (1995) Light-Induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81: 1003–1012.

98. KramerC, LorosJJ, DunlapJC, CrosthwaiteSK (2003) Role for antisense RNA in regulating circadian clock function in Neurospora crassa. Nature 421: 948–952.

99. DiernfellnerACR, SchafmeierT, MerrowMW, BrunnerM (2005) Molecular mechanism of temperature sensing by the circadian clock of Neurospora crassa. Genes Dev 19: 1968–1973.

100. ColotHV, LorosJJ, DunlapJC (2005) Temperature-modulated alternative splicing and promoter use in the circadian clock gene frequency. Mol Biol Cell 16: 5563–5571.

101. ChenCH, RingelbergCS, GrossRH, DunlapJC, LorosJJ (2009) Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J 28: 1029–1042.

102. ColotHV, ParkG, TurnerGE, RingelbergC, CrewCM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Nat Acad Sci USA 103: 10352–10357.

103. HanKH, HanKY, YuJH, ChaeKS, JahngKY, et al. (2001) The nsdD gene encodes a putative GATA-type transcription factor necessary for sexual development of Aspergillus nidulans. Mol Microbiol 41: 299–309.

104. NowrousianM, TeichertI, MasloffS, KückU (2012) Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3 (Bethesda) 2: 261–270.

105. SzewczykE, KrappmannS (2010) Conserved regulators of mating are essential for Aspergillus fumigatus cleistothecium formation. Eukaryot Cell 9: 774–783.

106. CorrochanoLM, GarreV (2010) Photobiology in the Zygomycota: multiple photoreceptor genes for complex responses to light. Fungal Genet Biol 47: 893–899.

107. TischD, SchmollM (2010) Light regulation of metabolic pathways in fungi. Appl Microbiol Biotechnol 85: 1259–1277.

108. HardingRW, TurnerRV (1981) Photoregulation of the carotenoid biosynthetic pathway in albino and white collar mutants of Neurospora crassa. Plant Physiol 68: 745–749.

109. SchmidhauserTJ, LauterFR, RussoVE, YanofskyC (1990) Cloning, sequence, and photoregulation of al-1, a carotenoid biosynthetic gene of Neurospora crassa. Mol Cell Biol 10: 5064–5070.

110. SchmidhauserTJ, LauterFR, SchumacherM, ZhouW, RussoVE, et al. (1994) Characterization of al-2, the phytoene synthase gene of Neurospora crassa. Cloning, sequence analysis, and photoregulation. J Biol Chem 269: 12060–12066.

111. NelsonMA, MorelliG, CarattoliA, RomanoN, MacinoG (1989) Molecular cloning of a Neurospora crassa carotenoid biosynthetic gene (albino-3) regulated by blue light and the products of the white collar locus. Mol Cell Biol 9: 1271–1276.

112. CarlileMJ, FriendJ (1956) Carotenoids and reproduction in Pyronema confluens. Nature 178: 369–370.

113. OlmedoM, Ruger-HerrerosC, LuqueEM, CorrochanoLM (2010) A complex photoreceptor system mediates the regulation by light of the conidiation genes con-10 and con-6 in Neurospora crassa. Fungal Genet Biol 47: 352–363.

114. van den BurgHA, WesterinkN, FrancoijsKJ, RothR, WoestenenkE, et al. (2003) Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. J Biol Chem 278: 27340–27346.

115. van den BurgHA, HarrisonSJ, JoostenMHAJ, VervoortJ, de WitPJ (2006) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19: 1420–1430.

116. FujiwaraS, ImaiJ, FujiwaraM, YaeshimaT, KawashimaT, et al. (1990) A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. J Biol Chem 265: 11333–11337.

117. BuletP, HetruC, DimarcqJL, HoffmannD (1999) Antimicrobial peptides in insects; structure and function. Dev Comp Immunol 23: 329–344.

118. MygindPH, FischerRL, SchnorrKM, HansenMT, SonksenCP, et al. (2005) Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 437: 975–980.

