Avian picornaviruses: Molecular evolution, genome diversity and unusual genome features of a rapidly expanding group of viruses in birds

Infection, Genetics and Evolution

Volumn 28, Issue , 2014, Pages 151-166

  Boros, Ákos ^a   Pankovics, Péter ^a   Reuter, Gábor ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Bird; Evolution; IRES; Pathogen; Picornavirus; Review

Indexed keywords

3' UNTRANSLATED REGION; AVIHEPATOVIRUS; BIRD; GENE CLUSTER; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; KOBUVIRUS; MEGRIVIRUS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PASSERIVIRUS; PICORNAVIRUS; REVIEW; RNA SEQUENCE; RNA VIRUS; SAPELOVIRUS; SEQUENCE ANALYSIS; SPECIES DIVERSITY; TAXONOMIC IDENTIFICATION; TAXONOMIC RANK; UNINDEXED SEQUENCE; VIRUS ENTRY; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS MORPHOLOGY; ANIMAL; BIRD DISEASE; CLASSIFICATION; GENETICS; PHYLOGENY; PHYLOGEOGRAPHY; PICORNAVIRIDAE; PICORNAVIRUS INFECTION; VETERINARY; VIROLOGY;

ANIMALS; BIRD DISEASES; BIRDS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, VIRAL; PHYLOGENY; PHYLOGEOGRAPHY; PICORNAVIRIDAE; PICORNAVIRIDAE INFECTIONS;

EID: 84907987614     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.09.027     Document Type: Review

References (109)

1. Al-Sunaidi M., Williams C.H., Hughes P.J., Schnurr D.P., Stanway G. Analysis of a new human parechovirus allows the definition of parechovirus types and the identification of RNA structural domains. J. Virol. 2007, 81:1013-1021.
2. Barbknecht M., Sepsenwol S., Leis E., Tuttle-Lau M., Gaikowski M., Knowles N.J., Lasee B., Hoffman M.A. Characterization of a new picornavirus isolated from the freshwater fish Lepomis macrochirus. J. Gen. Virol. 2014, 95:601-613.
3. Belsham G.J. Divergent picornavirus IRES elements. Virus Res. 2009, 139:183-192.
4. Boros Á., Kiss T., Kiss O., Pankovics P., Kapusinszky B., Delwart E., Reuter G. Genetic characterization of a novel picornavirus distantly related to the marine mammal-infecting aquamaviruses in a long-distance migrant bird species, European Roller (Coracias garrulus). J. Gen. Virol. 2013, 94:2029-2035.
5. Boros Á., Nemes C., Pankovics P., Kapusinszky B., Delwart E., Reuter G. Genetic characterization of a novel picornavirus in turkeys (Meleagris gallopavo) distinct from turkey galliviruses and megriviruses and distantly related to the members of the genus Avihepatovirus. J. Gen. Virol. 2013, 94:1496-1509.
6. Boros Á., Nemes C., Pankovics P., Kapusinszky B., Delwart E., Reuter G. Identification and complete genome characterization of a novel picornavirus in turkey (Meleagris gallopavo). J. Gen. Virol. 2012, 93:2171-2182.
7. Boros Á., Pankovics P., Knowles N.J., Nemes C., Delwart E., Reuter G. Comparative complete genome analysis of chicken and turkey megriviruses (family Picornaviridae): long 3' untranslated regions with a potential second open reading frame and evidence for possible recombination. J. Virol. 2014, 88:6434-6443.
8. Brown E.A., Zajac A.J., Lemon S.M. In vitro characterization of an internal ribosomal entry site (IRES) present within the 5' nontranslated region of hepatitis A virus RNA: comparison with the IRES of encephalomyocarditis virus. J. Virol. 1994, 68:1066-1074.
9. Bullman S., Kearney K., O' Mahony M., Kelly L., Whyte P., Fanning S., Morgan J.G. Identification and genetic characterisation of a novel picornavirus from chickens. J. Gen. Virol. 2014, 95:1094-1103.
