Transposable elements as a potential vectors for horizontal gene transfer in host-parasite system

O.I. Podgornaya and N.K. Galaktionov

Proceedings of the Zoological Institute RAS, 2009, 313(3): 283–296 · https://doi.org/10.31610/trudyzin/2009.313.3.283

Full text

Abstract

Horizontal gene transfer is one of the principle ways that maintain the genetic diversity in prokaryotes. However the genetic transfer between eukaryotes is assumptive. In light of this hypothesis DNA transposable elements are the likely candidates for the eukaryotic horizontally transmitted genetic elements. The directed horizontal transfer may only occur in the case of physical contact of organisms involved in this process. This sort of interaction takes place in host–parasite systems. Nowadays the hypothesis of horizontal gene transfer is based on the sequence similarity, sporadic distribution and conjectural ways of transposons transduction. However, all highly homologous elements found are inactive due to mutations within their ORFs. The percent of identity does not represent the origin of transposable element and therefore cannot testify to its transduction. Most of the transposable elements are inactive. Nevertheless the active copies may function as active mutators giving rise to genetic diversity under the ecological stress. In spite of the absence of direct proofs of horizontal gene transfer there are indirect data indicating that this process might occur many times in the course of eukaryotic evolution.

Key words

horizontal gene transfer, host–parasite system, transposons, genome, evolution

Submitted February 12, 2009 · Accepted June 1, 2009 · Published September 25, 2009

References

Abrusan G. and Krambeck H.J. 2006. Competition may determine the diversity of transposable elements. Theoretical Population Biology, 70: 364–375. https://doi.org/10.1016/j.tpb.2006.05.001

Andrake M.D. and Skalka A.M. 1996. Retroviral integrase, putting the pieces together. Journal of Biological Chemistry, 271: 19633–1966. https://doi.org/10.1074/jbc.271.33.19633

Arkhipova I. and Meselson M. 2000. Transposable elements in sexual and ancient asexual taxa. Proceedings of the National Academy of Sciences, 97: 14473–14477. https://doi.org/10.1073/pnas.97.26.14473

Buckler E.S., Gaut B.S. and McMullen M.D. 2006. Molecular and functional diversity of maize. Current Opinion in Plant Biology, 9: 172–176. https://doi.org/10.1016/j.pbi.2006.01.013

Capy P. 1998. Evolutionary biology. A plastic genome. Nature, 396: 522–523. https://doi.org/10.1038/25007

Capy P., Vitalis R., Langin T., Higuet D. and Bazin C. 1996. Relationships between transposable elements based upon the integrase-transposase domains: is there a common ancestor? Jounal of Molecular evolution, 42: 359–368. https://doi.org/10.1007/BF02337546

Cooper M.D. and Alder M.N. 2006. The evolution of adaptive immune systems. Cell, 124: 815–822. https://doi.org/10.1016/j.cell.2006.02.001

Dawson A.E., Hartswood T.P. and Finnegan D. 1997. A LINE-like transposable element in Drosophila, the I factor, encodes a protein with properties similar to those of retroviral nucleocapsids. EMBO Journal, 16: 4448–4455. https://doi.org/10.1093/emboj/16.14.4448

Doolittle W.F. and Sapienza C. 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature, 284: 601–603. https://doi.org/10.1038/284601a0

Feschotte C. and Pritham E.J. 2007. DNA transposons and the evolution of eukaryotic genomes. Annual Review of Genetics, 41: 331–368. https://doi.org/10.1146/annurev.genet.40.110405.090448

Feschotte C. and Wessler S.R. 2001. Treasures in the attic: rolling circle transposons discovered in eukaryotic genomes. Proceedings of the National Academy of Sciences, 98: 8923–8924. https://doi.org/10.1073/pnas.171326198

Garcia-Fernandez J., Marfany G., Baguna J. and Salo E. 1993 . Infiltration of mariner elements. Nature, 8: 109–110. https://doi.org/10.1038/364109b0

Garcia-Fernandez J., Bayascas-Ramirez J.R., Marfany G., Munoz-Marmol A.M., Casali A., Baguna J. and Salo E. 1995. High copy number of highly similar mariner-like transposons in planarian (Platyhelminthe): evidence for a trans-phyla horizontal transfer. Molecular Biology and Evolution, 12: 421–431.

