Journal of Molecular Evolution

, Volume 69, Issue 4, pp 372–385 | Cite as

Molecular Evolution of the mtDNA Encoded rps3 Gene Among Filamentous Ascomycetes Fungi with an Emphasis on the Ophiostomatoid Fungi

  • Jyothi Sethuraman
  • Anna Majer
  • Mahmood Iranpour
  • Georg Hausner
Article

Abstract

The mitochondrial ribosomal protein S3 (rps3) gene within the fungi is extremely diverse in location and organization, some versions of this gene have been incorporated into a group I intron, others appear to have gained large insertions, microsatellite expansions, or have been invaded by homing endonucleases. Among the ascomycetes fungi the group I intron encoded version of rps3 appears to have a rather complex evolutionary history including first the acquisition of rps3 by a group I intron (mL2449), the loss of the mL2499 intron and the establishment of rps3 as a free-standing gene, and the eventual loss of the intron derived version of rps3.

Keywords

Ribosomal proteins Group I intron encoded ORFs Fungal mitochondrial genome Ophiostoma 

Notes

Acknowledgments

This research was supported by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada to G. Hausner. We also would like to thank Dr. James Reid (University of Manitoba, Microbiology) for providing us with fungal cultures.

References

  1. Adams KL, Daley DO, Whelan J, Palmer JD (2002) Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell 14:931–943CrossRefPubMedGoogle Scholar
  2. Allers T, Mevarech M (2005) Archaeal genetics—the third way. Nat Rev Genet 6:58–73CrossRefPubMedGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  4. Bell JA, Monteiro-Vitorello CB, Hausner G, Fulbright DW, Bertrand H (1996) Physical and genetic map of the mitochondrial genome of Cryphonectria parasitica Ep155. Curr Genet 30:34–43CrossRefPubMedGoogle Scholar
  5. Blackwell M, Hibbett DS, Taylor JW, Spatafora JW (2006) Research coordination networks: a phylogeny for kingdom fungi (deep hypha). Mycologia 98:829–837CrossRefPubMedGoogle Scholar
  6. Bonen L, Calixte S (2006) Comparative analysis of bacterial-origin genes for plant mitochondrial ribosomal proteins. Mol Biol Evol 23:701–712CrossRefPubMedGoogle Scholar
  7. Bullerwell CE, Burger G, Lang BF (2000) A novel motif for identifying rps3 homologs in fungal mitochondrial genomes. Trends Biochem Sci 25:363–365CrossRefPubMedGoogle Scholar
  8. Bullerwell CE, Forget L, Lang BF (2003a) Evolution of monoblepharidalean fungi based on complete mitochondrial genome sequences. Nucleic Acids Res 31:1614–1623CrossRefPubMedGoogle Scholar
  9. Bullerwell CE, Leigh J, Forget L, Lang BF (2003b) A comparison of three fission yeast mitochondrial genomes. Nucleic Acids Res 31:759–768CrossRefPubMedGoogle Scholar
  10. Bullerwell CE, Leigh J, Seif E, Longcore JE, Lang BF (2003c) Evolution of the fungi and their mitochondrial genomes. In: Arora DK, Khachatourians GG (eds) Applied mycology and biotechnology. Volume III: Fungal genomics. Elsevier Science, New York, pp 133–159Google Scholar
  11. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716CrossRefPubMedGoogle Scholar
  12. Burke JM, RajBhandary UL (1982) Intron within the large rRNA gene of N. crassa mitochondria: a long open reading frame and a consensus sequence possibly important in splicing. Cell 31:509–520CrossRefPubMedGoogle Scholar
  13. Butow RA, Perlman PS, Grossman LI (1985) The unusual varl gene of yeast mitochondrial DNA. Science 228:1496–1501CrossRefPubMedGoogle Scholar
