Genome-wide analysis of intraspecific transposon diversity in yeast

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Bleykasten Grosshans, Claudine ^a   Friedrich, Anne ^a   Schacherer, Joseph ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Genome evolution; Intra specific diversity; Retrotransposons; Saccharomyces cerevisiae; Transposons; Ty elements; Ty1

Indexed keywords

DNA; RETROPOSON; TRANSPOSON;

ARTICLE; DNA POLYMORPHISM; FUNGAL STRAIN; FUNGUS ISOLATION; GENE EXPRESSION; GENE INSERTION SEQUENCE; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC CODE; GENOMICS; INTRASPECIFIC VARIATION; LONG TERMINAL REPEAT; NONHUMAN; SACCHAROMYCES CEREVISIAE; SPECIES DISTRIBUTION; TRANSPOSON; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETICS; MOLECULAR EVOLUTION; RETROPOSON; SPECIES DIFFERENCE;

SACCHAROMYCES CEREVISIAE;

DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENES, FUNGAL; MUTAGENESIS, INSERTIONAL; POLYMORPHISM, GENETIC; RETROELEMENTS; SACCHAROMYCES CEREVISIAE; SPECIES SPECIFICITY; TERMINAL REPEAT SEQUENCES;

EID: 84878894818     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-399     Document Type: Article

References (65)

