Comparative analysis of Fusarium mitochondrial genomes reveals a highly variable region that encodes an exceptionally large open reading frame

Fungal Genetics and Biology

Volumn 49, Issue 1, 2012, Pages 2-14

  Al Reedy, Rasha M ^a   Malireddy, Rahul ^a   Dillman, Casey B ^a,b   Kennell, John C ^a  

^a SAINT LOUIS UNIVERSITY   (United States)

^b VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

Author keywords

Comparative genomics; Filamentous fungi; Group I introns; Horizontal transmission; Mitochondrial DNA; Mobile genetic elements; Plant pathogens; Recombination

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA BASE COMPOSITION; FUNGAL GENOME; FUSARIUM GRAMINEARUM; FUSARIUM MONILIFORME; GENE DUPLICATION; GENE ORDER; GENE SEQUENCE; GENOME SIZE; INTRON; MITOCHONDRIAL GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATIVE PHOSPHORYLATION; PHYLOGENY; PRIORITY JOURNAL; SPECIES DIFFERENCE;

DNA, FUNGAL; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; FUSARIUM; GENE TRANSFER, HORIZONTAL; GENOME, MITOCHONDRIAL; INTRONS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; POLYMORPHISM, GENETIC; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA;

FUNGI; FUSARIUM; FUSARIUM SOLANI; GIBBERELLA MONILIFORMIS; GIBBERELLA ZEAE;

EID: 84856418702     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.11.008     Document Type: Article

References (72)

