The RNAs and Proteins of dsRNA Viruses


Edited by Peter. P. C. Mertens, Houssam Attoui and Dennis H. Bamford

Back to dsRNA virus Homepage 

Up ]


The dsRNA genome segments and proteins of Pseudomonas phage Phi 6  

(genus Cystovirus : family Cystoviridae


(available as a Word file)  last updated 11/09/2002


(Size, bp)


Open reading frames (ORFs)



(': protein structure/ function)

Size 'aa' (kDa )


protein copy number per particle






Gene 1






[2. 6]

inner particle shell

Self assembles with proteins P2, P4 and P7 into procapsid particles [9, 29]. Corresponds to the T=2 particle in BTV [11]. Controls procapsid size and organization. Binds minor proteins and RNA. Conserved in dsRNA viruses.



Gene 2

P2 (pol)

[3, 18, 19]





inner particle

Semi-conservative RNA dependent RNA polymerase [34, 35]. Isolated protein acts on ss and dsRNA templates [18, 19]. Three-dimensional structure homologous to HIV reverse transcriptase and hepatitis C polymerase [3]. Binding sites for nucleic acid, NTPs, Mn and Mg ions known [3].



Gene 3

P3 (spike)





extends from virion surface [17] and is attached to the integral membrane protein P6 [25]

Binds to the receptor [25] , the pilus IV of Pseudomonas syringae [30, 31]



Gene 4

P4 (NTPase)

[7, 10, 16]





inner particle at 5 fold axes


Hexameric NTPase, symmetry mismatched position [7, 10, 16]. Powers the packaging of ssRNA genomic precursors and is involved in transcription [27]. Nucleates the assembly of the procapsid with P1 [29]



Gene 5

P5 (mur)

[4, 12, 21]




between the membrane and NC


Muralytic enzyme exposed to host peptidoglycan layer after membrane fusion during viral entry. Also used to lyse the host cell late in infection to release the virus [4, 12, 21].



Gene 6

P6 (fus)







Integral membrane protein that has membrane fusion activity and binds the receptor -binding protein, P3 [1, 25, 32].



Gene 7

P7 (assembly factor) [29]





inner particle


Dimeric, stabilizes the procapsid [15]. Increases the assembly rate of the procapsid in vitro [29]



Gene 8

P8 (T=13)





[2, 29]

second protein layer


A trimer [29] that forms the T=13 nucleocapsid shell around the dsRNA-containing inner particle (core) [2]. During entry P8 drives the penetration of the nucleocapsid into the cytoplasm [26, 28].



Gene 9

P9 (env)

[13, 32, 33]






Major membrane protein, essential for membrane formation [13, 32, 33]


Gene 10

P10 (lys)






Needed for cell lysis [14]


Gene 12



[13. 22, 25]






Assembly factor active in viral membrane morphogenesis [13, 22, 25].


Gene 13







Minor, nonessential membrane protein [8, 24]


Gene 14





Non- structural


Nonessential [5].


': ': To facilitate comparisons of proteins across species, genera and families, protein structure / function indicators have been added to protein names, eg (pol) = RNA polymerase; (T=2) = capsid protein organized with icosahedral T=2 symmetry; (T=13) = capsid protein organized with icosahedral T=13 symmetry.


Constructed by Sarah Butcher and Dennis Bamford.


If you have any queries regarding this page please contact Peter Mertens on



  1. Bamford, D.H., Romantschuk, M. and Somerharju, P.J. (1987) Membrane fusion in prokaryotes: bacteriophage phi6 membrane fuses with the Pseudomonas syringae outer membrane. EMBO J., 6, 1467-1473.

  2. Butcher, S.J., Dokland, T., Ojala, P.M., Bamford, D.H. and Fuller, S.D. (1997) Intermediates in the assembly pathway of the double-stranded RNA virus f6. EMBO J., 16, 4477-4487.

