Structure and Diversity of Tc1/mariner Transposons in the Genome of the Jellyfish Aurelia aurita

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Transposable elements, DNA transposons and retrotransposons are DNA sequences capable of movement within the genome. It is assumed that they play one of their key roles in adaptive and evolutionary processes. One of the most studied groups of DNA transposons is the infraclass ITm, and in particular the superfamily Tc1/mariner. In this work, we considered the representation, structure, and evolution of Tc1/mariner DNA transposons in the jellyfish Aurelia aurita. It was found that the predominant proportion of Tc1/mariner elements of the jellyfish is represented by the TLE family. A new subfamily of TLE elements called Aurum has been identified. In addition, two groups of elements VS-aura and VS-beplau were found in the Visitor family, which are probably also separate subfamilies. Analysis of the structure and diversity of Tc1/mariner elements showed that at the moment Tc1/mariner transposons in the jellyfish genome are at the stage of degradation and elimination. Almost all elements are deleted or have structural changes, and, accordingly, do not have potentially functional copies.

About the authors

Yu. N. Ulupova

Federal Research Center “Kovalevsky Institute of Biology of the Southern Seas”,
Russian Academy of Sciences

Email: puzakov@ngs.ru
Russia, 299011, Sevastopol

L. V. Puzakova

Federal Research Center “Kovalevsky Institute of Biology of the Southern Seas”,
Russian Academy of Sciences

Email: puzakov@ngs.ru
Russia, 299011, Sevastopol

M. V. Puzakov

Federal Research Center “Kovalevsky Institute of Biology of the Southern Seas”,
Russian Academy of Sciences

