1887

Chapter 9 : Molecular Biology and Evolution of Toroviruses

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Molecular Biology and Evolution of Toroviruses, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815790/9781555814557_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555815790/9781555814557_Chap09-2.gif

Abstract:

Toroviruses were discovered in 1972, but in comparison to their more glamorous nidovirus cousins, the corona- and arteriviruses, they have received precious little attention. In this chapter the observations are combined with more recent findings, yielding a rough but intriguing picture of the molecular biology, life cycle, and evolution of this fascinating group of viruses. It therefore came as a bit of a blow—at least to torovirus aficionados—that Berne virus (BEV) turned out to be coronavirus-like after all, not only with respect to the organization and expression of its genome but also genetically. Indirect but convincing evidence for torovirus infection in various mammalian host species was obtained by heterotypic virus neutralization assay (VNA). BEV-neutralizing antibodies were detected not only in horses and cattle but also in swine, sheep, goats, rabbits, and mice. Like corona- and arteriviruses, toroviruses presumably employ subgenomic minus-strand RNAs as templates for sg mRNA synthesis. Computer-assisted analysis of torovirus replicase polyprotein sequences has revealed an array of characteristic domains, the presence and order of which are conserved among (most) nidoviruses; conspicuous differences notwithstanding, the 1ab polyproteins of toro- and coronaviruses are essentially collinear, with all key domains located at cognate positions. The N protein and the viral genomic RNA apparently autoassemble into tubular structures; whether the N protein can also form empty capsids is not known, nor is there information about the mechanism and specificity of the encapsidation process.

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9

Key Concept Ranking

Infectious salmon anemia virus
0.46983972
0.46983972
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1.
Figure 1.

Torovirus virion structure. A schematic model is presented with the virion depicted as a rod. Also shown are electron micrographs reprinted from the ( ) with permission of the publisher. (a) A purified BEV nucleocapsid with the envelope removed by ethyl ether treatment; note the transverse striation. (b) Cross section through a BEV virion. The particle appears as three concentric circles of high electron density. Note the electron lucent center, thought to represent the hollow inner space of the tubular nucleocapsid, which itself appears as the electron-dense inner ring. Bar markers represent 25 nm.

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2.
Figure 2.

Structural characteristics of torovirus N and M proteins. (Upper panel) Linear representations of the N protein, depicted either as a horizontal bar (top) or as boxes (below), indicating the location of a conserved potential protein kinase C phosphorylation site (lollipop) and the distribution of arginine residues (vertical bars; top box), of glutamine/asparagine residues (middle), and of the amino acid differences between the N proteins of BEV and BRV (bottom). (Lower panel) Linear representation of the M protein depicted as a box, with vertical bars indicating the locations of amino acid differences among all known equine torovirus, BToV, and PToV M proteins. The locations of predicted transmembrane domains are indicated by horizontal black boxes underneath. A topological model of the torovirus M protein (adapted from reference 14) is presented at the bottom.

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3.
Figure 3.

Structural characteristics of the torovirus S protein. Linear representations of S proteins of a torovirus (BEV) and a coronavirus (mouse hepatitis virus strain A59), depicted as boxes and on scale. The locations of signal peptides (SP), putative fusion peptides (FP), and transmembrane domains (TM) are indicated as black boxes. The locations of regions with heptad repeat periodicity (HR) are indicated by hatched boxes. Dashed vertical bars plus arrowheads indicate the positions of cleavage sites (CS) for furin-like cellular proteases. The middle box shows the distribution of amino acid differences (indicated by vertical bars) between the BEV and BRV S proteins.

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4.
Figure 4.