10. Calnek B.W. Other viral infections: avian encephalomyelitis. Diseases of Poultry 2008, 430-441. Blackwell Publishing Ltd., Oxford, (Chapter 14). 12th ed. Y.M. Saif (Ed.).
11. Cha S.Y., Roh J.H., Kang M., Kim B., Jang H.K. Isolation and characterization of a low pathogenic duck hepatitis A virus 3 from South Korea. Vet. Microbiol. 2013, 162:254-258.
12. Charini W.A., Todd S., Gutman G.A., Semler B.L. Transduction of a human RNA sequence by poliovirus. J. Virol. 1994, 68:6547-6552.
13. Chiu C.Y. Viral pathogen discovery. Curr. Opin. Microbiol. 2013, 16:468-478.
14. Clarke B.E., Sangar D.V., Burroughs J.N., Newton S.E., Carroll A.R., Rowlands D.J. Two initiation sites for foot-and-mouth disease virus polyprotein in vivo. J. Gen. Virol. 1985, 66:2615-2626.
15. Clements J.F. The Clements Checklist of Birds of the World 2007, Cornell University Press, Ithaca. sixth ed.
16. Day J.M., Zsak L. Recent progress in the characterization of avian enteric viruses. Avian Dis. 2013, 57:573-580.
17. Day J.M., Ballard L.L., Duke M.V., Scheffler B.E., Zsak L. Metagenomic analysis of the turkey gut RNA virus community. Virol. J. 2010, 7:313.
18. de Vries M., Pyrc K., Berkhout R., Vermeulen-Oost W., Dijkman R., Jebbink M.F., Bruisten S., Berkhout B., van der Hoek L. Human parechovirus type 1, 3, 4, 5, and 6 detection in picornavirus cultures. J. Clin. Microbiol. 2008, 46:759-762.
19. Delwart E. Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr. Opin. Virol. 2012, 2:344-352.
20. Ding C., Zhang D. Molecular analysis of duck hepatitis virus type 1. Virology 2007, 361:9-17.
21. Donnelly M.L., Luke G., Mehrotra A., Li X., Hughes L.E., Gani D., Ryan M.D. Analysis of the aphthovirus 2A/2B polyprotein 'cleavage' mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal 'skip'. J. Gen. Virol. 2001, 82:1013-1025.
22. Dvorak C.M., Hall D.J., Hill M., Riddle M., Pranter A., Dillman J., Deibel M., Palmenberg A.C. Leader protein of encephalomyocarditis virus binds zinc, is phosphorylated during viral infection, and affects the efficiency of genome translation. Virology 2001, 290:261-271.
23. Farkas T., Sestak K., Wei C., Jiang X. Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. J. Virol. 2008, 82:5408-5416.
24. Farkas T., Fey B., Hargitt E., Parcells M., Ladman B., Murgia M., Saif Y. Molecular detection of novel picornaviruses in chickens and turkeys. Virus Genes 2012, 44:262-272.
25. Fichtner D., Philipps A., Groth M., Schmidt-Posthaus H., Granzow H., Dauber M., Platzer M., Bergmann S.M., Schrudde D., Sauerbrei A., Zell R. Characterization of a novel picornavirus isolate from a diseased European eel (Anguilla anguilla). J. Virol. 2013, 87:10895-10899.
26. Gebhard L.G., Filomatori C.V., Gamarnik A.V. Functional RNA elements in the dengue virus genome. Viruses 2011, 3:1739-1756.
27. Gorbalenya A.E., Lauber C. Origin and evolution of the Picornaviridae proteome. The Picornaviruses 2010, 253-270. ASM Press, Washington DC, (Chapter 7). E. Ehrenfeld, E. Domingo, R.P. Roos (Eds.).
28. Hansen W.R., Gough R.E. Duck plague (duck virus enteritis). Infectious Diseases of Wild Birds 2007, 87-107. Wiley-Blackwell, San Diego, Oxford. N.J. Thomas, D.B. Hunter, C.T. Atkinson (Eds.).
