BMC Genomics | |
Characterization and potential evolutionary impact of transposable elements in the genome of Cochliobolus heterostrophus | |
Marisa V Queiroz4  B Gillian Turgeon1  Bradford J Condon1  Elza F Araújo4  Eduardo SG Mizubuti2  José CF Silva3  Mateus F Santana4  | |
[1] Present address: Department of Plant Pathology & Plant-Microbe Biology, Cornell University, Ithaca, USA;Present address: Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Brazil;Present address: Instituto Nacional de Ciência e Tecnologia em Interações Planta-Praga, Universidade Federal de Viçosa, Viçosa, Brazil;Present address: Laboratório de Genética Molecular e de Micro-organismo, Universidade Federal de Viçosa, Viçosa, Brazil | |
关键词: Genome; Repeat-induced point mutation; Cochliobolus heterostrophus; Transposable elements; | |
Others : 1216545 DOI : 10.1186/1471-2164-15-536 |
|
received in 2014-03-13, accepted in 2014-06-17, 发布年份 2014 | |
【 摘 要 】
Background
Cochliobolus heterostrophus is a dothideomycete that causes Southern Corn Leaf Blight disease. There are two races, race O and race T that differ by the absence (race O) and presence (race T) of ~ 1.2-Mb of DNA encoding genes responsible for the production of T-toxin, which makes race T much more virulent than race O. The presence of repetitive elements in fungal genomes is considered to be an important source of genetic variability between different species.
Results
A detailed analysis of class I and II TEs identified in the near complete genome sequence of race O was performed. In total in race O, 12 new families of transposons were identified. In silico evidence of recent activity was found for many of the transposons and analyses of expressed sequence tags (ESTs) demonstrated that these elements were actively transcribed. Various potentially active TEs were found near coding regions and may modify the expression and structure of these genes by acting as ectopic recombination sites. Transposons were found on scaffolds carrying polyketide synthase encoding genes, responsible for production of T-toxin in race T. Strong evidence of ectopic recombination was found, demonstrating that TEs can play an important role in the modulation of genome architecture of this species. The Repeat Induced Point mutation (RIP) silencing mechanism was shown to have high specificity in C. heterostrophus, acting only on transposons near coding regions.
Conclusions
New families of transposons were identified. In C. heterostrophus, the RIP silencing mechanism is efficient and selective. The co-localization of effector genes and TEs, therefore, exposes those genes to high rates of point mutations. This may accelerate the rate of evolution of these genes, providing a potential advantage for the host. Additionally, it was shown that ectopic recombination promoted by TEs appears to be the major event in the genome reorganization of this species and that a large number of elements are still potentially active. So, this study provides information about the potential impact of TEs on the evolution of C. heterostrophus.
【 授权许可】
2014 Santana et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150701043315216.pdf | 2035KB | download | |
Figure 3. | 278KB | Image | download |
Figure 2. | 16KB | Image | download |
Figure 1. | 37KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
【 参考文献 】
- [1]Hooker AL: Cytoplasmic susceptibility in plant disease. Ann Rev Phytopathol 1974, 12:167-179.
- [2]Drechsler C: Leafspot of maize caused by Ophiobolus heterostrophus n. sp., the ascigerous stage of a Helminthosporium exhibiting bipolar germination. J Agric Res 1925, 31:701-726.
- [3]Drechsler C: Phytopathological and taxonomic aspects of Ophiobolus, Pyrenophora, Helminthosporium, and a new genus Cochliobolus. Phytopathology 1934, 24:953-984.
- [4]Zwonitzer JC, Bubeck DM, Bhattranakki D, Goodman MM, Arellano C, Balint-Kurti PJ: Use of selection with recurrent backcrossing and QTL mapping to identify loci contributing to southern leaf blight resistance in a highly resistant maize line. Theor Appl Genet 2009, 118:911-925.
