Skip to main content
Log in

Phylogenetic analysis of classical swine fever virus isolates from China

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Classical swine fever (CSF), caused by classical swine fever virus (CSFV), is a severe disease that causes huge economic losses in the swine industry worldwide. In China, CSF has been under control due to extensive vaccination since 1954. However, there are still sporadic CSF outbreaks in China. Here, we isolated 27 CSFV strains from three Chinese provinces (Shaanxi, Gansu, and Ningxia) from 2011 to 2018. Phylogenetic analysis based on the full-length envelope glycoprotein E2 coding region revealed that 25 out of 27 CSFV isolates clustered within subgroups 2.1 and 2.2, while two strains from Gansu belonged to subgroup 1.1. The sequence identity among these 27 isolates varied from 79.3% to 99.8% (nucleotides) and from 83.1% to 99.7% (amino acids). Further analysis based on the E2 amino acid sequences showed that these new isolates have consistent amino acid substitutions, including R31K and N34S.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Data availability

The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Blome S, Staubach C, Henke J, Carlson J, Beer M (2017) Classical swine fever—an updated review. Viruses 9:4. https://doi.org/10.3390/v9040086

    Article  CAS  Google Scholar 

  2. Edwards S, Fukusho A, Lefevre PC, Lipowski A, Pejsak Z, Roehe P, Westergaard J (2000) Classical swine fever: the global situation. Vet Microbiol 73(2–3):103–119. https://doi.org/10.1016/s0378-1135(00)00138-3

    Article  CAS  PubMed  Google Scholar 

  3. Moennig V (2000) Introduction to classical swine fever: virus, disease and control policy. Vet Microbiol 73(2–3):93–102. https://doi.org/10.1016/s0378-1135(00)00137-1

    Article  CAS  PubMed  Google Scholar 

  4. Meyers G, Rumenapf T, Thiel HJ (1989) Molecular cloning and nucleotide sequence of the genome of hog cholera virus. Virology 171(2):555–567. https://doi.org/10.1016/0042-6822(89)90625-9

    Article  CAS  PubMed  Google Scholar 

  5. Thiel HJ, Stark R, Weiland E, Rumenapf T, Meyers G (1991) Hog cholera virus: molecular composition of virions from a pestivirus. J Virol 65(9):4705–4712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Yona S, Kim KW, Wolf Y, Mildner A, Varol D, Breker M, Strauss-Ayali D, Viukov S, Guilliams M, Misharin A, Hume DA, Perlman H, Malissen B, Zelzer E, Jung S (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38(1):79–91. https://doi.org/10.1016/j.immuni.2012.12.001

    Article  CAS  PubMed  Google Scholar 

  7. He F, Ling L, Liao Y, Li S, Han W, Zhao B, Sun Y, Qiu HJ (2014) Beta-actin interacts with the E2 protein and is involved in the early replication of classical swine fever virus. Virus Res 179:161–168. https://doi.org/10.1016/j.virusres.2013.10.016

    Article  CAS  PubMed  Google Scholar 

  8. Vuono EA, Ramirez-Medina E, Berggren K, Rai A, Pruitt S, Silva E, Velazquez-Salinas L, Gladue DP, Borca MV (2020) Swine host protein coiled-coil domain-containing 115 (CCDC115) interacts with classical swine fever virus structural glycoprotein E2 during virus replication. Viruses 12:4. https://doi.org/10.3390/v12040388

    Article  CAS  Google Scholar 

  9. Yang Z, Shi Z, Guo H, Qu H, Zhang Y, Tu C (2015) Annexin 2 is a host protein binding to classical swine fever virus E2 glycoprotein and promoting viral growth in PK-15 cells. Virus Res 201:16–23. https://doi.org/10.1016/j.virusres.2015.02.013

    Article  CAS  PubMed  Google Scholar 

  10. Risatti GR, Borca MV, Kutish GF, Lu Z, Holinka LG, French RA, Tulman ER, Rock DL (2005) The E2 glycoprotein of classical swine fever virus is a virulence determinant in swine. J Virol 79(6):3787–3796. https://doi.org/10.1128/JVI.79.6.3787-3796.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Weiland E, Ahl R, Stark R, Weiland F, Thiel HJ (1992) A second envelope glycoprotein mediates neutralization of a pestivirus, hog cholera virus. J Virol 66(6):3677–3682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Paton DJ, McGoldrick A, Greiser-Wilke I, Parchariyanon S, Song JY, Liou PP, Stadejek T, Lowings JP, Bjorklund H, Belak S (2000) Genetic typing of classical swine fever virus. Vet Microbiol 73(2–3):137–157. https://doi.org/10.1016/s0378-1135(00)00141-3