Organization and expression of the torovirus genome. The central portion shows a schematic representation of the torovirus genome (on scale), with the genes for the structural proteins (S, M, and N proteins and HE) and for the replicase polyproteins (pp1a and pp1ab) depicted as boxes. The various domains in the replicase polyproteins are indicated using the following abbreviations: A, ADP-ribose 1”-phosphatase; PP, papain-like proteinase; C, cyclic phosphodiesterase; Z, zinc-binding domain; Hel, helicase; Exo, 3’-to-5’exoribonuclease domain; U, nidoviral uridylate-specific endoribonuclease; and MT, ribose-2 methyltransferase. Hydrophobic segments in pp1a are indicated by cross-hatching. Arrowheads and vertical bars indicate M cleavage sites, established by N-terminal sequence analysis (closed) or predicted on the basis of the cleavage site consensus sequence and comparative sequence analysis (open). Two hypervariable regions in pp1a are indicated by brackets ( ). The lower set of boxes shows the amino acid sequence variation between the BEV and BRV proteomes, with amino acid differences indicated by vertical bars. The bottom graph shows the amino acid sequence identity between BEV and BRV. Sliding-window analysis of the BEV-BRV proteome alignment was performed for the replicase polyproteins and the S protein with a window size of 500 residues and a 250-residue step size; for the M (partial) and N proteins and HE, overall sequence identity is given. The upper panel shows the structure of the intracellular viral RNAs (1 through 5), with RNA1 representing the viral genome and RNA2 through -5 the sg mRNAs for the S and M proteins, HE, and N protein, respectively. Internal TREs, located upstream of the genes for the M and N proteins and HE, are indicated by black boxes. The genomic TRE, present at the 5’ ends of RNA1 and -2, is indicated by an open box. A, poly(A) tail.

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5.
Figure 5.

Genetic exchanges among PToV and BToV field variants. Torovirus genomes are depicted schematically, with the various genes represented by boxes. Types of PToVs and BToVs are indicated; question marks indicate parental toroviruses that have not been identified so far.

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6.
Figure 6.

Torovirus transcription. (Left panel) Structure of the BEV DTE in ORF1b and corresponding sequences in the PToV and BToV genomes ( ). The DTE consists of a hairpin followed by a region sharing sequence similarity with the 5’ end of the genome; ORF1b-genome alignments are shown, with asterisks indicating identical residues. The arrowhead indicates the mRNA2 leader-body fusion site; arrows indicate nucleotide substitutions in the PToV and BToV hairpins compared to that of BEV; note that base pairing is maintained. (Right panel) Current working model for the discontinuous synthesis of BEV mRNA2 and for the nondiscontinuous transcription of mRNA3 to -5. Details are explained in the text (adapted from reference ).

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 7.
Figure 7.

Single-cell replicative cycle of BEV. (a) Replicative cycle of BEV, with the open arrow indicating the chronological order of the various stages. It is not known whether entry occurs at the plasma membrane or via the endocytotic route. Similarly, it is not known whether torovirus replication occurs in association with double membrane vesicles. (b) Deposits of tubular structures in the cytoplasm of a BEV-infected cell. (c) Viruses budding through membranes of Golgi cisternae (arrowheads). (d to f) Various stages of viral budding into smooth membrane vesicles. Bar markers represent 100 nm (micrographs reprinted from the [74, 76] with permission of the publisher).

