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Diversity of mariner-like elements in Orthoptera

https://doi.org/10.18699/VJ19.581

Abstract

Mariner-like elements (MLEs) are among the most widespread DNA transposable elements in eukaryotes. Insects were the first organisms in which MLEs were identified, however the diversity of MLEs in the insect order Orthoptera has not yet been addressed. In the present study, we explore the diversity of MLEs elements in 16 species of Orthoptera belonging to three infraorders, Acridoidea (Caelifera), Grylloidea (Ensifera), and Tettigoniidea (Ensifera) by combining data mined from computational analysis of sequenced degenerative PCR MLE amplicons and available Orthoptera genomic scaffolds. In total, 75 MLE lineages (Ortmar) were identified in all the studied genomes. Automatic phylogeny-based classification suggested that the current known variability of MLEs can be assigned to seven statistically well-supported phylogenetic clusters (I–VII), and the identified Orthoptera lineages were distributed among all of them. The majority of the lineages (36 out of 75) belong to cluster I; 20 belong to cluster VI; and seven, six, four, one and one lineages belong to clusters II, IV, VII, III, and V, respectively. Two of the clusters (II and IV) were composed of a single Orthoptera MLE lineage each (Ortmar37 and Ortmar45, respectively) which were distributed in the vast majority of the studied Orthoptera genomes. Finally, for 16 Orthoptera MLE lineages, horizontal transfer from the distantly related taxa belonging to other insect orders may have occurred. We believe that our study can serve as a basis for future researches on the diversity, distribution, and evolution of MLEs in species of other taxa that are still lacking the sequenced genomes.

About the Authors

K. Ustyantsev
Institute of Cytology and Genetics, SB RAS
Russian Federation
Novosibirsk


M. Biryukov
Institute of Cytology and Genetics, SB RAS
Russian Federation
Novosibirsk


I. Sukhikh
Institute of Cytology and Genetics, SB RAS
Russian Federation
Novosibirsk


N. V. Shatskaya
Institute of Cytology and Genetics, SB RAS
Russian Federation
Novosibirsk


V. Fet
Marshall University
United States

Department of Biological Sciences

Huntington



A. Blinov
Institute of Cytology and Genetics, SB RAS; Institute of Molecular and Cellular Biology, SB RAS
Russian Federation
Novosibirsk


I. Konopatskaia
Institute of Cytology and Genetics, SB RAS
Russian Federation
Novosibirsk


References

1. Akaike H. Information Theory and an Extension of the Maximum Likelihood Principle. New York: Springer, 1998;199-213.

2. Bao W., Kojima K.K., Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob. DNA. 2015;6(1):11. DOI 10.1186/s13100-015-0041-9.

3. Blankers T., Oh K.P., Bombarely A., Shaw K.L. The genomic architecture of a rapid island radiation: mapping chromosomal rearrangements and recombination rate variation in Laupala. bioRxiv. 2017; 160952. DOI 10.1101/160952.

4. Bouallègue M., Filée J., Kharrat I., Mezghani-Khemakhem M., Rouault J.D., Makni M., Capy P. Diversity and evolution of marinerlike elements in aphid genomes. BMC Genomics. 2017;18(1):1-12. DOI 10.1186/s12864-017-3856-6.

5. Brillet B., Bigot Y., Augé-Gouillou C. Assembly of the Tc1 and mariner transposition initiation complexes depends on the origins of their transposase DNA binding domains. Genetica. 2007;130(2):105-120. DOI 10.1007/s10709-006-0025-2.

6. Bui Q.T., Casse N., Leignel V., Nicolas V., Chénais B. Widespread occurrence of mariner transposons in coastal crabs. Mol. Phylogenet. Evol. 2008;47(3):1181-1189. DOI 10.1016/j.ympev.2008.03.029.

7. Bui Q.T., Delaurière L., Casse N., Nicolas V., Laulier M., Chénais B. Molecular characterization and phylogenetic position of a new mariner-like element in the coastal crab, Pachygrapsus marmoratus. Gene. 2007;396(2):248-256. DOI 10.1016/j.gene.2007.03.004.

8. Chevreux B., Pfisterer T., Drescher B., Driesel A.J., Müller W.E.G., Wetter T., Suhai S. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 2004;14(6):1147-1159. DOI 10.1101/gr.1917404.

9. Delaurière L., Chénais B., Hardivillier Y., Gauvry L., Casse N. Mariner transposons as genetic tools in vertebrate cells. Genetica. 2009; 137(1):9-17. DOI 10.1007/s10709-009-9370-2.

