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Phylogenetic Analysis of Ruminant Theileria spp. from China Based on 28S Ribosomal RNA Gene

  • Gou, Huitian (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Guan, Guiquan (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Ma, Miling (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Liu, Aihong (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Liu, Zhijie (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Xu, Zongke (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Ren, Qiaoyun (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Li, Youquan (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Yang, Jifei (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Chen, Ze (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Yin, Hong (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science) ;
  • Luo, Jianxun (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Key Laboratory of Grazing Animal Diseases MOA, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science)
  • Received : 2013.01.15
  • Accepted : 2013.08.21
  • Published : 2013.10.31

Abstract

Species identification using DNA sequences is the basis for DNA taxonomy. In this study, we sequenced the ribosomal large-subunit RNA gene sequences (3,037-3,061 bp) in length of 13 Chinese Theileria stocks that were infective to cattle and sheep. The complete 28S rRNA gene is relatively difficult to amplify and its conserved region is not important for phylogenetic study. Therefore, we selected the D2-D3 region from the complete 28S rRNA sequences for phylogenetic analysis. Our analyses of 28S rRNA gene sequences showed that the 28S rRNA was useful as a phylogenetic marker for analyzing the relationships among Theileria spp. in ruminants. In addition, the D2-D3 region was a short segment that could be used instead of the whole 28S rRNA sequence during the phylogenetic analysis of Theileria, and it may be an ideal DNA barcode.

