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The P-Element Has Not Significant Effect on the Drosophila simulans Viability

  • EVOLUTIONARY, POPULATION, AND MEDICAL GENOMICS, TRANSCRIPTOMICS
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Abstract

Cases of horizontal transfer of transposable elements (TEs) between species are known for the Drosophilidae family. In the middle of the last century, the case of horizontal transfer of the P-element from the Drosophila willistoni to the D. melanogaster was described. A novel P-element invasion into the D. simulans genome from D. melanogaster occurred approximately 10 years ago. Currently, the P-element has spread across all D. melanogaster population and 30% of D. simulans populations in Europe, Africa and America. In this paper, we investigated the presence of the P-element in D. simulans lines caught in different years in three Asian populations (Tashkent, Nalchik and Sakhalin Island). We also examined the physiological characteristics (cytotype, lifespan, fecundity and locomotor activity) of D. simulans lines with and without the P-element to determine the significance of this new mobile element in the genome. The P-element was found in lines isolated from nature after 2012. The number of P-element copies per genome (two-to-three dozen according to fluorescence in situ hybridization data) was greater than in the American and comparable to the African populations. There were signs of intraspecific hybrid dysgenesis for some pairs of lines. However, in general the presence of the P-element did not adversely affect the physiological characteristics. Either adaptation to the new TE occurs very quickly, or the rate of movement of the P-element is so insignificant that its appearance in the genome remains unnoticed.

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REFERENCES

  1. Lipatov M., Lenkov K., Petrov D.A., Bergman C.M. 2005. Paucity of chimeric gene-transposable element transcripts in the Drosophila melanogaster genome. BMC Biol. 3, 24.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bargues N., Lerat E. 2017. Evolutionary history of LTR-retrotransposons among 20 Drosophila species. Mob. DNA. 8, 7.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Daniels S.B., Peterson K.R., Strausbaugh L.D., Kidwell M.G., Chovnick A. 1990. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics. 124, 339‒355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Depra M., Panzera Y., Ludwig A., Valente V.L., Loreto E.L. 2010. Hosimary: a new hAT transposon group involved in horizontal transfer. Mol. Genet. Genomics. 283, 451‒459.

    Article  CAS  PubMed  Google Scholar 

  5. Rossato D.O., Ludwig A., Deprá M., Loreto E.L., Ruiz A., Valente V.L. 2014. BuT2 is a member of the third major group of hAT transposons and is involved in horizontal transfer events in the genus Drosophila. Genome Biol. Evol. 6, 352‒365.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Palazzo A., Lovero D., D’Addabbo P., Caizzi R., Marsano R.M. 2016. Identification of Bari transposons in 23 sequenced Drosophila genomes reveals novel structural variants, MITEs and horizontal transfer. PLoS One. 11 (5), e0156014.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kotnova A.P., Glukhov I.A., Karpova N.N., Salenko V.B., Lyubomirskaya N.V., Ilyin Y.V 2007. Evidence for recent horizontal transfer of gypsy-homologous LTR-retrotransposon gtwin into Drosophila erecta followed by its amplification with multiple aberrations. Gene. 396, 39‒45.

    Article  CAS  PubMed  Google Scholar 

  8. Glukhov I.A., Kotnova A.P, Stefanov Y.E., Ilyin Y.V. 2016. The first complete Mag family retrotransposons discovered in Drosophila. Dokl. Biochem. Biophys. 466, 1‒4.

    Article  CAS  PubMed  Google Scholar 

  9. Wallau G.L., 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, 1094‒1109.

    Article  PubMed  Google Scholar 

  10. Loreto E.L., Valente V.L., Zaha A., Silva J.C., Kidwell M.G. 2001. Drosophila mediopunctata P-elements: a new example of horizontal transfer. J. Hered. 92, 375‒381.