- [5]Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kostil I, LaButti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GH, Lawrence C, Scott JA, Apatafora JW, Turgeon BG, de Wit PJ, Zhong S, Goodwin SB, Grigoriev IV: Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen dothideomycetes fungi. PLoS Pathog 2012, 8:e1003037.
- [6]Bronson CR, Taga M, Yoder OC: Genetic control and distorted segregation of the T-toxin production in field isolates of Cochliobolus heterostrophus. Phytopathology 1990, 80:819-823.
- [7]Turgeon BG, Baker SE: Genetic and genomic dissection of the Cochliobolus heterostrophus Tox1 locus controlling biosynthesis of the polyketide virulence factor T-toxin. Adv Genet 2007, 57:219-260.
- [8]Tzeng TH, Lyngholm LK, Ford CF, Bronson CR: A restriction fragment length polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 1992, 130:81-86.
- [9]Yang G, Rose MS, Turgeon BG, Yoder OC: A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Plant Cell 1996, 8:2139-2150.
- [10]Kodama M, Rose MS, Yang SH, Yoder OC, Turgeon BG: The translocation-associated Tox1 locus of Cochliobolus heterostrophus is two genetic elements on two different chromosomes. Genetics 1999, 151:585-596.
- [11]Baker SE, Kroken S, Inderbitzin P, Asvarak T, Li BY, Shi L, Yoder OC, Turgeon BG: Two polyketide synthase-encoding genes are required for biosynthesis of the polyketide virulence factor, T-toxin, by Cochliobolus heterostrophus. Mol Plant Microbe Interact 2006, 19:139-149.
- [12]Inderbitzin P, Asvarak T, Turgeon BG: Six new genes required for production of T-toxin, a polyketide determinant of high virulence of Cochliobolus heterostrophus to maize. Mol Plant Microbe Interact 2010, 23:458-472.
- [13]Rose MS, Yun SH, Asvarak T, Lu SW, Yoder OC, Turgeon BG: A decarboxylase encoded at the Cochliobolus heterostrophus translocation-associated Tox1B locus is required for polyketide (T-toxin) biosynthesis and high virulence on T-cytoplasm Maize. Mol Plant Microbe Interact 2002, 15:883-893.
- [14]Condon BJ: Genomic and molecular genetic analyses of secondary metabolism, toxin production, and iron homeostasis in Cochliobolus heterostrophus. Cornell University: Department of Plant Pathology & Plant-Microbe Biology; 2013. [PhD thesis]
- [15]Khang CH, Park S-Y, Lee Y-H, Valent B, Kang S: Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Mol Plant Microbe Interact 2008, 21:658-670.
- [16]Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshulk C, Xie X, Hu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, et al.: Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium oxysporum. Nature 2010, 464:367-373.
- [17]Wicker T, Sabot F, Huan-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH: A unified classification system for eukaryotic transposable elements. Nat Rev Genet 2007, 8:973-982.
- [18]Novikova O, Fet V, Blinov A: Non-LTR retrotransposons in fungi. Funct Integr Genomics 2009, 9:27-42.
- [19]Muszewska A, Hoffman-Sommer M, Grynberg M: LTR retrotransposons in fungi. PLoS One 2011, 6:e29425.
- [20]Havecker ER, Gao X, Voytas DF: The diversity of LTR retrotransposons. Genome Biol 2004, 5:225.
- [21]Neumann P, Pazarkova D, Macas J: Highly abundant pea LTR retrotransposon ogre is constitutively transcribed and partially spliced. Plant Mol Biol 2003, 3:399-410.
- [22]Kalendar R, Flavell AJ, Ellis TH, Sjakste T, Moisy C, Schulman AH: Analysis of plant diversity with retrotransposon-based molecular markers. Heredity 2011, 106:520-530.
- [23]Hua-Van A, Rouzic AL, Boutin TS, Filée J, Capy P: The struggle for life of the genome’s selfish architects. Biol Direct 2011, 6:19.