  14. Chambergo FS, Bonaccorsi ED, Ferreira AJ, Ramos AS, Ferreira JR Jr, Abrahao-Neto J, Farah JP, El-Dorry H (2002) Elucidation of the metabolic fate of glucose in the filamentous fungus Trichoderma reesei using expressed sequence tag (EST) analysis and cDNA microarrays. J Biol Chem 277:3983–13988CrossRefGoogle Scholar
  15. Copertino DW, Christopher DA, Hallick RB (1991) A mixed group II/group III twintron in the Euglena gracilis chloroplast ribosomal protein S3 gene: evidence for intron insertion during gene evolution. Nucleic Acids Res 19:6491–6497CrossRefPubMedGoogle Scholar
  16. Davis SC, Ellis SR (1995) Incorporation of the yeast mitochondrial ribosomal protein Mrp2 into ribosomal subunits requires the mitochondrially encoded Var1 protein. Mol Gen Genet 247:379–386CrossRefPubMedGoogle Scholar
  17. Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, supplement 3. National Biomedical Research Foundation, Washington, DC, pp 345–352Google Scholar
  18. De Cambiaire JC, Otis C, Lemieux C, Turmel M (2006) The complete chloroplast genome sequence of the chlorophycean green alga Senedesmus obliquus reveals a compact gene organization and a biased distribution of genes on the two DNA strands. BMC Evol Biol 6:37CrossRefPubMedGoogle Scholar
  19. Douglas MG, Butow RA (1976) Variant forms of mitochondrial translation products in yeast: evidence for location of determinants on mitochondrial DNA. Proc Natl Acad Sci USA 73:1083–1086CrossRefPubMedGoogle Scholar
  20. Dujon B (1979) Mutants in a mosaic gene reveal functions for introns. Nature 282:777–778CrossRefPubMedGoogle Scholar
  21. Dujon B (1980) Sequence of the intron and flanking exons of the mitochondrial 21S rRNA gene of yeast strains having different alleles at the omega and rib-1 loci. Cell 20:185–197CrossRefPubMedGoogle Scholar
  22. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  23. Felsenstein J (2006) PHYLIP (Phylogeny Inference Package) version 3.6a. Distributed by the author. Department of Genetics, University of Washington, Seattle. http://evolution.genetics.washington.edu/phylip/getme.html. Accessed 11 Jan 2009
  24. Forget L, Ustinova J, Wang Z, Huss VA, Lang BF (2002) Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. Mol Biol Evol 19:310–319PubMedGoogle Scholar
  25. Formighieri EF, Tiburcio RA, Armas ED, Medrano FJ, Shimo H, Carels N, Goes-Neto A, Cotomacci C, Carazzolle MF, Sardinha-Pinto N, Thomazella DP, Rincones J, Digiampietri L, Carraro DM, Azeredo-Espin AM, Reis SF, Deckmann AC, Gramacho K, Goncalves MS, Moura Neto JP, Barbosa LV, Meinhardt LW, Cascardo JC, Pereira GA (2008) The mitochondrial genome of the phytopathogenic basidiomycete Moniliophthora perniciosa is 109 kb in size and contains a stable integrated plasmid. Mycol Res 112:1136–1152CrossRefPubMedGoogle Scholar
  26. Gibb EA, Hausner G (2005) Optional mitochondrial introns and evidence for a homing-endonuclease gene in the mtDNA rnl gene in Ophiostoma ulmi s. lat. Mycol Res 109:1112–1126CrossRefPubMedGoogle Scholar
  27. Goddard MR, Burt A (1999) Recurrent invasion and extinction of a selfish gene. Proc Natl Acad Sci USA 96:13880–13885CrossRefPubMedGoogle Scholar
  28. Gonzales MJ, Dugan JM, Shafer RW (2002) Synonymous–non-synonymous mutation rates between sequences containing ambiguous nucleotides (syn-SCAN). Bioinformatics 18:886–887CrossRefPubMedGoogle Scholar
