Zisupton - A novel superfamily of DNA transposable elements recently active in fish

Molecular Biology and Evolution

Volumn 29, Issue 2, 2012, Pages 631-645

  Böhne, Astrid ^a   Zhou, Qingchun ^b   Darras, Amandine ^a   Schmidt, Cornelia ^b   Schartl, Manfred ^b   Galiana Arnoux, Delphine ^a   Volff, Jean Nicolas ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

HMGXB3; platyfish; sex chromosomes; SUMO; testis; transposon; Ulp1 protease

Indexed keywords

DNA; INTEGRASE; NUCLEIC ACID; NUCLEOTIDE; SUMO PROTEIN; TRANSPOSASE; UBIQUITIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZISUPTON;

ANIMAL TISSUE; ARTICLE; BASIDIOMYCETES; BROWN ALGA; CEPHALOCHORDATA; DNA POLYMORPHISM; EXON; FEMALE; FISH; GENE TRANSFER; GENOME; GREEN ALGA; HEMICHORDATA; MALE; NONHUMAN; PROTEIN BINDING; PROTEIN PROCESSING; TESTIS; TRANSPOSON; UROCHORDATA; Y CHROMOSOME;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; CYPRINODONTIFORMES; CYSTEINE ENDOPEPTIDASES; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME; MALE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PHYLOGENY; POLYMORPHISM, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SUMO-1 PROTEIN; TESTIS; TRANSPOSASES; Y CHROMOSOME;

CHLOROPHYTA; HEMICHORDATA; PHAEOPHYCEAE; POECILIIDAE; XIPHOPHORUS MACULATUS;

EID: 84855882097     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr208     Document Type: Article

References (91)