10. Dupeyron M., Leclercq S., Cerveau N., Bouchon D., Gilbert C. Horizontal transfer of transposons between and within crustaceans and insects. Mob. DNA. 2014;5(1):4. DOI 10.1186/1759-8753-5-4.

11. Emmons S.W., Yesner L., Ruan K.S., Katzenberg D. Evidence for a transposon in Caenorhabditis elegans. Cell. 1983;32(1):55-65.

12. Fernández-Medina R.D., Granzotto A., Ribeiro J.M., Carareto C.M.A. Transposition burst of mariner-like elements in the sequenced genome of Rhodnius prolixus. Insect Biochem. Mol. Biol. 2016;69: 14-24. DOI 10.1016/j.ibmb.2015.09.003.

13. Feschotte C., Pritham E.J. DNA transposons and the evolution of euka ryotic genomes. Annu. Rev. Genet. 2007;41(1):331-368. DOI 10.1146/annurev.genet.40.110405.090448.

14. Filée J., Rouault J.-D., Harry M., Hua-Van A. Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus. BMC Genomics. 2015;16:1061. DOI 10.1186/s12864-015-2060-9.

15. Green C.L., Frommer M. The genome of the Queensland fruit fly Bactrocera tryoni contains multiple representatives of the mariner family of transposable elements. Insect Mol. Biol. 2001;10(4): 371-386.

16. 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;83(22):8684-8688.

17. Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013;30(4):772-780. DOI 10.1093/molbev/mst010.

18. Lampe D.J., Churchill M.E., Robertson H.M. A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J. 1996; 15(19):5470-5479.

19. Lampe D.J., Witherspoon D.J., Soto-Adames F.N., Robertson H.M. Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. Mol. Biol. Evol. 2003;20(4):554-562. DOI 10.1093/molbev/msg069.

20. Lefort V., Longueville J.-E., Gascuel O. SMS: smart model selection in PhyML. Mol. Biol. Evol. 2017;34(9):2422-2424. DOI 10.1093/molbev/msx149.

21. Leroy H., Castagnone-Sereno P., Renault S., Augé-Gouillou C., Bigot Y., Abad P. Characterization of Mcmar1, a mariner-like element with large inverted terminal repeats (ITRs) from the phytoparasitic nematode Meloidogyne chitwoodi. Gene. 2003;304:35-41.

22. Lohe A.R., Moriyama E.N., Lidholm D.A., Hartl D.L. Horizontal transmission, vertical inactivation, and stochastic loss of marinerlike transposable elements. Mol. Biol. Evol. 1995;12(1):62-72. DOI 10.1093/oxfordjournals.molbev.a040191.

23. Loreto E.L.S., Carareto C.M.A., Capy P. Revisiting horizontal transfer of transposable elements in Drosophila. Heredity (Edinb.). 2008; 100(6):545-554. DOI 10.1038/sj.hdy.6801094.

24. Maruyama K., Hartl D.L. Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J. Mol. Evol. 1991;33(6):514-524.

25. McClintock B. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA. 1950;36(6):344-355. DOI 10.1073/pnas.36.6.344.

26. Montiel E.E., Cabrero J., Camacho J.P.M., López-León M.D. Gypsy, RTE and Mariner transposable elements populate Eyprepocnemis plorans genome. Genetica. 2012;140(7-9):365-374. DOI 10.1007/s10709-012-9686-1.

27. Oliveira S.G., Bao W., Martins C., Jurka J. Horizontal transfers of Mariner transposons between mammals and insects. Mob. DNA. 2012; 3(1):14. DOI 10.1186/1759-8753-3-14.

28. Peccoud J., Loiseau V., Cordaux R., Gilbert C. Massive horizontal transfer of transposable elements in insects. Proc. Natl. Acad. Sci. USA. 2017;114(18):4721-4726. DOI 10.1073/pnas.1621178114.

29. Plasterk R.H., Izsvák Z., Ivics Z. Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet. 1999;15(8):326-332.

30. Plasterk R.H.A., van Luenen H.G.A.M. The Tc1/Mariner family of transposable elements. In: Mobile DNA II. Washington, DC: American Society of Microbiology, 2002;519-532.

31. Ragonnet-Cronin M., Hodcroft E., Hué S., Fearnhill E., Delpech V., Brown A.J., Lycett S. Automated analysis of phylogenetic clusters. BMC Bioinformatics. 2013;14(1):317. DOI 10.1186/1471-2105-14-317.