  29. Graack HR, Wittmann-Liebold B (1998) Mitochondrial ribosomal proteins (MRPs) of yeast. Biochem J 329:433–448PubMedGoogle Scholar
  30. Gray MW, Lang BF, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Brossard N, Delage E, Littlejohn TG, Plante I, Rioux P, Saint-Louis D, Zhu Y, Burger G (1998) Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res 26:865–878CrossRefPubMedGoogle Scholar
  31. Groot GS, Mason TL, Van Harten-Loosbroek N (1979) Var1 is associated with the small ribosomal subunit of mitochondrial ribosomes in yeast. Mol Gen Genet 174:339–342CrossRefPubMedGoogle Scholar
  32. Groth C, Petersen RF, Piskur J (2000) Diversity in organization and the origin of gene orders in the mitochondrial DNA molecules of the genus Saccharomyces. Mol Biol Evol 17:1833–1841PubMedGoogle Scholar
  33. Guo QB, Akins RA, Garriga G, Lambowitz AM (1991) Structural analysis of the Neurospora mitochondrial large rRNA intron and construction of a mini-intron that shows protein-dependent splicing. J Biol Chem 266:1809–1819PubMedGoogle Scholar
  34. Hane JK, Lowe RGT, Solomon PS, Tan K-C, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Torriani SFF, McDonald BA, Oliver RP (2007) Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19:3347–3368CrossRefPubMedGoogle Scholar
  35. Harrington TC (1993a) Diseases of conifers caused by Ophiostoma and Leptographium. In: Wingfield MJ, Seifert KA, Webber JF (eds) Ceratocystis and ophiostoma, taxonomy, ecology and pathogenicity. APS Press, St. Paul, Minnesota, pp 161–172Google Scholar
  36. Harrington TC (1993b) Biology and taxonomy of fungi associated with bark beetles. In: Schowalter TD, Filip GM (eds) Beetle–pathogen interactions in conifer forests. Academic Press, London, San Diego, pp 37–58Google Scholar
  37. Hausner G (2003) Fungal mitochondrial genomes, plasmids and introns. In: Arora DK, Khachatourians GG (eds) Applied mycology and biotechnology. Volume III: Fungal genomics. Elsevier Science, New York, pp 101–131Google Scholar
  38. Hausner G, Reid J (2004) The nuclear small subunit ribosomal genes of Sphaeronaemella helvellae, Sphaeronaemella fimicola, Gabarnaudia betae and Cornuvesica falcata: phylogenetic implications. Can J Bot 82:752–762CrossRefGoogle Scholar
  39. Hausner G, Wang X (2005) Unusual compact rDNA gene arrangements within some members of the ascomycota: evidence for molecular co-evolution between ITS1 and ITS2. Genome 48:648–660CrossRefPubMedGoogle Scholar
  40. Hausner G, Reid J, Klassen GR (1992) Do galeate-ascospore members of the Cephaloascaceae, Endomycetaceae and Ophiostomataceae share a common phylogeny? Mycologia 84:870–881CrossRefGoogle Scholar
  41. Hausner G, Reid J, Klassen GR (1993) On the phylogeny of Ophiostoma, Ceratocystis s.s., Microascus, and relationships within Ophiostoma based on partial ribosomal DNA sequences. Can J Bot 71:1249–1265CrossRefGoogle Scholar
  42. Hausner G, Monteiro-Vitorello CB, Searles DB, Maland M, Fulbright DW, Bertrand H (1999) A long open reading frame in the mitochondrial LSU rRNA group-I intron of Cryphonectria parasitica encodes a putative S5 ribosomal protein fused to a maturase. Curr Genet 35:109–117CrossRefPubMedGoogle Scholar
  43. Hausner G, Iranpour M, Kim J-J, Breuil C, Davis CN, Gibb EA, Reid J, Loewen PC, Hopkin AA (2005) Fungi vectored by the introduced bark beetle Tomicus piniperda in Ontario, Canada and comments on the taxonomy of Leptographium lundbergii, L. terebrantis, L. truncatum and L. wingfieldii. Can J Bot 83:1222–1237CrossRefGoogle Scholar