Fried B. and Rosa-Brunet L.C. 1991. Exposure of Dugesia tigrina (Turbellaria) to cercariae of Echinostoma trivolvis and Echinostoma caproni (Trematoda). Journal of Parasitology, 77: 113–116. https://doi.org/10.2307/3282568

Galaktionov N.K., O.I. Podgornaya and Fedorov A.V. 2009 (in press). Characterization of mariner transposable element from the genome of Himasthla elongata. Cell and Tissue Biology, 3. https://doi.org/10.1134/S1990519X09060042

Gogarten J.P., Doolittle W.F. and Lawrence J.G. 2002. Prokaryotic evolution in light of gene transfer. Molecular Biology and Evolution, 19: 2226–2238. https://doi.org/10.1093/oxfordjournals.molbev.a004046

Haig D. 2004. The (dual) origin of epigenetics. Cold Spring Harb. Symp. Quantitative Biology, 69: 67–70. https://doi.org/10.1101/sqb.2004.69.67

Harris J.W., Strong D.D., Amoui M., Baylink D.J. and Lau K.H. 2002. Construction of a Tc1-like transposon Sleeping Beauty-based gene transfer plasmid vector for generation of stable transgenic mammalian cell clones. Analytical Biochemistry, 310: 15–26. https://doi.org/10.1016/S0003-2697(02)00316-0

Hartl D.L. 1997. Mariner sails into Leishmania. Science, 276: 1659–1660. https://doi.org/10.1126/science.276.5319.1659

Hickey D.A. 1982. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics, 101: 519–531. https://doi.org/10.1093/genetics/101.3-4.519

Holligan D., Zhang X., Jiang N., Pritham E.J. and Wessler S.R. 2006. The transposable element landscape of the model legume Lotus japonicus. Genetics, 174: 2215–2228. https://doi.org/10.1534/genetics.106.062752

Ivics Z., Hackett P.B., Plasterk R.H. and Izsvak Z. 1997. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell, 91: 501–510. https://doi.org/10.1016/S0092-8674(00)80436-5

Kapitonov V.V. and Jurka J. 2008. A universal classification of eukaryotic transposable elements implemented in Repbase. Nature Reviews Genetics, 9: 411–412. https://doi.org/10.1038/nrg2165-c1

Keng V.W., Yae K., Hayakawa T., Mizuno S., Uno Y., Yusa K., Kokubu C., Kinoshita T., Akagi K., Jenkins N.A., Copeland N.G., Horie K. and Takeda J. 2005. Region-specific saturation germline mutagenesis in mice using the Sleeping Beauty transposon system. Nature Methods, 2: 763–769. https://doi.org/10.1038/nmeth795

Koga A., Iida A., Hori H., Shimada A. and Shima A. 2006. Vertebrate DNA transposon as a natural mutator: the medaka fish Tol2 element contributes to genetic variation without recognizable traces. Molecular Biology and Evolution, 23: 1414–1419. https://doi.org/10.1093/molbev/msl003

Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C. et al. 2001. Initial sequencing and analysis of the human genome. Nature, 409: 860–921.