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555815790.ch09
1. Bayer, T. S.,, L. N. Booth,, S. M. Knudsen, and, A. D. Ellington. 2005. Arginine-rich motifs present multiple interfaces for specific binding by RNA. RNA 11:18481857.
2. Beards, G. M.,, D. W. Brown,, J. Green, and, T. H. Flewett. 1986. Preliminary characterisation of torovirus-like particles of humans: comparison with Berne virus of horses and Breda virus of calves. J. Med. Virol. 20:6778.
3. Beards, G. M.,, C. Hall,, J. Green,, T. H. Flewett,, F. Lamouliatte, and, P. Du Pasquier. 1984. An enveloped virus in stools of children and adults with gastroenteritis that resembles the Breda virus of calves. Lancet i:10501052.
4. Blom, N.,, T. Sicheritz-Ponten,, R. Gupta,, S. Gammeltoft, and, S. Brunak. 2004. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4:16331649.
5. Bosch, B. J.,, B. E. Martina,, R. Van Der Zee,, J. Lepault,, B. J. Haijema,, C. Versluis,, A. J. Heck,, R. De Groot,, A. D. Osterhaus, and, P. J. Rottier. 2004. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. USA 101:84558460.
6. Bosch, B. J.,, R. van der Zee,, C. A. de Haan, and, P. J. Rottier. 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77:88018811.
7. Boulikas, T. 1993. Nuclear localization signals (NLS). Crit. Rev. Eukaryot. Gene Expr. 3:193227.
8. Cavanagh, D.,, D. A. Brian,, M. A. Brinton,, L. Enjuanes,, K. V. Holmes,, M. C. Horzinek,, M. M. Lai,, H. Laude,, P. G. Plagemann,, S. G. Siddell, et al. 1993. The Coronaviridae now comprises two genera, coronavirus and torovirus: report of the Coronaviridae Study Group. Adv. Exp. Med. Biol. 342:255257.
9. Cavanagh, D., and, M. C. Horzinek. 1993. Genus Torovirus assigned to the Coronaviridae. Arch. Virol. 128:395396.
10. Cornelissen, L. A.,, P. A. van Woensel,, R. J. de Groot,, M. C. Horzinek,, N. Visser, and, H. F. Egberink. 1998. Cell culture-grown putative bovine respiratory torovirus identified as a coronavirus. Vet. Rec. 142:683686.
11. Cornelissen, L. A.,, C. M. Wierda,, F. J. van der Meer,, A. A. Herrewegh,, M. C. Horzinek,, H. F. Egberink, and, R. J. de Groot. 1997. Hemagglutinin-esterase, a novel structural protein of torovirus. J. Virol. 71:52775286.
12. de Groot, R. J. 2006. Structure, function and evolution of the hemagglutinin-esterase proteins of corona- and toroviruses. Glycoconj. J. 23:5972.
13. de Groot, R. J.,, W. Luytjes,, M. C. Horzinek,, B. A. van der Zeijst,, W. J. Spaan, and, J. A. Lenstra. 1987. Evidence for a coiled-coil structure in the spike proteins of coronaviruses. J. Mol. Biol. 196:963966.
14. Den Boon, J. A.,, E. J. Snijder,, J. K. Locker,, M. C. Horzinek, and, P. J. Rottier. 1991. Another triple-spanning envelope protein among intracellularly budding RNA viruses: the torovirus E protein. Virology 182:655663.
15. Draker, R.,, R. L. Roper,, M. Petric, and, R. Tellier. 2006. The complete sequence of the bovine torovirus genome. Virus Res. 115:5668.
16. Duckmanton, L.,, S. Carman,, E. Nagy, and, M. Petric. 1998. Detection of bovine torovirus in fecal specimens of calves with diarrhea from Ontario farms. J. Clin. Microbiol. 36:12661270.
17. Duckmanton, L.,, B. Luan,, J. Devenish,, R. Tellier, and, M. Petric. 1997. Characterization of torovirus from human fecal specimens. Virology 239:158168.
18. Duckmanton, L.,, R. Tellier,, C. Richardson, and, M. Petric. 1999. The novel hemagglutinin-esterase genes of human toro-virus and Breda virus. Virus Res. 64:137149.
19. Duckmanton, L. M.,, R. Tellier,, P. Liu, and, M. Petric. 1998. Bovine torovirus: sequencing of the structural genes and expression of the nucleocapsid protein of Breda virus. Virus Res. 58:8396.