1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 1997, 25:3389-3402.
2. Batzoglou S., Jaffe D.B., Stanley K., Butler J., Gnerre S., Mauceli E., Berger B., Mesirov J.P., Lander E.S. ARACHNE: a whole-genome shotgun assembler. Genome Res. 2002, 12:177-189.
3. Berbee M.L., Taylor J.W. Fungal molecular evolution: gene tree and geological time. The Mycota, Systematics and Evolution 2001, 229-245. Springer, Berlin. D.J. McLaughlin, E.G. McLaughlin, P.A. Lemke (Eds.).
4. Bruns T.D., Gardes M. Molecular tools for the identification of ectomycorrhizal fungi - taxon-specific oligonucleotide probes for suilloid fungi. Mol. Ecol. 1993, 2:233-242.
5. Bruns T.D., Szaro T.M. Rate and mode differences between nuclear and mitochondrial small-subunit rRNA genes in mushrooms. Mol. Biol. Evol. 1992, 9:836-855.
6. Bullerwell C.E., Lang B.F. Fungal evolution: the case of the vanishing mitochondrion. Curr. Opin. Microbiol. 2005, 8:362-369.
7. Bullerwell C.E., Burger G., Lang B.F. A novel motif for identifying rps3 homologs in fungal mitochondrial genomes. Trends Biochem. Sci. 2000, 25:363-365.
8. Bullerwell C.E., Forget L., Lang B.F. A comparison of three fission yeast mitochondrial genomes. Nucl. Acids Res. 2003, 31:1614-1623.
9. Burger G., Gray M.W., Lang B.F. Mitochondrial genomes: anything goes. Trends Genet. 2003, 19:709-716.
10. Burke J.M., RajBhandary U.L. Intron within the large rRNA gene of N. crassa mitochondria: a long open reading frame and a consensus sequence possibly important in splicing. Cell 1982, 31:509-520.
11. Cahan P., Kennell J.C. Identification and distribution of sequences having similarity to mitochondrial plasmids in mitochondrial genomes of filamentous fungi. Mol. Gen. Genom. 2005, 273:462-473.
12. Chambergo F.S., Bonaccorsi E.D., Ferreira A.J., Ramos A.S., Ferreira J.R., Abrahão-Neto J., Farah J.P., El-Dorry H. 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. 2002, 277:13983-13988.
13. Chevalier B.S., Stoddard B.L. Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucl. Acids Res. 2001, 29:3757-3774.
14. Coleman J.J., Rounsley S.D., Rodriguez-Carres M., Kuo A., Wasmann C.C., Grimwood J., Schmutz J., Taga M., White G.J., Zhou S., Schwartz D.C., Freitag M., Ma L.J., Danchin E.G., Henrissat B., Coutinho P.M., Nelson D.R., Straney D., Napoli C.A., Barker B.M., Gribskov M., Rep M., Kroken S., Molnár I., Rensing C., Kennell J.C., Zamora J., Farman M.L., Selker E.U., Salamov A., Shapiro H., Pangilinan J., Lindquist E., Lamers C., Grigoriev I.V., Geiser D.M., Covert S.F., Temporini E., Vanetten H.D. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLOS Genet. 2009, 5:8.
15. Cunnington J.H. Organization of the mitochondrial genome of Fusarium oxysporum (anamorphic Hypocreales). Mycoscience 2007, 48:403-406.
16. Cunnington J.H. The distribution of optional mitochondrial introns encoding putative homing endonuclease genes in the Fusarium oxysporum complex. Sydowia 2009, 61:1-9.
17. Cuomo C.A., Guldener U., Xu J.R., Trail F., Turgeon B.G., Di Pietro A., Walton J.D., Ma L.J., Baker S.E., Rep M. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317:1400-1402.
18. Davis R.H., de Serres F.J. Genetic and microbiological research techniques for Neurospora crassa. Meth. Enzymol. 1970, 17A:79-143.
19. Drescher A., Ruf S., Calsa T., Carrer H., Bock R. The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J. 2000, 22:97-104.
20. Forget L., Ustinova J., Wang Z., Huss A.R., Lang F.B. Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing and an evolutionary link to lower fungi. Mol. Biol. Evol. 2002, 19:310-319.
21. Galligan J.T., Kennell J.C. Retroplasmids: linear and circular plasmids that replicate via reverse transcription. Microbial Linear Plasmids 2007, 163-185. Springer, Berlin/Heidelberg. F. Meinhardt, R. Klassen (Eds.).
22. Ghikas D.V., Kouvelis V.N., Taylor M.A. The complete mitochondrial genome of the entomopathogenic fungus Metarhizium anisoplica var. anisopliac: gene order and trn gene clusters reveal a common evolutionary course for all Sordariomycete. Arch. Microbiol. 2006, 185:393-401.
23. Gilmore S.R., Gräfenhan T., Louis-Seize G., Seifert K.A. Multiple copies of cytochrome oxidase 1 in species of the fungal genus Fusarium. Mol. Eco. Res. 2009, 9:90-98.