1. Aravind L, Koonin EV. 2000. SAP-a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci. 25:112-114. (Pubitemid 30122420)
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 2010. Current protocols in molecular biology. Hoboken (NJ): Wiley.
3. Banerjee R, Dubois DY, Gauthier J, Lin SX, Roy S, Lapointe J. 2004. The zinc-binding site of a class I aminoacyl-tRNA synthetase is a SWIM domain that modulates amino acid binding via the tRNA acceptor arm. Eur J Biochem. 271:724-733. (Pubitemid 38250915)
4. Bao W, Kapitonov VV, Jurka J. 2010. Ginger DNA transposons in eukaryotes and their evolutionary relationships with long terminal repeat retrotransposons. Mob DNA. 1:3.
5. Barrett AJ, Rawlings ND. 2001. Evolutionary lines of cysteine peptidases. Biol Chem. 382:727-733. (Pubitemid 32631709)
6. Bennetzen JL. 2000. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. 42:251-269. (Pubitemid 30096120)
7. Böhne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff JN. 2008. Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res. 16:203-215. (Pubitemid 351294779)
8. Böhne A, Schultheis C, Galiana-Arnoux D, et al. (20 co-authors). 2009. Molecular analysis of the sex chromosomes of the platyfish Xiphophorus maculatus: towards the identification of a new type of master sexual regulator in vertebrates. Integr Zool. 4:277-284.
9. Bourque G. 2009. Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr Opin Genet Dev. 19:607-612.
10. Brayer KJ, Segal DJ. 2008. Keep your fingers off my DNA: proteinprotein interactions mediated by C2H2 zinc finger domains. Cell Biochem Biophys. 50:111-131.
11. Brown RS. 2005. Zinc finger proteins: getting a grip on RNA. Curr Opin Struct Biol. 15:94-98. (Pubitemid 40249515)
12. Cai M, Qiu D, Yuan T, Ding X, Li H, Duan L, Xu C, Li X, Wang S. 2008. Identification of novel pathogen-responsive cis-elements and their binding proteins in the promoter of OsWRKY13, a gene regulating rice disease resistance. Plant Cell Environ. 31:86-96. (Pubitemid 350212612)
13. Capy P, Maisonhaute C. 2002. Acquisition/loss of modules: the construction set of transposable elements. Genetika. 38:594-601. (Pubitemid 135704880)
14. Craig KL, Tyers M. 1999. The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol. 72:299-328. (Pubitemid 29485173)
15. Cummings ME, Gelineau-Kattner R. 2009. The energetic costs of alternative male reproductive strategies in Xiphophorus nigrensis. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 195:935-946.
16. Drag M, Salvesen GS. 2008. DeSUMOylating enzymes-SENPs. IUBMB Life. 60:734-742.
17. Edgar RC. 2004a. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 5:113.
18. Edgar RC. 2004b. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. (Pubitemid 38832724)
19. Ezaz T, Stiglec R, Veyrunes F, Marshall Graves JA. 2006. Relationships between vertebrate ZW and XY sex chromosome systems. Curr Biol. 16:736-743.
20. Fernandez AA, Fernandez LR, Toth L. 2008. Head over heels: an examination of a possible mating signal in female swordtails, Xiphophorus cortezi. Anim Behav. 76:1073-1081.
21. Feschotte C, Pritham EJ. 2005. Non-mammalian c-integrases are encoded by giant transposable elements. Trends Genet. 21:551-552. (Pubitemid 41278459)
22. Fischer C, Bouneau L, Coutanceau JP, Weissenbach J, Ozouf-Costaz C, Volff JN. 2005. Diversity and clustered distribution of retrotransposable elements in the compact genome of the pufferfish Tetraodon nigroviridis. Cytogenet Genome Res. 110:522-536. (Pubitemid 41159929)
23. Froschauer A, Körting C, Katagiri T, Aoki T, Asakawa S, Shimizu N, Schartl M, Volff JN. 2002. Construction and initial analysis of bacterial artificial chromosome (BAC) contigs from the sexdetermining region of the platyfish Xiphophorus maculatus. Gene 295:247-254. (Pubitemid 35279257)
24. Fujino K, Matsuda Y, Sekiguchi J. 2009. Transcriptional activity of rice autonomous transposable element Dart. J Plant Physiol. 166:1537-1543.
25. Gordon M. 1927. The genetics of a viviparous top-minnow platypoecilus; the inheritance of two kinds of melanophores. Genetics 12:253-283.
26. Gray YH. 2000. It takes two transposons to tango: transposableelement- mediated chromosomal rearrangements. Trends Genet. 16:461-468.
27. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59:307-321.
28. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704. (Pubitemid 37365050)
29. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 41:95-98.
30. Haun WJ, Danilevskaya ON, Meeley RB, Springer NM. 2009. Disruption of imprinting by mutator transposon insertions in the 5' proximal regions of the Zea mays Mez1 locus. Genetics 181:1229-1237.
