Comparative analysis of mitochondrial genomes from closely related Rhynchosporium species reveals extensive intron invasion

Fungal Genetics and Biology

Volumn 62, Issue , 2014, Pages 34-42

  Torriani, Stefano F F ^a   Penselin, Daniel ^b   Knogge, Wolfgang ^b   Felder, Marius ^c   Taudien, Stefan ^c   Platzer, Matthias ^c   McDonald, Bruce A ^a   Brunner, Patrick C ^a  

^a ETH ZURICH   (Switzerland)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

Genome architecture; Genome evolution; Horizontal intron transfer; Intron encoded proteins; PAC species

Indexed keywords

CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; FUNGAL PROTEIN; NUCLEOTIDE;

ARTICLE; CELL NUCLEUS; COMPARATIVE STUDY; CONTROLLED STUDY; COX1 GENE; COX2 GENE; EXON; GENE FUNCTION; GENE MUTATION; GENETIC CONSERVATION; GENETIC VARIABILITY; MITOCHONDRIAL GENE; MITOCHONDRIAL GENOME; MUTATION RATE; NAD5 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PRIORITY JOURNAL; RHYNCHOSPORIUM; SEQUENCE ANALYSIS; SPECIES COMPARISON;

RHYNCHOSPORIUM;

GENOME ARCHITECTURE; GENOME EVOLUTION; HORIZONTAL INTRON TRANSFER; INTRON ENCODED PROTEINS; PAC SPECIES;

ASCOMYCOTA; DNA, MITOCHONDRIAL; GENOME, MITOCHONDRIAL; INTRONS; MUTATION RATE; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 84890803314     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.11.001     Document Type: Article

References (67)

