Gene Expansion Shapes Genome Architecture in the Human Pathogen : An Evolutionary Genomics Analysis in the Ancient Terrestrial Mucorales (Mucoromycotina)

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Lichtheimia species are ubiquitous saprophytic fungi, which cause life-threating infections in humans. In contrast to the mucoralean pathogen R. oryzae, Lichtheimia species belong to the ancient mucoralean lineages. We determined the genome of L. corymbifera (formerly Mycocladus corymbifer ex Absidia corymbifera) and found high dissimilarities between L. corymbifera and other sequenced mucoralean fungi in terms of gene families and syntenies. A highly elevated number of gene duplications and expansions was observed, which comprises virulence-associated genes like proteases, transporters and iron uptake genes but also transcription factors and genes involved in signal transduction. In contrast to R. oryzae, we did not find evidence for a recent whole genome duplication in Lichtheimia. However, gene duplications create functionally diverse paralogs in L. corymbifera, which are differentially expressed in virulence-related compared to standard conditions. In addition, new potential virulence factors could be identified which may play a role in the regulation of the adaptation to iron-limitation. The L. corymbifera genome and the phylome will advance further research and better understanding of virulence mechanisms of these medically important pathogens at the level of genome architecture and evolution.

Vyšlo v časopise: Gene Expansion Shapes Genome Architecture in the Human Pathogen : An Evolutionary Genomics Analysis in the Ancient Terrestrial Mucorales (Mucoromycotina). PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004496
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004496

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Zdroje

1. HibbettDS, BinderM, BischoffJF, BlackwellM, CannonPF, et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111: 509–547 doi:10.1016/j.mycres.2007.03.004

2. RodenMM, ZaoutisTE, BuchananWL, Knudsen Ta, Sarkisova Ta, et al. (2005) Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis 41: 634–653 doi:10.1086/432579

3. Sugar AM (1992) Mucormycosis. Clin Infect Dis 14 Suppl 1: S126–9.

4. RibesJA, Vanover-SamsCL, BakerDJ (2000) Zygomycetes in human disease. Clin Microbiol Rev 13: 236–301.

5. ChakrabartiA, DasA, MandalJ, ShivaprakashMR, GeorgeVK, et al. (2006) The rising trend of invasive zygomycosis in patients with uncontrolled diabetes mellitus. Med Mycol 44: 335–342 doi:10.1080/13693780500464930

6. CornelyOA, VehreschildJJ, RüpingMJGT (2009) Current experience in treating invasive zygomycosis with posaconazole treatment options for zygomycosis. Clin Microbiol 15: 77–81.

7. SkiadaA, PaganoL, GrollA, ZimmerliS, DupontB, et al. (2011) Zygomycosis in Europe: analysis of 230 cases accrued by the registry of the European Confederation of Medical Mycology (ECMM) Working Group on Zygomycosis between 2005 and 2007. Clin Microbiol Infect 17: 1859–1867.

8. VitaleRG, de HoogGS, SchwarzP, DannaouiE, DengS, et al. (2012) Antifungal susceptibility and phylogeny of opportunistic members of the order mucorales. J Clin Microbiol 50: 66–75 doi:10.1128/JCM.06133-11

9. XessI, MohapatraS, ShivaprakashMR, ChakrabartiA, BennyGL, et al. (2012) Evidence implicating Thamnostylum lucknowense as an etiological agent of rhino-orbital mucormycosis. J Clin Microbiol 50: 1491–1494 doi:10.1128/JCM.06611-11

10. LanternierF, DannaouiE, MorizotG, ElieC, HuerreM, et al. (2012) A global analysis of mucormycosis in France: The RetroZygo Study (2005–2007). Clin Infect Dis 54: 35–43 doi:10.1093/cid/cir880

11. AlvarezE, SuttonDa, CanoJ, Fothergill aW, Stchigela, et al. (2009) Spectrum of zygomycete species identified in clinically significant specimens in the United States. J Clin Microbiol 47: 1650–1656 doi:10.1128/JCM.00036-09

