Advertisement

Journal of Molecular Evolution

, Volume 86, Issue 8, pp 566–580 | Cite as

An Analysis of IS630/Tc1/mariner Transposons in the Genome of a Pacific Oyster, Crassostrea gigas

  • M. V. Puzakov
  • L. V. Puzakova
  • S. V. Cheresiz
Original Article

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.

Keywords

Transposable elements IS630/Tc1/mariner Transposon activity Pacific oyster Mollusca 

Notes

Acknowledgements

Under the support of the Russian Academy of Sciences research Grant No. AAAA-A18-118021490093-4.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

239_2018_9868_MOESM1_ESM.pdf (116 kb)
Online Resource 1 (PDF 115 KB)
239_2018_9868_MOESM2_ESM.pdf (79 kb)
Online Resource 2 (PDF 78 KB)
239_2018_9868_MOESM3_ESM.pdf (155 kb)
Online Resource 3 (PDF 154 KB)
239_2018_9868_MOESM4_ESM.pdf (142 kb)
Online Resource 4 (PDF 141 KB)
239_2018_9868_MOESM5_ESM.pdf (148 kb)
Online Resource 5 (PDF 147 KB)

References

  1. Albertin CB, Simakov O, Mitros T et al (2015) The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524:220–224CrossRefGoogle Scholar
  2. 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 25:3389–3402CrossRefGoogle Scholar
  3. Arensburger P, Megy K, Waterhouse RM et al (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330:86–88CrossRefGoogle Scholar
  4. Bao W, Jurka J (2013a) DNA transposons from the Pacific oyster genome. Repbase Rep 13(1):599–633Google Scholar
  5. Bao W, Jurka J (2013b) DNA transposons from the Pacific oyster genome. Repbase Rep 13(3):1415–1426Google Scholar
  6. Bao W, Jurka J (2013c) DNA transposons from the Pacific oyster genome. Repbase Rep 13(4):1516–1517Google Scholar
  7. 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 CrossRefGoogle Scholar
  8. Bryan G, Garza D, Hartl D (1990) Insertion and excision of the transposable element mariner in Drosophila. Genetics 125:103–114PubMedPubMedCentralGoogle Scholar
  9. 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 42:359–368CrossRefGoogle Scholar
  10. 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 100:63–72CrossRefGoogle Scholar
  11. 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 25:29–41CrossRefGoogle Scholar
  12. Chow KC, Tung WL (2000) Magnetic field exposure stimulates transposition through the induction of DnaK/J synthesis. Biochem Biophys Res Commun 270(3):745–748CrossRefGoogle Scholar
  13. 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 37:1239–1247CrossRefGoogle Scholar
  14. Claudianos C, Brownlie J, Russell R et al (2002) maT: a clade of transposons intermediate between mariner. and Tc1. Mol Biol Evol 19:2101–2109CrossRefGoogle Scholar
  15. Collins J, Forbes E, Anderson P (1989) The Tc3 family of transposable genetic elements in Caenorhabditis elegans. Genetics 121:47–55PubMedPubMedCentralGoogle Scholar
  16. Daboussi MJ, Langin T, Brygoo Y (1992) Fot1, a new family of fungal transposable elements. Mol Gen Genet 232:12–16CrossRefGoogle Scholar
  17. 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:e1002384CrossRefGoogle Scholar
  18. 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):113–118CrossRefGoogle Scholar
  19. 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):942–946CrossRefGoogle Scholar
  20. Dupeyron M, Leclercq S, Cerveau N, Bouchon D, Gilbert C (2014) Horizontal transfer of transposons between and within crustaceans and insects. Mob DNA 5:4CrossRefGoogle Scholar
  21. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefGoogle Scholar
  22. Emmons SW, Yesner L, Ruan K, Katzenberg D (1983) Evidence for a transposon in Caenorhabditis elegans. Cell 32:55–65CrossRefGoogle Scholar
  23. 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 69:14–24CrossRefGoogle Scholar
  24. Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368CrossRefGoogle Scholar
  25. Finnegan DJ (1992) Transposable elements. Curr Opin Genet Dev 2(6):861–867CrossRefGoogle Scholar
  26. 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 19:6646CrossRefGoogle Scholar