24. Goloboff P.A., Farris J.S., Nixon K.C. TNT, a free program for phylogenetic analysis. Cladistics 2008, 24:774-786.
25. Griffiths A.J.F. Natural plasmids of filamentous fungi. Microbiol. Rev. 1995, 59:673-685.
26. Groot G.S., Mason T.L., Van Harten-Loosbroek N. Var1 is associated with the small ribosomal subunit of mitochondrial ribosomes in yeast. Mol. Gen. Genet. 1979, 174:339-342.
27. Gross S.R., Levine P.H., Metzger S., Glaser G. Recombination and replication of plasmid-like derivatives of a short section of the mitochondrial chromosome of Neurospora crassa. Genetics 1989, 121:693-701.
28. Haugen P., Simon D.M., Bhattacharya D. The natural history of group I introns. Trends Genet. 2005, 21:111-119.
29. Hausner G. Fungal mitochondrial genomes, plasmids and introns. Fungal Genomics 2003, vol. 3:101-131. Elsevier Science, BV.
30. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
31. Johansen S., Haugen P. A new nomenclature of group I introns in ribosomal DNA. RNA 2001, 7:935-936.
32. Juhász A., Pfeiffer I., Keszthelyi A., Kucsera J., Vágvölgyi C., Hamari Z. Comparative analysis of the complete mitochondrial genomes of Aspergillus niger mtDNA type1a and Aspergillus tubingensis mtDNA type 2b. FEMS Microbiol. Lett. 2008, 281:51-57.
33. Jung P.P., Friedrich A., Souciet J.L., Louis V., Potier S., de Montigny J., Schacherer J. Complete mitochondrial genome sequence of the yeast Pichia farinosa and comparative analysis of closely related species. Curr. Genet. 2010, 56:507-515.
34. Kistler H.C., Benny U. The mitochondrial genome of Fusarium oxysporum. Plasmid 1989, 22:86-89.
35. Koll F., Boulay J., Belcour L., d'Aubenton-Carafa Y. Contribution of ultra-short invasive elements to the evolution of the mitochondrial genome in the genus Podospora. Nucl. Acid Res. 1996, 24:1734-1741.
36. Kosa P., Valach M., Tomaska L., Wolfe K.H., Nosek J. Complete DNA sequences of the mitochondrial genomes of the pathogenic yeasts Candida orthopsilosis and Candida metapsilosis: insight into the evolution of linear DNA genomes from mitochondrial telomere mutants. Nucl. Acid Res. 2006, 34:2472-2481.
37. Kouvelis V., Ghikas D., Typas M.A. 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. Fung. Genet. Biol. 2004, 41:930-940.
38. Kumar L., Breakspear A., Kistler C., Ma L.J., Xie X. Systematic discovery of regulatory motifs in Fusarium graminearum by comparing four Fusarium genomes. BMC Genom. 2010, 11:208.
39. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982, 157:105-132.
40. Láday M., Stubnya V., Hamari Z., Hornok L. Characterization of a new mitochondrial plasmid from Fusarium proliferatum. Plasmid 2008, 59:127-133.
41. Lambowitz A.M. Preparation and analysis of mitochondrial ribosomes. Meth. Enzymol. 1979, 59:421-433.
42. Lambowitz A.M., Zimmerly S. Mobile group II introns. Annu. Rev. Genet. 2004, 38:1-35.
43. Lang F.B., Laforest M., Burger G. Mitochondrial introns: a critical view. Trends Genet. 2007, 23:119-125.
44. Lee J., Young J.P.W. The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus. New Phytologist. 2009, 183:200-211.
45. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA poly-morphism data. Bioinformatics 2009, 25:1451-1452.
46. Lievens B., Rep M., Thomma B.P. Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum. Pest. Manage. Sci. 2008, 64:781-7788.
47. Lowe T., Eddy S.R. TRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl. Acids Res. 1997, 25:955-964.
48. Ma L.J., van der Does H.C., Borkovich K.A., Coleman J.J., Daboussi M.J., Di Pietro A., Dufresne M., Freitag M., Grabherr M., Henrissat B., Houterman P.M., Kang S., Shim W.B., Woloshuk C., Xie X., Xu J.R., Antoniw J., Baker S.E., Bluhm B.H., Breakspear A., Brown D.W., Butchko R.A., Chapman S., Coulson R., Coutinho P.M., Danchin E.G., Diener A., Gale L.R., Gardiner D.M., Goff S., Hammond-Kosack K.E., Hilburn K., Hua-Van A., Jonkers W., Kazan K., Kodira C.D., Koehrsen M., Kumar L., Lee Y.H., Li L., Manners J.M., Miranda-Saavedra D., Mukherjee M., Park G., Park J., Park S.Y., Proctor R.H., Regev A., Ruiz-Roldan M.C., Sain D., Sakthikumar S., Sykes S., Schwartz D.C., Turgeon B.G., Wapinski I., Yoder O., Young S., Zeng Q., Zhou S., Galagan J., Cuomo C.A., Kistler H.C., Rep M. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010, 464:367-373.
