Sequencing of mitochondrial genomes of nine Aspergillus and Penicillium species identifies mobile introns and accessory genes as main sources of genome size variability

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Joardar, Vinita ^a   Abrams, Natalie F ^a   Hostetler, Jessica ^a   Paukstelis, Paul J ^b   Pakala, Suchitra ^a   Pakala, Suman B ^a   Zafar, Nikhat ^a   Abolude, Olukemi O ^c   Payne, Gary ^d   Andrianopoulos, Alex ^e   Denning, David W ^f   Nierman, William C ^a  

^a J CRAIG VENTER INSTITUTE   (United States)

^b Bldg 142   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; ENDONUCLEASE; LARGE SUBUNIT RIBOSOMAL RNA; MITOCHONDRIAL PROTEIN; RNA POLYMERASE;

ARTICLE; ASPERGILLUS; ASPERGILLUS CLAVATUS; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; ASPERGILLUS ORYZAE; ASPERGILLUS TERREUS; FUNGAL STRAIN; GENE SEQUENCE; GENE TRANSFER; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOME SIZE; INTRASPECIFIC VARIATION; INTRON; MITOCHONDRIAL GENOME; NEOSATORYA FISCHERI; NONHUMAN; NUCLEOTIDE SEQUENCE; PENICILLIUM; PENICILLIUM CHRYSOGENUM; PENICILLIUM MARNEFFEI; PHYLOGENY; TALAROMYCES STIPITATUS;

ASPERGILLUS; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENES, FUNGAL; GENES, MITOCHONDRIAL; GENETIC VARIATION; GENOME SIZE; GENOME, MITOCHONDRIAL; INTRONS; MOLECULAR SEQUENCE ANNOTATION; MUTAGENESIS, INSERTIONAL; PENICILLIUM; PHYLOGENY; PLASMIDS; SEQUENCE ANALYSIS;

ASPERGILLUS; ASPERGILLUS CLAVATUS; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; ASPERGILLUS ORYZAE; ASPERGILLUS TERREUS; FUNGI; NEOSARTORYA FISCHERI; PENICILLIUM; PENICILLIUM CHRYSOGENUM; PENICILLIUM MARNEFFEI; TALAROMYCES STIPITATUS;

EID: 84870870373     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-698     Document Type: Article

References (62)