  44. Hausner G, Olson R, Simon D, Johnson I, Sanders ER, Karol KG, McCourt RM, Zimmerly S (2006) Origin and evolution of the chloroplast trnK (matK) intron: a model for evolution of group II intron RNA structures. Mol Biol Evol 23:380–391CrossRefPubMedGoogle Scholar
  45. Hedge V, Kelley MR, Xu Y, Mian S, Deutsch WA (2001) Conversion of the bifunctional 8-oxoguanine/b-d apurine/apyrimidine DNA repair activates of Drosophila ribosomal protein S3 into the human S3 monofunctional β-elimination catalyst through a single amino acid change. J Biol Chem 276:27591–27596CrossRefGoogle Scholar
  46. Hoeben P, Clark-Walker GD (1986) An approach to yeast classification by mapping mitochondrial DNA from Dekkera/Brettanomyces and Eeniella genera. Curr Genet 10:371–379CrossRefPubMedGoogle Scholar
  47. Hudspeth ME, Vincent RD, Perlman PS, Shumard DS, Treisman LO, Grossman LI (1984) Expandable var1 gene of yeast mitochondrial DNA: in-frame insertions can explain the strain-specific protein size polymorphisms. Proc Natl Acad Sci USA 81:3148–3152CrossRefPubMedGoogle Scholar
  48. Iwamoto M, Pi M, Kurihara M, Morio T, Tanaka Y (1998) A ribosomal protein gene cluster is encoded in the mitochondrial DNA of Dictyostelium discoideum: UGA termination codons and similarity of gene order to Acanthamoeba castellanii. Curr Genet 33:304–310CrossRefPubMedGoogle Scholar
  49. Jang CY, Lee JY, Kim J (2004) RpS3, a DNA repair endonuclease and ribosomal protein, is involved in apoptosis. FEBS Lett 560:81–85CrossRefPubMedGoogle Scholar
  50. Jung SO, Lee JY, Kim J (2001) Yeast ribosomal protein S3 has an endonuclease activity on AP DNA. Mol Cells 12:84–90PubMedGoogle Scholar
  51. Kim TS, Kim HD, Kim J (2009) PKCdelta-dependent functional switch of rpS3 between translation and DNA repair. Biochim Biophys Acta 1793:395–405CrossRefPubMedGoogle Scholar
  52. Kittle JD Jr, Mohr G, Gianelos JA, Wang H, Lambowitz AM (1991) The Neurospora mitochondrial tyrosyl–tRNA synthetase is sufficient for group I intron splicing in vitro and uses the carboxy-terminal tRNA-binding domain along with other regions. Genes Dev 5:1009–1021CrossRefPubMedGoogle Scholar
  53. Kolařík M, Hulcr J (2009) Mycobiota associated with the ambrosia beetle Scolytodes unipunctatus (Coleoptera: Curculionidae, Scolytinae). Mycol Res 113:44–60CrossRefPubMedGoogle Scholar
  54. Kouvelis VN, Ghikas DV, Typas MA (2004) The analysis of the complete mitochondrial genome of Lecanicillium muscarium (synonym Verticillium lecanii) suggests a minimum common gene organization in mtDNAs of sordariomycetes: phylogenetic implications. Fungal Genet Biol 41:930–940CrossRefPubMedGoogle Scholar
  55. LaPolla RJ, Lambowitz AM (1981) Mitochondrial ribosome assembly in Neurospora crassa. Purification of the mitochondrially synthesized ribosomal protein, S-5. J Biol Chem 256:7064–7067PubMedGoogle Scholar
  56. Laroche J, Bousquet J (1999) Evolution of the mitochondrial rps3 intron in perennial and annual angiosperms and homology to nad5 intron 1. Mol Biol Evol 16:441–452PubMedGoogle Scholar
  57. Liu XQ, Huang C, Xu H (1993) The unusual rps3-like orf712 is functionally essential and structurally conserved in Chlamydomonas. FEBS Lett 336:225–230CrossRefPubMedGoogle Scholar
