Evidence for inter-specific recombination among the mitochondrial genomes of Fusarium species in the Gibberella fujikuroi complex

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Fourie, Gerda ^a   van der Merwe, Nicolaas A ^a   Wingfield, Brenda D ^a   Bogale, Mesfin ^a   Tudzynski, Bettina ^b   Wingfield, Michael J ^a   Steenkamp, Emma T ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Group I intron; Incongruent phylogenies; LAGLIDADG and GIY YIG homing endonucleases; Synteny

Indexed keywords

RIBOSOME RNA; TRANSFER RNA;

ARTICLE; CODON USAGE; FUNGAL GENE; FUNGAL GENOME; FUSARIUM; FUSARIUM CIRCINATUM; FUSARIUM FUJIKUROI; FUSARIUM MONILIFORME; GENE ORDER; GENETIC RECOMBINATION; GIBBERELLA FUJIKUROI; INTRON; MITOCHONDRIAL GENE; MITOCHONDRIAL GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENETIC TREE; PHYLOGENY; RNA GENE; SYNTENY;

EUKARYOTA; FUNGI; FUSARIUM; GIBBERELLA CIRCINATA; GIBBERELLA FUJIKUROI; GIBBERELLA FUJIKUROI COMPLEX; SORDARIOMYCETES;

COMPARATIVE GENOMIC HYBRIDIZATION; DNA, FUNGAL; EVOLUTION, MOLECULAR; FUSARIUM; GENOME SIZE; GENOME, FUNGAL; GENOME, MITOCHONDRIAL; PHYLOGENY; RECOMBINATION, GENETIC; SYNTENY;

EID: 84883508849     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-605     Document Type: Article

References (79)

