Structural variations generated by simian foamy virus-like (SFV) in Crocodylus siamensis

Abstract

Endogenous retrovirus (ERV) integrates into the germline of its host and could remain in the genome as a molecular fossil. ERV is one of sources that cause INDEL and recombination events in the vertebrate genomes, leading to various genomic and genetic changes in their hosts. There have been many studies conducted on ERVs in the vertebrate genomes to elucidate their evolutionary history. However, ERVs have not been studied well in Crocodylus siamensis. Here, we report structural variations among SFV1 elements (simian foamy virus-like), ERVs in C. siamensis. We initially identified 26 SFV1 candidates in the genome and experimentally verified 9 SFV1_1 and 5 SFV1_10 elements using PCR display. Their structural analyses showed that most of them are solitary-LTRs but two SFV1_1 elements are full-length. Through further analyses, we found that the two full-length elements retain intact ORFs. We examined transcription factor binding sites within their LTR sequences to predict promoter/enhancer activities. In sum, we identified 14 crocodile-specific SFV1 elements and the results of their structural analyses suggest that they could contribute to genomic or phenotypic variations in C. siamensis population.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Belshaw R, Pereira V, Katzourakis A, Talbot G, Paces J, Burt A, Tristem M (2004) Long-term reinfection of the human genome by endogenous retroviruses. Proc Natl Acad Sci USA 101:4894–4899

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Bohne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff JN (2008) Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 16:203–215

    Article  PubMed  Google Scholar 

  3. Brochu CA (2000) Phylogenetic relationships and divergence timing of crocodylus based on morphology andthe fossil record. Copeia 2000:657–673

    Article  Google Scholar 

  4. Chong AY, Kojima KK, Jurka J, Ray DA, Smit AF, Isberg SR, Gongora J (2014) Evolution and gene capture in ancient endogenous retroviruses: insights from the crocodilian genomes. Retrovirology 11:71

    Article  PubMed  PubMed Central  Google Scholar 

  5. Chong AY, Kjeldsen SR, Gongora J (2015) Surveys of endogenous retroviruses (ERVs) in the freshwater crocodile (Crocodylus johnstoni) suggest that ERVs in Crocodylus spp. vary between species. Virus Genes 50:329–332

    CAS  Article  PubMed  Google Scholar 

  6. Cui P, Lober U, Alquezar-Planas DE, Ishida Y, Courtiol A, Timms P, Johnson RN, Lenz D, Helgen KM, Roca AL et al (2016) Comprehensive profiling of retroviral integration sites using target enrichment methods from historical koala samples without an assembled reference genome. PeerJ 4:e1847

    Article  PubMed  PubMed Central  Google Scholar 

  7. Dinets V (2013) Long-distance signaling in Crocodylia. Copeia 3:517–526

    Article  Google Scholar 

  8. Fujiwara T, Mizuuchi K (1988) Retroviral DNA integration: structure of an integration intermediate. Cell 54:497–504

    CAS  Article  PubMed  Google Scholar 

  9. Goff SP (2007) Host factors exploited by retroviruses. Nat Rev Microbiol 5:253–263

    CAS  Article  PubMed  Google Scholar 

  10. Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, Vandewege MW, St John JA, Capella-Gutierrez S, Castoe TA et al (2014) Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346:1254449

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hall TA (1999) BioEdit: a user-friendly biolodgical sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Sympos 41:95–98

    CAS  Google Scholar 

  12. Hugall AF, Foster R, Lee MS (2007) Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Syst Biol 56:543–563

    CAS  Article  PubMed  Google Scholar 

  13. Jern P, Sperber GO, Blomberg J (2005) Use of endogenous retroviral sequences (ERVs) and structural markers for retroviral phylogenetic inference and taxonomy. Retrovirology 2:50

    Article  PubMed  PubMed Central  Google Scholar 

  14. Johnson WE, Coffin JM (1999) Constructing primate phylogenies from ancient retrovirus sequences. Proc Natl Acad Sci USA 96:10254–10260

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 275–282

  16. Kapitonov VV, Jurka J (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 9:411–412 (author reply 414)

    Article  PubMed  Google Scholar 

  17. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ (2004) The UCSC table browser data retrieval tool. Nucleic Acids Res 32:D493–D496

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Mol Evol Int J Org Evol 16:111–120

    CAS  Article  Google Scholar 

  19. Lee J, Mun S, Kim DH, Cho CS, Oh DY, Han K (2017) Chicken (Gallus gallus) endogenous retrovirus generates genomic variations in the chicken genome. Mob DNA 8:2

    Article  PubMed  PubMed Central  Google Scholar 

  20. Llorens C, Fares MA, Moya A (2008) Relationships of gag-pol diversity between Ty3/Gypsy and Retroviridae LTR retroelements and the three kings hypothesis. BMC Evol Biol 8:276

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lower R, Lower J, Kurth R (1996) The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences. Proc Natl Acad Sci USA 93:5177–5184

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Magiorkinis G, Gifford RJ, Katzourakis A, De Ranter J, Belshaw R (2012) Env-less endogenous retroviruses are genomic superspreaders. Proc Natl Acad Sci USA 109:7385–7390

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. McCarthy EM, McDonald JF (2004) Long terminal repeat retrotransposons of Mus musculus. Genome Biol 5:R14

    Article  PubMed  PubMed Central  Google Scholar 

  24. McVey M, Lee SE (2008) MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet 24:529–538

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Mun S, Lee J, Kim YJ, Kim HS, Han K (2014) Chimpanzee-specific endogenous retrovirus generates genomic variations in the chimpanzee genome. PLoS ONE 9:e101195

