Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-25T12:19:47.975Z Has data issue: false hasContentIssue false
  • English
  • Français

Curupira-1 and Curupira-2, two novel Mutator-like DNA transposons from the genomes of human parasites Schistosoma mansoni and Schistosoma japonicum

Published online by Cambridge University Press:  15 July 2011

DANIELE S. JACINTO ,
HELOISA DOS SANTOS MUNIZ ,
THIAGO M. VENANCIO ,
R. ALAN WILSON ,
SERGIO VERJOVSKI-ALMEIDA  and
RICARDO DEMARCO
DANIELE S. JACINTO
Affiliation:
Departamento de Física e Informática, Instituto de Física de São Carlos, Universidade de São Paulo, 13566-590 São Carlos, SP, Brazil
HELOISA DOS SANTOS MUNIZ
Affiliation:
Departamento de Física e Informática, Instituto de Física de São Carlos, Universidade de São Paulo, 13566-590 São Carlos, SP, Brazil
THIAGO M. VENANCIO
Affiliation:
Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, 05508-900 São Paulo, SP, Brazil
R. ALAN WILSON
Affiliation:
Centre for Immunology and Infection, Department of Biology, University of York, York YO10 5DD, UK
SERGIO VERJOVSKI-ALMEIDA
Affiliation:
Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, 05508-900 São Paulo, SP, Brazil
RICARDO DEMARCO*
Affiliation:
Departamento de Física e Informática, Instituto de Física de São Carlos, Universidade de São Paulo, 13566-590 São Carlos, SP, Brazil
*
*Corresponding author: Ricardo DeMarco. Departamento de Física e Informática, Instituto de Física de São Carlos, Universidade de São Paulo, Av. Trabalhador São Carlense, 400, 13566-590 São Carlos, SP, Brazil. Tel: +55 16 3373 8789. Fax: +55 16 3371 5381. E-mail: rdemarco@ifsc.usp.br
Get access Rights & Permissions [Opens in a new window]

Summary

Transposons of the Mutator superfamily have been widely described in plants, but only recently have metazoan organisms been shown to harbour them. In this work we describe novel Mutator superfamily transposons from the genomes of the human parasites Schistosoma mansoni and S. japonicum, which we name Curupira-1 and Curupira-2. Curupira elements do not have Terminal Inverted Repeats (TIRs) at their extremities and generate Target Site Duplications (TSDs) of 9 base pairs. Curupira-2 transposons code for a conserved transposase and SWIM zinc finger domains, while Curupira-1 elements comprise these same domains plus a WRKY zinc finger. Alignment of transcript sequences from both elements back to the genomes indicates that they are subject to splicing to produce mature transcripts. Phylogenetic analyses indicate that these transposons represent a new lineage of metazoan Mutator-like elements with characteristics that are distinct from the recently described Phantom elements. Description of these novel schistosome transposons provides new insights in the evolution of transposable elements in schistosomes.

Keywords

DNA transposonsplatyhelminthsrepetitive elementsgenome
Type
Research Article
Information
Parasitology , Volume 138 , Issue 9 , August 2011 , pp. 1124 - 1133
Copyright
Copyright © Cambridge University Press 2011