12. Tieghem, VanP (1876) Troisiéme mémoire sur les Mucorinées. Ann des Sci Nat Bot 4: 312–399.

13. HoffmannK, DischerS, VoigtK (2007) Revision of the genus Absidia (Mucorales, Zygomycetes) based on physiological, phylogenetic, and morphological characters; thermotolerant Absidia spp. form a coherent group, Mycocladiaceae fam. nov. Mycol Res 111: 1169–1183 doi:10.1016/j.mycres.2007.07.002

14. Alastruey-IzquierdoA, HoffmannK, de HoogGS, Rodriguez-TudelaJL, VoigtK, et al. (2010) Species recognition and clinical relevance of the zygomycetous genus Lichtheimia (syn. Absidia pro parte, Mycocladus). J Clin Microbiol 48: 2154–2170 doi:10.1128/JCM.01744-09

15. De Hoog, GS, Guarro, J, Gene, J, Figueras M (2000) Atlas of Clinical Fungi. 2nd ed. Centraalbureau voor Schimmelcultures. p. 58–114.

16. HaidleCW, StorckR (1966) Control of dimorphism in Mucor rouxii. J Bacteriol 92: 1236–1244.

17. CooperBH (1987) A case of pseudoparacoccidioidomycosis: Detection of the yeast phase of Mucor circinelloides in a clinical specimen Abstract. Mycopathologia 97: 189–193.

18. HesseltineCW, FeatherstonC (1985) Anaerobic growth of molds isolated from fermentation starters used for foods in Asian countries. Mycologia 77: 390–400.

19. SunH-Y, AguadoJM, BonattiH, ForrestG, GuptaKL, et al. (2009) Pulmonary zygomycosis in solid organ transplant recipients in the current era. Am J Transplant 9: 2166–2171 doi:10.1111/j.1600-6143.2009.02754.x

20. BellangerA-P, RebouxG, BotterelF, CandidoC, RousselS, et al. (2010) New evidence of the involvement of Lichtheimia corymbifera in farmer's lung disease. Med Mycol 48: 981–987 doi:10.3109/13693781003713711

21. CopettiMV, IamanakaBT, FrisvadJC, PereiraJL, TaniwakiMH (2011) Mycobiota of cocoa: from farm to chocolate. Food Microbiol 28: 1499–1504 doi:10.1016/j.fm.2011.08.005

22. MphandeFA, SiameBA, TaylorJE (2004) Fungi, aflatoxins, and cyclopiazonic acid associated with peanut retailing in Botswana. J Food Prot 67: 96–102.

23. BaffiMA, Romo-SánchezS, Ubeda-IranzoJ, Briones-PérezAI (2012) Fungi isolated from olive ecosystems and screening of their potential biotechnological use. N Biotechnol 29: 451–456 doi:10.1016/j.nbt.2011.05.004

24. HongS, KimD, LeeM, BaekS, KwonS, et al. (2012) Zygomycota associated with traditional meju, a fermented soybean starting material for soy sauce and soybean paste. J Microbiol 50: 386–393 doi:10.1007/s12275-012-1437-6

25. SchwartzeVU, HoffmannK, NyilasiI, PappT, VágvölgyiC, et al. (2012) Lichtheimia species exhibit differences in virulence potential. PLoS One 7: e40908 doi:10.1371/journal.pone.0040908

26. WangL, ChenW, FengY, RenY, GuZ, et al. (2011) Genome characterization of the oleaginous fungus Mortierella alpina. PLoS One 6: e28319 doi:10.1371/journal.pone.0028319

27. WöstemeyerJ, KreibichA (2002) Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet 41: 189–198 doi:10.1007/s00294-002-0306-y

28. 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 doi:10.1371/journal.pgen.1000549

29. BuchonN, VauryC (2006) RNAi: a defensive RNA-silencing against viruses and transposable elements. Heredity (Edinb) 96: 195–202 doi:10.1038/sj.hdy.6800789

30. JamesTY, LitvintsevaAP, VilgalysR, MorganJAT, TaylorJW, et al. (2009) Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog 5: e1000458 doi:10.1371/journal.ppat.1000458

31. XuX, PanS, ChengS, ZhangB, MuD, et al. (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189–195 doi:10.1038/nature10158

32. DeutscherMP (1984) Processing of tRNA in prokaryotes and eukaryotes. Crit Rev Biochem Mol Biol 17: 45–71.

33. KachouriR, StribinskisV, ZhuY, RamosKS, WesthofE, et al. (2005) A surprisingly large RNase P RNA in Candida glabrata. RNA 11: 1064–1072 doi:10.1261/rna.2130705

34. SchmittME, Clayton Da (1993) Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Mol Cell Biol 13: 7935–7941.

35. WalterP, IbrahimiI, BlobelG (1981) Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to in-vitro-assembled polysomes synthesizing secretory protein. J Cell Biol 91: 545–550.