29. Harvala H., Simmonds P. Human parechoviruses: biology, epidemiology and clinical significance. J. Clin. Virol. 2009, 45:1-9.
30. Hedges S.B., Parker P.H., Sibley C.G., Kumar S. Continental breakup and the ordinal diversification of birds and mammals. Nature 1996, 381:226-229.
31. Hellen C.U., de Breyne S. A distinct group of hepacivirus/pestivirus-like internal ribosomal entry sites in members of diverse picornavirus genera: evidence for modular exchange of functional noncoding RNA elements by recombination. J. Virol. 2007, 81:5850-5863.
32. Heuser, W., Kaleta, E., Giesow, K., Keil, G.M., Knowles, N.J., 2010. Genome sequence of virus "X", a picornavirus isolated from a spur-thighed tortoise (Testudo graeca). EUROPIC 2010: XVI Meeting of the European Study Group on the Molecular Biology of Picornaviruses, St. Andrews, Scotland, 11-16 September 2010, Abstract H15, p. 147.
33. Hollmén T., Docherty D.E. Orthoreoviruses. Infectious Diseases of Wild Birds 2007, 177-181. Wiley-Blackwell, San Diego, Oxford. N.J. Thomas, D.B. Hunter, C.T. Atkinson (Eds.).
34. Honkavuori K.S., Shivaprasad H.L., Briese T., Street C., Hirschberg D.L., Hutchison S.K., Lipkin W.I. Novel picornavirus in turkey poults with hepatitis, California. USA. Emerg. Infect. Dis. 2011, 17:480-487.
35. Hughes P.J., Stanway G. The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation. J. Gen. Virol. 2000, 81:201-207.
36. Jin X., Zhang W., Zhang W., Gu C., Cheng G., Hu X. Identification and molecular analysis of the highly pathogenic duck hepatitis virus type 1 in Hubei province of China. Res. Vet. Sci. 2008, 85:595-598.
37. Johansson E.S., Niklasson B., Tesh R.B., Shafren D.R., Travassos da Rosa A.P., Lindberg A.M. Molecular characterization of M1146, an American isolate of Ljungan virus (LV) reveals the presence of a new LV genotype. J. Gen. Virol. 2003, 84:837-844.
38. Johansson S., Niklasson B., Maizel J., Gorbalenya A.E., Lindberg A.M. Molecular analysis of three Ljungan virus isolates reveals a new, close-to-root lineage of the Picornaviridae with a cluster of two unrelated 2A proteins. J. Virol. 2002, 76:8920-8930.
39. Kapoor A., Victoria J., Simmonds P., Wang C., Shafer R.W., Nims R., Nielsen O., Delwart E. A highly divergent picornavirus in a marine mammal. J. Virol. 2008, 82:311-320.
40. Kennedy I.M., Haddow J.K., Clements J.B. A negative regulatory element in the human papillomavirus type 16 genome acts at the level of late mRNA stability. J. Virol. 1991, 65:2093-2097.
41. Khatchikian D., Orlich M., Rott R. Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus. Nature 1989, 340:156-157.
42. Kim M.C., Kwon Y.K., Joh S.J., Kim S.J., Tolf C., Kim J.H., Sung H.W., Lindberg A.M., Kwon J.H. Recent Korean isolates of duck hepatitis virus reveal the presence of a new geno- and serotype when compared to duck hepatitis virus type 1 type strains. Arch. Virol. 2007, 152:2059-2072.
43. Kim M.C., Kwon Y.K., Joh S.J., Lindberg A.M., Kwon J.H., Kim J.H., Kim S.J. Molecular analysis of duck hepatitis virus type 1 reveals a novel lineage close to the genus Parechovirus in the family Picornaviridae. J. Gen. Virol. 2006, 87:3307-3316.