- [24]Selker EU: Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 1990, 24:579-613.
- [25]Freitag M, Williams RL, Kothe GO, Selker EU: A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Natl Acad Sci U S A 2002, 99:8802-8807.
- [26]Clutterbuck AJ: Genomic evidence of the repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 2011, 48:306-326.
- [27]Amyotte SG, Tan X, Pennerman K, Jimenez-Casco Mdel M, Klosterman SJ, Ma LJ, Dobinson KF, Veronese P: Transposable elements in phytopathogenic Verticillium spp: insights into genome evolution and inter- and intra-specific diversification. BMC Genomics 2012, 13:314.
- [28]Shapiro JA: Mobile DNA and evolution in the 21th century. Mob DNA 2010, 1:1-14.
- [29]Condon BJ, Leng Y, Wu D, Bushley KE, Ohm RA, Otillar R, Martin J, Schackwitz W, Grimwood J, MohdZainudin N, Xue C, Wang R, Manning VA, Dhillon B, Tu ZJ, Steffenson BJ, Salamov A, Sun H, Lowry S, LaButti K, Han J, Copeland A, Lindquist E, Barry K, Schmutz J, Baker SE, Ciuffetti LM, Grigoriev IV, Zhong S, Turgeon BG: Comparative genome structure, secondary metabolite, and effector coding capacity across Cochliobolus pathogens. PLoS Genet 2013, 9:e1003233.
- [30]Manning VA, Pandelova I, Dhillon B, Wilhelm LJ, Goodwim SB, Berlin AM, Figueroa M, Freitag M, Hane JK, Henrissat B, Holman WH, Kodira CD, Martin J, Oliver RP, Robbertse B, Schackwitz W, Schwartz DC, Spatafora JW, Turgeon BG, Yandava C, Young S, Zhou S, Zeng Q, Grigoriev IV, Ma LJ, Ciuffetti LM: Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence. Genes Genomes Genet 2013, 3:41-63.
- [31]Kamper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O, Perlin MH, Wösten HA, de Vries R, Ruiz-Herrera J, Reynaga-Peña CG, Snetselaar K, McCann M, Pérez-Martín J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, González-Prieto JM, Kennel JC, Molina L, et al.: Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006, 444:97-101.
- [32]Parlange F, Oberhaensli S, Breen J, Platzer M, Taudien S, Simková H, Wicker T, Dolezel J, Keller B: A major invasion of transposable elements accounts for the large size of the Blumeria graminis f.sp. tritici genome. Funct Integr Genomic 2011, 11:671-677.
- [33]Daboussi MJ, Capy P: Transposable elements in filamentous fungi. Annu Rev Microbiol 2003, 57:275-299.
- [34]Han JS: Non-long terminal repeat (non-LTR) retrotransposons: mechanisms, recent developments, and unanswered question. Mob DNA 2010, 1:15.
- [35]Novikova OS, Fet V, Vlinov AG: Homology-dependent inactivation of LTR retrotransposons in Aspergillus fumigatus and A. nidulans genome. Mol Biol 2007, 41:886-893.
- [36]Hua-Van A, Rouzic AL, Maisonhaute C, Capy P: Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences. Cytogenet Genome Res 2005, 110:426-440.
- [37]Rouzic AL, Capy P: The first steps of transposable elements invasion: parasitic strategy vs genetic drift. Genet 2005, 169:1033-1043.
- [38]Johnson LJ: The genome strikes back: the evolutionary importance of defense against mobile elements. Evol Biol 2007, 34:121-129.
- [39]Rice PA, Baker TA: Comparative architecture of transposase and integrase complexes. Nat Struct Biol 2001, 8:302-307.
- [40]Nesmelova IV, Hackett PB: DDE transposases: structural similarity and diversity. Adv Drug Delivery Rev 2010, 62:1187-1195.
- [41]Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, Difazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, et al.: The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008, 452:88-92.
