Mitochondrial genome evolution in species belonging to the Phialocephala fortinii s.l. - Acephala applanata species complex

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Duò, Angelo ^a   Bruggmann, Rémy ^b   Zoller, Stefan ^a   Bernt, Matthias ^c   Grünig, Christoph R ^a,d  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d MICROSYNTH AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; MITOCHONDRIAL DNA; TRANSFER RNA;

ACEPHALA APPLANATA; ARTICLE; CONTROLLED STUDY; EXPRESSED SEQUENCE TAG; FUNGAL GENETICS; FUNGAL STRAIN; GENE DUPLICATION; GENE LOCUS; GENE ORDER; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC VARIABILITY; HELOTIALES; MITOCHONDRIAL GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATIVE PHOSPHORYLATION; PHIALOCEPHALA FORTINII; PHIALOCEPHALA SUBALPINA; PHYLOGENY; SEQUENCE ALIGNMENT; START CODON; STOP CODON;

ASCOMYCOTA; CONSERVED SEQUENCE; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE DUPLICATION; GENE ORDER; GENE REARRANGEMENT; GENETIC LOCI; GENETIC MARKERS; GENOME, FUNGAL; GENOME, MITOCHONDRIAL; OPEN READING FRAMES; PHYLOGENY; POLYMORPHISM, GENETIC; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; TRANSCRIPTOME;

ACEPHALA APPLANATA; ASCOMYCOTA; HELOTIALES; PEZIZOMYCOTINA; PHIALOCEPHALA FORTINII; SCLEROTINIA SCLEROTIORUM;

EID: 84860526488     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-166     Document Type: Article

References (77)