1. Beauregard A, Curcio MJ, Belfort M. The take and give between retrotransposable elements and their hosts. Annu Rev Genet 2008, 42:587-617. 10.1146/annurev.genet.42.110807.091549, 2665727, 18680436.
2. Gresham D, Usaite R, Germann SM, Lisby M, Botstein D, Regenberg B. Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. Proc Natl Acad Sci USA 2010, 107(43):18551-18556. 10.1073/pnas.1014023107, 2972935, 20937885.
3. Lisch D. How important are transposons for plant evolution?. Nat Rev Genet 2013, 14(1):49-61.
4. Wang X, Weigel D, Smith LM. Transposon variants and their effects on gene expression in Arabidopsis. PLoS Genet 2013, 9(2):e1003255. 10.1371/journal.pgen.1003255, 3567156, 23408902.
5. Chenais B, Caruso A, Hiard S, Casse N. The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene 2012, 509(1):7-15. 10.1016/j.gene.2012.07.042, 22921893.
6. Le Rouzic A, Capy P. Population genetics models of competition between transposable element subfamilies. Genetics 2006, 174(2):785-793. 10.1534/genetics.105.052241, 1602078, 16888345.
7. Pritham EJ. Transposable elements and factors influencing their success in eukaryotes. J Hered 2009, 100(5):648-655. 10.1093/jhered/esp065, 2877548, 19666747.
8. Vieira C, Fablet M, Lerat E, Boulesteix M, Rebollo R, Burlet N, Akkouche A, Hubert B, Mortada H, Biemont C. A comparative analysis of the amounts and dynamics of transposable elements in natural populations of Drosophila melanogaster and Drosophila simulans. J Environ Radioact 2012, 113:83-86.
9. Grzebelus D. Transposon insertion polymorphism as a new source of molecular markers. J Fruit Ornam Plant Res 2006, 14(14):21-19.
10. Huang CR, Schneider AM, Lu Y, Niranjan T, Shen P, Robinson MA, Steranka JP, Valle D, Civin CI, Wang T, et al. Mobile interspersed repeats are major structural variants in the human genome. Cell 2010, 141(7):1171-1182. 10.1016/j.cell.2010.05.026, 2943426, 20602999.
11. Guerreiro MP, Fontdevila A. Osvaldo and Isis retrotransposons as markers of the Drosophila buzzatii colonisation in Australia. BMC Evol Biol 2011, 11:111. 10.1186/1471-2148-11-111, 3098803, 21513573.
12. Zampicinini G, Cervella P, Biemont C, Sella G. Insertional variability of four transposable elements and population structure of the midge Chironomus riparius (Diptera). Mol Genet Genomics 2011, 286(3-4):293-305.
13. Zerjal T, Rousselet A, Mhiri C, Combes V, Madur D, Grandbastien MA, Charcosset A, Tenaillon MI. Maize genetic diversity and association mapping using transposable element insertion polymorphisms. Theor Appl Genet 2012, 124(8):1521-1537. 10.1007/s00122-012-1807-9, 22350086.
14. McLain AT, Meyer TJ, Faulk C, Herke SW, Oldenburg JM, Bourgeois MG, Abshire CF, Roos C, Batzer MA. An alu-based phylogeny of lemurs (infraorder: Lemuriformes). PLoS One 2012, 7(8):e44035. 10.1371/journal.pone.0044035, 3429421, 22937148.
15. Ray DA, Batzer MA. Reading TE leaves: new approaches to the identification of transposable element insertions. Genome Res 2011, 21(6):813-820. 10.1101/gr.110528.110, 3106314, 21632748.
16. Huang X, Lu G, Zhao Q, Liu X, Han B. Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice. Plant Physiol 2008, 148(1):25-40. 10.1104/pp.108.121491, 2528094, 18650402.
17. Cordaux R, Sen SK, Konkel MK, Batzer MA. Computational methods for the analysis of primate mobile elements. Methods Mol Biol 2010, 628:137-151. 2880165, 20238080.
18. Sabot F, Picault N, El-Baidouri M, Llauro C, Chaparro C, Piegu B, Roulin A, Guiderdoni E, Delabastide M, McCombie R, et al. Transpositional landscape of the rice genome revealed by paired-end mapping of high-throughput re-sequencing data. Plant J 2011, 66(2):241-246. 10.1111/j.1365-313X.2011.04492.x, 21219509.
19. Dujon B. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet 2006, 22(7):375-387. 10.1016/j.tig.2006.05.007, 16730849.
20. Bleykasten-Grosshans C, Neuveglise C. Transposable elements in yeasts. C R Biol 2011, 334(8-9):679-686.
21. Legras JL, Karst F. Optimisation of interdelta analysis for Saccharomyces cerevisiae strain characterisation. FEMS Microbiol Lett 2003, 221(2):249-255. 10.1016/S0378-1097(03)00205-2, 12725935.
22. Liti G, Peruffo A, James SA, Roberts IN, Louis EJ. Inferences of evolutionary relationships from a population survey of LTR-retrotransposons and telomeric-associated sequences in the Saccharomyces sensu stricto complex. Yeast 2005, 22(3):177-192. 10.1002/yea.1200, 15704235.