20. Durham, P. J.,, L. E. Hassard,, G. R. Norman, and, R. L. Yemen. 1989. Viruses and virus-like particles detected during examination of feces from calves and piglets with diarrhea. Can. Vet. J. 30:876881.
21. Dutch, R. E.,, T. S. Jardetzky, and, R. A. Lamb. 2000. Virus membrane fusion proteins: biological machines that undergo a metamorphosis. Biosci. Rep. 20:597612.
22. Fagerland, J. A.,, J. F. Pohlenz, and, G. N. Woode. 1986. A morphological study of the replication of Breda virus (proposed family Toroviridae) in bovine intestinal cells. J. Gen. Virol. 67:12931304.
23. Falk, K.,, V. Aspehaug,, R. Vlasak, and, C. Endresen. 2004. Identification and characterization of viral structural proteins of infectious salmon anemia virus. J. Virol. 78:30633071.
24. Finlaison, D. S. 1995. Faecal viruses of dogs—an electron microscope study. Vet. Microbiol. 46:295305.
25. Garzon, A.,, A. M. Maestre,, J. Pignatelli, and, M. T. Rejas, and, D. Rodriguez. 2006. New insights on the structure and morphogenesis of Berne virus. Adv. Exp. Med. Biol. 581:175180.
26. Gonzalez, J. M.,, P. Gomez-Puertas,, D. Cavanagh,, A. E. Gorbalenya, and, L. Enjuanes. 2003. A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch. Virol. 148:22072235.
27. Haschek, B.,, D. Klein,, V. Benetka,, C. Herrera,, I. Sommerfeld-Stur,, S. Vilcek,, K. Moestl, and, W. Baumgartner. 2006. Detection of bovine torovirus in neonatal calf diarrhoea in Lower Austria and Styria (Austria). J. Vet. Med. Ser. B 53:160165.
28. Hellebo, A.,, U. Vilas,, K. Falk, and, R. Vlasak. 2004. Infectious salmon anemia virus specifically binds to and hydrolyzes 4-O-acetylated sialic acids. J. Virol. 78:30553062.
29. Hoet, A. E.,, K. O. Chang, and, L. J. Saif. 2003. Comparison of ELISA and RT-PCR versus immune electron microscopy for detection of bovine torovirus (Breda virus) in calf fecal specimens. J. Vet. Diagn. Investig. 15:100106.
30. Hoet, A. E.,, K. O. Cho,, K. O. Chang,, S. C. Loerch,, T. E. Wittum, and, L. J. Saif. 2002. Enteric and nasal shedding of bovine torovirus (Breda virus) in feedlot cattle. Am. J. Vet. Res. 63:342348.
31. Hoet, A. E.,, P. R. Nielsen,, M. Hasoksuz,, C. Thomas,, T. E. Wittum, and, L. J. Saif. 2003. Detection of bovine torovirus and other enteric pathogens in feces from diarrhea cases in cattle. J. Vet. Diagn. Investig. 15:205212.
32. Hoet, A. E., and, L. J. Saif. 2004. Bovine torovirus (Breda virus) revisited. Anim. Health Res. Rev. 5:157171.
33. Horzinek, M. C. 1984. Nonarbo animal togaviruses and control perspectives, p. 163177. In E. Kurstak (ed.), Control of Virus Diseases. Academic Press, New York, NY.
34. Horzinek, M. C. 1993. Toroviruses—members of the corona-virus superfamily? Arch. Virol. Suppl. 7:7580.
35. Horzinek, M. C.,, J. Ederveen,, B. Kaeffer,, D. de Boer, and, M. Weiss. 1986. The peplomers of Berne virus. J. Gen. Virol. 67:24752483.
36. Horzinek, M. C.,, J. Ederveen, and, M. Weiss. 1985. The nucleocapsid of Berne virus. J. Gen. Virol. 66(Pt. 6):12871296.
37. Horzinek, M. C.,, T. H. Flewett,, L. J. Saif,, W. J. Spaan,, M. Weiss, and, G. N. Woode. 1987. A new family of vertebrate viruses: Toroviridae. Intervirology 27:1724.
38. Horzinek, M. C., and, M. Weiss. 1984. Toroviridae: a taxonomic proposal. Zbl. Veted. Reihe B 31:649659.
39. Horzinek, M. C.,, M. Weiss, and, J. Ederveen. 1984. Berne virus is not ‘coronavirus-like’. J. Gen. Virol. 65:645649.
40. Kaeffer, B.,, P. van Kooten,, J. Ederveen,, W. van Eden, and, M. C. Horzinek. 1989. Properties of monoclonal antibodies against Berne virus (Toroviridae). Am. J. Vet. Res. 50:11311137.
41. Kielian, M., and, F. A. Rey. 2006. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:6776.
