Abstract
Transposable elements represent the DNA fragments capable of increasing their copy number and moving within the genome. Class II mobile elements represents the DNA transposons, which transpose via excision and the subsequent reinsertion at random genomic loci. The increase of their copy number occurs only when the transposition event is coupled with the replication. IS630/Tc1/mariner DNA transposon superfamily is one of the largest and widely distributed among the Class II elements. In this work, we provide a detailed analysis of IS630/Tc1/mariner DNA transposons from the Pacific oyster, Crassostrea gigas. IS630/Tc1/mariner transposons represented in the genome of the Pacific oyster belong to four families, Tc1 (DD34E), mariner (DD34D), pogo (DDxD), and rosa (DD41D). More than a half of IS630/Tc1/mariner elements from C. gigas belong to Tc1 family. Furthermore, Mariner-31_CGi element was shown to represent a new and previously unknown family with DD37E signature. We also discovered the full-size transcripts of eight elements from Tc1, mariner, and pogo families, three of which can, presumably, retain their transposition activity.
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References
Albertin CB, Simakov O, Mitros T et al (2015) The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524:220–224
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Arensburger P, Megy K, Waterhouse RM et al (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330:86–88
Bao W, Jurka J (2013a) DNA transposons from the Pacific oyster genome. Repbase Rep 13(1):599–633
Bao W, Jurka J (2013b) DNA transposons from the Pacific oyster genome. Repbase Rep 13(3):1415–1426
Bao W, Jurka J (2013c) DNA transposons from the Pacific oyster genome. Repbase Rep 13(4):1516–1517
Bouallègue M, Filée J, Kharrat I et al (2017) Diversity and evolution of mariner-like elements in aphid genomes. BMC Genom 18:494. https://doi.org/10.1186/s12864-017-3856-6
Bryan G, Garza D, Hartl D (1990) Insertion and excision of the transposable element mariner in Drosophila. Genetics 125:103–114
Capy P, Vitalis R, Langin T et al (1996) Relationships between transposable elements based upon the integrase-transposase domains: is there a common ancestor? J Mol Evol 42:359–368
Capy P, Langin T, Higuet D et al (1997) Do the integrases of LTR-retrotransposons and class II element transposases have a common ancestor? Genetica 100:63–72
Casola C, Hucks D, Feschotte C (2008) Convergent domestication of pogo-like transposases into centromere-binding proteins in fission yeast and mammals. Mol Biol Evol 25:29–41
Chow KC, Tung WL (2000) Magnetic field exposure stimulates transposition through the induction of DnaK/J synthesis. Biochem Biophys Res Commun 270(3):745–748
Clark KJ, Carlson DF, Leaver MJ et al (2009) Passport, a native Tc1 transposon from flatfish, is functionally active in vertebrate cells. Nucleic Acids Res 37:1239–1247
Claudianos C, Brownlie J, Russell R et al (2002) maT: a clade of transposons intermediate between mariner. and Tc1. Mol Biol Evol 19:2101–2109
Collins J, Forbes E, Anderson P (1989) The Tc3 family of transposable genetic elements in Caenorhabditis elegans. Genetics 121:47–55
Daboussi MJ, Langin T, Brygoo Y (1992) Fot1, a new family of fungal transposable elements. Mol Gen Genet 232:12–16
de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7:e1002384
Del Re B, Garoia F, Mesirca P et al (2003) Extremely low frequency magnetic fields affect transposition activity in Escherichia coli. Radiat Environ Biophys 42(2):113–118
Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common “D35E” motif. Proc Natl Acad Sci USA 91(3):942–946
Dupeyron M, Leclercq S, Cerveau N, Bouchon D, Gilbert C (2014) Horizontal transfer of transposons between and within crustaceans and insects. Mob DNA 5:4
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Emmons SW, Yesner L, Ruan K, Katzenberg D (1983) Evidence for a transposon in Caenorhabditis elegans. Cell 32:55–65
Fernández-Medina RD, Granzotto A, Ribeiro JM, Carareto CM (2016) Transposition burst of mariner-like elements in the sequenced genome of Rhodnius prolixus. Insect Biochem Mol Biol 69:14–24
Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368
Finnegan DJ (1992) Transposable elements. Curr Opin Genet Dev 2(6):861–867
Franz G, Savakis C (1991) Minos, a new transposable element from Drosophila hydei, is a member of the Tc1-like family of transposons. Nucleic Acids Res 19:6646
Gomulski LM, Torti C, Bonizzoni M et al (2001) A new basal subfamily of mariner elements in Ceratitis rosa and other tephritid flies. J Mol Evol 53:597–606
Haymer DS, Marsh JL (1986) Germ line and somatic instability of a white mutation in Drosophila mauritiana due to a transposable genetic element. Dev Genet 6:281–291
Henikoff S (1992) Detection of Caenorhabditis transposon homologs in diverse organisms. New Biol 4:382–388
Hernandez-Hernandez EM, Fernández-Medina RD, Navarro-Escalante L et al (2017) Genome-wide analysis of transposable elements in the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae): description of novel families. Mol Genet Genom 292(3):565–583. https://doi.org/10.1007/s00438-017-1291-7