    Article  CAS  PubMed  Google Scholar 

  13. Deng MC, Huang CC, Huang TS, Chang CY, Lin YJ, Chien MS, Jong MH (2005) Phylogenetic analysis of classical swine fever virus isolated from Taiwan. Vet Microbiol 106(3–4):187–193. https://doi.org/10.1016/j.vetmic.2004.12.014

    Article  CAS  PubMed  Google Scholar 

  14. Postel A, Schmeiser S, Perera CL, Rodriguez LJ, Frias-Lepoureau MT, Becher P (2013) Classical swine fever virus isolates from Cuba form a new subgenotype 1.4. Vet Microbiol 161(3–4):334–338. https://doi.org/10.1016/j.vetmic.2012.07.045

    Article  CAS  PubMed  Google Scholar 

  15. Lowings P, Ibata G, Needham J, Paton D (1996) Classical swine fever virus diversity and evolution. J Gen Virol 77(Pt 6):1311–1321. https://doi.org/10.1099/0022-1317-77-6-1311

    Article  CAS  PubMed  Google Scholar 

  16. Leifer I, Hoeper D, Blome S, Beer M, Ruggli N (2011) Clustering of classical swine fever virus isolates by codon pair bias. BMC Res Notes 4:521. https://doi.org/10.1186/1756-0500-4-521

    Article  PubMed  PubMed Central  Google Scholar 

  17. Beer M, Goller KV, Staubach C, Blome S (2015) Genetic variability and distribution of Classical swine fever virus. Anim Health Res Rev 16(1):33–39. https://doi.org/10.1017/S1466252315000109

    Article  PubMed  Google Scholar 

  18. Tu C, Lu Z, Li H, Yu X, Liu X, Li Y, Zhang H, Yin Z (2001) Phylogenetic comparison of classical swine fever virus in China. Virus Res 81(1–2):29–37. https://doi.org/10.1016/s0168-1702(01)00366-5

    Article  CAS  PubMed  Google Scholar 

  19. Choe S, Le VP, Shin J, Kim JH, Kim KS, Song S, Cha RM, Park GN, Nguyen TL, Hyun BH, Park BK, An DJ (2020) Pathogenicity and genetic characterization of Vietnamese classical swine fever virus: 2014–2018. Pathogens 9:3. https://doi.org/10.3390/pathogens9030169

    Article  CAS  Google Scholar 

  20. Postel A, Schmeiser S, Bernau J, Meindl-Boehmer A, Pridotkas G, Dirbakova Z, Mojzis M, Becher P (2012) Improved strategy for phylogenetic analysis of classical swine fever virus based on full-length E2 encoding sequences. Vet Res 43:50. https://doi.org/10.1186/1297-9716-43-50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Rios L, Coronado L, Naranjo-Feliciano D, Martinez-Perez O, Perera CL, Hernandez-Alvarez L, Diaz de Arce H, Nunez JI, Ganges L, Perez LJ (2017) Deciphering the emergence, genetic diversity and evolution of classical swine fever virus. Sci Rep 7(1):17887. https://doi.org/10.1038/s41598-017-18196-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1(1):vev003. https://doi.org/10.1093/ve/vev003

    Article  PubMed  PubMed Central  Google Scholar 

  23. Postel A, Schmeiser S, Oguzoglu TC, Indenbirken D, Alawi M, Fischer N, Grundhoff A, Becher P (2015) Close relationship of ruminant pestiviruses and classical Swine Fever virus. Emerg Infect Dis 21(4):668–672. https://doi.org/10.3201/eid2104.141441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhang D, Gao F, Jakovlic I, Zou H, Zhang J, Li WX, Wang GT (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour 20(1):348–355. https://doi.org/10.1111/1755-0998.13096

    Article  PubMed  Google Scholar 

  27. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274. https://doi.org/10.1093/molbev/msu300