  3. Butcher, S.J., Grimes, J.M., Makeyev, E.V., Bamford, D.H. and Stuart, D.I. (2001) A mechanism for initiating RNA-dependent RNA polymerization. Nature, 410, 235-40.

  4. Caldentey, J. and Bamford, D.H. (1992) The lytic enzyme of the Pseudomonas phage phi 6. Purification and biochemical characterization. Biochim Biophys Acta, 1159, 44-50.

  5. Casini, G. and Revel, H.R. (1994) A new small low-abundant nonstructural protein encoded by the L segment of the dsRNA bacteriophage phi 6. Virology, 203, 221-8.

  6. Day, L.A. and Mindich, L. (1980) The molecular weight of bacteriophage phi6 and its nucleocapsid. Virology, 103, 376-385.

  7. de Haas, F., Paatero, A.O., Mindich, L., Bamford, D.H. and Fuller, S.D. (1999) A symmetry mismatch at the site of RNA packaging in the polymerase complex of dsRNA bacteriophage phi6. J Mol Biol, 294, 357-72.

  8. Gottlieb, P., Metzger, S., Romantschuk, M., Carton, J., Strassman, J., Bamford, D.H., Kalkkinen, N. and Mindich, L. (1988a) Nucleotide sequence of the middle dsRNA segment of bacteriophage phi 6: placement of the genes of membrane-associated proteins. Virology, 163, 183-90.

  9. Gottlieb, P., Strassman, J., Bamford, D. and Mindich, L. (1988b) Production of a polyhedral particle in Escherichia coli from a cDNA copy of the large genome segment of Phi 6. J. Virol., 62, 181-187.

  10. Gottlieb, P., Strassman, J. and Mindich, L. (1992) Protein P4 of the bacteriophage phi 6 procapsid has a nucleoside triphosphate-binding site with associated nucleoside triphosphate phosphohydrolase activity. J. Virol., 66, 6220-2.

  11. Grimes, J.M., Burroughs, J.N., Gouet, P., Diprose, J.M., Malby, R., Zientara, S., Mertens, P.P. and Stuart, D.I. (1998) The atomic structure of the bluetongue virus core. Nature, 395, 470-8.

  12. Hantula, J. and Bamford, D.H. (1988) Chemical crosslinking of bacteriophage 6 nucleocapsid proteins. Virology, 165, 482-488.

  13. Johnson, M.D. and Mindich, L. (1994a) Plasmid-directed assembly of the lipid-containing membrane of bacteriophage phi 6. J Bacteriol, 176, 4124-32.

  14. Johnson, M.D. (3rd) and Mindich, L. (1994b) Isolation and characterization of nonsense mutations in gene 10 of bacteriophage phi 6. J. Virol., 68, 2331-8.

  15. Juuti, J.T. and Bamford, D.H. (1997) Protein P7 of phage phi6 RNA polymerase complex, acquiring of RNA packaging activity by in vitro assembly of the purified protein onto deficient particles. J Mol Biol, 266, 891-900.

  16. Juuti, J.T., Bamford, D.H., Tuma, R. and Thomas, G.J., Jr. (1998) Structure and NTPase activity of the RNA-translocating protein (P4) of bacteriophage phi 6. J Mol Biol, 279, 347-59.

  17. Kenney, J.M., Hantula, J., Fuller, S.D., Mindich, L., Ojala, P.M. and Bamford, D.H. (1992) Bacteriophage phi 6 envelope elucidated by chemical cross-linking, immunodetection, and cryoelectron microscopy. Virology, 190, 635-644.

  18. Makeyev, E.V. and Bamford, D.H. (2000a) The polymerase subunit of a dsRNA virus plays a central role in the regulation of viral RNA metabolism. EMBO J., 19, 6275-6284.

  19. Makeyev, E.V. and Bamford, D.H. (2000b) Replicase activity of purified recombinant protein P2 of double- stranded RNA bacteriophage phi6. EMBO J, 19, 124-133.