1. Grünig CR, Sieber TN, Rogers SO, Holdenrieder O. Genetic variability among strains of Phialocephala fortinii and phylogenetic analysis of the genus Phialocephala based on rDNA ITS sequence comparisons. Can J Bot 2002, 80(12):1239-1249.
2. Wang Z, Binder M, Schoch CL, Johnston PR, Spatafora JW, Hibbett DS. Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): A nuclear rDNA phylogeny. Mol Phylogenet Evol 2006, 41(2):295-312. 10.1016/j.ympev.2006.05.031, 16837216.
3. Grünig CR, Queloz V, Duò A, Sieber TN. Phylogeny of Phaeomollisia piceae gen. sp. nov.: a dark-septate conifer-needle endophyte and its relationships to Phialocephala and Acephala. Mycol Res 2009, 113(2):207-221. 10.1016/j.mycres.2008.10.005, 19015028.
4. Queloz V, Sieber TN. Holdenrieder, McDonald BA, Grünig CR: No biogeographical pattern for a root-associated fungal species complex. Global Ecol Biogeogr 2011, 20(1):160-169.
5. Piercey MM, Graham SW, Currah RS. Patterns of genetic variation in Phialocephala fortinii across a broad latitudinal transect in Canada. Mycol Res 2004, 108(8):955-964. 10.1017/S0953756204000528, 15449601.
6. Grünig CR, Queloz V, Sieber TN, Holdenrieder O. Dark septate endophytes (DSE) of the Phialocephala fortinii s.l. - Acephala applanata species complex in tree roots-classification, population biology and ecology. Botany 2008, 86(12):1355-1369.
7. Zhang C, Yin L, Dai S. Diversity of root-associated fungal endophytes in Rhododendron fortunei in subtropical forests of China. Mycorrhiza 2009, 19(6):417-423. 10.1007/s00572-009-0246-1, 19396474.
8. Grünig CR, Duò A, Sieber TN, Holdenrieder O. Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii s.l.-Acephala applanata species complex. Mycologia 2008, 100(1):47-67. 10.3852/mycologia.100.1.47, 18488352.
9. Grünig CR, Sieber TN. Molecular and phenotypic description of the widespread root symbiont Acephala applanata gen. et sp. nov., formerly known as dark septate endophyte Type 1. Mycologia 2005, 97(3):628-640. 10.3852/mycologia.97.3.628, 16392252.
10. Grünig CR, McDonald BA, Sieber TN, Rogers SO, Holdenrieder O. Evidence for subdivision of the root-endophyte Phialocephala fortinii into cryptic species and recombination within species. Fung Genet Biol 2004, 41(7):676-687.
11. Grünig CR, Duò A, Sieber TN. Population genetic analysis of Phialocephala fortinii s.l. and Acephala applanata in two undisturbed forests in Switzerland and evidence for new cryptic species. Fung Genet Biol 2006, 43(6):410-421.
12. Queloz V, Grünig CR, Sieber TN. Holdenrieder O: Monitoring the spatial and temporal dynamics of a community of the tree-root endophyte Phialocephala fortinii s.l. New Phytol 2005, 168(3):651-660. 10.1111/j.1469-8137.2005.01529.x, 16313647.
13. Peay KG, Kennedy PG, Bruns TD. Fungal Community Ecology: A Hybrid Beast with a Molecular Master. Bioscience 2008, 58(9):799-810.
14. Grünig CR, Brunner PC, Duò A, Sieber TN. Suitability of methods for species recognition in the Phialocephala fortinii - Acephala applanata species complex using DNA analysis. Fung Genet Biol 2007, 44(8):773-788.
15. Queloz V, Duo A, Sieber TN, Grünig CR. Microsatellite size homoplasies and null alleles do not affect species diagnosis and population genetic analysis in a fungal species complex. Mol Ecol Resour 2010, 10:348-367. 10.1111/j.1755-0998.2009.02757.x, 21565031.
16. Pantou MP, Kouvelis VN, Typas MA. 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(2):125-136. 10.1007/s00294-006-0079-9, 16733756.
17. Seifert KA, Samson RA, Dewaard JR, Houbraken J, Lévesque CA, Moncalvo J-M, Louis-Seize G, Hebert PDN. Prospects for fungus identification using CO1 DNA barcodes, with Penicillium as a test case. Proc Natl Acad Sci USA 2007, 104(10):3901-3906. 10.1073/pnas.0611691104, 1805696, 17360450.
18. Kouvelis VN, Sialakouma A, Typas MA. Mitochondrial gene sequences alone or combined with ITS region sequences provide firm molecular criteria for the classification of Lecanicillium species. Mycol Res 2008, 112:829-844. 10.1016/j.mycres.2008.01.016, 18501578.
19. Burger G, Gray M, Lang B. Mitochondrial genomes: anything goes. Trends Genet 2003, 19(12):709-716. 10.1016/j.tig.2003.10.012, 14642752.
20. Ghikas DV, Kouvelis VN, Typas MA. Phylogenetic and biogeographic implications inferred by mitochondrial intergenic region analyses and ITS1-5.8S-ITS2 of the entomopathogenic fungi Beauveria bassiana and B. brongniartii. BMC Microbiol 2010, 10:174. 10.1186/1471-2180-10-174, 2896372, 20553589.
21. Gray M, Burger G, Lang B. Mitochondrial evolution. Science 1999, 283(5407):1476-1481. 10.1126/science.283.5407.1476, 10066161.
22. Lavin JL, Oguiza JA, Ramirez L, Pisabarro AG. Comparative genomics of the oxidative phosphorylation system in fungi. Fungal Genet Biol 2008, 45(9):1248-1256. 10.1016/j.fgb.2008.06.005, 18647654.