    Article  CAS  PubMed  Google Scholar 

  29. Minh BQ, Nguyen MA, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30(5):1188–1195. https://doi.org/10.1093/molbev/mst024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Letunic I, Bork P (2019) Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47(W1):W256–W259. https://doi.org/10.1093/nar/gkz239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Rios L, Nunez JI, Diaz de Arce H, Ganges L, Perez LJ (2018) Revisiting the genetic diversity of classical swine fever virus: a proposal for new genotyping and subgenotyping schemes of classification. Transbound Emerg Dis 65(4):963–971. https://doi.org/10.1111/tbed.12909

    Article  PubMed  Google Scholar 

  32. Zhang H, Leng C, Feng L, Zhai H, Chen J, Liu C, Bai Y, Ye C, Peng J, An T, Kan Y, Cai X, Tian Z, Tong G (2015) A new subgenotype 2.1d isolates of classical swine fever virus in China, 2014. Infect Genet Evol 34:94–105. https://doi.org/10.1016/j.meegid.2015.05.031

    Article  CAS  PubMed  Google Scholar 

  33. Luo Y, Li S, Sun Y, Qiu HJ (2014) Classical swine fever in China: a minireview. Vet Microbiol 172(1–2):1–6. https://doi.org/10.1016/j.vetmic.2014.04.004

    Article  PubMed  Google Scholar 

  34. Luo Y, Ji S, Liu Y, Lei JL, Xia SL, Wang Y, Du ML, Shao L, Meng XY, Zhou M, Sun Y, Qiu HJ (2017) Isolation and characterization of a moderately virulent classical swine fever virus emerging in China. Transbound Emerg Dis 64(6):1848–1857. https://doi.org/10.1111/tbed.12581

    Article  CAS  PubMed  Google Scholar 

  35. Gong W, Wu J, Lu Z, Zhang L, Qin S, Chen F, Peng Z, Wang Q, Ma L, Bai A, Guo H, Shi J, Tu C (2016) Genetic diversity of subgenotype 2.1 isolates of classical swine fever virus. Infect Genet Evol 41:218–226. https://doi.org/10.1016/j.meegid.2016.04.002

    Article  CAS  PubMed  Google Scholar 

  36. Gong W, Li J, Wang Z, Sun J, Mi S, Lu Z, Cao J, Dou Z, Sun Y, Wang P, Yuan K, Zhang L, Zhou X, He S, Tu C (2019) Virulence evaluation of classical swine fever virus subgenotype 2.1 and 2.2 isolates circulating in China. Vet Microbiol 232:114–120. https://doi.org/10.1016/j.vetmic.2019.04.001

    Article  PubMed  Google Scholar 

  37. Holland BR, Penny D, Hendy MD (2003) Outgroup misplacement and phylogenetic inaccuracy under a molecular clock—a simulation study. Syst Biol 52(2):229–238. https://doi.org/10.1080/10635150390192771

    Article  CAS  PubMed  Google Scholar 

  38. de la Torre-Barcena JE, Kolokotronis SO, Lee EK, Stevenson DW, Brenner ED, Katari MS, Coruzzi GM, DeSalle R (2009) The impact of outgroup choice and missing data on major seed plant phylogenetics using genome-wide EST data. PLoS One 4(6):e5764. https://doi.org/10.1371/journal.pone.0005764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research was supported by funds from the Programs for Science and Technology of Xianyang City [2019k02-63].

Author information

Authors and Affiliations

Authors

Contributions

XFZ, MJL, and WTM designed the study. XFZ, MJL, XJW, XDZ, and WTM performed the experiments and collected data. MJL analyzed the data. MJL AND XFZ wrote and revised the manuscript. XFZ provided the funding. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Xiaofu Zhu.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

The collection of clinical samples was approved by the Animal Ethics Committee of Xianyang Vocational Technical College and performed in accordance with animal ethics guidelines and approved protocols.

Additional information

Handling Editor: Patricia Aguilar.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLS 39 KB)

Supplementary file2 (TXT 39 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, X., Liu, M., Wu, X. et al. Phylogenetic analysis of classical swine fever virus isolates from China. Arch Virol 166, 2255–2261 (2021). https://doi.org/10.1007/s00705-021-05084-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-021-05084-0

Navigation