Evidence of widespread natural recombination among field isolates of equine herpesvirus 4 but not among field isolates of equine herpesvirus 1 Open Access

Abstract

Recombination in alphaherpesviruses allows evolution to occur in viruses that have an otherwise stable DNA genome with a low rate of nucleotide substitution. High-throughput sequencing of complete viral genomes has recently allowed natural (field) recombination to be studied in a number of different alphaherpesviruses, however, such studies have not been applied to equine herpesvirus 1 (EHV-1) or equine herpesvirus 4 (EHV-4). These two equine alphaherpesviruses are genetically similar, but differ in their pathogenesis and epidemiology. Both cause economically significant disease in horse populations worldwide. This study used high-throughput sequencing to determine the full genome sequences of EHV-1 and EHV-4 isolates (11 and 14 isolates, respectively) from Australian or New Zealand horses. These sequences were then analysed and examined for evidence of recombination. Evidence of widespread recombination was detected in the genomes of the EHV-4 isolates. Only one potential recombination event was detected in the genomes of the EHV-1 isolates, even when the genomes from an additional 11 international EHV-1 isolates were analysed. The results from this study reveal another fundamental difference between the biology of EHV-1 and EHV-4. The results may also be used to help inform the future safe use of attenuated equine herpesvirus vaccines.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000378
2016-03-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/3/747.html?itemId=/content/journal/jgv/10.1099/jgv.0.000378&mimeType=html&fmt=ahah