36. DieciG, FiorinoG, CastelnuovoM, TeichmannM, PaganoA (2007) The expanding RNA polymerase III transcriptome. Trends Genet 23: 614–622 doi:10.1016/j.tig.2007.09.001

37. StankeM, DiekhansM, BaertschR, HausslerD (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637–644 doi:10.1093/bioinformatics/btn013

38. ConesaA, GötzS, García-GómezJM, TerolJ, TalónM, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676 doi:10.1093/bioinformatics/bti610

39. 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. Nucleic Acids Res 39: D556–60 doi:10.1093/nar/gkq1109

40. GabaldónT (2008) Large-scale assignment of orthology: back to phylogenetics? Genome Biol 9: 235 doi:10.1186/gb-2008-9-10-235

41. DelsucF, BrinkmannH, PhilippeH (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6: 361–375 doi:10.1038/nrg1603

42. WeheA, BansalMS, BurleighJG, EulensteinO (2008) DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony. Bioinformatics 24: 1540–1541 doi:10.1093/bioinformatics/btn230

43. BöckerS, JahnK, MixtackiJ, StoyeJ (2009) Computation of median gene clusters. J Comput Biol 16: 1085–1099 doi:10.1089/cmb.2009.0098

44. JahnK (2011) Efficient computation of approximate gene clusters based on reference occurrences. J Comput Biol 18: 1255–1274 doi:10.2144/000113833

45. Marcet-HoubenM, MarcedduG, GabaldónT (2009) Phylogenomics of the oxidative phosphorylation in fungi reveals extensive gene duplication followed by functional divergence. BMC Evol Biol 9: 295 doi:10.1186/1471-2148-9-295

46. Huerta-CepasJ, DopazoJ, GabaldónT (2010) ETE: a python Environment for Tree Exploration. BMC Bioinformatics 11: 24 doi:10.1186/1471-2105-11-24

47. PuntaM, CoggillPC, EberhardtRY, MistryJ, TateJ, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290–301 doi:10.1093/nar/gkr1065

48. FinnRD, ClementsJ, EddySR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29–37 doi:10.1093/nar/gkr367

49. PaolettiM, SaupeSJ, ClaveC (2007) Genesis of a Fungal Non-Self Recognition Repertoire. PlosOne e283 doi:10.1371/Citation

50. Alastruey-IzquierdoA, CuestaI, WaltherG, Cuenca-EstrellaM, Rodriguez-TudelaJL (2010) Antifungal susceptibility profile of human-pathogenic species of Lichtheimia. Antimicrob Agents Chemother 54: 3058–3060 doi:10.1128/AAC.01270-09

51. CannonSB, MitraA, BaumgartenA, YoungND, MayG (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4: 10 doi:10.1186/1471-2229-4-10

52. HanadaK, ZouC, Lehti-ShiuMD, ShinozakiK, ShiuS-H (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148: 993–1003 doi:10.1104/pp.108.122457

53. HirschmanJE, BalakrishnanR, ChristieKR, CostanzoMC, DwightSS, et al. (2006) Genome Snapshot: a new resource at the Saccharomyces Genome Database (SGD) presenting an overview of the Saccharomyces cerevisiae genome. Nucleic Acids Res 34: D442–5 doi:10.1093/nar/gkj117

54. KimE, MagenA, AstG (2007) Different levels of alternative splicing among eukaryotes. Nucleic Acids Res 35: 125–131 doi:10.1093/nar/gkl924

55. MarshallAN, MontealegreMC, Jiménez-LópezC, LorenzMC, van HoofA (2013) Alternative splicing and subfunctionalization generates functional diversity in fungal proteomes. PLoS Genet 9: e1003376 doi:10.1371/journal.pgen.1003376

56. SchrettlM, BignellE, KraglC, JoechlC, RogersT, et al. (2004) Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 200: 1213–1219 doi:10.1084/jem.20041242

57. RamananN (2000) A High-Affinity iron permease essential for Candida albicans virulence. Science (80-) 288: 1062–1064 doi:10.1126/science.288.5468.1062

58. HowardDH (1999) Acquisition, transport, and storage of iron by pathogenic fungi. Clin Microbiol Rev 12: 394–404.

59. FuY, LeeH, CollinsM, TsaiH-F, SpellbergB, et al. (2004) Cloning and functional characterization of the Rhizopus oryzae high affinity iron permease (rFTR1) gene. FEMS Microbiol Lett 235: 169–176 doi:10.1016/j.femsle.2004.04.031

60. IbrahimAS, GebremariamT, LinL, LuoG, HusseinyMI, et al. (2010) The high affinity iron permease is a key virulence factor required for Rhizopus oryzae pathogenesis. Mol Microbiol 77: 587–604 doi:10.1111/j.1365-2958.2010.07234.x

61. SymeonidisaS (2009) The role of iron and iron chelators in zygomycosis. Clin Microbiol Infect 15 Suppl 5: 26–32 doi:10.1111/j.1469-0691.2009.02976.x

62. IbrahimAS, SpellbergB, WalshTJ, KontoyiannisDP (2012) Pathogenesis of Mucormycosis. Clin Infect Dis 54: 1–7 doi:10.1093/cid/cir865

63. ZieglerL, TerzulliA, GaurR, McCarthyR, KosmanDJ (2011) Functional characterization of the ferroxidase, permease high-affinity iron transport complex from Candida albicans. Mol Microbiol 81: 473–485 doi:10.1111/j.1365-2958.2011.07704.x

64. Thiekena, WinkelmannG (1992) Rhizoferrin: a complexone type siderophore of the Mucorales and entomophthorales (Zygomycetes). FEMS Microbiol Lett 73: 37–41.

65. DrechselH, TschierskeM, ThiekenA, JungG (1995) The carboxylate type siderophore rhizoferrin and its analogs produced by directed fermentation. J Ind Microbiol Microbiol 14: 105–112.

66. BoelaertJR, de LochtM, Van CutsemJ, KerrelsV, CantinieauxB, et al. (1993) Mucormycosis during deferoxamine therapy is a siderophore-mediated infection: In vitro and in vivo animal studies. J Clin Invest 91: 1979–1986 doi:10.1172/JCI116419

67. IbrahimAS, GebermariamT, FuY, LinL, HusseinyMI, et al. (2007) The iron chelator deferasirox protects mice from mucormycosis through iron starvation. J Clin Invest 117: 2649–2657 doi:10.1172/JCI32338

68. SchmittI, Partida-MartinezLP, WinklerR, VoigtK, EinaxE, et al. (2008) Evolution of host resistance in a toxin-producing bacterial-fungal alliance. ISME J 2: 632–641 doi:10.1038/ismej.2008.19

69. Partida-MartinezLP, de LoossCF, IshidaK, IshidaM, RothM, et al. (2007) Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl Environ Microbiol 73: 793–797 doi:10.1128/AEM.01784-06

70. LarcherG, DiasM, RazafimandimbyB, BomalD, BoucharaJ-P (2013) Siderophore production by pathogenic Mucorales and uptake of deferoxamine B. Mycopathologia doi:10.1007/s11046-013-9693-5

71. CarranoCJ, BöhnkeR, MatzankeBF (1996) Fungal ferritins: the ferritin from mycelia of Absidia spinosa is a bacterioferritin. FEBS Lett 390: 261–264.