    Article  PubMed  PubMed Central  Google Scholar 

  26. Nelson PN, Hooley P, Roden D, Davari Ejtehadi H, Rylance P, Warren P, Martin J, Murray PG, Molecular Immunology Research Group (2004) Human endogenous retroviruses: transposable elements with potential? Clin Exp Immunol 138:1–9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Pray LA (2008) Transposons: the jumping genes. Nat Educ 1:204

    Google Scholar 

  28. Roos J, Aggarwal RK, Janke A (2007) Extended mitogenomic phylogenetic analyses yield new insight into crocodylian evolution and their survival of the cretaceous-tertiary boundary. Mol Phylogenet Evol 45:663–673

    CAS  Article  PubMed  Google Scholar 

  29. Ross JP (1988) Crocodiles, 2nd edn. IUCN, Gland

    Google Scholar 

  30. Ross FD, Mayer GC (1983) On the dorsal armor of the Crocodilia. Adv Herpetol Evol Biol 305–331

  31. Shin W, Lee J, Son SY, Ahn K, Kim HS, Han K (2013) Human-specific HERV-K insertion causes genomic variations in the human genome. PLoS ONE 8:e60605

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Sperber G, Lovgren A, Eriksson NE, Benachenhou F, Blomberg J (2009) RetroTector online, a rational tool for analysis of retroviral elements in small and medium size vertebrate genomic sequences. BMC Bioinform 10(Suppl 6):S4

    Article  Google Scholar 

  33. Srikulnath K, Thongpan A, Suputtitada S, Apisitwanich S (2012) New haplotype of the complete mitochondrial genome of Crocodylus siamensis and its species-specific DNA markers: distinguishing C. siamensis from C. porosus in Thailand. Mol Biol Rep 39:4709–4717

    CAS  Article  PubMed  Google Scholar 

  34. Srikulnath K, Thapana W, Muangmai N (2015) Role of chromosome changes in Crocodylus evolution and diversity. Genom Inform 13:102–111

    Article  Google Scholar 

  35. St John JA, Braun EL, Isberg SR, Miles LG, Chong AY, Gongora J, Dalzell P, Moran C, Bed’hom B, Abzhanov A et al (2012) Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes. Genome Biol 13:415

    Article  PubMed  PubMed Central  Google Scholar 

  36. Stocking C, Kozak CA (2008) Murine endogenous retroviruses. Cell Mol Life Sci 65:3383–3398

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Stoye JP (2001) Endogenous retroviruses: still active after all these years? Curr Biol 11:R914–916

    CAS  Article  PubMed  Google Scholar 

  38. Supikamolseni A, Ngaoburanawit N, Sumontha M, Chanhome L, Suntrarachun S, Peyachoknagul S, Srikulnath K (2015) Molecular barcoding of venomous snakes and species-specific multiplex PCR assay to identify snake groups for which antivenom is available in Thailand. Genet Mol Res 14:13981–13997

    CAS  Article  PubMed  Google Scholar 

  39. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Tsangaras K, Mayer J, Alquezar-Planas DE, Greenwood AD (2015) An evolutionarily young polar bear (Ursus maritimus) endogenous retrovirus identified from next generation sequence data. Viruses 7:6089–6107

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Vizcaino C, Mansilla S, Portugal J (2015) Sp1 transcription factor: a long-standing target in cancer chemotherapy. Pharmacol Ther 152:111–124

    CAS  Article  PubMed  Google Scholar 

  42. Weiss RA (2006) The discovery of endogenous retroviruses. Retrovirology 3:67

    Article  PubMed  PubMed Central  Google Scholar 

  43. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982

    CAS  Article  PubMed  Google Scholar 

  44. Zhang X, Diab IH, Zehner ZE (2003) ZBP-89 represses vimentin gene transcription by interacting with the transcriptional activator, Sp1. Nucleic Acids Res 31:2900–2914

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The present work was conducted with funding from the Research Fund of Dankook University in 2015.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kyudong Han.

Ethics declarations

Conflict of interest

Panupon Twilprawat declares that he/she does not have conflict of interest. Songmi Kim declares that he/she does not have conflict of interest. Kornsorn Srikulnath declares that he/she does not have conflict of interest. Kyudong Han declares that he/she does not have conflict of interest.

Ethical approval

Animal care and all experimental procedures were approved by the Animal Experiment Committee, Kasetsart University, Thailand (approval no. ACKU04959), and conducted according to the Regulations on Animal Experiments at Kasetsart University.

Electronic supplementary material

Below is the link to the electronic supplementary material.

13258_2017_581_MOESM1_ESM.pptx

Supplementary Fig. 1 Cladogram between the SFV1_1 and SFV1_10 subfamilies.The maximum-likelihood cladogram of SFV1_1 and SFV1_10 subfamilies was constructed using 14 LTR sequences from SFV1 elements. The pink and green highlights represent SFV1_1 and SFV1_10 subfamilies, respectively. The red- and green-colored characters indicate SFV1_1 and SFV1_10 consensus LTR sequences, respectively. (PPTX 117 KB)

Supplementary material 2 (XLSX 10 KB)

Supplementary material 3 (XLSX 16 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Twilprawat, P., Kim, S., Srikulnath, K. et al. Structural variations generated by simian foamy virus-like (SFV) in Crocodylus siamensis . Genes Genom 39, 1129–1138 (2017). https://doi.org/10.1007/s13258-017-0581-0

Download citation

Keywords

  • Crocodylus siamensis
  • Endogenous retrovirus (ERV)
  • Non-homologous end joining (NHEJ)
  • SFV1
  • Structural variation