Jacobson JW, Medhora MM, Hartl DL (1986) Molecular structure of a somatically unstable transposable element in Drosophila. Proc Natl Acad Sci USA 83:8684–8688
Jarvik T, Lark KG (1998) Characterization of Soymar1, a mariner element in soybean. Genetics 149:1569–1574
Jurka J (2012) DNA transposons from the Pacific oyster genome. Repbase Rep 12(12):2460–2461
Jurka J (2013) DNA transposons from the Pacific oyster genome. Repbase Rep 13(4):1547
Kapitonov VV, Jurka J (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 9(5):411–412
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Langin T, Capy P, Daboussi MJ (1995) The transposable element impala, a fungal member of the Tc1-mariner superfamily. Mol Gen Genet 246:19–28
Liu Y, Yang G (2014) Tc1-like transposable elements in plant genomes. Mob DNA 5:17
Mateo L, Gonzalez J (2014) Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins. Genome Biol Evol 6:2008–2016. https://doi.org/10.1093/gbe/evu153
Mesquita RD, Vionette-Amaral RJ, Lowenberger C et al (2015) Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection. Proc Natl Acad Sci USA 112:14936–14941
Munoz-Lopez M, Siddique A, Bischerour J et al (2008) Transposition of Mboumar-9: identification of a new naturally active mariner-family transposon. J Mol Evol 382:567–572
Piacentini L, Fanti L, Specchia V et al (2014) Transposons, environmental changes, and heritable induced phenotypic variability. Chromosoma 123:345–354
Puzakov MV, Puzakova LV, Zakharov IK (2017) Diversity and distribution of mobile genetic elements in marine invertebrates genomes. Vavilov J Genet Breed 21(2):269–283. https://doi.org/10.18699/VJ16.16-o
Robertson HM (1995) The Tc1-mariner superfamily of transposons in animals. J Insect Physiol 41:99–105
Robertson HM, Asplund ML (1996) Bmmar1: a basal lineage of the mariner family of transposable elements in the silkworm moth, Bombyx mori. Insect Biochem Mol Biol 26(8–9):945–954
Robertson HM, Lampe DJ (1995) Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol Biol Evol 12:850–862
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
Sergeeva EM, Salina EA (2011) Transposable elements and plant genome evolution. Russ J Genet: Appl Res 1(6):565–576. https://doi.org/10.1134/S2079059711060086
Shao H, Tu Z (2001) Expanding the diversity of the IS630-Tc1-mariner superfamily: discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons. Genetics 159(3):1103–1115
Simakov O, Marletaz F, Cho SJ et al (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–531
Smit AFA, Riggs AD (1996) Tiggers and other DNA transposon fossils in the human genome. Proc Natl Acad Sci USA 93:1443–1448
Strand DJ, McDonald JF (1989) Insertion of a copia element 5′ to the Drosophila melanogaster alcohol dehydrogenase gene (adh) is associated with altered developmental and tissue-specific patterns of expression. Genetics 121(4):787–794
Takeuchi T, Kawashima T, Koyanagi R et al (2012) Draft genome of the pearl oyster Pinctada fucata: a platform for understanding bivalve biology. DNA Res 19:117–130
Wallau GL, Capy P, Loreto E, Le Rouzic A, Hua-Van A (2016) VHICA, a new method to discriminate between vertical and horizontal transposon transfer: application to the mariner family within Drosophila. Mol Biol Evol 33(4):1094–1109
Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982. https://doi.org/10.1038/nrg2165
Yoshida MA, Ishikura Y, Moritaki T et al (2011) Genome structure analysis of molluscs revealed whole genome duplication and lineage specific repeat variation. Gene 483:63–71
Zakharenko LP, Zakharov IK, Voloshina MA, Gracheva EM, Romanova OA, Kochieva EZ, Simonova OB, Georgiev P, Golubovsky MD (2000) hobo-induced rearrangements are responsible mutation bursts at the yellow locus in natural population of Drosophila melanogaster. Mol Gen Genet MGG 263(2):335–341
Zakharenko LP, Kovalenko LV, Zakharov IK, Perepelkina MP (2006) The effect of γ-radiation on induction of the hobo element transposition in Drosophila melanogaster. Russ J Genet 42(6):619–622
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214
Zhang G, Fang X, Guo X et al (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490(7418):49–54. https://doi.org/10.1038/nature11413
Zhang HH, Li GY, Xiong XM, Min-Jin Han MJ, Zhang XG, Dai FY (2016a) TRT, a vertebrate and protozoan Tc1-like transposon: current activity and horizontal transfer. Genome Biol Evol 8(9):2994–3005. https://doi.org/10.1093/gbe/evw213
Zhang HH, Shen YH, Xiong XM et al (2016b) Identification and evolutionary history of the DD41D transposons in insects. Genes Genom 38:109–117. https://doi.org/10.1007/s13258-015-0356-4
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Under the support of the Russian Academy of Sciences research Grant No. AAAA-A18-118021490093-4.
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Puzakov, M.V., Puzakova, L.V. & Cheresiz, S.V. An Analysis of IS630/Tc1/mariner Transposons in the Genome of a Pacific Oyster, Crassostrea gigas. J Mol Evol 86, 566–580 (2018). https://doi.org/10.1007/s00239-018-9868-2
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DOI: https://doi.org/10.1007/s00239-018-9868-2