44. Knowles, N., Delwart, E., Gorbalenya, A.E., Hovi, T., Hyypia, T., King, A.M.Q., Lindberg, A.M., Pallansch, M.A., Palmenberg, A.C., Reuter, G., Simmonds, P., Skern, T., Stanway, G., Yamashita, T., Zell, R., 2014. Picornaviridae: 26 genera, 46 species and growing. EUROPIC 2014: XVIII Meeting of the European Study Group on the Molecular Biology of Picornaviruses. Blankenberge, Belgium, 9-14 March 2014, Abstract C09, p. 98.
45. Knowles N.J., Hovi T., Hyypiä T., King A.M.Q., Lindberg A.M., Pallansch M.A., Palmenberg A.C., Simmonds P., Skern T., Stanway G., Yamashita T., Zell R. Picornaviridae. Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses 2011, 855-880. Elsevier Academic Press, London. A.M.Q. King, M.J. Adams, E.B. Carstens, E.J. Lefkowitz (Eds.).
46. Kofstad T., Jonassen C.M. Screening of feral and wood pigeons for viruses harbouring a conserved mobile viral element: characterization of novel astroviruses and picornaviruses. PLoS One 2011, 6(10):e25964.
47. Lai M.M.C. Recombination and its evolutionary effect on viruses with RNA genomes. Molecular Basis of Virus Evolution 1995, 119-132. Cambridge University Press, (Chapter 9). J. Adrian, C.H. Gibbs, C.F. García-Arenal (Eds.).
48. Lange J., Groth M., Fichtner D., Granzow H., Keller B., Walther M., Platzer M., Sauerbrei A., Zell R. Virus isolate from carp: genetic characterisation reveals a novel picornavirus with two aphthovirus 2A-like sequences. J. Gen. Virol. 2014, 95:80-90.
49. Leighton F.A., Heckert R.A. Newcastle disease and related avian paramyxoviruses. Infectious Diseases of Wild Birds 2007, 3-16. Wiley-Blackwell, San Diego, Oxford. N.J. Thomas, D.B. Hunter, C.T. Atkinson (Eds.).
50. Lewis-Rogers N., Crandall K.A. Evolution of Picornaviridae: an examination of phylogenetic relationships and cophylogeny. Mol. Phylogenet. Evol. 2010, 54:995-1005.
51. Liao Q., Zheng L., Yuan Y., Shi J., Zhang D. Genomic characterization of a novel picornavirus in Pekin ducks. Vet. Microbiol. 2014, 10.1016/j.vetmic.2014.05.002.
52. Liu Y., Wimmer E., Paul A.V. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochem. Biophys. Acta 2009, 1789:495-517.
53. Liu M., Fanyi-Meng, Li X.J., Zhang Z., Liu S., Zhang Y. Goose haemorrhagic hepatitis caused by a new subtype duck hepatitis type 1 virus. Vet. Microbiol. 2011, 152:280-283.
54. Luke G., Escuin H., De Felipe P., Ryan M. 2A to the fore - research, technology and applications. Biotechnol. Genet. Eng. Rev. 2010, 26:223-260.
55. Luttrell P., Fischer J.R. Mycoplasmosis. Infectious Diseases of Wild Birds 2007, 317-331. Wiley-Blackwell, San Diego, Oxford. N.J. Thomas, D.B. Hunter, C.T. Atkinson (Eds.).
56. Marvil P., Knowles N.J., Mockett A.P.A., Britton P., Brown T.D.K., Cavanagh D. Avian encephalomyelitis virus is a picornavirus and is most closely related to hepatitis A virus. J. Gen. Virol. 1999, 80:653-662.
57. McLean R.G., Ubico S.R. Arboviruses in birds. Infectious Diseases of Wild Birds 2007, 17-62. Wiley-Blackwell, San Diego, Oxford. N.J. Thomas, D.B. Hunter, C.T. Atkinson (Eds.).
58. Monceyron C., Grinde B., Jonassen T.O. Molecular characterisation of the 3'-end of the astrovirus genome. Arch. Virol. 1997, 142:699-706.
59. Ng T.F., Cheung A.K., Wong W., Lager K.M., Kondov N.O., Cha Y., Murphy D.A., Pogranichniy R.M., Delwart E. Divergent picornavirus from a Turkey with gastrointestinal disease. Genome Announc. 2013, 2:e00134-13.