49. Maizels J., Lenk R. Enhanced graphic matrix analysis of nucleic acid and protein sequences. Proc. Natl. Acad. Sci. USA 1981, 78:7665-7669.
50. Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans (LA), 2010, November 14, pp. 1-8.
51. Nargang F.E., Pande S., Kennell J.C., Akins R.A., Lambowitz A.M. Evidence that a 1.6 kilobase region of Neurospora mtDNA was derived by insertion of part of the LaBelle mitochondrial plasmid. Nucl. Acids Res. 1992, 20:1101-1108.
52. O'Donnell K., Gueidan C., Sink S., Johnston P.R., Crous P.W., Glenn A., Riley R., Zitomer N.C., Colyer P., Waalwijk C., Lee T., Moretti A., Kang S., Kim H.S., Geiser D.M., Juba J.H., Baayen R.P., Cromey M.G., Bithell S., Sutton D.A., Skovgaard K., Ploetz R., Kistler H., Elliott M., Davis M., Sarver B.A. A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet. Biol. 2009, 46:936-948.
53. Pantou M.P., Kouvelis V.N., Typas M.A. 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. 2006, 50:125-136.
54. Pantou M.P., Kouvelis V.N., Typas M.A. The complete mitochondrial genome of Fusarium oxysporum: insights into fungal mitochondrial evolution. Gene 2008, 419:7-15.
55. Paquin B., Laforest M.J., Franz L. Interspecific transfer of mitochondrial genes in fungi and creation of a homologous hybrid gene. Proc. Natl. Acad. Sci. USA 1994, 91:11807-11810.
56. Paquin B., Laforest M.-J., Forget L., Roewer I., Wang Z., Longcore J., Lang B.F. The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr. Genet. 1997, 31:380-395.
57. Paquin B., Laforest M., Lang B.F. Double-hairpin elements in the mitochondrial DNA of Allomyces: evidence for mobility. Mol. Biol. Evol. 2000, 17:1760-1768.
58. Rep M., Kistler H.C. The genomic organization of plant pathogenicity in Fusarium species. Curr. Opin. Plant Biol. 2010, 13:420-426.
59. Saccone S., Gissi C., Reyes A., Larizza A., Sbisa E., Pesole G. Mitochondrial DNA in metazoa: degree of freedom in a frozen event. Gene 2002, 286:3-12.
60. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY). second ed.
61. Schäfer B. Genetic conservation versus variability in mitochondria: the architecture of the mitochondrial genome in the petite-negative yeast Schizosaccharomyces pombe. Curr. Genet. 2003, 43:311-326.
62. Sethuraman J., Majer A., Friedrich N.C., Edgell D.R., Hausner G. Genes within genes: multiple LAGLIDADG homing endonucleases target the ribosomal protein S3 gene encoded within an rnl group I intron of Ophiostoma and related taxa. Mol. Biol. Evol. 2009, 26:2299-2315.
63. Sethuraman J., Majer A., Iranpour M., Hausner G. Molecular evolution of the mtDNA encoded rps3 gene among filamentous ascomycetes fungi with an emphasis on the Ophiostomatoid fungi. J. Mol. Evol. 2009, 69:372-385.
64. Sommerhalder R.J., McDonald B.A., Zhan J. Concordant evolution of mitochondrial and nuclear genomes in the wheat pathogen Phaeosphaeria nodorum. Fungal Genet. Biol. 2007, 44:764-772.
65. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
66. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 1997, 25:4876-4882.
67. Torriani S.F., Goodwin S.B., Kema G.H., Pangilinan J.L., McDonald B.A. Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet. Biol. 2008, 45:628-637.
68. Tudzynski P., Esser K. Extrachromosomal genetics of Claviceps purpurea. II. Plasmids in various wild type strains and integrated plasmid sequences in mitochondrial genomic DNA. Curr. Genet. 1986, 10:463-467.
69. Walther T.C., Kennell J.C. Linear mitochondrial plasmids of F. oxysporum are novel, telomere-like retroelements. Mol. Cell. 1999, 4:229-238.
70. Woo P.C.Y., Zhen H., Cai J.J., Yang J., Lau S.K.P., Wang J., Teng J.L.L., Wong S.S.Y., Tse R.H., Chen R., Yang H., Liu B. The mitochondrial genome of the thermal dimorphic fungus Penicillium marneffei is more closely related to those of molds than yeasts. FEBS Lett. 2003, 555:469-477.
71. Wu Y., Yang J., Yang F., Liu T., Leng W., Chu Y., Jin Q. Recent dermatophyte divergence revealed by comparative and phylogenetic analysis of mitochondrial genomes. BMC Genom. 2009, 10:238.
72. Yin S., Heckman J., Rajbhandary U.L. Highly conserved GC-Rich palindromic DNA sequences flank tRNA genes in Neurospora crassa mitochondria. Cell 1981, 26:325-332.