31. Hoen DR, Park KC, Elrouby N, Yu Z, Mohabir N, Cowan RK, Bureau TE. 2006. Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol Biol Evol. 23:1254-1268. (Pubitemid 43781599)
32. Hrbek T, Seckinger J, Meyer A. 2007. A phylogenetic and biogeographic perspective on the evolution of poeciliid fishes. Mol Phylogenet Evol. 43:986-998. (Pubitemid 46777372)
33. Iuchi S. 2001. Three classes of C2H2 zinc finger proteins. Cell Mol Life Sci. 58:625-635.
34. Jackson PK, Eldridge AG. 2002. The SCF ubiquitin ligase: an extended look. Mol Cell. 9:923-925. (Pubitemid 34626661)
35. Jentsch S, Seufert W, Hauser HP. 1991. Genetic analysis of the ubiquitin system. Biochim Biophys Acta. 1089:127-139.
36. Jurka J, Kapitonov VV, Kohany O, Jurka MV. 2007. Repetitive sequences in complex genomes: structure and evolution. Annu Rev Genomics Hum Genet. 8:241-259.
37. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 110:462-467. (Pubitemid 41159923)
38. Jurka J, Kohany O, Pavlicek A, Kapitonov VV, Jurka MV. 2004. Duplication, coclustering, and selection of human Alu retrotransposons. Proc Natl Acad Sci U S A. 101:1268-1272. (Pubitemid 38182678)
39. Kallman KD, Kazianis S. 2006. The genus Xiphophorus in Mexico and central America. Zebrafish 3:271-285. (Pubitemid 44569738)
40. Kang XL, Yadao F, Gietz RD, Kunz BA. 1992. Elimination of the yeast RAD6 ubiquitin conjugase enhances base-pair transitions and G. C-T. A transversions as well as transposition of the Ty element: implications for the control of spontaneous mutation. Genetics 130:285-294.
41. Kapitonov VV, Jurka J. 2001. Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A. 98:8714-8719. (Pubitemid 32678093)
42. Kapitonov VV, Jurka J. 2006. Self-synthesizing DNA transposons in eukaryotes. Proc Natl Acad Sci U S A. 103:4540-4545.
43. Kapitonov VV, Jurka J. 2007. Helitrons on a roll: eukaryotic rollingcircle transposons. Trends Genet. 23:521-529. (Pubitemid 47503448)
44. Kapitonov VV, Jurka J. 2008. Universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet. 9:411-412. (Pubitemid 351556058)
45. Kohany O, Gentles AJ, Hankus L, Jurka J. 2006. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics. 7:474.
46. Kosswig C. 1928. Über Kreuzungen zwischen Teleostiern Xiphophorus hellerii und Platypoecilius maculatus. Z Indukt Abstamm Vererbungsl. 47:150-158.
47. Lampert KP, Schmidt C, Fischer P, Volff JN, Hoffmann C, Muck J, Lohse MJ, Ryan MJ, Schartl M. 2010. Determination of onset of sexual maturation and mating behavior by melanocortin receptor 4 polymorphisms. Curr Biol. 20:1729-1734.
48. Lerat E, Brunet F, Bazin C, Capy P. 1999. Is the evolution of transposable elements modular? Genetica 107:15-25. (Pubitemid 129574947)
49. Lin R, Teng Y, Park HJ, Ding L, Black C, Fang P, Wang H. 2008. Discrete and essential roles of the multiple domains of Arabidopsis FHY3 in mediating phytochrome A signal transduction. Plant Physiol. 148:981-992. (Pubitemid 352847554)
50. Lippman Z, Gendrel AV, Black M, et al. (14 co-authors). 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471-476. (Pubitemid 38987911)
51. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 25:402-408. (Pubitemid 34164012)
52. Makarova KS, Aravind L, Koonin EV. 2000. A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem Sci. 25:50-52. (Pubitemid 30100365)
53. Makarova KS, Aravind L, Koonin EV. 2002. SWIM, a novel Znchelating domain present in bacteria, archaea and eukaryotes. Trends Biochem Sci. 27:384-386. (Pubitemid 34874743)
54. Marín I. 2010. GIN transposons: genetic elements linking retrotransposons and genes. Mol Biol Evol. 27:1903-1911.
55. Marquez CP, Pritham EJ. 2010. Phantom, a new subclass of Mutator DNA transposons found in insect viruses and widely distributed in animals. Genetics 185:1507-1517.
56. Meierjohann S, Schartl M. 2006. From Mendelian to molecular genetics: the Xiphophorus melanoma model. Trends Genet. 22:654-661. (Pubitemid 44738129)
57. Menees TM, Sandmeyer SB. 1996. Cellular stress inhibits transposition of the yeast retrovirus-like element Ty3 by a ubiquitindependent block of virus-like particle formation. Proc Natl Acad Sci U S A. 93:5629-5634. (Pubitemid 26159503)
58. Meyer A, Salzburger W, Schartl M. 2006. Hybrid origin of a swordtail species (Teleostei: Xiphophorus clemenciae) driven by sexual selection. Mol Ecol. 15:721-730. (Pubitemid 43344788)
59. Muffato M, Louis A, Poisnel CE, Roest Crollius H. 2010. Genomicus: a database and a browser to study gene synteny in modern and ancestral genomes. Bioinformatics 26:1119-1121.
60. Nelson JS. 2006. Fishes of the world. 4th ed. Hoboken (NJ): John Wiley & Sons, Inc.
61. Nishito Y, Hasegawa M, Inohara N, Núñez G. 2006. MEX is a testisspecific E3 ubiquitin ligase that promotes death receptorinduced apoptosis. Biochem J. 396:411-417. (Pubitemid 44228156)