60. Ng T.F.F., Mesquita J.R., Nascimento M.S.J., Kondov N.O., Wong W., Reuter G., Knowles N.J., Vega E., Esona M.D., Deng X., Vinjé J., Delwart E. Feline fecal virome reveals novel and prevalent enteric viruses. Vet. Microbiol. 2014, 171:102-111.
61. Nilsson A.I., Koskiniemi S., Eriksson S., Kugelberg E., Hinton J.C., Andersson D.I. Bacterial genome size reduction by experimental evolution. Proc. Natl. Acad. Sci. 2005, 102:12112-12116.
62. Oberste M.S., Maher K., Pallansch M.A. Genomic evidence that simian virus 2 and six other simian picornaviruses represent a new genus in Picornaviridae. Virology 2003, 314:283-293.
63. OIE, 2010. Chapter 2.3.8.: Duck virus hepatitis. In Manual of Diagnostic Tests & Vaccines for Terrestrial Animals, 7th ed., Paris: OIE (Office International des Epizooties). (accessed 04.04.2014). http://www.oie.int/manual-of-diagnostic-tests-and-vaccines-for-terrestrial-animals/.
64. Palmenberg A.C., Neubauer D., Skern T. Genome organization and encoded proteins. The Picornaviruses 2010, 3-17. ASM Press, Washington DC, (Chapter 1). E. Ehrenfeld, E. Domingo, R.P. Roos (Eds.).
65. Pan M., Yang X., Zhou L., Ge X., Guo X., Liu J., Zhang D., Yang H. Duck Hepatitis A virus possesses a distinct type IV internal ribosome entry site element of picornavirus. J. Virol. 2012, 86:1129-1144.
66. Pankovics P., Boros A., Reuter G. Novel picornavirus in domesticated common quail (Coturnix coturnix) in Hungary. Arch. Virol. 2012, 157:525-530.
67. Pantin-Jackwood M.J., Day J.M., Jackwood M.W., Spackman E. Enteric viruses detected by molecular methods in commercial chicken and turkey flocks in the United States between 2005 and 2006. Avian Dis. 2008, 52:235-244.
68. Pantin-Jackwood M.J., Spackman E., Day J.M., Rives D. Periodic monitoring of commercial turkeys for enteric viruses indicates continuous presence of astrovirus and rotavirus on the farms. Avian Dis. 2007, 51:674-680.
69. Phan T.G., Kapusinszky B., Wang C., Rose R.K., Lipton H.L., Delwart E. The fecal viral flora of wild rodents. PLoS Pathog. 2011, 7(9):e1002218.
70. Phan T.G., Vo N.P., Boros Á., Pankovics P., Reuter G., Li O.T.W., Wang C., Deng X., Poon L.L.M., Delwart E. The viruses of wild pigeon droppings. PLoS One 2013, 8:e72787.
71. Phelps N.B.D., Mor S.K., Armien A.G., Batts W., Goodwin A.E., Hopper L., McCann R., Ng T.F.F., Puzach C., Waltzek T.B., Delwart E., Winton J., Goyal S.M. Isolation and molecular characterization of a novel picornavirus from baitfish in the USA. PLoS One 2014, 9:e87593.
72. Pilipenko E.V., Maslova S.V., Sinyakov A.N., Agol V.I. Towards identification of cis-acting elements involved in the replication of enterovirus and rhinovirus RNAs: a proposal for the existence of tRNA-like terminal structures. Nucleic Acids Res. 1992, 11:1739-1745.
73. Racaniello V. Picornaviridae: the viruses and their replication. Fields Virology 2007, 795-838. Lippincott Williams & Wilkins, Philadelphia. 5th ed. D.M. Knipe, P.M. Howley (Eds.).
74. Reuter G., Boldizsár A., Pankovics P. Complete nucleotide and amino acid sequences and genetic organization of porcine kobuvirus, a member of a new species in the genus Kobuvirus, family Picornaviridae. Arch Virol. 2009, 154:101-108.