23. 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 Genomics 2009, 10:238. 10.1186/1471-2164-10-238, 2693141, 19457268.
24. Sethuraman J, Majer A, Friedrich NC, Edgell DR, 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(10):2299-2315. 10.1093/molbev/msp145, 19597163.
25. Monteiro-Vitorello CB, Hausner G, Searles DB, Gibb EA, Fulbright DW, Bertrand H. The Cryphonectria parasitica mitochondrial rns gene: Plasmid-like elements, introns and homing endonucleases. Fungal Genet Biol 2009, 46(11):837-848. 10.1016/j.fgb.2009.07.005, 19607930.
26. Gibb E, Hausner G. Optional mitochondrial introns and evidence for a homing-endonuclease gene in the mtDNA rnl gene in Ophiostoma ulmi s. lat. Mycol Res 2005, 109:1112-1126. 10.1017/S095375620500376X, 16279406.
27. Torriani SFF, Goodwin SB, Kema GHJ, 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. 10.1016/j.fgb.2007.12.005, 18226935.
28. Kirk PM, Cannon PF, David JC, Stalpers JA. (Eds): Dictionary of the fungi 2001, CAB International, Oxon, UK, 9.
29. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst Biol 2002, 51(3):492-508. 10.1080/10635150290069913, 12079646.
30. Polevoda B, Sherman F. The diversity of acetylated proteins. Genome Biol 2002, 3(5):reviews0006-reviews0006.6. 139359, 12049668.
31. Yoshikawa A, Isono S, Sheback A, Isono K. Cloning and nucleotide sequencing of the genes rimI and rimJ which encode enzymes acetylating ribosomal proteins S18 and S5 of Escherichia coli K12. Mol Gen Genet 1987, 209(3):481-488. 10.1007/BF00331153, 2828880.
32. Isono K, Isono S. Ribosomal protein modification in Escherichia coli. II. Studies of a mutant lacking the N-terminal acetylation of protein S18. Mol Gen Genet 1980, 177(4):645-651.
33. Hane JK, Lowe RGT, Solomon PS, Tan K-C, 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. 10.1105/tpc.107.052829, 2174895, 18024570.
34. 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(4):372-385. 10.1007/s00239-009-9291-9, 19826748.
35. Debuchy R, Brygoo Y. Cloning of opal suppressor tRNA genes of a filamentous fungus reveals two tRNASerUGA genes with unexpected structural differences. EMBO J 1985, 4(13A):3553-3556. 554696, 3937728.
36. Grimm M, Nass A, Schüll C, Beier H. Nucleotide sequences and functional characterization of two tobacco UAG suppressor tRNA(Gln) isoacceptors and their genes. Plant Mol Biol 1998, 38(5):689-697. 10.1023/A:1006068303683, 9862487.
37. Baum M, Beier H. Wheat cytoplasmic arginine tRNA isoacceptor with a U*CG anticodon is an efficient UGA suppressor in vitro. Nucleic Acids Res 1998, 26(6):1390-1395. 10.1093/nar/26.6.1390, 147420, 9490782.
38. Beier H, Grimm M. Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Res 2001, 29(23):4767-4782. 10.1093/nar/29.23.4767, 96686, 11726686.
39. Faure E, Delaye L, Tribolo S, Levasseur A, Seligmann H, Barthélémy R-M. Probable presence of an ubiquitous cryptic mitochondrial gene on the antisense strand of the cytochrome oxidase I gene. Biol Direct 2011, 6:56. 10.1186/1745-6150-6-56, 3214167, 22024028.
40. Seligmann H. Two genetic codes, one genome: frameshifted primate mitochondrial genes code for additional proteins in presence of antisense antitermination tRNAs. Biosystems 2011, 105(3):271-285. 10.1016/j.biosystems.2011.05.010, 21669250.
41. Covello PS, Gray MW. Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J 1992, 11(11):3815-3820. 556890, 1382979.
42. Harismendy O, Ng PC, Strausberg RL, Wang XY, Stockwell TB, Beeson KY, Schork NJ, Murray SS, Topol EJ, Levy S, et al. Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome Biol 2009, 10(3):R32. 10.1186/gb-2009-10-3-r32, 2691003, 19327155.
43. Costanzo MC, Fox TD. Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu Rev Genet 1990, 24:91-113. 10.1146/annurev.ge.24.120190.000515, 2088182.
44. 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. 10.1007/BF00334517, 2357736.
45. Kunisawa T. Inference of the phylogenetic position of the phylum Deferribacteres from gene order comparison. Antonie Van Leeuwenhoek 2011, 99(2):417-422. 10.1007/s10482-010-9492-7, 20706870.
46. Sankoff D, Leduc G, Antoine N, Paquin B, Lang B, Cedergren R. Gene order comparisons for phylogenetic inference - Evolution of the mitochondrial genome. Proc Natl Acad Sci USA 1992, 89(14):6575-6579. 10.1073/pnas.89.14.6575, 49544, 1631158.
47. Sun X, Li H, Yu D. Complete mitochondrial genome sequence of the phytopathogenic fungus Penicillium digitatum and comparative analysis of closely related species. FEMS Microbiol Lett 2011, 323(1):29-34. 10.1111/j.1574-6968.2011.02358.x, 22092677.