1. Gray MW, Burger G, Lang BF. Mitochondrial evolution. Science 1999, 283:1476-1481.
2. Lang FB, Gray MW, Burger B. Mitochondrial genome evolution and the origin of Eukaryotes. Annu Rev Genet 1999, 33:351-397.
3. Bullerwell CE, Lang BF. Fungal evolution: the case of the vanishing mitochondrion. Curr Opin Microbiol 2005, 8(4):362-369.
4. Gray MW, Burger G, Lang BF. The origin and early evolution of mitochondria. Genome Biol 2001, 2:10181-10185.
5. Adams KL, Palmer JD. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 2003, 29:380-395.
6. Burger G, Gray MW, Franz Lang B. Mitochondrial genomes: anything goes. Trends Genet 2003, 19(12):709-716.
7. Taylor JW. Fungal evolutionary biology and mitochondrial DNA. Exp Mycol 1986, 10(4):259-269.
8. Cahan P, Kennell JC. Identification and distribution of sequences having similarity to mitochondrial plasmids in mitochondrial genomes of filamentous fungi. Mol Genet Genomics 2005, 273:462-473.
9. Stoddard BL. Homing endonuclease structure and function. Q Rev Biophys 2006, 38:49-95.
10. Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe H, Lang BF. Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol Biol 2009, 9:272.
11. Avila-Adame C, Gomez-Alpizar L, Zismann V, Jones KM, Buell CR, Ristaino JB. Mitochondrial genome sequences and molecular evolution of the Irish potato famine pathogen, Phytophthora infestans. Curr Genet 2006, 49:39-46.
12. Haridas S, Gantt S. The mitochondrial genome of the wood degrading Basidiomycete Trametes cingulata. FEMS Microbiol Lett 2010, 308:29-34.
13. Stone CL, Buitrago MLP, Boore JL, Frederick RD. Analysis of the complete mitochondrial genome sequences of the soybean rust pathogens Phakopsora pachyrhizi and P. meibomiae. Mycologia 2010, 102(4):887-897.
14. Formighieri EF, Tiburcio RA, Armas ED, Medrano FJ, Shimo H, Carels N, Góes-Neto A, Cotomacci C, Carazzolle MF, Sardinha-Pinto N, et al. The mitochondrial genome of the phytopathogenic basidiomycete Moniliophthora perniciosa is 109 kb in size and contains a stable integrated plasmid. Mycol Res 2008, 112(10):1136-1152.
15. Bullerwell CE, Leigh J, Forget L, Lang BF. A comparison of three fission yeast mitochondrial genomes. Nucleic Acids Res 2003, 31:759-768.
16. 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 2007, 45:628-637.
17. Juhasz A, Pfeiffer I, Keszthelyi A, Kucsera J, Vagvolgyi G, 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.
18. Pantou M, Kouvelis V, Typas M. 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.
19. Pantou MP, Kouvelis VN, Typas MA. The complete mitochondrial genome of Fusarium oxysporum: insights into fungal mitochondrial evolution. Gene 2008, 419:7-15.
20. Ghikas D, Kouvelis V, Typas M. 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.
21. Kouvelis VN, Ghikas DV, Typas MA. 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 2004, 41(10):930-940.
22. Al-Reedy RM RM, Dillman CB, Kennell JC. 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.
23. Kvas M, Marasas WFO, Wingfield BD, Wingfield MJ, Steenkamp ET. Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex. Fungal Divers 2009, 34:1-21.
24. Leslie JF, Summerell BA. The Fusarium laboratory manual 2006, Hoboken, NJ: Blackwell Publishing-Wiley.
25. O'Donnell K, Cigelnik E, Nirenberg HI. Molecular systematic and phylogeography of the Gibberella fujikuroi species complex. Mycologia 1998, 90:465-493.
26. O'Donnell K, Nirenberg H, Aoki T, Cigelnik E. A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additional phylogenetically distinct species. Mycoscience 2000, 41(1):61-78.
27. Steenkamp ET, Coutinho TA, Desjardins AE, Wingfield BD, Marasas WFO, Wingfield MJ. Gibberella fujikuroi mating population E is associated with maize and teosinte. Mol Plant Pathol 2001, 2:215-221.
28. Jacobs A, Van Wyk PS, Marasas WFO, Wingfield BD, Wingfield MJ, Coutinho TA. Fusarium ananatum sp. nov. in the Gibberella fujikuroi species complex from pineapples with fruit rot in South Africa. Fungal Biol 2010, 114:515-527.
29. Geiser DM, Lewis Ivey ML, Hakiza G, Juba JH, Miller SA. Gibberella xylarioides (anamorph: Fusarium xylarioides), a causative agent of coffee wilt disease in Africa, is a previously unrecognized member of the G. fujikuroi species complex. Mycologia 2005, 97(1):191-201.
30. Lima CS, Pfenning LH, Costa SS, Campos MA, Leslie JF. A new Fusarium lineage within the Gibberella fujikuroi species complex is the main causal agent of mango malformation disease in Brazil. Plant Pathol 2009, 58:33-42.
31. Maddison WP. Gene trees in species trees. Syst Biol 1997, 46:523-536.
32. Rosenberg NA. The probability of topological concordance of gene trees and species trees. Theor Popul Biol 2002, 61:225-247.
33. Degnan JH, Rosenberg NA. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 2009, 24(6):332-340.
34. Nichols R. Gene trees and species trees are not the same. Trends Ecol Evol 2001, 16(7):358-364.
35. Rokas A, Williams BL, King N, Carroll SB. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 2003, 425:798-804.
36. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbert DS, Fisher MC. Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 2000, 31:21-31.
37. Geiser DM, Jimenez-Gasco MM, Kang S, Makalowski I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O' Donnell K. FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. Eur J Plant Pathol 2004, 110:473-479.
38. Wingfield MJ, Hammerbacher A, Ganley RJ, Steenkamp ET, Gordon TR, Wingfield BD, Coutinho TA. Pitch canker caused by Fusarium circinatum - a growing threat to pine plantations and forests worldwide. Australas Plant Pathol 2008, 37:319-334.