72. Capella-GutierrezS, Marcet-HoubenM, GabaldonT (2012) Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol 10: 47 doi:10.1186/1741-7007-10-47

73. HaasH, EisendleM, TurgeonBG (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46: 149–187 doi:10.1146/annurev.phyto.45.062806.094338

74. SilvaMG, SchrankA, BailãoEFLC, BailãoAM, BorgesCL, et al. (2011) The homeostasis of iron, copper, and zinc in paracoccidioides brasiliensis, Cryptococcus neoformans var. grubii, and Cryptococcus gattii: a comparative analysis. Front Microbiol 2: 49 doi:10.3389/fmicb.2011.00049

75. HaasH (2012) Iron - a key nexus in the virulence of Aspergillus fumigatus. Front Microbiol 3: 28 doi:10.3389/fmicb.2012.00028

76. HwangLH, SethE, Gilmore Sa, SilA (2012) SRE1 regulates iron-dependent and -independent pathways in the fungal pathogen Histoplasma capsulatum. Eukaryot Cell 11: 16–25 doi:10.1128/EC.05274-11

77. SchoenC, ReichardU, MonodM, KratzinHD, RüchelR (2002) Molecular cloning of an extracellular aspartic proteinase from Rhizopus microsporus and evidence for its expression during infection. Med Mycol 40: 61–71.

78. SpreerA, RüchelR, ReichardU (2006) Characterization of an extracellular subtilisin protease of Rhizopus microsporus and evidence for its expression during invasive rhinoorbital mycosis. Med Mycol 44: 723–731 doi:10.1080/13693780600936399

79. SchallerM, BorelliC, KortingHC, HubeB (2005) Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48: 365–377 doi:10.1111/j.1439-0507.2005.01165.x

80. ParkS-Y, ChoiJ, LimS-E, LeeG-W, ParkJ, et al. (2013) Global expression profiling of transcription factor genes provides new insights into pathogenicity and stress responses in the rice blast fungus. PLoS Pathog 9: e1003350 doi:10.1371/journal.ppat.1003350

81. ShelestE (2008) Transcription factors in fungi. FEMS Microbiol Lett 286: 145–151 doi:10.1111/j.1574-6968.2008.01293.x

82. EulgemT, RushtonPJ, RobatzekS, SomssichIE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199–206.

83. LeeSC, NiM, LiW, ShertzC, HeitmanJ (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74: 298–340 doi:10.1128/MMBR.00005-10

84. MessenguyF, DuboisE (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316: 1–21 doi:10.1016/S0378-1119(03)00747-9

85. GoodrichJA, TjianR (2011) Unexpected roles for core promoter recognition factors in cell-type-specific transcription and gene regulation. Nat Rev Genet 11: 549–558 doi:10.1038/nrg2847

86. LeachMD, CowenLE (2013) Surviving the heat of the moment: a fungal pathogens perspective. PLoS Pathog 9: e1003163 doi:10.1371/journal.ppat.1003163

87. HaselwandterK, EbnerMR (1994) Microorganisms surviving for 5300 years. FEMS Microbiol Lett 116: 189–193.

88. ChevreuxB, WetterT, SuhaiS (1999) Genome sequence assembly using trace signals and additional sequence information. Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB) 45–56.

89. SommerDD, DelcherAL, SalzbergSL, PopM (2007) Minimus: a fast, lightweight genome assembler. BMC Bioinformatics 8: 64 doi:10.1186/1471-2105-8-64

90. KurtzS, PhillippyA, DelcherAL, SmootM, ShumwayM, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12 doi:10.1186/gb-2004-5-2-r12

91. JurkaJ, KapitonovVV, Pavliceka, KlonowskiP, KohanyO, et al. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110: 462–467 doi:10.1159/000084979

92. KohanyO, GentlesAJ, HankusL, JurkaJ (2006) Annotation, submission and screening of repetitive elements in Repbase: Repbase Submitter and Censor. BMC Bioinformatics 7: 474 doi:10.1186/1471-2105-7-474

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

94. LagesenK, HallinP, RødlandEA, StaerfeldtH-H, RognesT, et al. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100–3108 doi:10.1093/nar/gkm160

95. GardnerPP, DaubJ, TateJ, MooreBL, OsuchIH, et al. (2011) Rfam: Wikipedia, clans and the “decimal” release. Nucleic Acids Res 39: D141–5 doi:10.1093/nar/gkq1129

96. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410 doi:10.1016/S0022-2836(05)80360-2

97. NawrockiEP, KolbeDL, EddySR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335–1337 doi:10.1093/bioinformatics/btp157

98. GautheretD, MajorF, CedergrenR (1990) Pattern searching/alignment with RNA primary and secondary structures: an effective descriptor for tRNA. CABIOS 6: 325–331.