62. Notredame C, Higgins D, Heringa J. 2000. T-Coffee: a novel method for multiple sequence alignments. J Mol Biol. 302:205-217.
63. Offen N, Meyer A, Begemann G. 2009. Identification of novel genes involved in the development of the sword and gonopodium in swordtail fish. Dev Dyn. 238:1674-1687.
64. Papadopoulos JS, Agarwala R. 2007. COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 23:1073-1079. (Pubitemid 47050558)
65. Parks CL, Chang LS, Shenk T. 1991. A polymerase chain reaction mediated by a single primer: cloning of genomic sequences adjacent to a serotonin receptor protein coding region. Nucleic Acids Res. 19:7155-7160. (Pubitemid 21897007)
66. Pritham EJ, Putliwala T, Feschotte C. 2007. Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. Gene 390:3-17. (Pubitemid 46241741)
67. Rio DC. 1990. Molecular mechanisms regulating Drosophila P element transposition. Annu Rev Genet. 24:543-578. (Pubitemid 120011559)
68. Rosenfeld R, Margalit H. 1993. Zinc fingers: conserved properties that can distinguish between spurious and actual DNA-binding motifs. J Biomol Struct Dyn. 11:557-570. (Pubitemid 24027866)
69. Schaack S, Gilbert C, Feschotte C. 2010. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol. 25:537-546.
70. Schultheis C, Zhou Q, Froschauer A, et al. (22 co-authors). 2006. Molecular analysis of the sex-determining region of the platyfish Xiphophorus maculatus. Zebrafish 3:299-309. (Pubitemid 44569740)
71. Sinzelle L, Izsvak Z, Ivics Z. 2009. Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cell Mol Life Sci. 66:1073-1093.
72. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, et al. (40 co-authors). 2003. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825-837. (Pubitemid 36781267)
73. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219. (Pubitemid 27456388)
74. Smit AF. 2002. Initial survey of interspersed repeats in Takifugu rubripes. Repbase Rep 2:74.
75. Suzuki R, Shindo H, Tase A, Kikuchi Y, Shimizu M, Yamazaki T. 2009. Solution structures and DNA binding properties of the N-terminal SAP domains of SUMO E3 ligases from Saccharomyces cerevisiae and Oryza sativa. Proteins 75:336-347.
76. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599. (Pubitemid 47236692)
77. Thomas JO. 2001. HMG1 and 2: architectural DNA-binding proteins. Biochem Soc Trans. 29:395-401.
78. Van de Peer Y. 2004. Tetraodon genome confirms Takifugu findings: most fish are ancient polyploids. Genome Biol. 5:250.
79. van Leeuwen H, Monfort A, Puigdomenech P. 2007. Mutator-like elements identified in melon, Arabidopsis and rice contain ULP1 protease domains. Mol Genet Genomics. 277:357-364. (Pubitemid 46452266)
80. Volff JN. 2005. Genome evolution and biodiversity in teleost fish. Heredity 94:280-294.
81. Volff JN. 2006. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28:913-922.
82. Volff JN, Bouneau L, Ouzouf-Costaz C, Fischer C. 2003. Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet. 19:674-678. (Pubitemid 37464841)
83. Volff JN, Körting C, Altschmied J, Duschl J, Sweeney K, Wichert K, Froschauer A, Schartl M. 2001. Jule from the fish Xiphophorus is the first complete vertebrate Ty3/Gypsy retrotransposon from the Mag family. Mol Biol Evol. 18:101-111. (Pubitemid 32118855)
84. Volff JN, Körting C, Froschauer A, Sweeney K, Schartl M. 2001. Non-LTR retrotransposons encoding a restriction enzyme-like endonuclease in vertebrates. J Mol Evol. 52:351-360. (Pubitemid 32368245)
85. Volff JN, Körting C, Sweeney K, Schartl M. 1999. The non-LTR retrotransposon Rex3 from the fish Xiphophorus is widespread among teleosts. Mol Biol Evol. 16:1427-1438. (Pubitemid 29510886)
86. Weiner AM, Deininger PL, Efstratiadis A. 1986. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem. 55:631-661. (Pubitemid 16070783)
87. Wicker T, Sabot F, Hua-Van A, et al. (13 co-authors). 2007. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 8:973-982. (Pubitemid 350129169)
88. Yeh ET. 2009. SUMOylation and De-SUMOylation: wrestling with life's processes. J Biol Chem. 284:8223-8227.
89. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J. 2006. KaKs Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 4:259-263. (Pubitemid 46771391)
90. Zhou Q, Braasch I, Froschauer A, Böhne A, Schultheis C, Schartl M, Volff JN. 2010. A novel marker for the platyfish (Xiphophorus maculatus) W chromosome is derived from a Polinton transposon. J Genet Genomics. 37:181-188.
91. Zhou Q, Froschauer A, Schultheis C, Schmidt C, Bienert GP, Wenning M, Dettai A, Volff JN. 2006. Helitron transposons on the sex chromosomes of the platyfish Xiphophorus maculatus and their evolution in animal genomes. Zebrafish 3:39-52.