Keywords

References

  1. Levine ND. Erhardorina n. g., Ascogregarina polynesiensis n. sp., Eimeria golemanskii n. sp., Isospora tamariscini n. sp., Gregarina kazumii n. nom., new combinations and emendations in the names of apicomplexan protozoa. J Protozool 1985; 32: 359-363. https://doi.org/10.1111/j.1550-7408.1985.tb03068.x
  2. Bai Q, Liu G, Hen G. An unidentified species of Theileria infective for cattle discovered in China. Trop Anim Health Prod 1997; 29: 43-47. https://doi.org/10.1007/BF02632917
  3. Luo J, Lu W. Cattle theileriosis in China. Trop Anim Health Prod 1997; 29: 4-7. https://doi.org/10.1007/BF02632906
  4. Yin H, Schnittger L, Luo J, Seitzer U, Ahmed JS. Ovine theileriosis in China: a new look at an old story. Parasitol Res 2007; 101: 191-195. https://doi.org/10.1007/s00436-007-0689-2
  5. Liu Z, Hou J, Bakheit MA, Salih DA, Luo J, Yin H, Ahmed JS, Seitzer U. Development of loop-mediated isothermal amplification (LAMP) assay for rapid diagnosis of ovine theileriosis in China. Parasitol Res 2008; 103: 1407-1412. https://doi.org/10.1007/s00436-008-1149-3
  6. Yin H, Liu Z, Guan G, Liu A, Ma M, Ren Q, Luo J. Detection and differentiation of Theileria luwenshuni and T. uilenbergi infection in small ruminants by PCR. Transbound Emerg Dis 2008; 55: 233-237. https://doi.org/10.1111/j.1865-1682.2008.01031.x
  7. Zhang Z. A general review on the prevention and treatment of Theileria annulata in China. Vet Parasitol 1997; 70: 77-81. https://doi.org/10.1016/S0304-4017(96)01127-2
  8. Stewart N, Uilenberg G, De Vos A. Review of Australian species of Theileria, with special reference toTheileria buffeli of cattle. Trop Anim Health Prod 1996; 28: 81-90. https://doi.org/10.1007/BF02250731
  9. Kakuda T, Shiki M, Kubota S, Sugimoto C, Brown WC, Kosum C, Nopporn S, Onuma M. Phylogeny of benign Theileria species from cattle in Thailand, China and the USA based on the major piroplasm surface protein and small subunit ribosomal RNA genes. Int J Parasitol 1998; 28: 1261-1267. https://doi.org/10.1016/S0020-7519(98)00113-1
  10. Jeong W, Yoon S, An D, Cho SH, Lee KK, Kim JY. A molecular phylogeny of the benign Theileria parasites based on major piroplasm surface protein (MPSP) gene sequences. Parasitology 2010; 137: 241-249. https://doi.org/10.1017/S0031182009991090
  11. Liu Q, Zhou YQ, He GS, Oosthuizen MC, Zhou DN, Zhao JL. Molecular phylogenetic studies on Theileria spp. isolates (China) based on small subunit ribosomal RNA gene sequences. Trop Anim Health Prod 2010; 42: 109-114. https://doi.org/10.1007/s11250-009-9392-x
  12. Uilenberg G. Theileria sergenti. Vet Parasitol 2011; 175: 386. https://doi.org/10.1016/j.vetpar.2010.09.029
  13. Chae J, Allsopp BA, Waghela SD, Park J, Kakuda T, Sugimoto C, Allsopp MTEP, Gale Wagner G, Holman PJ. A study of the systematics of Theileria spp. based upon small-subunit ribosomal RNA gene sequences. Parasitol Res 1999; 85: 877-883. https://doi.org/10.1007/s004360050651
  14. Gubbels MJ, Hong Y, van der Weide M, Qi B, Nijman IJ, Guangyuan L, Jongejan F. Molecular characterisation of the Theileria buffeli/orientalis group. Int J Parasitol 2000; 30: 943-952. https://doi.org/10.1016/S0020-7519(00)00074-6
  15. Long EO, Dawid IB. Repeated genes in eukaryotes. Ann Rev Biochem 1980; 49: 727-764. https://doi.org/10.1146/annurev.bi.49.070180.003455
  16. Mugridge NB, Morrison DA, Heckeroth AR, Johnson AM, Tenter AM. Phylogenetic analysis based on full-length large subunit ribosomal RNA gene sequence comparison reveals that Neospora caninum is more closely related to Hammondia heydorni than to Toxoplasma gondii. Int J Parasitol 1999; 29: 1545-1556. https://doi.org/10.1016/S0020-7519(99)00150-2
  17. Redmond NE, Raleigh J, van Soest RW, Kelly M, Travers SA, Bradshaw B, Vartia S, Stephens KM, McCormack GP. Phylogenetic relationships of the marine Haplosclerida (Phylum Porifera) employing ribosomal (28S rRNA) and mitochondrial (cox1, nad1) gene sequence data. PLoS One 2011; 6: e24344. https://doi.org/10.1371/journal.pone.0024344
  18. Van Spaendonk RML, Ramesar J, van Wigcheren A, Eling W, Beetsma AL, van Gemert GJ, Hooghof J, Janse CJ, Waters AP. Functional equivalence of structurally distinct ribosomes in the malaria parasite, Plasmodium berghei. J Biol Chem 2001; 276: 22638- 22647. https://doi.org/10.1074/jbc.M101234200
  19. Hassouna N, Mithot B, Bachellerie JP. The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 1984; 12: 3563-3583. https://doi.org/10.1093/nar/12.8.3563
  20. Subbotin SA, Ragsdale EJ, Mullens T, Roberts PA, Mundo-Ocampo M, Baldwin JG. A phylogenetic framework for root lesion nematodes of the genus Pratylenchus (Nematoda): Evidence from 18S and D2-D3 expansion segments of 28S ribosomal RNA genes and morphological characters. Mol Phylogenet Evol 2008; 48: 491-505. https://doi.org/10.1016/j.ympev.2008.04.028