  20. McGraw, T., Mindich, L. and Frangione, B. (1986) Nucleotide sequence of the small double-stranded RNA segment of bacteriophage phi 6: novel mechanism of natural translational control. J. Virol., 58, 142-151.

  21. Mindich, L. and Lehman, J.F. (1979) Cell wall lysin as a component of the bacteriophage 6 virion. J. Virology, 30, 489-496.

  22. Mindich, L. and Lehman, J.F. (1983) Characterization of phi6 mutants that are temperature sensitive in the morphogenetic protein P12. Virology,127, 438-445.

  23. Mindich, L., Nemhauser, I., Gottlieb, P., Romantschuk, M., Carton, J., Frucht, S., Strassman, J., Bamford, D.H. and Kalkkinen, N. (1988) Nucleotide sequence of the large double-stranded RNA segment of bacteriophage phi 6: genes specifying the viral replicase and transcriptase. J.Virol., 62, 1180-5.

  24. Mindich, L., Qiao, X., Onodera, S., Gottlieb, P. and Strassman, J. (1992) Heterologous recombination in the double-stranded RNA bacteriophage phi 6. J. Virol., 66, 2605-10.

  25. Mindich, L., Sinclair, J.F. and Cohen, J. (1976) The morphogenesis of bacteriophage phi6: particles formed by nonsense mutants. Virology, 75,224-231.

  26. Olkkonen, V.M., Ojala, P.M. and Bamford, D.H. (1991) Generation of infectious nucleocapsids by in vitro assembly of the shell protein on to the polymerase complex of the dsRNA bacteriophage phi 6. J Mol Biol, 218, 569-581.

  27. Pirttimaa, M.J., Paatero, A.O., Frilander, M.J. and Bamford, D.H. (2002) Nonspecific nucleoside triphosphatase P4 of double-stranded RNA bacteriophage phi6 is required for single-stranded RNA packaging and transcription. J Virol, 76.

  28. Poranen, M.M., Daugelavicius, R., Ojala, P.M., Hess, M.W. and Bamford, D.H. (1999) A novel virus-host cell membrane interaction. Membrane voltage-dependent endocytic-like entry of bacteriophage phi6 nucleocapsid. J Cell Biol, 147, 671-82.

  29. Poranen, M.M., Paatero, A.O., Tuma, R. and Bamford, D.H. (2001) Self assembly of a viral molecular machine from purified protein and RNA constituents. Molecular Cell, 7, 845-854.

  30. Roine, E., Raineri, D.M., Romantschuk, M., Wilson, M. and Nunn, D.N. (1998) Characterization of type IV pilus genes in Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact, 11, 1048-56.

  31. Romantschuk, M. and Bamford, D.H. (1985) Function of pili in bacteriophage phi6 penetration. J. Gen. Virol., 66, 2461-2469.

  32. Sinclair, J.F., Tzagoloff, A., Levine, D. and Mindich, L. (1975) Proteins of the bacteriophage phi6. Virology, 75, 685-695.

  33. Stitt, B.L. and Mindich, L. (1983) Morphogenesis of bacteriophage phi6: a presumptive viral membrane precursor. Virology, 127, 446-458.

  34. Usala, S.J., Brownstein, B.H. and Haselkorn, R. (1980) Displacement of parental RNA strands during in vitro transcription by bacteriophage phi6 nucleocapsids. Cell, 19, 855-862.

  35. Van Etten, J.L., Burbank, D.E., Cuppels, D.A., Lane, L.C. and Vidaver, A.K. (1980) Semiconservative synthesis of single-stranded RNA by bacteriophage phi6 polymerase. J. Virol., 33, 769-773.

Hit Counter



(The RNAs and Proteins  of dsRNA Viruses:  Edited by Peter. P. C. Mertens, Houssam Attoui and Dennis H. Bamford)