23. Dunn B, Sherlock G. Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res 2008, 18(10):1610-1623. 10.1101/gr.076075.108, 2556262, 18787083.
24. Dunn B, Richter C, Kvitek DJ, Pugh T, Sherlock G. Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res 2012, 22(5):908-924. 10.1101/gr.130310.111, 3337436, 22369888.
25. Neuveglise C, Feldmann H, Bon E, Gaillardin C, Casaregola S. Genomic evolution of the long terminal repeat retrotransposons in hemiascomycetous yeasts. Genome Res 2002, 12(6):930-943. 10.1101/gr.219202, 1383729, 12045146.
26. Carr M, Bensasson D, Bergman CM. Evolutionary genomics of transposable elements in Saccharomyces cerevisiae. PLoS One 2012, 7(11):e50978. 10.1371/journal.pone.0050978, 3511429, 23226439.
27. Lesage P, Todeschini AL. Happy together: the life and times of Ty retrotransposons and their hosts. Cytogenet Genome Res 2005, 110(1-4):70-90.
28. Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 1998, 8(5):464-478.
29. Wilke CM, Adams J. Fitness effects of Ty transposition in Saccharomyces cerevisiae. Genetics 1992, 131(1):31-42. 1204961, 1317316.
30. Winzeler EA, Castillo-Davis CI, Oshiro G, Liang D, Richards DR, Zhou Y, Hartl DL. Genetic diversity in yeast assessed with whole-genome oligonucleotide arrays. Genetics 2003, 163(1):79-89. 1462430, 12586698.
31. Gabriel A, Dapprich J, Kunkel M, Gresham D, Pratt SC, Dunham MJ. Global mapping of transposon location. PLoS Genet 2006, 2(12):e212. 10.1371/journal.pgen.0020212, 1698948, 17173485.
32. Wheelan SJ, Scheifele LZ, Martinez-Murillo F, Irizarry RA, Boeke JD. Transposon insertion site profiling chip (TIP-chip). Proc Natl Acad Sci USA 2006, 103(47):17632-17637. 10.1073/pnas.0605450103, 1693798, 17101968.
33. Wei W, McCusker JH, Hyman RW, Jones T, Ning Y, Cao Z, Gu Z, Bruno D, Miranda M, Nguyen M, et al. Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc Natl Acad Sci USA 2007, 104(31):12825-12830. 10.1073/pnas.0701291104, 1933262, 17652520.
34. Borneman AR, Forgan AH, Pretorius IS, Chambers PJ. Comparative genome analysis of a Saccharomyces cerevisiae wine strain. FEMS Yeast Res 2008, 8(7):1185-1195. 10.1111/j.1567-1364.2008.00434.x, 18778279.
35. Novo M, Bigey F, Beyne E, Galeote V, Gavory F, Mallet S, Cambon B, Legras JL, Wincker P, Casaregola S, et al. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci USA 2009, 106(38):16333-16338. 10.1073/pnas.0904673106, 2740733, 19805302.
36. Argueso JL, Carazzolle MF, Mieczkowski PA, Duarte FM, Netto OV, Missawa SK, Galzerani F, Costa GG, Vidal RO, Noronha MF, et al. Genome structure of a Saccharomyces cerevisiae strain widely used in bioethanol production. Genome Res 2009, 19(12):2258-2270. 10.1101/gr.091777.109, 2792172, 19812109.
37. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, et al. Population genomics of domestic and wild yeasts. Nature 2009, 458(7236):337-341. 10.1038/nature07743, 2659681, 19212322.
38. Akao T, Yashiro I, Hosoyama A, Kitagaki H, Horikawa H, Watanabe D, Akada R, Ando Y, Harashima S, Inoue T, et al. Whole-genome sequencing of sake yeast Saccharomyces cerevisiae Kyokai no. 7. DNA Res 2011, 18(6):423-434. 10.1093/dnares/dsr029, 3223075, 21900213.
39. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 2009, 458(7236):342-345. 10.1038/nature07670, 2782482, 19212320.
40. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ. Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 2011, 7(2):e1001287. 10.1371/journal.pgen.1001287, 3033381, 21304888.
41. Ruderfer DM, Pratt SC, Seidel HS, Kruglyak L. Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 2006, 38(9):1077-1081. 10.1038/ng1859, 16892060.
42. Dowell RD, Ryan O, Jansen A, Cheung D, Agarwala S, Danford T, Bernstein DA, Rolfe PA, Heisler LE, Chin B, et al. Genotype to phenotype: a complex problem. Science 2010, 328(5977):469. 10.1126/science.1189015, 20413493.
43. Nishant KT, Wei W, Mancera E, Argueso JL, Schlattl A, Delhomme N, Ma X, Bustamante CD, Korbel JO, Gu Z, et al. The baker's yeast diploid genome is remarkably stable in vegetative growth and meiosis. PLoS Genet 2010, 6(9):e1001109. 10.1371/journal.pgen.1001109, 2936533, 20838597.
44. Fablet M, McDonald JF, Biemont C, Vieira C. Ongoing loss of the tirant transposable element in natural populations of Drosophila simulans. Gene 2006, 375:54-62.