1. Adams K.L., Palmer J.D. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol. Phylogenet. Evol. 2003, 29:380-395.
2. Adams K.L., Daley D.O., Qiu Y.L., Whelan J., Palmer J.D. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 2000, 408:354-357.
3. Al-Reedy R.M., Malireddy R., Dillman C.B. Comparative analysis of Fusarium mitochondrial genomes reveals a highly variable region that encodes an exceptionally large open reading frame. Fungal Genet. Biol. 2012, 49:2-14.
4. Altschul S.F., Gish W., Miller W., Myers E.W. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
5. Avise J.C., Arnold J., Ball R.M., Bermingham E. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 1987, 18:489-522.
6. Ballard J.W., Kreitman M. Is mitochondrial DNA a strictly neutral marker?. Trends Ecol. Evol. 1995, 10:485-488.
7. Beaudet D., Nadimi M., Iffis B., Hijri M. Rapid mitochondrial genome evolution through invasion of mobile elements in two closely related species of arbuscular mycorrhizal fungi. PLoS One 2013, 8:e60768.
8. Burger G., Gray M.W., Lang B.F. Mitochondrial genomes: anything goes. Trends Genet. 2003, 19:709-716.
9. Caldwell R.M. Rhynchosporium scald of Barley, Rye, and other grasses. J. Agric. Res. 1937, 55:175-198.
10. Campbell A., Mrázek J., Karlin S. Genome signature comparisons among prokaryote, plasmid, and mitochondrial DNA. Proc. Natl. Acad. Sci. USA 1999, 96:9184-9189.
11. Chen J.Z., Hebert P.D. Intraindividual sequence diversity and a hierarchical approach to the study of mitochondrial DNA mutations. Mutat. Res. 1999, 434:205-217.
12. Croll D., McDonald B.A. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog. 2012, 8:e1002608.
13. Cummings D.J., McNally K.L., Domenico J.M., Matsuura E.T. The complete DNA sequence of the mitochondrial genome of Podospora anserina. Curr. Genet. 1990, 17:375-402.
14. Déquard-Chablat M., Sellem C.H., Golik P., Bidard F., Martos A., Bietenhader M., di Rago J.-P., Sainsard-Chanet A., Hermann-Le Denmat S., Contamine V. Two nuclear life cycle-regulated genes encode interchangeable subunits c of mitochondrial ATP synthase in Podospora anserina. Mol. Biol. Evol. 2011, 28:2063-2075.
15. Drummond A.J., Rambaut A., Shapiro B., Pybus O.G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 2005, 22:1185-1192.
16. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214.
17. Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., Wilson, A., 2011. Geneious v5.5.
18. Duò A., Bruggmann R., Zoller S., Bernt M., Grunig C.R. Mitochondrial genome evolution in species belonging to the Phialocephala fortinii s.l. - Acephala applanata species complex. BMC Genomics 2012, 13:166.
19. Ghikas D.V., Kouvelis V.N., Typas M.A. 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, 185:393-401.
20. Ghikas D.V., Kouvelis V.N., Typas M.A. 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.
21. Gibb E.A., 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.
22. Goddard M.R., Burt A. Recurrent invasion and extinction of a selfish gene. Proc. Natl. Acad. Sci. USA 1999, 96:13880-13885.
23. Gogarten J.P., Hilario E. Inteins, introns, and homing endonucleases: recent revelations about the life cycle of parasitic genetic elements. BMC Evol. Biol. 2006, 6:94.
24. Goodwin S. The barley scald pathogen Rhynchosporium secalis is closely related to the discomycetes Tapesia and Pyrenopeziza. Mycol. Res. 2002, 106:645-654.
25. Gray M.W. Mitochondrial evolution. Science 1999, 283:1476-1481.
26. Hane J.K., Lowe R.G.T., Solomon P.S., Tan K.-C., Schoch C.L., Spatafora J.W., Crous P.W., Kodira C., Birren B.W., Galagan J.E., Torriani S.F.F., McDonald B.A., Oliver R.P. Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 2007, 19:3347-3368.
27. Hane J.K., Rouxel T., Howlett B.J., Kema G.H., Goodwin S.B., Oliver R.P. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol. 2011, 12:R45.
28. Herrmann J.M. Converting bacteria to organelles: evolution of mitochondrial protein sorting. Trends Microbiol. 2003, 11:74-79.
29. Jacobs M.A., Payne S.R., Bendich A.J. Moving pictures and pulsed-field gel electrophoresis show only linear mitochondrial DNA molecules from yeasts with linear-mapping and circular-mapping mitochondrial genomes. Curr. Genet. 1996, 30:3-11.
30. Joardar V., Abrams N.F., Hostetler J., Paukstelis P.J., Pakala S., Pakala S.B., Zafar N., Abolude O.O., Payne G., Andrianopoulos A., Denning D.W., Nierman W.C. 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 2012, 13:698.
31. John P., Whatley F.R. Paracoccus denitrificans and the evolutionary origin of the mitochondrion. Nature 1975, 254:495-498.