Author for correspondence.
Email: puzakov@ngs.ru
Russia, 299011, Sevastopol

References

  1. McClintock B. Chromosome organization and genetic expression // Cold Spring Harbor Symp. Quant. Biol. 1951. V. 16. P. 13–47. https://doi.org/10.1101/sqb.1951.016.01.004
  2. Guo B., Zou M., Gan X., He S. Genome size evolution in pufferfish: an insight from BAC clone-based Diodon holocanthus genome sequencing // BMC Genomics. 2010. V. 11. P. 396. https://doi.org/10.1186/1471-2164-11-396
  3. Feschotte C., Pritham E.J. DNA transposons and the evolution of eukaryotic genomes // Annu. Rev. Genet. 2007. V. 41. P. 331–368. https://doi.org/10.1146/annurev.genet.40.110405.090448
  4. Bourque G., Burns K.H., Gehring M. et al. Ten things you should know about transposable elements // Genome Biology. 2018. V. 19. № 1. P. 199. https://doi.org/10.1186/s13059-018-1577-z
  5. Piacentini L., Fanti L., Specchia V. et al. Transposons, environmental changes, and heritable induced phenotypic variability // Chromosoma. 2014. V. 123. № 4. P. 345–354. https://doi.org/10.1007/s00412-014-0464-y
  6. Kojima K.K. Structural and sequence diversity of e-ukaryotic transposable elements // Genes Genet. Syst. 2020. V. 94. P. 233–252. Epub. 2018. Nov. 9.https://doi.org/10.1266/ggs.18-00024
  7. Dupeyron M., Baril T., Bass C., Hayward A. Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements // Mobile DNA. 2020. V. 11. P. 21. https://doi.org/10.1186/s13100-020-00212-0
  8. Gao B., Wang Y., Diaby M. et al. Evolution of pogo, a separate superfamily of IS630-Tc1-mariner ransposons, revealing recurrent domestication events in vertebrates // Mobile DNA. 2020. V. 11. P. 25. https://doi.org/10.1186/s13100-020-00220-0
  9. Lee C.C., Wang J. Rapid expansion of a highly germline-expressed Mariner element acquired by horizontal transfer in the fire ant genome // Genome Biol. Evol. 2018. V. 10. № 12. P. 3262–3278. https://doi.org/10.1093/gbe/evy220
  10. Xie L.Q., Wang P.L., Jiang S.H. et al. Genome-wide identification and evolution of TC1/Mariner in the silkworm (Bombyx mori) genome // Genes Genomics. 2018. V. 40. № 5. P. 485–495. https://doi.org/10.1007/s13258-018-0648-6
  11. Shen D., Gao B., Miskey C. et al. Multiple invasions of visitor, a DD41D family of Tc1/mariner transposons, throughout the evolution of vertebrates // Genome Biol. Evol. 2020. V. 12. № 7. P. 1060–1073. https://doi.org/10.1093/gbe/evaa135
  12. Claudianos C., Brownlie J., Russell R. et al. maT – a clade of transposons intermediate between mariner and Tc1 // Mol. Biol. Evol. 2002. V. 19. № 12. P. 2101–2109. https://doi.org/10.1093/oxfordjournals.molbev.a004035
  13. Zhang H.H., Shen Y.H., Xiong X.M. et al. Identification and evolutionary history of the DD41D transposons in insects // Genes Genomics. 2016. V. 38. P. 109–117. https://doi.org/10.1007/s13258-015-0356-4
  14. Ivics Z., Izsvák Z. Sleeping Beauty transposition // Microbiol. Spectrum. 2015. V. 3. № 2. MDNA3-0042-2-14. https://doi.org/10.1128/microbiolspec.MDNA3-0042-2014
  15. Ivics Z., Hackett P.B., Plasterk R.H., Izsvák Z. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells // Cell. 1997. V. 91. № 4. P. 501–510. https://doi.org/10.1016/s0092-8674(00)80436-5
  16. Plasterk R.H., Izsvák Z., Ivics Z. Resident aliens: the Tc1/mariner superfamily of transposable elements // Trends in Genet. 1999. V. 15. № 8. P. 326–332. https://doi.org/10.1016/s0168-9525(99)01777-1
  17. Tellier M., Bouuaert C.C., Chalmers R. Mariner and the ITm superfamily of transposons // Microbiol. Spectrum. 2015. V 3. № 2. MDNA3-0033-2014. https://doi.org/10.1128/microbiolspec.MDNA3-0033-2014
  18. Shi S., Puzakov M., Guan Z. et al. Prokaryotic and eukaryotic horizontal transfer of Sailor (DD82E), a new superfamily of IS630-Tc1-mariner DNA transposons // Biology (Basel). 2021. V. 10. № 10. P. 1005. https://doi.org/10.3390/biology10101005
  19. Wang S., Diaby M., Puzakov M. et al. Divergent evolution profiles of DD37D and DD39D families of Tc1/mariner transposons in eukaryotes // Mol. Phylogenet. Evol. 2021. V. 161. P. 107143. https://doi.org/10.1016/j.ympev.2021.107143
  20. Shao H., Tu Z. Expanding the diversity of the IS630-Tc1-mariner superfamily: Discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons // Genetics. 2001. V. 159. № 3. P. 1103–1115. https://doi.org/10.1093/genetics/159.3.1103
  21. 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. 2018. V. 86. № 8. P. 566–580. https://doi.org/10.1007/s00239-018-9868-2
  22. Lawley J.W., Gamero-Mora E., Maronna M.M. et al. The importance of molecular characters when morphological variability hinders diagnosability: Systematics of the moon jellyfish genus Aurelia (Cnidaria: Scyphozoa) // Peer J. 2021. V. 9. e11954. https://doi.org/10.7717/peerj.11954
  23. Dawson M.N., Sen Gupta A., England M.H. Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species // Proc. Natl Acad. Sci. USA. 2005. V. 102. P. 11968–11973. https://doi.org/10.1073/pnas.0503811102