References

  1. Allen G., Kydd J., Slater J. 2004; Equid herpesvirus 1 and equid herpesvirus 4 infections. In Infectious Diseases of Livestock pp 829–859Edited by Coetzer J., Tustin R. Newmarket: Oxford University Press;
    [Google Scholar]
  2. Bagust T. J., Pascoe R. R. 1968; Isolation of equine rhinopnemonitis virus from acute respiratory disease in a horse in queensland. Vet J 44:296
    [Google Scholar]
  3. Bagust T. J., Pascoe R. R. 1970; Studies on equine herpesviruses. 1. Characterisation of a strain of equine rhinopneumonitis virus isolated in Queensland. Aust Vet J 46:421–427[PubMed] [CrossRef]
    [Google Scholar]
  4. Bruen T. C., Philippe H., Bryant D. 2006; A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681 [View Article][PubMed]
    [Google Scholar]
  5. Crabb B. S., Studdert M. J. 1990; Comparative studies of the proteins of equine herpesviruses 4 and 1 and asinine herpesvirus 3: antibody response of the natural hosts. J Gen Virol 71:2033–2041 [View Article][PubMed]
    [Google Scholar]
  6. Crabb B. S., Studdert M. J. 1995; Equine herpesviruses 4 (equine rhinopneumonitis virus) and 1 (equine abortion virus). Adv Virus Res 45:153–190 [View Article][PubMed]
    [Google Scholar]
  7. Edington N., Smyth B., Griffiths L. 1991; The role of endothelial cell infection in the endometrium, placenta and foetus of equid herpesvirus 1 (EHV-1) abortions. J Comp Pathol 104:379–387 [View Article][PubMed]
    [Google Scholar]
  8. Gilkerson J. R., Whalley J. M., Drummer H. E., Studdert M. J., Love D. N. 1999; Epidemiological studies of equine herpesvirus 1 (EHV-1) in Thoroughbred foals: a review of studies conducted in the Hunter Valley of New South Wales between 1995 and 1997. Vet Microbiol 68:15–25 [View Article][PubMed]
    [Google Scholar]
  9. Gleeson L. J., Sullivan N. D., Studdert M. J. 1976; Equine herpesviruses: type 3 as an abortigenic agent. Aust Vet J 52:349–354 [View Article][PubMed]
    [Google Scholar]
  10. Horner G. W. 1981; Serological relationship between abortifacient and respiratory strains of equine herpesvirus type 1 in New Zealand. N Z Vet J 29:7–8 [View Article][PubMed]
    [Google Scholar]
  11. Huang Ja J. A., Ficorilli N., Hartley C. A., Allen G. P., Studdert M. J. 2002; Polymorphism of open reading frame 71 of equine herpesvirus-4 (EHV-4) and EHV-1. J Gen Virol 83:525–531 [View Article][PubMed]
    [Google Scholar]
  12. Huson D. H. 1998; SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73 [View Article][PubMed]
    [Google Scholar]
  13. Katoh K., Standley D. M. 2013; MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780 [View Article][PubMed]
    [Google Scholar]
  14. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., other authors. 2012; Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649 [View Article][PubMed]
    [Google Scholar]
  15. Kolb A. W., Ané C., Brandt C. R. 2013; Using HSV-1 genome phylogenetics to track past human migrations. PLoS One 8:e76267 [View Article][PubMed]
    [Google Scholar]
  16. Lee S. W., Markham P. F., Markham J. F., Petermann I., Noormohammadi A. H., Browning G. F., Ficorilli N. P., Hartley C. A., Devlin J. M. 2011; First complete genome sequence of infectious laryngotracheitis virus. BMC Genomics 12:197 [View Article][PubMed]
    [Google Scholar]
  17. Lee S. W., Markham P. F., Coppo M. J., Legione A. R., Markham J. F., Noormohammadi A. H., Browning G. F., Ficorilli N., Hartley C. A., Devlin J. M. 2012; Attenuated vaccines can recombine to form virulent field viruses. Science 337:188 [View Article][PubMed]
    [Google Scholar]
  18. Lee S. W., Devlin J. M., Markham J. F., Noormohammadi A. H., Browning G. F., Ficorilli N. P., Hartley C. A., Markham P. F. 2013; Phylogenetic and molecular epidemiological studies reveal evidence of multiple past recombination events between infectious laryngotracheitis viruses. PLoS One 8:e55121 [View Article][PubMed]
    [Google Scholar]
  19. Martin D., Murrell B., Golden M., Khoosal A., Muhire B. 2015; RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evolution 1:vev003 [View Article]
    [Google Scholar]
  20. Norberg P., Liljeqvist J. A., Bergström T., Sammons S., Schmid D. S., Loparev V. N. 2006; Complete-genome phylogenetic approach to varicella-zoster virus evolution: genetic divergence and evidence for recombination. J Virol 80:9569–9576 [View Article][PubMed]
    [Google Scholar]
  21. Norberg P., Depledge D. P., Kundu S., Atkinson C., Brown J., Haque T., Hussaini Y., MacMahon E., Molyneaux P., other authors. 2015; Recombination of globally circulating varicella-zoster virus. J Virol 89:7133–7146 [View Article][PubMed]
    [Google Scholar]
  22. Patel J. R., Heldens J. 2005; Equine herpesviruses 1 (EHV-1) and 4 (EHV-4) – epidemiology, disease and immunoprophylaxis: a brief review. Vet J 170:14–23 [View Article][PubMed]
    [Google Scholar]
  23. Peet R. L., Coackley W., Smith V. W., Main C. 1978; Equine abortion associated with herpesvirus. Aust Vet J 54:151 [View Article][PubMed]
    [Google Scholar]
  24. Peters G. A., Tyler S. D., Grose C., Severini A., Gray M. J., Upton C., Tipples G. A. 2006; A full-genome phylogenetic analysis of varicella-zoster virus reveals a novel origin of replication-based genotyping scheme and evidence of recombination between major circulating clades. J Virol 80:9850–9860 [View Article][PubMed]
    [Google Scholar]
  25. Pignatti P. F., Cassai E., Meneguzzi G., Chenciner N., Milanesi G. 1979; Herpes simplex virus DNA isolation from infected cells with a novel procedure. Virology 93:260–264 [View Article][PubMed]
    [Google Scholar]
  26. Posada D. 2002; Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708–717 [View Article][PubMed]
    [Google Scholar]
  27. Posada D., Crandall K. A. 2001; Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762 [View Article][PubMed]
    [Google Scholar]
  28. Studdert M. J. 1971; Equine herpesviruses. 4. Concurrent infection in horses with strangles and conjunctivitis. Aust Vet J 47:434–436 [View Article][PubMed]
    [Google Scholar]
  29. Studdert M. J., Blackney M. H. 1979; Equine herpesviruses: on the differentiation of respiratory from foetal strains of type 1. Aust Vet J 55:488–492 [View Article][PubMed]
    [Google Scholar]
  30. Studdert M. J., Gleeson L. J. 1977; Isolation of equine rhinovirus type 1. Aust Vet J 53:452 [View Article][PubMed]
    [Google Scholar]
  31. Studdert M. J., Turner A. J., Peterson J. E. 1970; Equine herpesviruses. I. Isolation and characterisation of equine rhinopneumonitis virus and other equine herpesviruses from horses. Aust Vet J 46:83–89 [View Article][PubMed]
    [Google Scholar]
  32. Studdert M. J., Fitzpatrick D. R., Horner G. W., Westbury H. A., Gleeson L. J. 1984; Molecular epidemiology and pathogenesis of some equine herpesvirus type 1 (equine abortion virus) and type 4 (equine rhinopneumonitis virus) isolates. Aust Vet J 61:345–348 [View Article][PubMed]
    [Google Scholar]
  33. Studdert M. J., Hartley C. A., Dynon K., Sandy J. R., Slocombe R. F., Charles J. A., Milne M. E., Clarke A. F., El-Hage C. 2003; Outbreak of equine herpesvirus type 1 myeloencephalitis: new insights from virus identification by PCR and the application of an EHV-1-specific antibody detection ELISA. Vet Rec 153:417–423 [View Article][PubMed]
    [Google Scholar]
  34. Telford E. A., Watson M. S., McBride K., Davison A. J. 1992; The DNA sequence of equine herpesvirus-1. Virology 189:304–316 [View Article][PubMed]
    [Google Scholar]
  35. Telford E. A., Watson M. S., Perry J., Cullinane A. A., Davison A. J. 1998; The DNA sequence of equine herpesvirus-4. J Gen Virol 79:1197–1203 [View Article][PubMed]
    [Google Scholar]
  36. Thiry E., Meurens F., Muylkens B., McVoy M., Gogev S., Thiry J., Vanderplasschen A., Epstein A., Keil G., Schynts F. 2005; Recombination in alphaherpesviruses. Rev Med Virol 15:89–103 [View Article][PubMed]
    [Google Scholar]
  37. Varrasso A., Dynon K., Ficorilli N., Hartley C. A., Studdert M. J., Drummer H. E. 2001; Identification of equine herpesviruses 1 and 4 by polymerase chain reaction. Aust Vet J 79:563–569 [View Article][PubMed]
    [Google Scholar]
  38. Weller S. K., Sawitzke J. A. 2014; Recombination promoted by DNA viruses: phage λ to herpes simplex virus. Annu Rev Microbiol 68:237–258 [View Article][PubMed]
    [Google Scholar]
  39. Zell R., Taudien S., Pfaff F., Wutzler P., Platzer M., Sauerbrei A. 2012; Sequencing of 21 varicella-zoster virus genomes reveals two novel genotypes and evidence of recombination. J Virol 86:1608–1622 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000378
Loading
/content/journal/jgv/10.1099/jgv.0.000378
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited Most Cited RSS feed