75. Reuter G., Boros Á., Kiss T., Delwart E., Pankovics P. Complete genome characterization of mosavirus (family Picornaviridae) identified in dropping of European roller (Coracias garrulus) in Hungary. Arch. Virol. 2014, 10.1007/s00705-014-2113-4.
76. Reuter G., Boros Á., Pankovics P. Kobuviruses - a comprehensive review. Rev. Med. Virol. 2011, 21:32-41.
77. Reuter G., Pankovics P., Knowles N.J., Boros Á. Two closely related novel picornaviruses in cattle and sheep in Hungary from 2008 to 2009, proposed as members of a new genus in the family Picornaviridae. J. Virol. 2012, 86:13295-13302.
78. Rohll J.B., Moon D.H., Evans D.J., Almond J.W. The 3' untranslated region of picornavirus RNA: features required for efficient genome replication. J. Virol. 1995, 69:7835-7844.
79. Ryan M.D., King A.M., Thomas G.P. Cleavage of foot-and-mouth disease virus polyprotein is mediated by residues located within a 19 amino acid sequence. J. Gen. Virol. 1991, 72:2727-2732.
80. Sauvage V., Ar Gouilh M., Cheval J., Muth E., Pariente K., Burguiere A., Caro V., Manuguerra J.C., Eloit M. A member of a new Picornaviridae genus is shed in pig feces. J. Virol. 2012, 86:10036-10046.
81. Seipelt J., Guarné A., Bergmann E., James M., Sommergruber W., Fita I., Skern T. The structures of picornaviral proteinases. Virus Res. 1999, 62:159-168.
82. Shi S., Chen H., Chen Z., Fu G., Wan C., Huang Y., Lin S., Cheng L., Fu Q., Lin J., Lin F. Complete genome sequence of a duck hepatitis a virus 1 isolated from a pigeon in China. Genome Announc. 2013, 1:E00451-13.
83. Siew N., Fischer D. Analysis of singleton ORFans in fully sequenced microbial genomes. Proteins 2003, 52:241-251.
84. Simmonds P. Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J. Virol. 2006, 80:11124-11140.
85. Smits S.L., Rahman M., Schapendonk C.M., van Leeuwen M., Faruque A.S., Haagmans B.L., Endtz H.P., Osterhaus A.D. Calicivirus from novel Recovirus genogroup in human diarrhea, Bangladesh. Emerg. Infect. Dis. 2012, 18:1192-1195.
86. Smits S.L., Raj V.S., Oduber M.D., Schapendonk C.M., Bodewes R., Provacia L., Stittelaar K.J., Osterhaus A.D., Haagmans B.L. Metagenomic analysis of the ferret fecal viral flora. PLoS One 2013, 8:E71595.
87. Snoeyenbos G.H., Bosch H.I., Sevoian M. An infectious agent producing hepatitis in turkeys. Avian Dis. 1959, 3:377-388.
88. Stallknecht D.E., Nagy E., Hunter D.B., Slemons R.D. Avian influenza. Infectious Diseases of Wild Birds 2007, 108-130. Wiley-Blackwell, San Diego, Oxford. N.J. Thomas, D.B. Hunter, C.T. Atkinson (Eds.).
89. Stanway G. Structure, function and evolution of picornaviruses. J. Gen. Virol. 1990, 71:2483-2501.
90. Sweeney T.R., Dhote V., Yu Y., Hellen C.U. A distinct class of internal ribosomal entry site in members of the Kobuvirus and proposed Salivirus and Paraturdivirus genera of the Picornaviridae. J. Virol. 2012, 86:1468-1486.
91. Tannock G.A., Shafren D.R. Avian encephalomyelitis: a review. Avian Pathol. 1994, 23:603-620.
92. Taylor L.H., Latham S.M., Woolhouse M.E. Risk factors for human disease emergence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 29:983-989.
93. Tengs T., Kristoffersen A.B., Bachvaroff T.R., Jonassen C.M. A mobile genetic element with unknown function found in distantly related viruses. Virol. J. 2013, 25(10):132.