    Article  CAS  PubMed  Google Scholar 

  11. Kofler R., Hill T., Nolte V., Betancourt A.J., Schlötterer C. 2015. The recent invasion of natural Drosophila simulans populations by the P-element. Proc. Natl. Acad. Sci. U. S. A. 112, 6659‒6663.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hill T., Schlötterer C., Betancourt A.J. 2016. Hybrid dysgenesis in Drosophila simulans associated with a rapid invasion of the P-element. PLoS Genet. 12 (3), e1005920.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Yoshitake Y., Inomata N., Sano M., Kato Y., Itoh M. 2018. The P-element invaded rapidly and caused hybrid dysgenesis in natural populations of Drosophila simulans in Japan. Ecol. Evol. 8, 9590‒9599.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Houck M.A., Clark J.B., Peterson K.R., Kidwell M.G. 1991. Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science. 253, 1125–1128.

    Article  CAS  PubMed  Google Scholar 

  15. Coates B.S. 2015. Horizontal transfer of a non-autonomous Helitron among insect and viral genomes. BMC Genomics. 16, 137. https://doi.org/10.1186/s12864-015-1318-6

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wallau G.L., Vieira C., Loreto É.L.S. 2018. Genetic exchange in eukaryotes through horizontal transfer: connected by the mobilome. Mobile DNA. 9, 6.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Goulielmos G.N., Alahiotis S.N. 1989. Interspecific hybridization between Drosophila species group melanogaster sibling species: isozymic patterns and reproductive relationships. Genome. 32, 146‒154.

    Article  Google Scholar 

  18. Kilias G., Goulielmos G., Alahiotis S. 1989. Interspecific hybridization between Drosophila species group melanogaster sibling species. Fitness components. Hereditas. 110, 267‒274.

    Article  Google Scholar 

  19. Peccoud J., Loiseau V., Cordaux R., Gilbert C. 2017. Massive horizontal transfer of transposable elements in insects. Proc. Natl. Acad. Sci. U. S. A. 114, 4721–4726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Vieira C., Fablet M., Lerat E., Boulesteix M., Rebollo R., Burlet N., Akkouche A., Hubert B., Mortada H., Biémont C. 2012. A comparative analysis of the amounts and dynamics of transposable elements in natural populations of Drosophila melanogaster and Drosophila simulans. J. Environ. Radioact. 13, 83‒86.

    Article  Google Scholar 

  21. Sessegolo C., Burlet N., Haudry A. 2016. Strong phylogenetic inertia on genome size and transposable element content among 26 species of flies. Biol. Lett. 12 (8), 20160407.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Sturtevant A.H. 1919. A new species closely resembling Drosophila melanogaster. Psyche. 26, 153‒154.

    Article  Google Scholar 

  23. Bender W., Spierer P., Hogness D.S. 1983. Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J. Mol. Biol. 168:17–33.

    Article  CAS  PubMed  Google Scholar 

  24. Ogienko A.A., Yarinich L.A., Fedorova E.V., Lebedev M.O., Andreyeva E.N., Pindyurin A.V., Baricheva E.M. 2018. New slbo-Gal4 driver lines for the analysis of border cell migration during Drosophila oogenesis. Chromosoma. 127, 475–487.

    Article  CAS  PubMed  Google Scholar 

  25. Ignatenko O.M., Zakharenko L.P., Dorogova N.V., Fedorova S.A. 2015. P-Elements and the determinants of hybrid dysgenesis have different dynamics of propagation in Drosophila melanogaster populations. Genetica. 143, 751‒759.

    Article  PubMed  Google Scholar 

  26. Kidwell M.G., Kidwell J.F., Sved J.A. 1977. Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics. 86, 813‒833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bland J.M., Altman D.G. 2004. The logrank test. BMJ. 328, 1073.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kozeretska I., Bondarenko V, Shulga V., Serga S., Rozhok A., Protsenko O., Nelson M.G. 2016. Phenotypic and genomic analysis of P-elements in natural populations of Drosophila melanogaster. BioRxiv. https://doi.org/10.1101/047910