42. Koonin, E. V. 1991. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72:21972206.
43. Koopmans, M., and, M. C. Horzinek. 1994. Toroviruses of animals and humans: a review. Adv. Virus Res. 43:233273.
44. Koopmans, M.,, E. J. Snijder, and, M. C. Horzinek. 1991. cDNA probes for the diagnosis of bovine torovirus (Breda virus) infection. J. Clin. Microbiol. 29:493497.
45. Koopmans, M.,, U. van den Boom,, G. Woode, and, M. C. Horzinek. 1989. Seroepidemiology of Breda virus in cattle using ELISA. Vet. Microbiol. 19:233243.
46. Krishnan, T., and, T. N. Naik. 1997. Electronmicroscopic evidence of torovirus like particles in children with diarrhoea. Indian J. Med. Res. 105:108110.
47. Kroneman, A.,, L. A. Cornelissen,, M. C. Horzinek,, R. J. de Groot, and, H. F. Egberink. 1998. Identification and characterization of a porcine torovirus. J. Virol. 72:35073511.
48. Lissenberg, A.,, M. M. Vrolijk,, A. L. van Vliet,, M. A. Langereis,, J. D. de Groot-Mijnes,, P. J. Rottier, and, R. J. de Groot. 2005. Luxury at a cost? Recombinant mouse hepatitis viruses expressing the accessory hemagglutinin esterase protein display reduced fitness in vitro. J. Virol. 79:1505415063.
49. Matiz, K.,, S. Kecskemeti,, I. Kiss,, Z. Adam,, J. Tanyi, and, B. Nagy. 2002. Torovirus detection in faecal specimens of calves and pigs in Hungary: short communication. Acta Vet. Hung. 50:293296.
50. Moussa, A.,, G. Dannacher, and, M. Fedida. 1983. Nouveaux virus intervenant dans l’etiologie des enteritis neonatales des bovins. Recl. Med. Vet. 159:185190.
51. Muir, P.,, D. A. Harbour,, T. J. Gruffydd-Jones,, P. E. Howard,, C. D. Hopper,, E. A. Gruffydd-Jones,, H. M. Broadhead,, C. M. Clarke, and, M. E. Jones. 1990. A clinical and microbiological study of cats with protruding nictitating membranes and diarrhoea: isolation of a novel virus. Vet. Rec. 127:324330.
52. Penrith, M. L., and, G. H. Gerdes. 1992. Breda virus-like particles in pigs in South Africa. J. S. Afr. Vet. Assoc. 63:102.
53. Rosenthal, P. B.,, X. Zhang,, F. Formanowski,, W. Fitz,, C. H. Wong,, H. Meier-Ewert,, J. J. Skehel, and, D. C. Wiley. 1998. Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 396:9296.
54. Schibli, D. J., and, W. Weissenhorn. 2004. Class I and class II viral fusion protein structures reveal similar principles in membrane fusion. Mol. Membr. Biol. 21:361371.
55. Schütze, H.,, R. Ulferts,, B. Schelle,, S. Bayer,, H. Granzow,, B. Hoffmann,, T. C. Mettenleiter, and, J. Ziebuhr. 2006. Characterization of white bream virus reveals a novel genetic cluster of nidoviruses. J. Virol. 80:84938502.
56. Scott, A. C.,, M. J. Chaplin,, M. J. Stack, and, L. J. Lund. 1987. Porcine torovirus? Vet. Rec. 120:583.
57. Scott, F. M.,, A. Holliman,, G. W. Jones,, E. W. Gray, and, J. Fitton. 1996. Evidence of torovirus infection in diarrhoeic cattle. Vet. Rec. 138:284285.
58. Smits, S. L.,, G. J. Gerwig,, A. L. van Vliet,, A. Lissenberg,, P. Briza,, J. P. Kamerling,, R. Vlasak, and, R. J. de Groot. 2005. Nidovirus sialate-O-acetylesterases: evolution and substrate specificity of coronaviral and toroviral receptor-destroying enzymes. J. Biol. Chem. 280:69336941.
59. Smits, S. L.,, A. Lavazza,, K. Matiz,, M. C. Horzinek,, M. P. Koopmans, and, R. J. de Groot. 2003. Phylogenetic and evolutionary relationships among torovirus field variants: evidence for multiple intertypic recombination events. J. Virol. 77:95679577.
60. Smits, S. L.,, E. J. Snijder, and, R. J. de Groot. 2006. Characterization of a torovirus main proteinase. J. Virol. 80:41574167.