  27. 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 53:597–606CrossRefGoogle Scholar
  28. 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 6:281–291CrossRefGoogle Scholar
  29. Henikoff S (1992) Detection of Caenorhabditis transposon homologs in diverse organisms. New Biol 4:382–388PubMedGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. Jacobson JW, Medhora MM, Hartl DL (1986) Molecular structure of a somatically unstable transposable element in Drosophila. Proc Natl Acad Sci USA 83:8684–8688CrossRefGoogle Scholar
  32. Jarvik T, Lark KG (1998) Characterization of Soymar1, a mariner element in soybean. Genetics 149:1569–1574PubMedPubMedCentralGoogle Scholar
  33. Jurka J (2012) DNA transposons from the Pacific oyster genome. Repbase Rep 12(12):2460–2461Google Scholar
  34. Jurka J (2013) DNA transposons from the Pacific oyster genome. Repbase Rep 13(4):1547Google Scholar
  35. Kapitonov VV, Jurka J (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 9(5):411–412CrossRefGoogle Scholar
  36. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  37. Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921CrossRefGoogle Scholar
  38. Langin T, Capy P, Daboussi MJ (1995) The transposable element impala, a fungal member of the Tc1-mariner superfamily. Mol Gen Genet 246:19–28CrossRefGoogle Scholar
  39. Liu Y, Yang G (2014) Tc1-like transposable elements in plant genomes. Mob DNA 5:17CrossRefGoogle Scholar
  40. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 112:14936–14941CrossRefGoogle Scholar
  42. 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 382:567–572Google Scholar
  43. Piacentini L, Fanti L, Specchia V et al (2014) Transposons, environmental changes, and heritable induced phenotypic variability. Chromosoma 123:345–354CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. Robertson HM (1995) The Tc1-mariner superfamily of transposons in animals. J Insect Physiol 41:99–105CrossRefGoogle Scholar
  46. 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):945–954CrossRefGoogle Scholar
  47. Robertson HM, Lampe DJ (1995) Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol Biol Evol 12:850–862PubMedGoogle Scholar
  48. Schaack S, Gilbert C, Feschotte C (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–546CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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):1103–1115PubMedPubMedCentralGoogle Scholar
  51. Simakov O, Marletaz F, Cho SJ et al (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–531CrossRefGoogle Scholar
  52. Smit AFA, Riggs AD (1996) Tiggers and other DNA transposon fossils in the human genome. Proc Natl Acad Sci USA 93:1443–1448CrossRefGoogle Scholar
  53. 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):787–794PubMedPubMedCentralGoogle Scholar
  54. 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 19:117–130CrossRefGoogle Scholar
  55. 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):1094–1109CrossRefGoogle Scholar
  56. 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 420:520–562CrossRefGoogle Scholar
  57. 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 CrossRefPubMedGoogle Scholar
  58. Yoshida MA, Ishikura Y, Moritaki T et al (2011) Genome structure analysis of molluscs revealed whole genome duplication and lineage specific repeat variation. Gene 483:63–71CrossRefGoogle Scholar
  59. 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):335–341CrossRefGoogle Scholar
  60. 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):619–622CrossRefGoogle Scholar
  61. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214CrossRefGoogle Scholar
  62. 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 CrossRefGoogle Scholar
  63. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.The A.O. Kovalevsky Institute of Marine Biology Research of RASSevastopolRussia
  2. 2.Department of MedicineNovosibirsk State UniversityNovosibirskRussia
  3. 3.State Scientific Research Institute of Physiology and Basic MedicineNovosibirskRussia

Personalised recommendations