  24. Луппова Н.Е. Динамика численности и биомассы популяций черноморского макрозоопланктона // Бюл. науки и практики. 2020. Т. 6. № 5. С. 74–82. https://doi.org/10.33619/2414-2948/54/09
  25. Zhang H.H., Li G.Y., Xiong X.M. et al. TRT, a vertebrate and protozoan Tc1-like transposon: Current activity and horizontal transfer // Genome Biol. Evol. 2016. V. 8. № 9. P. 2994–3005. https://doi.org/10.1093/gbe/evw213
  26. Sang Y., Gao B., Diaby M. et al. Incomer, a DD36E family of Tc1/mariner transposons newly discovered in animals // Mobile DNA. 2019. V. 10. P. 45. https://doi.org/10.1186/s13100-019-0188-x
  27. Zong W., Gao B., Diaby M. et al. Traveler, a new DD35E family of Tc1/mariner transposons, invaded vertebrates very recently // Genome Biol. Evol. 2020. V. 12. № 3. P. 66–76. https://doi.org/10.1093/gbe/evaa034
  28. Gao B., Zong W., Miskey C. et al. Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals // Mobile DNA. 2020. V. 11. № 1. P. 32. https://doi.org/10.1186/s13100-020-00227-7
  29. Zhang Z., Schwartz S., Wagner L.W. et al. A greedy algorithm for aligning DNA sequences // J. Computational Biol. 2000. V. 7. № 1–2. P. 203–214. https://doi.org/10.1089/10665270050081478
  30. De Castro E., Sigrist C.J., Gattiker A. et al. ScanProsite: Detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins // Nucl. Acids Res. 2006. V. 34. P. W362–W365. https://doi.org/10.1093/nar/gkl124
  31. Buchan D.W., Minneci F., Nugent T.C. et al. Scalable web services for the PSIPRED Protein Analysis Workbench // Nucl. Acids Res. 2013. V. 41 (W1). P. W349–W357. https://doi.org/10.1093/nar/gkt381
  32. Edgar R.C. MUSCLE: A multiple sequence alignment method with reduced time and space complexity // Nucl. Acids Res. 2004. V. 32. P. 1792–1797. https://doi.org/10.1093/nar/gkh340
  33. Kumar S., Stecher G., Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets // Mol. Biol. Evol. 2016. V. 33. № 7. P. 1870–1874. https://doi.org/10.1093/molbev/msw054
  34. Пузаков М.В., Пузакова Л.В. Распространенность, разнообразие и эволюция ДНК-транспозонов L18 (DD37E) в геномах стрекающих (Cnidaria) // Мол. биология. 2022. Т. 56. № 3. С. 1–15 https://doi.org/10.31857/S0026898422030120
  35. Puzakov M.V., Puzakova L.V., Cheresiz S.V., Sang Y. The IS630/Tc1/mariner transposons in three ctenophore genomes // Mol. Phylogenet. Evol. 2021. V. 163. P. 107231. https://doi.org/10.1016/j.ympev.2021.107231
  36. Bouallègue M., Filée J., Kharrat I. et al. Diversity and evolution of mariner-like elements in aphid genomes // BMC Genomics. 2017. V. 18. № 1. P. 494. https://doi.org/10.1186/s12864-017-3856-6
  37. Benjamin B., Yves B., Corinne A.G. Assembly of the Tc1 and mariner transposition initiation complexes depends on the origins of their transposase DNA binding domains // Genetica. 2007. V. 130. № 2. P. 105–120. https://doi.org/10.1007/s10709-006-0025-2
  38. Gomulski L.M., Torti C., Bonizzoni M. et al. A new basal subfamily of mariner elements in Ceratitis rosa and other tephritid flies // J. Mol. Evol. 2001. V. 53. № 6. P. 597–606. https://doi.org/10.1007/s002390010246
  39. Robertson H.M., Lampe D.J. Distribution of transposable elements in arthropods // Annual Rev. Entomol. 1995. V. 40. P. 333–357. https://doi.org/10.1146/annurev.en.40.010195.002001
  40. Jacobson J.W., Medhora M.M., Hartl D.L. Molecular structure of a somatically unstable transposable element in Drosophila // Proc. Natl Acad. Sci. USA. 1986. V. 83. № 22. P. 8684–8688. https://doi.org/10.1073/pnas.83.22.8684
  41. Emmons S.W., Yesner L. High-frequency excision of transposable element Tc1 in the nematode Caenorhabditis elegans is limited to somatic cells // Cell. 1984. V. 36. № 3. P. 599–605. https://doi.org/10.1016/0092-8674(84)90339-8
  42. Eide D., Anderson P. Transposition of Tc1 in the nematode Caenorhabditis elegans // Proc. Natl Acad. Sci. USA. 1985. V. 82. № 6. P. 1756–1760. https://doi.org/10.1073/pnas.82.6.1756
  43. Guo X.M., Zhang Q.Q., Sun Y.W. et al. Tc1-like transposase Thm3 of silver carp (Hypophthalmichthys molitrix) can mediate gene transposition in the genome of blunt snout bream (Megalobrama amblycephala) // G3: Genes, Genomes, Genetics. 2015. V. 5. № 12. P. 2601–2610. https://doi.org/10.1534/g3.115.020933
  44. Puzakov M.V., Puzakova L.V., Cheresiz S.V. The Tc1-like elements with the spliceosomal introns in mollusk genomes // Mol. Genet. Genomics. 2020. V. 295. № 3. P. 621–633. https://doi.org/10.1007/s00438-020-01645-1
  45. Capy P., Vitalis R., Langin T. et al. Relationships between transposable elements based upon the integrase-transposase domains: is there a common ancestor? // J. Mol. Evol. 1996. V. 42. № 3. P. 359–368. https://doi.org/10.1007/BF02337546

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2.

Download (390KB)
Indexing metadata
3.

Download (2MB)
Indexing metadata

Copyright (c) 2023 Ю.Н. Улупова, Л.В. Пузакова, М.В. Пузаков

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies