Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-24T23:00:02.171Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolutionary characterization of Ty3/gypsy-like LTR retrotransposons in the parasitic cestode Echinococcus granulosus

Published online by Cambridge University Press:  30 August 2016

YOUNG-AN BAE
YOUNG-AN BAE*
Affiliation:
Department of Microbiology, Gachon University College of Medicine, 191 Hambakmoe-ro, Yeonsu-gu, Incheon 21936, Republic of Korea
*
*Corresponding author: Department of Microbiology, Gachon University College of Medicine, 191 Hambakmoe-ro, Yeonsu-gu, Incheon 21936, Korea. E-mail: yabae03@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Cyclophyllidean cestodes including Echinococcus granulosus have a smaller genome and show characteristics such as loss of the gut, a segmented body plan, and accelerated growth rate in hosts compared with other tissue-invading helminths. In an effort to address the molecular mechanism relevant to genome shrinkage, the evolutionary status of long-terminal-repeat (LTR) retrotransposons, which are known as the most potent genomic modulators, was investigated in the E. granulosus draft genome. A majority of the E. granulosus LTR retrotransposons were classified into a novel characteristic clade, named Saci-2, of the Ty3/gypsy family, while the remaining elements belonged to the CsRn1 clade of identical family. Their nucleotide sequences were heavily corrupted by frequent base substitutions and segmental losses. The ceased mobile activity of the major retrotransposons and the following intrinsic DNA loss in their inactive progenies might have contributed to decrease in genome size. Apart from the degenerate copies, a gag gene originating from a CsRn1-like element exhibited substantial evidences suggesting its domestication including a preserved coding profile and transcriptional activity, the presence of syntenic orthologues in cestodes, and selective pressure acting on the gene. To my knowledge, the endogenized gag gene is reported for the first time in invertebrates, though its biological function remains elusive.

Keywords

Echinococcus granulosuslong-terminal-repeat retrotransposonSaci-2 cladegenome sizedomestication of gag gene
Type
Research Article
Information
Parasitology , Volume 143 , Issue 13 , November 2016 , pp. 1691 - 1702
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bae, Y. A., Moon, S. Y., Kong, Y., Cho, S. Y. and Rhyu, M. G. (2001). CsRn1, a novel active retrotransposon in a parasitic trematode, Clonorchis sinensis, discloses a new phylogenetic clade of Ty3/gypsy-like LTR retrotransposons. Molecular Biology and Evolution 18, 1474–1483.Google Scholar
Bae, Y. A., Ahn, J. S., Kim, S. H., Rhyu, M. G., Kong, Y. and Cho, S. Y. (2008). PwRn1, a novel Ty3/gypsy-like retrotransposon of Paragonimus westermani: molecular characters and its differentially preserved mobile potential according to host chromosomal polyploidy. BMC Genomics 9, 482.Google Scholar
Bennett, H. M., Mok, H. P., Gkrania-Klotsas, E., Tsai, I. J., Stanley, E. J., Antoun, N. M., Coghlan, A., Harsha, B., Traini, A., Ribeiro, D. M., Steinbiss, S., Lucas, S. B., Allinson, K. S., Price, S. J., Santarius, T. S., Carmichael, A. J., Chiodini, P. L., Holroyd, N., Dean, A. F. and Berriman, M. (2014). The genome of the sparganosis tapeworm Spirometra erinaceieuropaei isolated from the biopsy of a migrating brain lesion. Genome Biology 15, 510.Google Scholar
Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A. et al. (2009). The genome of the blood fluke Schistosoma mansoni . Nature 460, 352–358.CrossRefGoogle ScholarPubMed
Blumenstiel, J. P. (2011). Evolutionary dynamics of transposable elements in a small RNA world. Trends in Genetics 27, 23–31.CrossRefGoogle Scholar
Boeke, J. D. and Stoye, J. P. (1997). Retrotransposons, endogenous retroviruses, and the evolution of retroelements. In Retroviruses (ed. Coffin, J. M., Hughes, S. H. and Varmus, H. E.), pp. 343–435. Cold Spring Harbor Laboratory Press, New York.Google ScholarPubMed
Capy, P. (2005). Classsification and nomenclature of retrotransposable elements. Cytogenetic and Genome Research 110, 457–461.CrossRefGoogle Scholar
Collins, J. J. 3rd, Wang, B., Lambrus, B. G., Tharp, M. E., Iyer, H. and Newmark, P. A. (2013). Adult somatic stem cells in the human parasite Schistosoma mansoni . Nature 494, 476–479.CrossRefGoogle ScholarPubMed
Charlesworth, B. and Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annual Review of Genetics 23, 251–287.Google Scholar
Craig, P. S., McManus, D. P., Lightowlers, M. W., Chabalgoity, J. A., Garcia, H. H., Gavidia, C. M., Gilman, R. H., Gonzalez, A. E., Lorca, M., Naquira, C., Nieto, A. and Schantz, P. M. (2007). Prevention and control of cystic echinococcosis. Lancet Infectious Diseases 7, 385–394.Google Scholar
da Silva, A. M. (2010). Human echinococcosis: a neglected disease. Gastroenterology Research and Practice 2010, 583297.Google Scholar
DeMarco, R., Kowaltowski, A. T., Machado, A. A., Soares, M. B., Gargioni, C., Kawano, T., Rodrigues, V., Madeira, A. M., Wilson, R. A., Menck, C. F., Setubal, J. C., Dias-Neto, E., Leite, L. C. and Verjovski-Almeida, S. (2004). Saci-1, -2, and -3 and Perere, four novel retrotransposons with high transcriptional activities from the human parasite Schistosoma mansoni . Journal of Virology 78, 2967–2978.CrossRefGoogle ScholarPubMed
Dufresne, F. and Jeffery, N. (2011). A guided tour of large genome size in animals: what we know and where we are heading. Chromosome Research 19, 925–938.Google Scholar
Gorelick, R. J., Henderson, L. E., Hanser, J. P. and Rein, A. (1988). Point mutants of Moloney murine leukemia virus that fail to package viral RNA: evidence for specific RNA recognition by a “zinc finger-like” protein sequence. Proceedings of the National Academy of Sciences of the United States of America 85, 8420–8424.Google Scholar
Haig, D. (2012). Retroviruses and the placenta. Current Biology 22, R609–R613.Google Scholar
Harigaya, Y., Tanaka, H., Yamanaka, S., Tanaka, K., Watanabe, Y., Tsutsumi, C., Chikashige, Y., Hiraoka, Y., Yamashita, A. and Yamamoto, M. (2006). Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442, 45–50.CrossRefGoogle ScholarPubMed
Huang, Y., Chen, W., Wang, X., Liu, H., Chen, Y., Guo, L., Luo, F., Sun, J., Mao, Q., Liang, P., Xie, Z., Zhou, C., Tian, Y., Lv, X., Huang, L., Zhou, J., Hu, Y., Li, R., Zhang, F., Lei, H., Li, W., Hu, X., Liang, C., Xu, J., Li, X. and Yu, X. (2013). The carcinogenic liver fluke, Clonorchis sinensis: new assembly, reannotation and analysis of the genome and characterization of tissue transcriptomes. PLoS ONE 8, e54732.Google Scholar
Jenkins, D. J., Romig, T. and Thompson, R. C. (2005). Emergence/re-emergence of Echinococcus spp.-a global update. International Journal for Parasitology 35, 1205–1219.Google Scholar
Jiang, K. and Goertzen, L. R. (2011). Spliceosomal intron size expansion in domesticated grapevine (Vitis vinifera). BMC Research Notes 4, 52.Google Scholar
Kidwell, M. G. (2002). Transposable elements and the evolution of genome size in eukaryotes. Genetica 115, 49–63.Google Scholar
Koziol, U., Radio, S., Smircich, P., Zarowiecki, M., Fernández, C. and Brehm, K. (2015). A novel terminal-repeat retrotransposon in miniature (TRIM) is massively expressed in Echinococcus multilocularis stem cells. Genome Biology and Evolution 7, 2136–2153.Google Scholar
Lavergne, S., Muenke, N. J. and Molofsky, J. (2010). Genome size reduction can trigger rapid phenotypic evolution in invasive plants. Annals of Botany 105, 109–116.Google Scholar
Littlewood, D. T. J. (2006). The evolution of parasitism in flatworms. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 1–36. CABI Pub., Cambridge.Google Scholar
Lochmann, T. L., Bann, D. V., Ryan, E. P., Beyer, A. R., Mao, A., Cochrane, A. and Parent, L. J. (2013). NC-mediated nucleolar localization of retroviral Gag proteins. Virus Research 171, 304–318.Google Scholar
Long, A. D., Lyman, R. F., Morgan, A. H., Langley, C. H. and Mackay, T. F. (2000). Both naturally occurring insertions of transposable elements and intermediate frequency polymorphisms at the achaete-scute complex are associated with variation in bristle number in Drosophila melanogaster . Genetics 154, 1255–1269.Google Scholar
Maldonado, J. O., Martin, J. L., Mueller, J. D., Zhang, W. and Mansky, L. M. (2014). New insights into retroviral Gag-Gag and Gag-membrane interactions. Frontiers in Microbiology 5, 302.Google Scholar
Malik, H. S. and Eickbush, T. H. (1999). Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. Journal of Virology 73, 5186–5190.Google Scholar
McDonald, J. F. (1990). Macroevolution and retroviral elements. Bioscience 40, 183–191.CrossRefGoogle Scholar
Muriaux, D., Costes, S., Nagashima, K., Mirro, J., Cho, E., Lockett, S. and Rein, A. (2004). Role of murine leukemia virus nucleocapsid protein in virus assembly. Journal of Virology 78, 12378–12385.Google Scholar
Oliver, M. J., Petrov, D., Ackerly, D., Falkowski, P. and Schofield, O. M. (2007). The mode and tempo of genome size evolution in eukaryotes. Genome Research 17, 594–601.Google Scholar
Olson, P. D. and Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic platyhelminthes. Advances in Parasitology 60, 165–243.CrossRefGoogle ScholarPubMed
Olson, P. D., Zarowiecki, M., Kiss, F. and Brehm, K. (2012). Cestode genomics-progress and prospects for advancing basic and applied aspects of flatworm biology. Parasite Immunology 34, 130–150.Google Scholar
Page, R. D. (1996). Tree View: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google Scholar
Petrov, D. A., Lozovskaya, E. R. and Hartl, D. L. (1996). High intrinsic rate of DNA loss in Drosophila . Nature 384, 346–349.CrossRefGoogle ScholarPubMed
Protasio, A. V., Tsai, I. J., Babbage, A., Nichol, S., Hunt, M., Aslett, M. A., De Silva, N., Velarde, G. S., Anderson, T. J., Clark, R. C., Davidson, C., Dillon, G. P., Holroyd, N. E., LoVerde, P. T., Lloyd, C., McQuillan, J., Oliveira, G., Otto, T. D., Parker-Manuel, S. J., Quail, M. A., Wilson, R. A., Zerlotini, A., Dunne, D. W. and Berriman, M. (2012). A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni . PLoS Neglected Tropical Diseases 6, e1455.Google Scholar
Schulman, A. H. (2012). Hitching a ride: nonautonomous retrotransposons and parasitism as a lifestyle; Plant transposable elements: impact on genome structure and function. Topics in Current Genetics 24, 71–88.Google Scholar
Sinzelle, L., Izsvák, Z. and Ivics, Z. (2009). Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cellular and Molecular Life Sciences 66, 1073–1093.Google Scholar
Smyth, J. D. and McManus, D. P. (1989). The Physiology and Biochemistry of Cestodes. Cambridge University Press, Cambridge.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2727–2729.Google Scholar
Thompson, R. C. and McManus, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus . Trends in Parasitology 18, 452–457.CrossRefGoogle ScholarPubMed
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Tsai, I. J., Zarowiecki, M., Holroyd, N., Garciarrubio, A., Sanchez-Flores, A., Brooks, K. L., Tracey, A., Bobes, R. J., Fragoso, G., Sciutto, E., Aslett, M., Beasley, H., Bennett, H. M., Cai, J., Camicia, F., Clark, R., Cucher, M., De Silva, N., Day, T. A., Deplazes, P., Estrada, K., Fernández, C., Holland, P. W., Hou, J., Hu, S., Huckvale, T., Hung, S. S., Kamenetzky, L., Keane, J. A., Kiss, F. et al. (2013). The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63.Google Scholar
Volff, J. N. (2006). Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28, 913–922.Google Scholar
Volff, J. N., Bouneau, L., Ozouf-Costaz, C. and Fischer, C. (2003). Diversity of retrotransposable elements in compact pufferfish genomes. Trends in Genetics 19, 674–678.Google Scholar
Wang, X., Chen, W., Huang, Y., Sun, J., Men, J., Liu, H., Luo, F., Guo, L., Lv, X., Deng, C., Zhou, C., Fan, Y., Li, X., Huang, L., Hu, Y., Liang, C., Hu, X., Xu, J. and Yu, X. (2011). The draft genome of the carcinogenic human liver fluke Clonorchis sinensis . Genome Biology 12, R107.Google Scholar
Wang, B., Collins, J. J. 3rd and Newmark, P. A. (2013). Functional genomic characterization of neoblast-like stem cells in larval Schistosoma mansoni . Elife 2, e00768.Google Scholar
Xiong, Y. and Eickbush, T. H. (1990). Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO Journal 9, 3353–3362.Google Scholar
Zheng, H., Zhang, W., Zhang, L., Zhang, Z., Li, J., Lu, G., Zhu, Y., Wang, Y., Huang, Y., Liu, J., Kang, H., Chen, J., Wang, L., Chen, A., Yu, S., Gao, Z., Jin, L., Gu, W., Wang, Z., Zhao, L., Shi, B., Wen, H., Lin, R., Jones, M. K., Brejova, B., Vinar, T., Zhao, G., McManus, D. P., Chen, Z., Zhou, Y. et al. (2013). The genome of the hydatid tapeworm Echinococcus granulosus . Nature Genetics 45, 1168–1175.Google Scholar
Supplementary material: File

Bae supplementary material

Figures S1-S2

Download Bae supplementary material(File)
File 889.7 KB
Supplementary material: File

Bae supplementary material

Tables S1-S3

Download Bae supplementary material(File)
File 29.3 KB