- [42]Ogasawara H, Obata H, Hata Y, Takahashi S, Gomi K: Crawler, a novel Tc1/mariner-type transposable element in Aspergillus oryzae transposes under stress conditions. Fungal Genet Biol 2009, 46:441-449.
- [43]Bouvet GF, Jacobi V, Plourde KV, Bernier L: Stress-induced mobility of OPHIO1 and OPHIO2, DNA transposons of the Dutch elm disease fungi. Fungal Genet Biol 2008, 45:565-578.
- [44]Bowen NJ, Jordan LK: Transposable elements and the evolution of eukaryotic complexity. Mol Biol 2002, 4:65-76.
- [45]Rouzic AL, Boutin TS, Capy P: Long-term evolution of transposable elements. Evolution 2007, 104:9375-19380.
- [46]Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, et al.: The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
- [47]Hane JK, Lowe RG, Solomon PS, Tan KC, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, Torriani SF, McDonald BA, Oliver RP: Dothideomycete–plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 2007, 19:3347-3368.
- [48]Braumann I, Berg M, Kempken F: Repeat induced point mutation in two asexual fungi, Aspegillus niger and Penicillium chrysogenum. Curr Genet 2008, 53:287-297.
- [49]Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O’Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, et al.: Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet 2013, 9:e1003323.
- [50]Santana MF, Silva JCF, Batista AD, Ribeiro LE, Silva GF, Araújo EF, Queiroz MV: Abundance, distribution and potential impact of transposable elements in the genome of Mycosphaerella fijiensis. BMC Genomics 2012, 13:720.
- [51]Reimann S, Deising HB: Inhibition of efflux transporter-mediated fungicide resistance in Pyrenophora tritici-repentis by a derivative of 4’-hydroxyflavone and enhancement of fungicide activity. Appl Environ Microbiol 2005, 71:3269-3275.
- [52]Waard MA, Andrade AC, Hayashi K, Schoonbeek HJ, Stergiopoulos I, Zwiers LH: Impact of fungal drug transporter on fungicide sensitivity, multidrug resistance and virulence. Pest Manag Sci 2006, 62:195-207.
- [53]Panaccione DG, Pitkin JW, Walton JD, Annis SL: Transposon-like sequences at the TOX2 locus of the plant pathogenic fungus Cochliobolus carbonum. Gene 1996, 176:103-109.
- [54]Shaaban M, Palmer JM, El-Naggar WA, El-Sokkary MA, el SE H, Keller NP: Involvement of transposon-like elements in penicillin gene cluster regulation. Fungal Genet Biol 2010, 47:423-432.
- [55]Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J: Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110:462-467.
- [56]Xu Z, Wang H: LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 2007, 35:265-268.
- [57]Altschul SF, Madden TL, Schäffer AA, Zhang J, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
- [58]Kapitonov VV, Jurka J: A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 2008, 9:411-412.
- [59]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
- [60]Hane JK, Oliver RP: RIPCAl: a tool for alignment-based analyses of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics 2008, 9:478.
- [61]Martin D, Rybicki EP: RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000, 16:562-563.
- [62]Padidam M, Sawyer S, Fauquet CM: Possible emergence of new geminiviruses by frequent recombination. Virology 1999, 265:218-224.
- [63]Martin DP, Posada D, Crandall KA, Willianmson C: A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 2005, 21:98-102.
- [64]Smith JM: Analyzing the mosaic structure of genes. J Mol Evol 1992, 34:126-129.
- [65]Posada D, Crandall KA: Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 2001, 98:13757-13762.
- [66]Gibbs MJ, Armstrong JS, Gibbs AJ: Sister-scanning: a Monte Carlo procedure for assessing signal in recombination sequences. Bioinformatics 2000, 16:573-582.
- [67]Boni MF, Posada D, Feldman MW: An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007, 176:1035-1047.
- [68]Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P: RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010, 26:2462-2463.