45. Granzotto A, Lopes FR, Lerat E, Vieira C, Carareto CM. The evolutionary dynamics of the Helena retrotransposon revealed by sequenced Drosophila genomes. BMC Evol Biol 2009, 9:174. 10.1186/1471-2148-9-174, 3087515, 19624823.
46. Naito K, Cho E, Yang G, Campbell MA, Yano K, Okumoto Y, Tanisaka T, Wessler SR. Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA 2006, 103(47):17620-17625. 10.1073/pnas.0605421103, 1693796, 17101970.
47. Ibeas JI, Jimenez J. Genomic complexity and chromosomal rearrangements in wine-laboratory yeast hybrids. Curr Genet 1996, 30(5):410-416. 10.1007/s002940050150, 8929393.
48. Dunn B, Levine RP, Sherlock G. Microarray karyotyping of commercial wine yeast strains reveals shared, as well as unique, genomic signatures. BMC Genomics 2005, 6(1):53. 10.1186/1471-2164-6-53, 1097725, 15833139.
49. Fritsch ES, Schacherer J, Bleykasten-Grosshans C, Souciet JL, Potier S, de Montigny J. Influence of genetic background on the occurrence of chromosomal rearrangements in Saccharomyces cerevisiae. BMC Genomics 2009, 10:99. 10.1186/1471-2164-10-99, 2674068, 19267901.
50. Hosid E, Brodsky L, Kalendar R, Raskina O, Belyayev A. Diversity of long terminal repeat retrotransposon genome distribution in natural populations of the wild diploid wheat Aegilops speltoides. Genetics 2012, 190(1):263-274. 10.1534/genetics.111.134643, 3249373, 22042572.
51. Hani J, Feldmann H. tRNA genes and retroelements in the yeast genome. Nucleic Acids Res 1998, 26(3):689-696. 10.1093/nar/26.3.689, 147333, 9443958.
52. Schacherer J, Ruderfer DM, Gresham D, Dolinski K, Botstein D, Kruglyak L. Genome-wide analysis of nucleotide-level variation in commonly used Saccharomyces cerevisiae strains. PLoS One 2007, 2(3):e322. 10.1371/journal.pone.0000322, 1829191, 17389913.
53. Morillon A, Benard L, Springer M, Lesage P. Differential effects of chromatin and Gcn4 on the 50-fold range of expression among individual yeast Ty1 retrotransposons. Mol Cell Biol 2002, 22(7):2078-2088. 10.1128/MCB.22.7.2078-2088.2002, 133697, 11884596.
54. Bleykasten-Grosshans C, Jung PP, Fritsch ES, Potier S, de Montigny J, Souciet JL. The Ty1 LTR-retrotransposon population in Saccharomyces cerevisiae genome: dynamics and sequence variations during mobility. FEMS Yeast Res 2011, 11(4):334-344. 10.1111/j.1567-1364.2011.00721.x, 21272231.
55. Baucom RS, Estill JC, Leebens-Mack J, Bennetzen JL. Natural selection on gene function drives the evolution of LTR retrotransposon families in the rice genome. Genome Res 2009, 19(2):243-254. 2652206, 19029538.
56. Jordan IK, McDonald JF. Evidence for the role of recombination in the regulatory evolution of Saccharomyces cerevisiae Ty elements. J Mol Evol 1998, 47(1):14-20. 10.1007/PL00006358, 9664692.
57. Du J, Tian Z, Bowen NJ, Schmutz J, Shoemaker RC, Ma J. Bifurcation and enhancement of autonomous-nonautonomous retrotransposon partnership through LTR Swapping in soybean. Plant Cell 2010, 22(1):48-61. 10.1105/tpc.109.068775, 2828711, 20081112.
58. Roeder GS, Rose AB, Pearlman RE. Transposable element sequences involved in the enhancement of yeast gene expression. Proc Natl Acad Sci USA 1985, 82(16):5428-5432. 10.1073/pnas.82.16.5428, 390582, 2991923.
59. Roelants F, Potier S, Souciet JL, de Montigny J. Delta sequence of Ty1 transposon can initiate transcription of the distal part of the URA2 gene complex in Saccharomyces cerevisiae. FEMS Microbiol Lett 1997, 148(1):69-74. 10.1111/j.1574-6968.1997.tb10269.x, 9066113.
60. Todeschini AL, Morillon A, Springer M, Lesage P. Severe adenine starvation activates Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol 2005, 25(17):7459-7472. 10.1128/MCB.25.17.7459-7472.2005, 1190277, 16107695.
61. Servant G, Pennetier C, Lesage P. Remodeling yeast gene transcription by activating the Ty1 long terminal repeat retrotransposon under severe adenine deficiency. Mol Cell Biol 2008, 28(17):5543-5554. 10.1128/MCB.00416-08, 2519716, 18591253.
62. Sabot F, Schulman AH. Parasitism and the retrotransposon life cycle in plants: a hitchhiker's guide to the genome. Heredity 2006, 97(6):381-388. 10.1038/sj.hdy.6800903, 16985508.
63. Altschul SF, Madden TL, Schaffer 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.
64. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948. 10.1093/bioinformatics/btm404, 17846036.
65. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27(2):221-224. 10.1093/molbev/msp259, 19854763.