32. Jurica M.S., Stoddard B.L. Homing endonucleases: structure, function and evolution. CMLS. Cell. Mol. Life Sci. 1999, 55:1304-1326.
33. Kasuga T.T., White T.J.T., Taylor J.W.J. Estimation of nucleotide substitution rates in Eurotiomycete fungi. Mol. Biol. Evol. 2002, 19:2318-2324.
34. Krogh A., Larsson B.È., Heijne, Von G. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
35. Lang B.F., Gray M.W., Burger G. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 1999, 33:351-397.
36. Lang B.F., Laforest M.-J., Burger G. Mitochondrial introns: a critical view. Trends Genet. 2007, 23:119-125.
37. Lehnackers H., Knogge W. Cytological studies on the infection of barley cultivars with known resistance genotypes by Rhynchosporium secalis. Can. J. Botany 1990, 68:1953-1961.
38. Li W., Tucker A.E., Sung W., Thomas W.K., Lynch M. Extensive, recent intron gains in Daphnia populations. Science 2009, 326:1260-1262.
39. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
40. Lowe T.M., Eddy S.R. TRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997, 25:955-964.
41. Lynch M. The Origins of Genome Architecture 2007, Sinauer Associates Inc.
42. Lynch M., Sung W., Morris K., Coffey N., Landry C.R., Dopman E.B., Dickinson W.J., Okamoto K., Kulkarni S., Hartl D.L., Thomas W.K. A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl. Acad. Sci. USA 2008, 105:9272-9277.
43. Maleszka R., Clark-Walker G.D. In vivo conformation of mitochondrial DNA in fungi and zoosporic moulds. Curr. Genet. 1992, 22:341-344.
44. Moore W.S. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 1995, 49:718-726.
45. Mota E.M., Collins R.A. Independent evolution of structural and coding regions in a Neurospora mitochondrial intron. Nature 1988, 332:654-656.
46. Palmer J.D., Adams K.L., Cho Y., Parkinson C.L., Qiu Y.L., Song K. Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc. Natl. Acad. Sci. USA 2000, 97:6960-6966.
47. 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.
48. Parmakelis A., Kotsakiozi P., Rand D. Animal mitochondria, positive selection and cyto-nuclear coevolution: insights from pulmonates. PLoS One 2013, 8:e61970.
49. Rand D.M. The units of selection on mitochondrial DNA. Annu. Rev. Ecol. Syst. 2001, 32:415-448.
50. Roca M.G., Read N.D. Conidial anastomosis tubes in filamentous fungi - Gabriela Roca - 2006 - FEMS Microb. Let. - Wiley Online Library. FEMS Microbiol. Lett. 2005, 249:191-199.
51. Rohe M., Searle J., Newton A.C., Knogge W. Transformation of the plant pathogenic fungus, Rhynchosporium secalis. Curr. Genet. 1996, 29:587-590.
52. Sanchez-Puerta M.V., Cho Y., Mower J.P., Alverson A.J., Palmer J.D. Frequent, phylogenetically local horizontal transfer of the cox1 Group I intron in flowering plant mitochondria. Mol. Biol. Evol. 2008, 25:1762-1777.
53. Saraste M. Oxidative phosphorylation at the fin de siècle. Science 1999, 283:1488-1493.
54. Sellem C.H., Belcour L. Intron open reading frames as mobile elements and evolution of a group I intron. Mol. Biol. Evol. 1997, 14:518-526.
55. 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.
56. Shipton W., Boyd W.J.R., Ali S.M. Scald of barley. Rev. Plant Pathol. 1974, 53:839-861.
57. Syvanen M. Evolutionary implications of horizontal gene transfer. Annu. Rev. Genet. 2012, 46:341-358.
58. Torriani S.F.F., Goodwin S.B., Kema G.H.J., 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.
59. Torriani S.F.F., Brunner P.C., McDonald B.A., Sierotzki H. QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag. Sci. 2009, 65:155-162.
60. Torriani S.F.F., Brunner P.C., McDonald B.A., Croll D. Evidence for extensive recent intron transposition in closely related fungi. Curr. Biol. 2011, 21:2017-2022.
61. Welty R., Metzger R. First report of scald of triticale caused by Rhynchosporium secalis in North America. Plant Dis. 1996, 80:1220-1223.
62. Wolfe K.H., Li W.H., Sharp P.M. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 1987, 84:9054-9058.
63. Zaffarano P.L., McDonald B.A., Linde C.C. Rapid speciation following recent host shifts in the plant pathogenic fungus Rhynchosporium. Evolution 2008, 62:1418-1436.
64. Zaffarano P.L., McDonald B.A., Linde C.C. Phylogeographical analyses reveal global migration patterns of the barley scald pathogen Rhynchosporium secalis. Mol. Ecol. 2009, 18:279-293.
65. Zaffarano P.L., McDonald B.A., Linde C.C. Two new species of Rhynchosporium. Mycologia 2011, 103:195-202.
66. Zdobnov E.M., Apweiler R. InterProScan an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17:847-848.
67. Zhu S., Cao Y.Z., Jiang C., Tan B.Y., Wang Z. Sequencing the genome of Marssonina brunnea reveals fungus-poplar co-evolution. BMC Genomics 2012, 13:382.