  29. Teixeira F.K., Okuniewska M., Malone C.D., Coux R.X., Rio D.C., Lehmann R. 2017. piRNA-mediated regulation of transposon alternative splicing in the soma and germ line. Nature. 552, 268‒272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bergman C.M, Nelson M.G., Bondarenko V, Kozeretska I. 2017. Genomic analysis of P-elements in natural populations of Drosophila melanogaster. PeerJ. 5, e3824.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Wakisaka K.T., Ichiyanagi K., Ohno S., Itoh M. 2017. Diversity of P-element piRNA production among M' and Q strains and its association with P-M hybrid dysgenesis in Drosophila melanogaster. Mob. DNA. 8, 13.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Presgraves D.C. 2013. Hitchhiking to speciation. PLoS Biol. 11, e1001498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Chen C., E Z., Lin H.X. 2016. Evolution and molecular control of hybrid incompatibility in plants. Front. Plant Sci. 7, 1208.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Bundus J.D., Wang D., Cutter A.D. 2018. Genetic basis to hybrid inviability is more complex than hybrid male sterility in Caenorhabditis nematodes. Heredity (Edinb.). 121, 169‒182.

    Article  PubMed  Google Scholar 

  35. Kerwin R.E., Sweigart A.L. 2017. Mechanisms of transmission ratio distortion at hybrid sterility loci within and between Mimulus species. G3 (Bethesda). 7, 3719‒3730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Shirata M., Araye Q., Maehara K., Enya S., Takano-Shimizu T., Sawamura K. 2014. Allelic asymmetry of the Lethal hybrid rescue (Lhr) gene expression in the hybrid between Drosophila melanogaster and D. simulans: confirmation by using genetic variations of D. melanogaster. Genetica. 142, 43‒48.

    Article  CAS  PubMed  Google Scholar 

  37. Brideau N.J., Flores H.A., Wang J., Maheshwari S., Wang X., Barbash D.A 2006. Two Dobzhansky–Muller genes interact to cause hybrid lethality in Drosophila. Science. 314, 1292‒1295.

    Article  CAS  PubMed  Google Scholar 

  38. Gerland T.A., Sun B., Smialowski P., Lukacs A., Thomae A.W., Imhof A. 2017. The Drosophila speciation factor HMR localizes to genomic insulator sites. PLoS One. 12 (2), e0171798.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Hägele K. 1995. The HLE hybrid dysgenesis syndrome in the midge Chironomus thummi—differences in the dysgenic potential between strains. Genetica. 96, 239‒245.

    Article  Google Scholar 

  40. Eggleston W.B., Rim N.R., Lim J.K. 1996. Molecular characterization of hobo-mediated inversions in Drosophila melanogaster. Genetics. 144, 647‒656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zakharenko L.P., Zakharov I.K., Voloshina M.A., Romanova O.M., Alekseenko A.A., Georgiev P.G. 2004. The reason for the preservation of high instability at the yellow gene in Drosophila melanogaster strains isolated from the natural population of Uman’ during the “mode for mutation.” Russ. J. Genet. 40, 239–243.

    Article  CAS  Google Scholar 

  42. Platt II R.N., Vandewege M.W., Ray D.A. 2018. Mammalian transposable elements and their impacts on genome evolution. Chromosome Res. 26, 25‒43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Khurana J.S., Wang J., Xu J., Koppetsch B.S., Thomson T.C., Nowosielska A., Li C., Zamore P.D., Weng Z., Theurkauf W.E. 2011. Adaptation to P-element transposon invasion in Drosophila melanogaster. Cell. 147, 1551‒1563.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

The authors thank Voloshina M.A. for the Drosophila lines and Skvortzova L.I. for technical assistance.

Funding

The work was supported by Ministry of Science and Higher Education of the Russian Federation, project no. FWNR-2022-0019.

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Authors and Affiliations

  1. Institute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences, 630090, Novosibirsk, Russia

    L. P. Zakharenko, D. V. Petrovskii & R. A. Bykov

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  1. L. P. Zakharenko
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  2. D. V. Petrovskii
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  3. R. A. Bykov
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Correspondence to L. P. Zakharenko.

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The authors declare that they have no conflicts of interest. This article does not contain any research involving humans or animals as subjects of research.

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Abbreviations: HD, hybrid dysgenesis; HT, horizontal transfer; TE, transposable element.

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Zakharenko, L.P., Petrovskii, D.V. & Bykov, R.A. The P-Element Has Not Significant Effect on the Drosophila simulans Viability. Mol Biol 57, 366–373 (2023). https://doi.org/10.1134/S0026893323020231

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  • DOI: https://doi.org/10.1134/S0026893323020231

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