119. SchneiderT, KruseT, WimmerR, WiedemannI, SassV, et al. (2010) Plectasin, a fungal defensin, targets the bacterial cell wall precursor lipid II. Science 328: 1168–1172.

120. BokJW, ChiangY-M, SzewczykE, Reyes-DominguezY, DavidsonAD, et al. (2009) Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol 5: 462–464.

121. BokJW, NoordermeerD, KaleSP, KellerNP (2006) Secondary metabolic gene cluster silencing in Aspergillus nidulans. Mol Microbiol 61: 1636–1645.

122. RichardsTA, LeonardG, SoanesDM, TalbotNJ (2011) Gene transfer into the fungi. Fungal Biol Rev 25: 98–110.

123. MoranNA, JarvikT (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328: 624–627.

124. IottiM, RubiniA, TisserantE, KholerA, PaolocciF, et al. (2012) Self/nonself recognition in Tuber melanosporum is not mediated by a heterokaryon incompatibility system. Fungal Biol 116: 261–275.

125. DeleuC, ClavéC, BégueretJ (1993) A single amino acid difference is sufficient to elicit vegetative incompatibility in the fungus Podospora anserina. Genetics 135: 45–52.

126. SaupeSJ, KuldauGA, SmithML, GlassNL (1996) The product of the het-C heterokaryon incompatibility gene of Neurospora crassa has characteristics of a glycine-rich cell wall protein. Genetics 143: 1589–1600.

127. GlassNL, KanekoI (2003) Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2: 1–8.

128. KrokenS, GlassNL, TaylorJW, YoderOC, TurgeonBG (2003) Phylogenomic analyis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Nat Acad Sci USA 100: 15670–15675.

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

130. Teichert I, Nowrousian M (2011) Evolution of genes for secondary metabolism in fungi. In: Pöggeler S, Wöstemeyer J, editors. Evolution of fungi and fungal-like organisms, The Mycota XIV. Berlin, Heidelberg: Springer-Verlag. pp. 231–255.

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

132. HaasH, EisendleM, TurgeonBG (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46: 149–187.

133. ChiangY-M, SzewczykE, NayakT, DavidsonAD, SanchezJF, et al. (2008) Molecular genetic mining of the Aspergillus secondary metabolome: discovery of the Emericellamide biosynthetic pathway. Chem Biol 15: 527–532.

134. KempkenF (2011) Fungal defences against animal antagonists - lectins & more. Mol Ecol 20: 2876–2877.

135. KempkenF, RohlfsM (2010) Fungal secondary metabolite biosynthesis - a chemical defense strategy against antagonistic animals? Fungal Ecol 3: 107–114.

136. BorkovichKA, AlexLA, YardenO, FreitagM, TurnerGE, 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.

137. SonH, SeoYS, MinK, ParkAR, LeeJ, et al. (2011) A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7: e1002310.

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

139. MontaniniB, LevatiE, BolchiA, KohlerA, MorinE, et al. (2011) Genome-wide search and functional identification of transcription factors in the mycorrhizal fungus Tuber melanosporum. New Phytol 189: 736–750.

140. JohnsonAD (1995) Molecular mechanisms of cell-type determination in budding yeast. Curr Opin Genet Dev 5: 552–558.

141. NoltingN, PöggelerS (2006) A STE12 homologue of the homothallic ascomycete Sordaria macrospora interacts with the MADS box protein MCM1 and is required for ascosporogenesis. Mol Microbiol 62: 853–868.

142. LiD, BobrowiczP, WilkinsonHH, EbboleDJ (2005) A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170: 1091–1104.

143. VallimMA, MillerKY, MillerBL (2000) Aspergillus SteA (sterile12-like) is a homeodomain-C2/H2-Zn+2 finger transcription factor required for sexual reproduction. Mol Microbiol 36: 290–301.

144. StuartJM, SegalE, KollerD, KimSK (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302: 249–255.

145. RomeroIG, RuvinskyI, GiladY (2012) Comparative studies of gene expression and the evolution of gene regulation. Nat Rev Genet 13: 505–516.

146. HansenK, PfisterDH (2006) Systematics of the Pezizomycetes - the operculate discomycetes. Mycologia 98: 1029–1040.

147. LandvikS, EggerKN, SchumacherT (1997) Towards a subordinal classification of the Pezizales (Ascomycota): phylogenetic analyses of SSU rDNA sequences. Nord J Bot 17: 403–418.

148. Esser K (1982) Cryptogams - Cyanobacteria, Algae, Fungi, Lichens. London: Cambridge University Press.

149. MyersEW, SuttonGG, DelcherAL, DewIM, FasuloDP, et al. (2000) A whole-genome assembly of Drosophila. Science 287: 2196–2204.

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

151. HuangX, MadanA (1999) CAP3: A DNA sequence assembly program. Genome Res 9: 868–877.

152. NowrousianM, RingelbergC, DunlapJC, LorosJJ, KückU (2005) Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol Genet Genomics 273: 137–149.

153. GrabherrMG, HaasBJ, YassourM, LevinJZ, ThompsonDA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotech 29: 644–652.

154. HaasBJ, DelcherAL, MountSM, WortmanJR, SmithRKJr, et al. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucl Acids Res 31: 5654–5666.

155. KorfI (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59.

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

157. StankeM, WaackS (2003) Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19 (suppl. 2) ii215–225.

158. BesemerJ, BorodovskyM (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucl Acids Res 33: W451–454.

159. 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.

160. FinnRD, TateJ, MistryJ, CoggillPC, SammutSJ, et al. (2008) The Pfam protein families database. Nucl Acids Res 36: D281–288.

161. EddySR (2011) Accelerated profile HMM searches. PLoS Comp Biol 7: e1002195.

162. LaslettD, CanbackB (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucl Acids Res 32: 11–16.

163. NawrockiEP, KolbeDL, EddySR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335–1337.

164. TaquistH, CuiY, ArdellDH (2007) TFAM 1.0: an online tRNA function classifier. Nucl Acids Res 35: W350–353.

165. LoweTM, EddySR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 25: 955–964.

166. JurkaJ, KapitonovVV, PavlicekA, KlonowskiP, KohanyO, et al. (2005) Repbase Update, a database of eukyrotic repetitive elements. Cytogenet Genome Res 110: 462–467.

167. LewisZA, HondaS, KhlafallahTK, JeffressJK, FreitagM, et al. (2009) Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res 19: 427–437.

168. MargolinBS, Garrett-EngelePW, StevensJN, FritzDY, Garrett-EngeleC, et al. (1998) A methylated Neurospora 5S rRNA pseudogene contains a transposable element inactivated by repeat-induced point mutation. Genetics 149: 1787–1797.

169. SelkerEU, TountasNA, CrossSH, MargolinBS, MurphyJG, et al. (2003) The methylated component of the Neurospora crassa genome. Nature 422: 893–897.

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

171. MorinE, KohlerA, BakerAR, Foulongne-OriolM, LombardV, et al. (2012) Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Nat Acad Sci USA 109: 17501–17506.

172. SpanuPD, AbbottJ, C., AmselemJ, BurgisTA, SoanesDM, et al. (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543–1546.

173. SharptonTJ, StajichJE, RounsleySD, GardnerMJ, WortmanJR, et al. (2009) Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives. Genome Res 19: 1722–1731.

174. GalaganJE, CalvoSE, CuomoC, MaL-J, WortmanJR, et al. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105–1115.

175. MartinF, AertsA, AhrenD, BrunA, DanchinEGJ, et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88–92.

176. GoodwinSB, M'barekSB, DhillonB, WittenbergAH, 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.

177. FedorovaND, KhaldiN, JoardarVS, MaitiR, AmedeoP, et al. (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLOS Genet 4: e1000046.

178. GalaganJE, CalvoSE, BorkovichKA, SelkerEU, ReadND, et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859–868.

179. HaneJK, LoweRGT, SolomonPS, TanK-C, SchochCL, et al. (2007) Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19: 3347–3368.

180. GoffeauA, BarrellBG, BusseyH, DavisRW, DujonB, et al. (1996) Life with 6000 genes. Science 274: 546–567.

181. WoodV, GwilliamR, RajandreamMA, LyneM, LyneR, et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415: 871–880.

182. AmselemJ, CuomoCA, van KanJAL, ViaudM, BenitoEP, et al. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230.

183. DujonB, ShermanD, FischerG, DurrensP, CasaregolaS, et al. (2004) Genome evolution in yeasts. Nature 430: 35–44.

184. Huerta-CepasJ, Capella-GutierrezS, PryszczLP, DenisovI, KormesD, et al. (2011) PhylomeDB v3.0: an expanding repository of genome-wide collections of trees, alignments and phylogeny-based orthology and paralogy predictions. Nucl Acids Res 39: D556–560.

185. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32: 1792–1797.

186. KatohK, KumaK, TohH, MiyataT (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucl Acids Res 33: 511–518.

187. SubramanianAR, KaufmannM, MorgensternB (2008) DIALIGN-TX: greedy and progressive approaches for segment-based multiple sequence alignment. Algorithms Mol Biol 3: 6.

188. LandanG, GraurD (2007) Heads or tails: a simple reliability check for multiple sequence alignments. Mol Biol Evol 24: 1380–1383.

189. WallaceIM, O'SullivanO, HigginsDG, NotredameC (2006) M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucl Acids Res 34: 1692–1699.

190. Capella-GutierrezS, Silla-MartinezJM, GabaldónT (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinf 25: 1972–1973.

191. GuindonS, DufayardJF, LefortV, AnisimovaM, HordijkW, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.

192. GascuelO (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14: 685–695.

193. Huerta-CepasJ, DopazoJ, GabaldónT (2010) ETE: a python Environment for Tree Exploration. Bioinf 11: 24.

194. LeSQ, GascuelO (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307–1320.

195. WeheA, BansalMS, BurleighJG, EulensteinO (2008) DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony. Bioinf 24: 1540–1541.

196. HedgesSB, DudleyJ, KumarS (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinf 22: 2971–2972.

197. HeckmanDS, GeiserDM, EidellBR, StaufferRL, KardosNL, et al. (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293: 1129–1133.

198. ZhangZ, López-GiráldezF, TownsendJP (2010) LOX: inferring Level Of eXpression from diverse methods of census sequencing. Bioinf 26: 1918–1919.

199. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.

200. HardcastleTJ, KellyKA (2010) baySeq: empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinf 11: 422.

201. FraleyC, RafteryAE (2002) Model-based clustering, discriminant analysis, and density estimation J Amer Stat Assoc. 97: 611–631.

202. KlixV, NowrousianM, RingelbergC, LorosJJ, DunlapJC, et al. (2010) Functional characterization of MAT1-1-specific mating-type genes in the homothallic ascomycete Sordaria macrospora provides new insights into essential and non-essential sexual regulators. Eukaryot Cell 9: 894–905.

203. NowrousianM, MasloffS, PöggelerS, KückU (1999) Cell differentiation during sexual development of the fungus Sordaria macrospora requires ATP citrate lyase activity. Mol Cell Biol 19: 450–460.

204. ThompsonJD, GibsonTJ, PlewniakF, JeanmouginF, HigginsDG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24: 4876–4882.

205. WaterhouseAM, ProcterJB, MartinDMA, ClampM, BartonGJ (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189–1191.

206. PageR (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Appl Biosci 12: 357–358.

207. MaL-J, IbrahimAS, SkoryC, GrabherrMG, BurgerG, et al. (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5: e1000549.

208. MartinezD, ChallacombeJ, MorgensternI, HibbettD, SchmollM, et al. (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Nat Acad Sci USA 106: 1954–1959.

209. StajichJE, WilkeSK, AhrénD, AuCH, BirrenBW, et al. (2010) Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Nat Acad Sci USA 107: 11889–11894.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 9
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#