32. Rice P., Longden I., Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet. 2000;16(6):276-277.

33. Robertson H.M. The mariner transposable element is widespread in insects. Nature. 1993;362(6417):241-245. DOI 10.1038/362241a0.

34. Robertson H.M. Multiple mariner transposons in flatworms and hydras are related to those of insects. J. Hered. 1997;88(3):195-201. DOI 10.1093/oxfordjournals.jhered.a023088.

35. Robertson H.M. Evolution of DNA transposons in eukaryotes. In: Mobile DNA II. Washington, DC: American Society of Microbiology, 2002;1093-1110.

36. Robertson H.M., Lampe D.J. Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol. Biol. Evol. 1995;12(5):850-862.

37. Robertson H.M., MacLeod E.G. Five major subfamilies of mariner transposable elements in insects, including the Mediterranean fruit fly, and related arthropods. Insect Mol. Biol. 1993;2(3):125-139.

38. Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61(3):539-542. DOI 10.1093/sysbio/sys029.

39. Schaack S., Gilbert C., Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol. Evol. 2010;25(9):537-546. DOI 10.1016/j.tree.2010.06.001.

40. Silva J.C., Bastida F., Bidwell S.L., Johnson P.J., Carlton J.M. A potentially functional mariner transposable element in the protist Trichomonas vaginalis. Mol. Biol. Evol. 2005;22(1):126-134. DOI 10.1093/molbev/msh260.

41. Silva J.C., Loreto E.L., Clark J.B. Factors that affect the horizontal transfer of transposable elements. Curr. Issues Mol. Biol. 2004;6(1): 57-71.

42. Tellier M., Bouuaert C.C., Chalmers R. Mariner and the ITm superfamily of transposons. Microbiol. Spectr. 2015;3(2):MDNA3-00332014. DOI 10.1128/microbiolspec.MDNA3-0033-2014.

43. Tevy F., Guzman N., Gonzalez G., Lia V., Poggio L., Confalonieri V.A. Mobile elements and inverted rearrangements in Trimerotropis pallidipennis (Orthoptera: Acrididae). Caryologia. 2007;60(3):212-221. DOI 10.1080/00087114.2007.10797939.

44. Tosi L.R., Beverley S.M. Cis and trans factors affecting Mos1 mariner evolution and transposition in vitro, and its potential for functional genomics. Nucleic Acids Res. 2000;28(3):784-790.

45. Wallau G.L., Capy P., Loreto E., Hua-Van A. Genomic landscape and evolutionary dynamics of mariner transposable elements within the Drosophila genus. BMC Genomics. 2014;15(1):1-19. DOI 10.1186/1471-2164-15-727.

46. Wallau G.L., Capy P., Loreto E., Le Rouzic A., Hua-Van A. VHICA, a new method to discriminate between vertical and horizontal transposon transfer: application to the Mariner family within Drosophila. Mol. Biol. Evol. 2016;33(4):1094-1109. DOI 10.1093/molbev/msv341.

47. Wang X., Fang X., Yang P., Jiang X., Jiang F., Zhao D., Li B., Cui F., Wei J., Ma C., Wang Y., He J., Luo Y., Wang Z., Guo X., Guo W., Wang X., Zhang Y., Yang M., Hao S., Chen B., Ma Z., Yu D., Xiong Z., Zhu Y., Fan D., Han L., Wang B., Chen Y., Wang J., Yang L., Zhao W., Feng Y., Chen G., Lian J., Li Q., Huang Z., Yao X., Lv N., Zhang G., Li Y., Wang J., Wang J., Zhu B., Kang L. The locust genome provides insight into swarm formation and long-distance flight. Nat. Commun. 2014;5:2957. DOI 10.1038/ncomms3957.

48. Wicker T., Sabot F., Hua-Van A., Bennetzen J.L., Capy P., Chalhoub B., Flavell A., Leroy P., Morgante M., Panaud O., Paux E., SanMiguel P., Schulman A.H. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 2007;8(12):973-982. DOI 10.1038/nrg2165.

49. Yoshiyama M., Tu Z., Kainoh Y., Honda H., Shono T., Kimura K. Possible horizontal transfer of a transposable element from host to parasitoid. Mol. Biol. Evol. 2001;18(10):1952-1958. DOI 10.1093/oxfordjournals.molbev.a003735.


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