  58. Lyamouri M, Enerly E, Lambertsson A (2002) Organization, sequence, and phylogenetic analysis of the ribosomal protein S3 gene from Drosophila virilis. Gene 294:147–156CrossRefPubMedGoogle Scholar
  59. Martini M, Lee IM, Bottner KD, Zhao Y, Botti S, Bertaccini A, Harrison NA, Carraro L, Marcone C, Khan AJ, Osler R (2007) Ribosomal protein gene-based phylogeny for finer differentiation and classification of phytoplasmas. Int J Syst Evol Microbiol 57:2037–2051CrossRefPubMedGoogle Scholar
  60. Mason TL, Pan C, Sanchirico ME, Sirum-Connolly K (1996) Molecular genetics of the peptidyl transferase center and the unusual Var1 protein in yeast mitochondrial ribosomes. Experientia 52:1148–1157CrossRefPubMedGoogle Scholar
  61. Mohr G, Rennard R, Cherniack AD, Stryker J, Lambowitz AM (2002) Function of the Neurospora crassa mitochondrial tyrosyl-tRNA synthetase in RNA splicing. Role of the idiosyncratic N-terminal extension and different modes of interaction with different group I introns. J Mol Biol 307:75–92CrossRefGoogle Scholar
  62. Müller EC, Wittmann-Liebold B (1997) Phylogenetic relationship of organisms obtained by ribosomal protein comparison. Cell Mol Life Sci 53:34–50CrossRefPubMedGoogle Scholar
  63. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  64. Neu R, Goffart S, Wolf K, Schafer B (1998) Relocation of urf a from the mitochondrion to the nucleus cures the mitochondrial mutator phenotype in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 258:389–396CrossRefPubMedGoogle Scholar
  65. Nicholas KB, Nicholas HB, Deerfield DW Jr (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW NEWS 4:14Google Scholar
  66. Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  67. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annual Rev Entomol 42:179–206CrossRefGoogle Scholar
  68. Pantou MP, Kouvelis VN, Typas MA (2006) The complete mitochondrial genome of the vascular wilt fungus Verticillium dahliae: a novel gene order for Verticillium and a diagnostic tool for species identification. Curr Genet 50:125–136CrossRefPubMedGoogle Scholar
  69. Paquin B, Lang BF (1996) The mitochondrial DNA of Allomyces macrogynus: the complete genomic sequence from an ancestral fungus. J Mol Biol 255:688–701CrossRefPubMedGoogle Scholar
  70. Paquin B, Laforest MJ, Forget L, Roewer I, Wang Z, Longcore J, Lang BF (1997) The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr Genet 31:380–395CrossRefPubMedGoogle Scholar
  71. Regina TM, Picardi E, Lopez L, Pesole G, Quagliariello C (2005) A novel additional group II intron distinguishes the mitochondrial rps3 gene in gymnosperms. J Mol Evol 60:196–206CrossRefPubMedGoogle Scholar
  72. Ronquist F (2004) Bayesian inference of character evolution. Trends Ecol Evol 19:475–481CrossRefPubMedGoogle Scholar
  73. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  74. Schafer B, Hansen M, Lang BF (2005) Transcription and RNA-processing in fission yeast mitochondria. RNA 11:785–795CrossRefPubMedGoogle Scholar
  75. Sethuraman J (2009) Bio-prospecting and characterization of optional elements present in the mtDNA rnl-region within species of ophiostomatoid fungi. PhD Thesis, University of ManitobaGoogle Scholar
  76. Sethuraman J, Okoli CV, Majer A, Corkery TL, Hausner G (2008) The sporadic occurrence of a group I intron-like element in the mtDNA rnl gene of Ophiostoma novo-ulmi subsp. americana. Mycol Res 112:564–582CrossRefPubMedGoogle Scholar