99. TimothyTL, ElkanC (1994) Fitting a mixture model by exceptation maximization to discover motifs in biopolymers. Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology 28–36.

100. GriebelT, BrinkmeyerM, BöckerS (2008) EPoS: a modular software framework for phylogenetic analysis. Bioinformatics 24: 2399–2400 doi:10.1093/bioinformatics/btn364

101. KongY (2011) Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics 98: 152–153 doi:10.1016/j.ygeno.2011.05.009

102. KimD, PerteaG, TrapnellC, PimentelH, KelleyR, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36 doi:10.1186/gb-2013-14-4-r36

103. WöstemeyerJ (1985) Strain-dependent variation in ribosomal DNA arrangement in Absidia glauca. Eur J Biochem 146: 443–448.

104. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140 doi:10.1093/bioinformatics/btp616

105. EdgarRC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113 doi:10.1186/1471-2105-5-113

106. KatohK, KumaK, TohH, MiyataT (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511–518 doi:10.1093/nar/gki198

107. LandanG, GraurD (2007) Heads or tails: a simple reliability check for multiple sequence alignments. Mol Biol Evol 24: 1380–1383 doi:10.1093/molbev/msm060

108. WallaceIM, O'SullivanO, HigginsDG, NotredameC (2006) M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res 34: 1692–1699 doi:10.1093/nar/gkl091

109. Capella-GutiérrezS, Silla-MartínezJM, GabaldónT (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972–1973 doi:10.1093/bioinformatics/btp348

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

111. GuindonS, DufayardJ-F, 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 doi:10.1093/sysbio/syq010

112. AkaikeH (1973) Information theory and extension of the maximum likelihood principle. Proceedings of the 2nd international symposium on information theory 267–281.

113. LeSQ, GascuelO (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307–1320 doi:10.1093/molbev/msn067

114. SchmidtT, StoyeJ (2007) Gecko and GhostFam. Methods in Molecular Biology Vol. 396 165–182 doi:_10.1007/978-1-59745-515-2_12

115. NiermanWC, PainA, AndersonMJ, WortmanJR, KimHS, et al. (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438: 1151–1156 doi:10.1038/nature04332

116. 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 doi:10.1038/nature04341

117. KatinkaMD, DupratS, CornillotE, MéténierG, ThomaratF, et al. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450–453 doi:10.1038/35106579

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

119. CornmanRS, ChenYP, SchatzMC, StreetC, ZhaoY, et al. (2009) Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog 5: e1000466 doi:10.1371/journal.ppat.1000466

120. CuomoCA, DesjardinsCA, BakowskiMA, GoldbergJ, MaAT, et al. (2012) Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth:. 2478–2488 doi:10.1101/gr.142802.112.2478

121. DuplessisS, CuomoCA, LinY, AertsA, TisserantE, et al. (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. doi: 10.1073/pnas.1019315108

122. 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 Natl Acad Sci U S A 107: 11889–11894 doi:10.1073/pnas.1003391107

123. MartinezD, LarrondoLF, PutnamN, GelpkeMDS, HuangK, et al. (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22: 695–700 doi:10.1038/nbt967

124. MartinF, Aertsa, AhrénD, Bruna, DanchinEGJ, et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88–92 doi:10.1038/nature06556

125. PutnamNH, SrivastavaM, HellstenU, DirksB, ChapmanJ, et al. (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317: 86–94 doi:10.1126/science.1139158

126. KingN, WestbrookMJ, YoungSL, KuoA, AbedinM, et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783–788 doi:10.1038/nature06617

127. EastwoodDC, FloudasD, BinderM, MajcherczykA, SchneiderP, et al. (2011) The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333: 762–765 doi:10.1126/science.1205411

128. JonesonS, StajichJE, ShiuS-H, RosenblumEB (2011) Genomic transition to pathogenicity in chytrid fungi. PLoS Pathog 7: e1002338 doi:10.1371/journal.ppat.1002338

129. GalaganJE, CalvoSE, BorkovichKa, SelkerEU, ReadND, et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859–868 doi:10.1038/nature01554

130. Stamatakisa, LudwigT, MeierH (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456–463 doi:10.1093/bioinformatics/bti191