  21. Subbotin SA, Sturhan D, Chizhov VN, Vovlas N, Baldwin JG. Phylogenetic analysis of Tylenchida Thorne, 1949 as inferred from D2 and D3 expansion fragments of the 28S rRNA gene sequences. Nematology 2006; 8: 455-474. https://doi.org/10.1163/156854106778493420
  22. Nadler SA, De Ley P, Mundo-Ocampo M, Smythe AB, Patricia Stock S, Bumbarger D, Adams BJ, De Ley IT, Holovachov O, Baldwin JG. Phylogeny of Cephalobina (Nematoda): molecular evidence for recurrent evolution of probolae and incongruence with traditional classifications. Mol Phylogenet Evol 2006; 40: 696- https://doi.org/10.1016/j.ympev.2006.04.005
  23. He Y, Subbotin SA, Rubtsova TV, Lamberti F, Brown DJF, Moens M. A molecular phylogenetic approach to Longidoridae (Nematoda: Dorylaimida). Nematology 2005; 7: 111-124. https://doi.org/10.1163/1568541054192108
  24. Sonnenberg R, Nolte AW, Tautz D. An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Front Zool 2007; 4: 1-12. https://doi.org/10.1186/1742-9994-4-1
  25. Gou H, Guan G, Ma M, Liu A, Liu Z, Ren Q, Li Y, Yang J, Chen Z, Yin H, Luo J. Phylogenetic analysis based on 28S rRNA of Babesia spp. in ruminants in China. Exp Appl Acarol 2013; 59: 463-472. https://doi.org/10.1007/s10493-012-9607-0
  26. Luo J, Yin H, Liu Z, Yang D, Guan G, Liu A, Ma M, Dang S, Lu B, Sun C. Molecular phylogenetic studies on an unnamed bovine Babesia sp. based on small subunit ribosomal RNA gene sequences. Vet Parasitol 2005; 133: 1-6. https://doi.org/10.1016/j.vetpar.2005.02.014
  27. Swofford D. PAUP 4.0 b10: Phylogenetic analysis using parsimony. Sunderland, MA, USA. Sinauer Associates. 2002.
  28. Posada D. Using Modeltest and PAUP* to select a model of nucleotide substitution. Curr Protoc Bioinformatics 2003; 6.5. 1-6.5. 14.
  29. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19: 1572- 1574. https://doi.org/10.1093/bioinformatics/btg180
  30. Niu Q, Luo J, Guan G, Liu Z, Ma M, Liu A, Gao J, Ren Q, Li Y, Qiu J. Differentiation of two ovine Babesia based on the ribosomal DNA internal transcribed spacer (ITS) sequences. Exp Parasitol 2009; 121: 64-68. https://doi.org/10.1016/j.exppara.2008.09.021
  31. Li Y, Guan G, Ma M, Liu J. Theileria ovis discovered in China. Exp Parasitol 2011; 127: 304-307. https://doi.org/10.1016/j.exppara.2010.07.002
  32. Rosas-Valdez R, Morrone JJ, García-Varela M. Molecular Phylogenetics of Floridosentis Ward, 1953 (Acanthocephala: Neoechinorhynchidae) Parasites of Mullets (Osteichthyes) from Mexico, Using 28S rDNA Sequences. J Parasitol 2012; 98: 855-862. https://doi.org/10.1645/GE-2963.1
  33. Brant S, Pomajbíková K, Modry D, Petrželková K, Todd A, Loker E. Molecular phylogenetics of the elephant schistosome Bivitellobilharzia loxodontae (Trematoda: Schistosomatidae) from the Central African Republic. J Helminthol 2012; 17: 1-6.
  34. Subbotin SA, Sturhan D, Vovlas N, Castillo P, Tambe JT, Moens M, Baldwin JG. Application of the secondary structure model of rRNA for phylogeny: D2-D3 expansion segments of the LSU gene of plant-parasitic nematodes from the family Hoplolaimidae Filipjev, 1934. Mol Phylogenet Evol 2007; 43: 881-890. https://doi.org/10.1016/j.ympev.2006.09.019
  35. Aktas M, Bendele KG, Altay K, Dumanli N, Tsuji M, Holman PJ. Sequence polymorphism in the ribosomal DNA internal transcribed spacers differs among Theileria species. Vet Parasitol 2007; 147: 221-230. https://doi.org/10.1016/j.vetpar.2007.04.007
  36. Alani A, Herbert I. Pathogenesis of infection with Theileria recondita (Wales) isolated from Haemaphysalis punctata from North Wales. Vet Parasitol 1988; 28: 293-301. https://doi.org/10.1016/0304-4017(88)90076-3
  37. Bai Q, Liu G, Yin H, Zhao Q, Liu D, Ren J, Li X. Theileria sinensis sp nov: A new species of Bovine Theileria-Molecular Taxonomic studies. Acta Veterinaria et Zootechnica Sinica 2002; 33: 185-190.
  38. Yin H, Luo J, Schnittger L, Lu B, Beyer D, Ma M, Guan G, Bai Q, Lu C, Ahmed J. Phylogenetic analysis of Theileria species transmitted by Haemaphysalis qinghaiensis. Parasitol Res 2004; 92: 36- https://doi.org/10.1007/s00436-003-0900-z
  39. Liu A, Guan G, Liu Z, Liu J, Leblanc N, Li Y, Gao J, Ma M, Niu Q, Ren Q, Bai Q, Yin H, Luo J. Detecting and differentiating Theileria sergenti and Theileria sinensis in cattle and yaks by PCR based on major piroplasm surface protein (MPSP). Exp Parasitol 2010; 126: 476-481. https://doi.org/10.1016/j.exppara.2010.05.024
  40. Liu J, Guan G, Liu Z, Liu A, Ma M, Bai Q, Yin H, Luo J. Additional data for a new Theileria sp. from China based on the sequences of ribosomal RNA internal transcribed spacers. Exp Parasitol 2012; 133: 217-221.

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