61. Smits, S. L.,, A. L. van Vliet,, K. Segeren,, H. el Azzouzi,, M. van Essen, and, R. J. de Groot. 2005. Torovirus non-discontinuous transcription: mutational analysis of a subgenomic mRNA promoter. J. Virol. 79:82758281.
62. Snijder, E. J.,, P. J. Bredenbeek,, J. C. Dobbe,, V. Thiel,, J. Ziebuhr,, L. L. Poon,, Y. Guan,, M. Rozanov,, W. J. Spaan, and, A. E. Gorbalenya. 2003. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331:9911004.
63. Snijder, E. J.,, J. A. den Boon,, P. J. Bredenbeek,, M. C. Horzinek,, R. Rijnbrand, and, W. J. Spaan. 1990. The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and coronaviruses are evolutionarily related. Nucleic Acids Res. 18:45354542.
64. Snijder, E. J.,, J. A. den Boon,, M. C. Horzinek, and, W. J. Spaan. 1991. Characterization of defective interfering RNAs of Berne virus. J. Gen. Virol. 72:16351643.
65. Snijder, E. J.,, J. A. den Boon,, M. C. Horzinek, and, W. J. Spaan. 1991. Comparison of the genome organization of toro- and coronaviruses: evidence for two nonhomologous RNA recombination events during Berne virus evolution. Virology 180:448452.
66. Snijder, E. J.,, J. A. den Boon,, W. J. Spaan,, G. M. Verjans, and, M. C. Horzinek. 1989. Identification and primary structure of the gene encoding the Berne virus nucleocapsid protein. J. Gen. Virol. 70(Pt. 12):33633370.
67. Snijder, E. J.,, J. A. Den Boon,, W. J. Spaan,, M. Weiss, and, M. C. Horzinek. 1990. Primary structure and post-translational processing of the Berne virus peplomer protein. Virology 178:355363.
68. Snijder, E. J.,, J. Ederveen,, W. J. Spaan,, M. Weiss, and, M. C. Horzinek. 1988. Characterization of Berne virus genomic and messenger RNAs. J. Gen. Virol. 69:21352144.
69. Snijder, E. J., and, M. C. Horzinek. 1993. Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. J. Gen. Virol. 74:23052316.
70. Snijder, E. J.,, M. C. Horzinek, and, W. J. Spaan. 1990. A 3’-coterminal nested set of independently transcribed mRNAs is generated during Berne virus replication. J. Virol. 64:331338.
71. Snijder, E. J.,, M. C. Horzinek, and, W. J. Spaan. 1993. The coronaviruslike superfamily. Adv. Exp. Med. Biol. 342:235244.
72. Spann, K. M., and, R. J. G. Lester. 1997. Special topic review: viral diseases of penaeid shrimp with particular reference to four viruses recently found in shrimp from Queensland. World J. Microbiol. Biotechnol. 13:419426.
73. van Vliet, A. L.,, S. L. Smits,, P. J. Rottier, and, R. J. de Groot. 2002. Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. EMBO J. 21:65716580.
74. Weiss, M., and, M. C. Horzinek. 1986. Morphogenesis of Berne virus (proposed family Toroviridae). J. Gen. Virol. 67:13051314.
75. Weiss, M., and, M. C. Horzinek. 1986. Resistance of Berne virus to physical and chemical treatment. Vet. Microbiol. 11:4149.
76. Weiss, M.,, F. Steck, and, M. C. Horzinek. 1983. Purification and partial characterization of a new enveloped RNA virus (Berne virus). J. Gen. Virol. 64:18491858.
77. Weiss, M.,, F. Steck,, R. Kaderli, and, M. C. Horzinek. 1984. Antibodies to Berne virus in horses and other animals. Vet. Microbiol. 9:523531.
78. Woode, G. N.,, D. E. Reed,, P. L. Runnels,, M. A. Herrig, and, H. T. Hill. 1982. Studies with an unclassified virus isolated from diarrheic calves. Vet. Microbiol. 7:221240.
79. Woode, G. N.,, L. J. Saif,, M. Quesada,, N. J. Winand,, J. F. Pohlenz, and, N. K. Gourley. 1985. Comparative studies on three isolates of Breda virus of calves. Am. J. Vet. Res. 46:10031010.

Tables

Generic image for table
Table 1.

Torovirus species

Citation: de Groot R. 2008. Molecular Biology and Evolution of Toroviruses, p 133-146. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch9

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error