39. Sun S-K, Snyder WC. The bakane disease of the rice plant. Fusarium: Diseases, biology and taxonomy 1918, 104-113. University Park: Pennsylvania State University Press, Nelson PE, Toussoun TA, Cook RJ.
40. Kommedahl T, Windels CE. Root-, stalk-, and ear-infecting Fusarium species on corn in the USA. Fusarium: Diseases, Biology and Taxonomy 1981, 94-103. University Park: The Pennsylvania State University Press, Nelson PE, Toussoun TA, Cook RJ.
41. Cunnington JH. Organization of the mitochondrial genome of Fusarium oxysporum (anamorphic Hypocreales). Mycoscience 2007, 48(6):403-406.
42. O'Donnell K, Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 1997, 7(1):103-116.
43. Ballard JWO, Whitlock MC. The incomplete natural history of mitochondria. Mol Ecol 2004, 13(4):729-744.
44. Barr CM, Neiman M, Taylor DR. Inheritance and recombination of mitochondrial genomes in Plants, Fungi and Animals. New Phytol 2005, 168:39-50.
45. Sekito T, Okamoto K, Kitano H, Yoshida K. The complete mitochondrial DNA sequence of Hansenula wingei reveals new characteristics of yeast mitochondria. Curr Genet 1995, 28:39-53.
46. Dalgaard JZ, Klar AJ, Moser MJ, Holley WR, Chatterjee A, Saira Mian I. Statistical modeling and analysis of the LAGLIDADG family of site-specific endonucleases and identification of an intein that encodes a site-specific endonuclease of the HNH family. Nucleic Acids Res 1997, 25(22):4626-4638.
47. Swofford DL. PAUP. Phylogenetic analysis using parsimony, Version 4.0b10 1998, Sunderland, Massachcetts, USA: Sinauer Associated Inc.
48. Gaillardin C, Neuveglise C, Kerscher S, Nicaud J-M. Mitochondrial genomes of yeasts of the Yarrowia clade. FEMS Yeast Res 2012, 12:317-331.
49. Aguileta G, Hood ME, Refrégier G, Giraud T, Jean-Claude K, Michel D. Chapter 3 Genome evolution in plant pathogenic and symbiotic Fungi. Adv Bot Res 2009, 49:151-193. Academic Press.
50. Rosewich UL, Kistler HC. Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 2000, 38:325-363.
51. Garcia-Vallvé S, Romeu A, Palau J. Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res 2012, doi:10.1101/gr.130000.
52. Mullineux S-T, Willows K, Hausner G. Evolutionary dynamics of the mS952 Intron: a novel mitochondrial group II Intron encoding a LAGLIDADG homing endonuclease gene. J Mol Evol 2011, 72:433-449.
53. Mavridou A, Cannone J, Typas MA. Identification of Group-I Introns at three different positions within the 28S rDNA gene of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae. Fungal Genet Biol 2000, 31(2):79-90.
54. Paquin B, Laforest M-J, Forget L, Roewer I, Wang Z, Longcore J, Lang BF. The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr Genet 1997, 31:380-395.
55. Férandon C, Moukha S, Callac P, Benedetto J-P, Castroviejo M, Barroso G. The Agaricus bisporus cox1 gene: the longest mitochondrial gene and the largest reservoir of mitochondrial Group I Introns. PLOS One 2010, 5:e14048.
56. Yin L-F, Hu M-J, Wang F, Kuang H, Zhang Y, Schnabel G, Li G-Q, Luo C-X. Frequent gain and loss of introns in fungal cytochrome b Genes. PLOS One 2012, 7:e49096.
57. Jeffares DC, Mourier T, Penny D. The biology of intron gain and loss. Trends Genet 2006, 22:16-22.
58. Saldana R, Belfort GMM, Lambowitz AM. Group I and II introns. FASEB 1993, 7:15-24.
59. 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.
60. Edgell DR, Chalamcharla VR, Belfort M. Learning to live together: mutualism between self-splicing introns and their hosts. BMC Biol 2011, 9:22.
61. Goddard MR, Burt A. Recurrent invasion and extinction of a selfish gene. PNAS 1999, 96:13880-13885.
62. Burt A, Koufopanou V. Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr Opin Genet Dev 2004, 14(6):609-615.
63. Hurst GDD, Jiggins FM. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. PR Soc B 2005, 272:1525-1534.
64. Griffiths AJF. Mitochondrial inheritance in filamentous fungi. J Genet 1996, 75:403-414.
65. Wingfield BD, Steenkamp ET, Santana Q, Coetzee MPA, Bam S, Barnes I, Beukes CW, Chan A, de Vos L, Fourie G, et al. First fungal genome sequence from Africa: a preliminary analysis. S Afr J Sci 2012, 108:1-2.
66. Wiemann P, Sieber CMK, von Bargen KW, Studt L, Niehaus E-M, Espino JJ, Huß K, Michielse CB, Albermann S, Wagner D, et al. Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog 2013, 9(6):e1003475.
67. Fox TD. Natural variation in the genetic code. Annu Rev Genet 1987, 21:67-91.
68. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25(5):955-964.
69. Lang FB, Laforest M-J, Burger G. Mitochondrial introns: a critical view. Trends Genet 2007, 23:119-125.
70. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. TIG 2000, 16:226-227.
71. Guidon S, Gascuel O. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
72. Kazutaka K, Kazuharu M, Kei-ichi K, Takashi M. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30(14):3059-3066.
73. Katoh K, Kuma K-I, Toh H, Miyata T. MAFFT Version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005, 33(2):511-518.
74. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
75. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
76. Chambergo FS, Bonaccorsi ED, Ferreira AJS, Ramos ASP, Ferreira JR, Chambergo FS, Bonaccorsi ED, Ferreira AJS, Ramos ASP, Ferreira JR, Junior JR Abrahao-Neto J, Farah JPS, 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(16):13983-13988.
77. Tavare S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci 1986, 17:57-86.
78. Adachi J, Hasegawa M. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol 1996, 42:459-468.
79. Kimura M. Estamation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci U S A 1981, 78:454-458.