  77. Simossis VA, Heringa J (2003) The PRALINE online server: optimising progressive multiple alignment on the web. Comput Biol Chem 27:511–519CrossRefPubMedGoogle Scholar
  78. Simossis VA, Heringa J (2005) PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res 33:W289–W294CrossRefPubMedGoogle Scholar
  79. Smits P, Smeitink JA, van den Heuvel LP, Huynen MA, Ettema TJ (2007) Reconstructing the evolution of the mitochondrial ribosomal proteome. Nucleic Acids Res 35:4686–4703CrossRefPubMedGoogle Scholar
  80. Spatafora JW, Blackwell M (1994) Polyphyletic origins of ophiostomatoid fungi. Mycol Res 98:1–9CrossRefGoogle Scholar
  81. Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, Fujiwara M, Sato N (2007) The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol 24:699–709CrossRefPubMedGoogle Scholar
  82. Terpstra P, Butow RA (1979) The role of var1 in the assembly of yeast mitochondrial ribosomes. J Biol Chem 254:12662–12669PubMedGoogle Scholar
  83. Terpstra P, Zanders E, Butow RA (1979) The association of var1 with the 38 S mitochondrial ribosomal subunit in yeast. J Biol Chem 254:12653–12661PubMedGoogle Scholar
  84. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedGoogle Scholar
  85. Turmel M, Otis C, Lemieux C (2003) The mitochondrial genome of Chara vulgaris: insights into the mitochondrial architecture of the last ancestor of green algae and land plants. Plant Cell 15:1888–1903CrossRefPubMedGoogle Scholar
  86. Verbruggen H, Leliaert F, Maggs CA, Shimada S, Schils T, Provan J, Booth D, Murphy S, De Clerck O, Littler DS, Littler MM, Coppejans E (2007) Species boundaries and phylogenetic relationships within the green algal genus Codium (Bryopsidales) based on plastid DNA sequences. Mol Phylogenet Evol 44:240–254CrossRefPubMedGoogle Scholar
  87. Wang Y, Zeng F, Hon CC, Zhang Y, Leung FC (2008) The mitochondrial genome of the basidiomycete fungus Pleurotus ostreatus (oyster mushroom). FEMS Microbiol Lett 280:34–41CrossRefPubMedGoogle Scholar
  88. Wenzlau JM, Perlman PS (1990) Mobility of two optional G+C-rich clusters of the var1 gene of yeast mitochondrial DNA. Genetics 126:53–62PubMedGoogle Scholar
  89. Wilson DN, Nierhaus KH (2005) Ribosomal proteins in the spotlight. Crit Rev Biochem Mol Biol 40:243–267CrossRefPubMedGoogle Scholar
  90. Wingfield MJ, Seifert KA, Webber JF (eds) (1993) Ceratocystis and ophiostoma. Biology, taxonomy and ecology. American Phytopathological Society Press, St. PaulGoogle Scholar
  91. Zimmer M, Schiebner T, Krabusch M, Wolf K (1990) Nucleotide sequence of the unassigned reading frame urf a in the mitochondrial genome of three Schizosaccharomyces pombe strains. Nucleic Acids Res 18:6686CrossRefPubMedGoogle Scholar
  92. Zimmer M, Krabusch M, Wolf K (1991) Characterization of a novel open reading frame, urf a, in the mitochondrial genome of fission yeast: correlation of urf a mutations with a mitochondrial mutator phenotype and a possible role of frameshifting in urf a expression. Curr Genet 19:95–102CrossRefPubMedGoogle Scholar
  93. Zipfel RD, de Beer ZW, Jacobs K, Wingfield BD, Wingfield MJ (2006) Multi-gene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Stud Mycol 55:75–97PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Jyothi Sethuraman
    • 1
  • Anna Majer
    • 1
  • Mahmood Iranpour
    • 1
  • Georg Hausner
    • 1
  1. 1.Department of MicrobiologyUniversity of ManitobaWinnipegCanada

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