1. Hoffmeister D, Keller NP. Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 2007, 24(2):393-416.
2. Enoch DA, Ludlam HA, Brown NM. Invasive fungal infections: a review of epidemiology and management options. J Med Microbiol 2006, 55(Pt 7):809-818.
3. Cummings DJ, McNally KL, Domenico JM, Matsuura ET. The complete DNA sequence of the mitochondrial genome of Podospora anserina. Curr Genet 1990, 17(5):375-402.
4. Amlacher S, Sarges P, Flemming D, van Noort V, Kunze R, Devos DP, Arumugam M, Bork P, Hurt E. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 2011, 146(2):277-289.
5. Osiewacz HD, Brust D, Hamann A, Kunstmann B, Luce K, Muller-Ohldach M, Scheckhuber CQ, Servos J, Strobel I. Mitochondrial pathways governing stress resistance, life, and death in the fungal aging model Podospora anserina. Ann N Y Acad Sci 2010, 1197:54.
6. Sanglard D, Ischer F, Bille J. Role of ATP-binding-cassette transporter genes in high-frequency acquisition of resistance to azole antifungals in Candida glabrata. Antimicrob Agents Chemother 2001, 45(4):1174-1183.
7. Ferrari S, Sanguinetti M, Torelli R, Posteraro B, Sanglard D. Contribution of CgPDR1-regulated genes in enhanced virulence of azole-resistant Candida glabrata. PLoS One 2011, 6(3):e17589.
8. Martins VP, Dinamarco TM, Soriani FM, Tudella VG, Oliveira SC, Goldman GH, Curti C, Uyemura SA. Involvement of an alternative oxidase in oxidative stress and mycelium-to-yeast differentiation in Paracoccidioides brasiliensis. Eukaryot Cell 2011, 10(2):237-248.
9. Scheckhuber CQ, Hamann A, Brust D, Osiewacz HD. Cellular homeostasis in fungi: impact on the aging process. Sub-cellular biochemistry 57:233-250.
10. Santamaria M, Vicario S, Pappada G, Scioscia G, Scazzocchio C, Saccone C. Towards barcode markers in fungi: an intron map of Ascomycota mitochondria. BMC Bioinforma 2009, 10(Suppl 6):S15.
11. Hamari Z, Juhasz A, Kevei F. Role of mobile introns in mitochondrial genome diversity of fungi (a mini review). Acta Microbiol Immunol Hung 2002, 49(2-3):331-335.
12. Wallace DC. Mitochondrial DNA mutations in disease and aging. Environ Mol Mutagen 2010, 51(5):440-450.
13. Tavare A. Scientists are to investigate " three parent IVF" for preventing mitochondrial diseases. BMJ (Clinical research ed) 2012, 344:e540.
14. Juhasz A, Pfeiffer I, Keszthelyi A, Kucsera J, Vagvolgyi C, Hamari Z. Comparative analysis of the complete mitochondrial genomes of Aspergillus niger mtDNA type 1a and Aspergillus tubingensis mtDNA type 2b. FEMS Microbiol Lett 2008, 281(1):51-57.
15. Juhasz A, Engi H, Pfeiffer I, Kucsera J, Vagvolgyi C, Hamari Z. Interpretation of mtDNA RFLP variability among Aspergillus tubingensis isolates. Antonie Van Leeuwenhoek 2007, 91(3):209-216.
16. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, et al. Genome sequencing and analysis of Aspergillus oryzae. Nature 2005, 438(7071):1157-1161.
17. Woo PC, Zhen H, Cai JJ, Yu J, Lau SK, Wang J, Teng JL, Wong SS, Tse RH, Chen R, et al. The mitochondrial genome of the thermal dimorphic fungus Penicillium marneffei is more closely related to those of molds than yeasts. FEBS Lett 2003, 555(3):469-477.
18. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, et al. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438(7071):1151-1156.
19. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Basturkmen M, Spevak CC, Clutterbuck J, et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 2005, 438(7071):1105-1115.
20. van Den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, Driessen AJ, Garcia-Estrada C, Fedorova ND, Harris DM, Heijne WH, et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat Biotechnol 2008, 26(10):1161-1168.
21. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, et al. Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 2008, 4(4):e1000046.
22. van Diepeningen AD, Goedbloed DJ, Slakhorst SM, Koopmanschap AB, Maas MF, Hoekstra RF, Debets AJ. Mitochondrial recombination increases with age in Podospora anserina. Mech Ageing Dev 2010, 131(5):315.
23. Samson RA, Pitt JI. Advances in Penicillium and Aspergillus systematics 1985, New York: Plenum Press.
24. Berbee M, Yoshimura A, Sugiyama J, Taylor JW. Is Penicillium monophyletic? An evaluation of phylogeny in the family Trichocomaceae from 18S, 5.8S And ITS ribosomal DNA sequence data. Mycologia 1995, 87(2):210-222.
25. Geiser DM, Samson RA, Varga J, Rokas A, Witiak SM. A review of molecular phylogenetics in Aspergillus, and prospects for a robust genus-wide phylogeny. Aspergillus in the genomics era 2008, 17-32. Wageningen: Wageningen Academic Publishers, Varga J, Sampson RA.
26. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, et al. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nature biotechnology 2007, 25(2):221-231.
27. Rokas A, Galagan JE. Aspergillus nidulans genome and a comparative analysis of genome evolution in Aspergillus. The aspergilli: genomics, medical aspects, biotechnology, and research methods 2007, 43-55. Boca Raton: CRC Press, Osmani SA, Goldman GH.
28. Peterson SW. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 2008, 100(2):205-226.