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

Almeida, L. and Portella, A. (2006). Brazilian folktales, Libraries Unlimited, Westport, USA.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., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G. and El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature, London 460, 352–358. doi: nature08160 [pii] 10.1038/nature08160.CrossRefGoogle ScholarPubMed
Chalvet, F., Grimaldi, C., Kaper, F., Langin, T. and Daboussi, M. J. (2003). Hop, an active Mutator-like element in the genome of the fungus Fusarium oxysporum. Molecular Biology and Evolution 20, 1362–1375. doi: 10.1093/molbev/msg155 msg155 [pii].CrossRefGoogle ScholarPubMed
Charlesworth, B., Sniegowski, P. and Stephan, W. (1994). The evolutionary dynamics of repetitive DNA in eukaryotes. Nature, London 371, 215–220. doi: 10.1038/371215a0.CrossRefGoogle ScholarPubMed
DeMarco, R., Venancio, T. M. and Verjovski-Almeida, S. (2006). SmTRC1, a novel Schistosoma mansoni DNA transposon, discloses new families of animal and fungi transposons belonging to the CACTA superfamily. BMC Evolutionary Biology 6, 89. doi: 1471-2148-6-89 [pii] 10.1186/1471-2148-6-89.CrossRefGoogle Scholar
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797. doi: 10.1093/Nar/Gkh340.CrossRefGoogle ScholarPubMed
Feschotte, C. (2004). Merlin, a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. Molecular Biology and Evolution 21, 1769–1780. doi: 10.1093/molbev/msh188 msh188 [pii].CrossRefGoogle Scholar
Feschotte, C. and Pritham, E. J. (2007). DNA transposons and the evolution of eukaryotic genomes. Annual Review of Genetics 41, 331–368. doi: 10.1146/annurev.genet.40.110405.090448.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704. doi: 54QHX07WB5K5XCX4 [pii].CrossRefGoogle ScholarPubMed
Hershberger, R. J., Benito, M. I., Hardeman, K. J., Warren, C., Chandler, V. L. and Walbot, V. (1995). Characterization of the major transcripts encoded by the regulatory MuDR transposable element of maize. Genetics 140, 1087–1098.CrossRefGoogle ScholarPubMed
Hua-Van, A. and Capy, P. (2008). Analysis of the DDE motif in the Mutator superfamily. Journal of Molecular Evolution 67, 670–681. doi: 10.1007/s00239-008-9178-1.CrossRefGoogle ScholarPubMed
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. doi: S0092-8674(00)80436-5 [pii].CrossRefGoogle ScholarPubMed
Kidwell, M. G. and Lisch, D. (1997). Transposable elements as sources of variation in animals and plants. Proceedings of the National Academy of Sciences, USA 94, 7704–7711.CrossRefGoogle ScholarPubMed
Le, S. Q. and Gascuel, O. (2008). An improved general amino acid replacement matrix. Molecular Biology and Evolution 25, 1307–1320. doi: msn067 [pii] 10.1093/molbev/msn067.CrossRefGoogle ScholarPubMed
Lisch, D. (2002). Mutator transposons. Trends in Plant Science 7, 498–504. doi: S1360138502023476 [pii].CrossRefGoogle ScholarPubMed
Lopes, F. R., Silva, J. C., Benchimol, M., Costa, G. G., Pereira, G. A. and Carareto, C. M. (2009). The protist Trichomonas vaginalis harbors multiple lineages of transcriptionally active Mutator-like elements. BMC Genomics 10, 330. doi: 1471-2164-10-330 [pii] 10.1186/1471-2164-10-330.CrossRefGoogle ScholarPubMed
Marquez, C. P. and Pritham, E. J. (2010). Phantom, a new subclass of Mutator DNA transposons found in insect viruses and widely distributed in animals. Genetics 185, 1507–1517. doi: genetics.110.116673 [pii] 10.1534/genetics.110.116673.CrossRefGoogle ScholarPubMed
Price, M. N., Dehal, P. S. and Arkin, A. P. (2010). FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490. doi: 10.1371/journal.pone.0009490.CrossRefGoogle ScholarPubMed
Pritham, E. J., Feschotte, C. and Wessler, S. R. (2005). Unexpected diversity and differential success of DNA transposons in four species of entamoeba protozoans. Molecular Biology and Evolution 22, 1751–1763. doi: msi169 [pii] 10.1093/molbev/msi169.CrossRefGoogle ScholarPubMed
Rossi, M., Araujo, P. G., de Jesus, E. M., Varani, A. M. and Van Sluys, M. A. (2004). Comparative analysis of Mutator-like transposases in sugarcane. Molecular Genetics and Genomics 272, 194–203. doi: 10.1007/s00438-004-1036-2.CrossRefGoogle ScholarPubMed
Smith, N. J. H. (1996). The Enchanted Amazon Rain Forest: Stories from a Vanishing World. University Press of Florida, Gainesville, FL, USA.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599. doi: 10.1093/molbev/msm092.CrossRefGoogle ScholarPubMed
Venancio, T. M., Wilson, R. A., Verjovski-Almeida, S. and DeMarco, R. (2010). Bursts of transposition from non-long terminal repeat retrotransposon families of the RTE clade in Schistosoma mansoni. International Journal for Parasitology 40, 743–749. doi: S0020-7519(09)00448-2 [pii] 10.1016/j.ijpara.2009.11.013.CrossRefGoogle ScholarPubMed
Wheelan, S. J., Church, D. M. and Ostell, J. M. (2001). Spidey: a tool for mRNA-to-genomic alignments. Genome Research 11, 1952–1957. doi: 10.1101/gr.195301.CrossRefGoogle ScholarPubMed
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. and Schulman, A. H. (2007). A unified classification system for eukaryotic transposable elements. Nature Reviews. Genetics 8, 973–982. doi: 10.1038/nrg2165.CrossRefGoogle ScholarPubMed
Xu, Z., Yan, X., Maurais, S., Fu, H., O'Brien, D. G., Mottinger, J. and Dooner, H. K. (2004). Jittery, a Mutator distant relative with a paradoxical mobile behavior: excision without reinsertion. Plant Cell 16, 1105–1114. doi: 10.1105/tpc.019802 tpc.019802 [pii].CrossRefGoogle ScholarPubMed
Zhou, Y., Zheng, H. J., Chen, Y. Y., Zhang, L., Wang, K., Guo, J., Huang, Z., Zhang, B., Huang, W., Jin, K., Dou, T. H., Hasegawa, M., Wang, L., Zhang, Y., Zhou, J., Tao, L., Cao, Z. W., Li, Y. X., Vinar, T., Brejova, B., Brown, D., Li, M., Miller, D. J., Blair, D., Zhong, Y., Chen, Z., Hu, W., Wang, Z. Q., Zhang, Q. H., Song, H. D., Chen, S. J., Xu, X. N., Xu, B., Ju, C., Huang, Y. C., Brindley, P. J., McManus, D. P., Feng, Z., Han, Z. G., Lu, G., Ren, S. X., Wang, Y. Z., Gu, W. Y., Kang, H., Chen, J., Chen, X. Y., Chen, S. T., Wang, L. J., Yan, J., Wang, B. Y., Lv, X. Y., Jin, L., Wang, B. F., Pu, S. Y., Zhang, X. L., Zhang, W., Hu, Q. P., Zhu, G. F., Wang, J., Yu, J., Wang, J., Yang, H. M., Ning, Z. M., Beriman, M., Wei, C. L., Ruan, Y. J., Zhao, G. P., Wang, S. Y., Liu, F., Wang, Z. Q., Zheng, H. J., Zhang, Q. H., Wang, S. Y. and Han, Z. G. (2009). The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature, London 460, 345–351. doi: 10.1038/Nature08140.Google Scholar