48. Kunisawa T. The phylogenetic placement of the non-phototrophic, Gram-positive thermophile 'Thermobaculum terrenum' and branching orders within the phylum 'Chloroflexi' inferred from gene order comparisons. Int J Systematic Evol Microbiol 2011, 61:1944-1953.
49. Saccone C, Gissi C, Reyes A, Larizza A, Sbisa E, Pesole G. Mitochondrial DNA in metazoa: degree of freedom in a frozen event. Gene 2002, 286(1):3-12. 10.1016/S0378-1119(01)00807-1, 11943454.
50. Jühling F, Pütz J, Bernt M, Donath A, Middendorf M. Florentz C 2011, Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements. Nucleic Acids Res, Stadler PF.
51. Sommerhalder RJ, McDonald BA, Zhan J. Concordant evolution of mitochondrial and nuclear genomes in the wheat pathogen Phaeosphaeria nodorum. Fungal Genet Biol 2007, 44(8):764-772. 10.1016/j.fgb.2007.01.003, 17293135.
52. Anderson J, Wickens C, Khan M, Cowen L, Federspiel N, Jones T, Kohn L. Infrequent genetic exchange and recombination in the mitochondrial genome of Candida albicans. J Bacteriol 2001, 183(3):865-872. 10.1128/JB.183.3.865-872.2001, 94952, 11208783.
53. van Diepeningen AD, Goedbloed DJ, Slakhorst SM, Koopmanschap AB, Maas MFPM, Hoekstra RF, Debets AJM. Mitochondrial recombination increases with age in Podospora anserina. Mech Ageing Dev 2010, 131(5):315-322. 10.1016/j.mad.2010.03.001, 20226205.
54. Barr CM, Neiman M, Taylor DR. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol 2005, 168(1):39-50. 10.1111/j.1469-8137.2005.01492.x, 16159319.
55. Seifert KA. Progress towards DNA barcoding of fungi. Mol Ecol Resour 2009, 9:83-89.
56. Ghikas DV, Kouvelis VN, Typas MA. The complete mitochondrial genome of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae: gene order and trn gene clusters reveal a common evolutionary course for all Sordariomycetes, while intergenic regions show variation. Arch Microbiol 2006, 185(5):393-401. 10.1007/s00203-006-0104-x, 16552580.
57. Zaffarano PL, Duò A, Grünig CR. Characterization of the mating type (MAT) locus in the Phialocephala fortinii s.l. -Acephala applanata species complex. Fungal Genet Biol 2010, 47(9):761-772. 10.1016/j.fgb.2010.06.001, 20541616.
58. NCBI ORF finder:. http://www.ncbi.nlm.nih.gov/gorf/gorf.html.
59. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
60. EMBOSS tools:. http://www.ebi.ac.uk/Tools/pfa/iprscan/.
61. Lowe T, Eddy S. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25(5):955-964. 146525, 9023104.
62. Lang BF, Laforest M-J, Burger G. Mitochondrial introns: a critical view. Trends Genet 2007, 23(3):119-125. 10.1016/j.tig.2007.01.006, 17280737.
63. Sonnhammer EL, Durbin R. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 1995, 167(1-2):GC1-GC10.
64. Gremme G, Brendel V, Sparks M, Kurtz S. Engineering a software tool for gene structure prediction in higher organisms. Inform Software Tech 2005, 47(15):965-978.
65. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements. Genome Res 2004, 14(7):1394-1403. 10.1101/gr.2289704, 442156, 15231754.
66. MAFFT:. http://mafft.cbrc.jp/alignment/server/index.html.
67. Gblocks 0.91b:. http://www.phylogeny.fr/version2_cgi/one_task.cgi?task_type=gblocks.
68. Bernt M, Merkle D, Ramsch K, Fritzsch G, Perseke M, Bernhard D, Schlegel M, Stadler PF, Middendorf M. CREx: inferring genomic rearrangements based on common intervals. Bioinformatics 2007, 23(21):2957-2958. 10.1093/bioinformatics/btm468, 17895271.
69. Bernt M, Merkle D, Middendorf M: An Algorithm for Inferring Mitochondrial Genome Rearrangements in a Phylogenetic Tree. In Comparative Genomics International Workshop, RECOMB-CG Paris, Lecture Notes in Computer Sciences (LNCS). Berlin: Springer 2008, 2008:143-157. Bernt M, Merkle D, Middendorf M: An Algorithm for Inferring Mitochondrial Genome Rearrangements in a Phylogenetic Tree. In Comparative Genomics International Workshop, RECOMB-CG.
70. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19(18):2496-2497. 10.1093/bioinformatics/btg359, 14668244.
71. Hey J, Wakeley J. A coalescent estimator of the population recombination rate. Genetics 1997, 145:833-846. 1207867, 9055092.
72. Su X, Wu Y, Sifri C, Wellems T. Reduced extension temperatures required for PCR amplification of extremely A + T-rich DNA. Nucleic Acids Res 1996, 24(8):1574-1575. 10.1093/nar/24.8.1574, 145803, 8628694.
73. Jobb G. TREEFINDER version of November 2010. http://www.treefinder.de/.
74. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27(8):1164-1165. 10.1093/bioinformatics/btr088, 21335321.
75. Swofford DL. PAUP: pylogenetic analysis using parsimony, version 3.1.1 1993, Illinois Natural History Survey, Champaign, IL.
76. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25(7):1253-1256. 10.1093/molbev/msn083, 18397919.
77. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574. 10.1093/bioinformatics/btg180, 12912839.