29. Griffiths AJ. Natural plasmids of filamentous fungi. Microbiol Rev 1995, 59(4):673-685.
30. Maheshwari R, Navaraj A. Senescence in fungi: the view from Neurospora. FEMS Microbiol Lett 2008, 280(2):135-143.
31. Maas MF, Sellem CH, Hoekstra RF, Debets AJ, Sainsard-Chanet A. Integration of a pAL2-1 homologous mitochondrial plasmid associated with life span extension in Podospora anserina. Fungal Genet Biol 2007, 44(7):659-671.
32. Court DA, Griffiths AJ, Kraus SR, Russell PJ, Bertrand H. A new senescence-inducing mitochondrial linear plasmid in field-isolated Neurospora crassa strains from India. Curr Genet 1991, 19(2):129-137.
33. Belfort M, Roberts RJ. Homing endonucleases: keeping the house in order. Nucleic Acids Res 1997, 25(17):3379-3388.
34. Delahodde A, Goguel V, Becam AM, Creusot F, Perea J, Banroques J, Jacq C. Site-specific DNA endonuclease and RNA maturase activities of two homologous intron-encoded proteins from yeast mitochondria. Cell 1989, 56(3):431-441.
35. Wenzlau JM, Saldanha RJ, Butow RA, Perlman PS. A latent intron-encoded maturase is also an endonuclease needed for intron mobility. Cell 1989, 56(3):421-430.
36. Basse CW. Mitochondrial inheritance in fungi. Curr Opin Microbiol 2010, 13(6):712-719.
37. Stoddard BL. Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure 2011, 19(1):7-15.
38. Torriani SF, Goodwin SB, Kema GH, Pangilinan JL, McDonald BA. Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 2008, 45(5):628-637.
39. Foury F, Roganti T, Lecrenier N, Purnelle B. The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett 1998, 440(3):325-331.
40. Field DJ, Sommerfield A, Saville BJ, Collins RA. A group II intron in the Neurospora mitochondrial coI gene: nucleotide sequence and implications for splicing and molecular evolution. Nucleic Acids Res 1989, 17(22):9087-9099.
41. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, et al. Life with 6000 genes. Science New York, NY 996, 274(5287):546. 563-547.
42. LaPolla RJ, Lambowitz AM. Mitochondrial ribosome assembly in Neurospora crassa. Purification of the mitochondrially synthesized ribosomal protein, S-5. J Biol Chem 1981, 256(13):7064-7067.
43. Lapolla RJ, Lambowitz AM. Mitochondrial ribosome assembly in Neurospora. Structural analysis of mature and partially assembled ribosomal subunits by equilibrium centrifugation in CsCl gradients. J Cell Biol 1982, 95(1):267-277.
44. Guo QB, Akins RA, Garriga G, Lambowitz AM. Structural analysis of the Neurospora mitochondrial large rRNA intron and construction of a mini-intron that shows protein-dependent splicing. J Biol Chem 1991, 266(3):1809-1819.
45. Kamper U, Kuck U, Cherniack AD, Lambowitz AM. The mitochondrial tyrosyl-tRNA synthetase of Podospora anserina is a bifunctional enzyme active in protein synthesis and RNA splicing. Mol Cell Biol 1992, 12(2):499-511.
46. Hur M, Geese WJ, Waring RB. Self-splicing activity of the mitochondrial group-I introns from Aspergillus nidulans and related introns from other species. Curr Genet 1997, 32(6):399-407.
47. Paukstelis PJ, Lambowitz AM. Identification and evolution of fungal mitochondrial tyrosyl-tRNA synthetases with group I intron splicing activity. Proc Natl Acad Sci U S A 2008, 105(16):6010-6015.
48. Goddard MR, Burt A. Recurrent invasion and extinction of a selfish gene. Proc Natl Acad Sci U S A 1999, 96(24):13880-13885.
49. Hane JK, Lowe RG, Solomon PS, Tan KC, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, et al. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 2007, 19(11):3347-3368.
50. Hamari Z, Toth B, Beer Z, Gacser A, Kucsera J, Pfeiffer I, Juhasz A, Kevei F. Interpretation of intraspecific variability in mtDNAs of Aspergillus niger strains and rearrangement of their mtDNAs following mitochondrial transmissions. FEMS Microbiol Lett 2003, 221(1):63-71.
51. Miller JR, Delcher AL, Koren S, Venter E, Walenz BP, Brownley A, Johnson J, Li K, Mobarry C, Sutton G. Aggressive assembly of pyrosequencing reads with mates. Bioinformatics (Oxford, England) 2008, 24(24):2818-2824.
52. Delcher AL, Phillippy A, Carlton J, Salzberg SL. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 2002, 30(11):2478-2483.
53. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
54. Parsons JD. Miropeats: graphical DNA sequence comparisons. Comput Appl Biosci 1995, 11(6):615-619.
55. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics (Oxford, England) 2000, 16(10):944-945.
56. Michel F, Westhof E. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 1990, 216(3):585-610.
57. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13(9):2178-2189.
58. Wang H, Su Y, Mackey AJ, Kraemer ET, Kissinger JC. SynView: a GBrowse-compatible approach to visualizing comparative genome data. Bioinformatics (Oxford, England) 2006, 22(18):2308-2309.
59. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
60. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17(4):540-552.
61. Stamatakis A, Ludwig T, Meier H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics (Oxford, England) 2005, 21(4):456-463.
62. Felsenstein J. PHYLIP-phylogeny inference package (version 3.2). Cladistics 1989, 5:164-166.