94. Todd D., Smyth V.J., Ball N.W., Donnelly B.M., Wylie M., Knowles N.J., Adair B.M. Identification of chicken enterovirus-like viruses, duck hepatitis virus type 2 and duck hepatitis virus type 3 as astroviruses. Avian Pathol. 2009, 38:21-30.
95. Todd S., Towner J.S., Brown D.M., Semler B.L. Replication-competent picornaviruses with complete genomic RNA 3' noncoding region deletions. J. Virol. 1997, 71:8868-8874.
96. Toplu N., Alcigir G. Avian encephalomyelitis in naturally infected pigeons in Turkey. Avian Pathol. 2004, 33:381-386.
97. Tseng C.H., Tsai H.J. Sequence analysis of a duck picornavirus isolate indicates that it together with porcine enterovirus type 8 and simian picornavirus type 2 should be assigned to a new picornavirus genus. Virus Res. 2007, 129:104-114.
98. Tseng C.H., Knowles N.J., Tsai H.J. Molecular analysis of type 1 duck hepatitis virus indicated that it should be assigned to a new genus. Virus Res. 2007, 123:190-203.
99. Uetz, P., Jirí Hošek (Eds.), The Reptile Database,. http://www.reptile-database.org,%20accessed%20Jan%208,%202014.
100. Wang X., Liu N., Wang F., Ning K., Li Y., Zhang D. Genetic characterization of a novel duck-origin picornavirus with six 2A proteins. J. Gen. Virol. 2014, 95:1289-1296.
101. Wang L., Pan M., Fu Y., Zhang D. Classification of duck hepatitis virus into three genotypes based on molecular evolutionary analysis. Virus Genes 2008, 37:52-59.
102. Wang X., Zhang J., Lu J., Yi F., Liu C., Hu Y. Sequence analysis and genomic organization of a new insect picorna-like virus, Ectropis obliqua picorna-like virus, isolated from Ectropis obliqua. J. Gen. Virol. 2004, 85:1145-1151.
103. Welchman Dde B., Cox W.J., Gough R.E., Wood A.M., Smyth V.J., Todd D., Spackman D. Avian encephalomyelitis virus in reared pheasants: a case study. Avian Pathol. 2009, 38:251-256.
104. Wilson D.E., Reeder D.M. Preface and introductory material. Mammal Species of the World 2005, Johns Hopkins University Press, (p. xxvi. ISBN 978-0-8018-8221-0. OCLC 62265494). third ed.
105. Woo P.C., Lau S.K., Choi G.K., Huang Y., Teng J.L., Tsoi H.W., Tse H., Yeung M.L., Chan K.H., Jinm D.Y., Yuen K.Y. Natural occurrence and characterization of two internal ribosome entry site elements in a novel virus, canine picodicistrovirus, in the picornavirus-like superfamily. J. Virol. 2012, 86:2797-2808.
106. Woo P.C., Lau S.K., Huang Y., Lam C.S., Poon R.W., Tsoi H.W., Lee P., Tse H., Chan A.S., Luk G., Chan K.H., Yuen K.Y. Comparative analysis of six genome sequences of three novel picornaviruses, turdiviruses 1, 2 and 3, in dead wild birds and proposal of two novel genera, Orthoturdivirus and Paraturdivirus, in Picornaviridae. J. Gen. Virol. 2010, 91:2433-2448.
107. Woolcock P.R. Duck hepatitis virus type I: studies with inactivated vaccines in breeder ducks. Avian Pathol. 1991, 20:509-522.
108. Wu C.Y., Lo C.F., Huang C.J., Yu H.T., Wang C.H. The complete genome sequence of Perina nuda picorna-like virus, an insect-infecting RNA virus with a genome organization similar to that of the mammalian picornaviruses. Virology 2002, 294:312-323.
109. Zoll J., Heus H.A., van Kuppeveld F.J., Melchers W.J. The structure-function relationship of the enterovirus 3'-UTR. Virus Res. 2009, 139:209-216.