Lawrence J.G. and Hartl D.L. 1992. Inference of horizontal genetic transfer from molecular data: an approach using the bootstrap. Genetics, 131: 753–760. https://doi.org/10.1093/genetics/131.3.753

Leaver M.J. 2001. A family of Tc1-like transposons from the genomes of fishes and frogs: evidence for horizontal transmission. Gene, 271: 203–214. https://doi.org/10.1016/S0378-1119(01)00530-3

Lerat E., Brunet F., Bazin C. and Capy P. 2000. Is the evolution of transposable elements modular? Genetica, 107: 15–25. https://doi.org/10.1007/978-94-011-4156-7_3

Liu D., Bischerour J., Siddique A., Buisine N., Bigot Y. and Chalmers R. 2007. The human SETMAR protein preserves most of the activities of the ancestral Hsmar1 transposase. Molecular and Cellular Biology, 27: 1125–1132. https://doi.org/10.1128/MCB.01899-06

Lohe A.R., Moriyama E.N., Lidholm D.A. and Hartl D.L. 1995. Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Molecular Biology and Evolution, 12: 62–72. https://doi.org/10.1093/oxfordjournals.molbev.a040191

Maruyama K. and Hartl D.L. 1991. Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. Journal of Molecular Evolution, 33: 514–524. https://doi.org/10.1007/BF02102804

Manuelidis L. 1990. A view of interphase chromosomes. Science, 250: 1533–1540. https://doi.org/10.1126/science.2274784

McClintock B. 1951. Chromosome organization and genic expression. Cold Spring Harbor Symposia on Quantitative Biology, 16: 13–47. https://doi.org/10.1101/SQB.1951.016.01.004

McClintock B. 1956. Controlling elements and the gene. Cold Spring Harbor Symposia on Quantitative Biology, 21: 197–216. https://doi.org/10.1101/SQB.1956.021.01.017

Miskey C., Izsvák Z., Kawakami K. and Ivics Z. 2005. DNA transposons in vertebrate functional genomics. Cellular and Molecular Life Sciences, 62: 629-641. https://doi.org/10.1007/s00018-004-4232-7

Nakashima K., Yamada L., Satou Y., Azuma J.-I. and Satoh N. 2004. The evolutionary origin of animal cellulose synthase. Development Genes and Evolution, 214: 81–88. https://doi.org/10.1007/s00427-003-0379-8

Pritham E.J. and Feschotte C. 2006. Mobile DNA: genomes under the influence. Genome Biology, 7: 320. https://doi.org/10.1186/gb-2006-7-6-320

Robertson H.M. 1993. The mariner transposable element is widespread in insects. Nature, 362: 241–245. https://doi.org/10.1038/362241a0

Robertson H.M. and MacLeod E.G. 1993. Five major subfamilies of mariner transposable elements in insects, including the Mediterranean fruit fly, and related arthropods. Insect Molecular Biology, 2: 125–139. https://doi.org/10.1111/j.1365-2583.1993.tb00132.x

Robertson H.M. and Lampe D.J. 1995. Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Molecular Biology and Evolution, 12: 850–862.

Robertson H.M. 1997. Multiple Mariner transposons in flatworms and hydras are related to those of insects. Journal of Heredity, 88: 195–201. https://doi.org/10.1093/oxfordjournals.jhered.a023088

Robertson H.M. and Martos R. 1997. Molecular evolution of the second ancient human mariner transposon, Hsmar2, illustrates patterns of neutral evolution in the human genome lineage. Gene, 205: 219–228. https://doi.org/10.1016/S0378-1119(97)00471-X

Robertson H.M. and Zumpano K.L. 1997. Molecular evolution of an ancient mariner transposon, Hsmar1, in the human genome. Gene, 205: 203–217. https://doi.org/10.1016/S0378-1119(97)00472-1

Sedensky M.M., Hudson S.J., Everson B. and Morgan P.G. 1994. Identification of a mariner-like repetitive sequence in C. elegans. Nucleic Acids Research, 22: 1719–1723. https://doi.org/10.1093/nar/22.9.1719

Sijen T. and Plasterk R.H. 2003. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature, 426: 310–314. https://doi.org/10.1038/nature02107

Slotkin R.K. and Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics, 8: 272–285. https://doi.org/10.1038/nrg2072

Yoshiyama M., Tu Z., Kainoh Y., Honda H., Shono T. and Kimura K. 2001. Possible horizontal transfer of a transposable element from host to parasitoid. Molecular Biology and Evolution, 18: 1952–1958. https://doi.org/10.1093/oxfordjournals.molbev.a003735