Skip to main content
SpringerLink
Log in

Evolution of viral DNA-dependent RNA polymerases

  • Part B: Molecular Processes Involved In The Evolution Of RNA And DNA Viruses
  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

The DNA-dependent RNA polymerase (DdRP or RNAP) is an essential enzyme of transcription of replicating systems of prokaryotic and eukaryotic organisms as well as cytoplasmic DNA viruses. DdRPs are complex multisubunit enzymes consisting of 8–14 subunits, including two large subunits and several smaller polypeptides (small subunits). An extensive search between the amino acid sequences of the known largest subunit of DNA-dependent RNA polymerases (RPO1) of different organisms indicates that all these polypeptides possess auniversal heptapeptideNADFDGD in domain D. All RPO1 harbor a second well-conserved hexapeptideRQP(TS)LH upstream (26–31 amino acids) of the universal motif. The genes encoding the largest subunit of DdRP of insect iridescent virus type 6 (IIV6), fish lymphocystis disease virus (LCDV), and molluscum contagiosum virus (MCV-1), all members of the group of cytoplasmic DNA viruses, were identified by PCR technology. With the exception of IIV6, all other viral RPO1 possess the two C-terminal conserved regions G and H. The lack of C-terminal repetitive heptapeptide (YSPTSPS), which is a common feature of the largest subunit of eukaryotic RNAPII, is an additional characteristic of RPO1 proteins of LCDV and of MCV-1. All viral RPO1 proteins were found to be lacking the amino acid N at a distinct position in domain F. This amino acid is known to be highly conserved in α-amanitin-sensitive eukaryotic RNA polymerases II. Comparison of the amino acid sequences of the RPO1 polypeptides of IIV6, LCDV, and MCV-1 with the corresponding prokaryotic, eukaryotic, and viral proteins revealed differences in amino acid similarity and phylogenetic relationships. IIV6 RPO1 possesses the closest similarity to the homologous subunit of eukaryotic RNAPII and lower but also significant similarity to that of eukaryotic RNAPI and RNAPIII, archaeal, eubacterial, and viral polymerases. The similarity between RPO1 of IIV6 and the cellular polymerase subunits is consistently higher than to the RPO1 of other cytoplasmic DNA viruses, for example, vaccinia and variola virus, African swine fever virus (ASFV), and MCV-1. The RPO1 of LCDV shows the highest similarity to the RPO1 of IIV6 and significant lower similarity to the eukaryotic polymerases II and III as well as to the archaebacterial subunit. However, it is still considerably more similar to the cellular polymerase subunits than to the homologous viral proteins. The RPO1 of IIV6 possesses more similarity to cellular polymerases than the complete RPO1 of LCDV, indicating that there is a substantial difference in the organization of the RPO1 genes between these members of two genera of the Iridoviridae family. Analysis of the MCV-1 RPO1 revealed high amino acid homologies to the corresponding polypeptides of vaccinia and variola virus. The viral RPO1 proteins, including vaccinia and variola virus, MCV-1, ASFV, IIV6, and LCDV, share the common feature of showing the highest similarity to the largest subunit of eukaryotic RNAPII than to that of RNAPI, RNAPIII, and RPO1 of archaebacterias, eubacterias, ASFV, IIV6, and LCDV. Evolution of the individual largest subunit of DdRPs was tentatively investigated by generating phylogenetic trees using multiple amino acid alignments. These indicate that the RPO1 proteins of IIV6 and LCDV might have evolved from the largest subunit of eukaryotic RNAPII after divergence from the homologous subunits of RNAPI and RNAPIII. In contrast, evolutionary development of the RPO1 of vaccinia and variola virus, MCV-1, and ASFV seems to be quite different, with their common ancestor diverging from cellular homologues before the separation of the three types of eukaryotic polymerases and having probably diverged earlier from their common lineage with cellular proteins.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Young R.A., Annu Rev Biochem60 689–715, 1991.

    Google Scholar 

  2. Ingles C.J., Himmelfarb H.J., Shales M., Greenleaf A.L., and Friesen J.D., Proc Natl Acad Sci USA81 2157–2161, 1984.

    Google Scholar 

  3. Riva M., Memet S., Micoin J.-Y., Huet J., Treich I., Dassa J., Young R., Buhler J.-M., Sentenac A., and Fromageot P., Proc Natl Acad Sci USA83 1554–1558, 1986.

    Google Scholar 

  4. Darst S.A., Kubalek E.W., and Kornberg R., Nature340 730–732, 1989.

    Google Scholar 

  5. Darst S.A., Edwards A.M., Kubalek E.W., and Kornberg R., Cell66 121–128, 1991.

    Google Scholar 

  6. Ollis D.L., Brick P., Hamlin R., Xuong N.G., and Steitz A.T., Nature313 762–766, 1985.

    Google Scholar 

  7. Schultz P., Célia H., Riva M., Darst S.A., Colin P., Kornberg R.D., Sentenac A., and Oudet P., J Mol Biol216 353–362, 1990.

    Google Scholar 

  8. Riva M., Carles C., Sentenac A., Grachev M.A., Mustaev A.A., and Zaychikov E.F., J Biol Chem265 16598–16503, 1990.

    Google Scholar 

  9. Sentenac A., Crit Rev Biochem18 31–91, 1985.

    Google Scholar 

  10. Sentenac A., Hall B., Strathern J.N., Jones E.W., and Broach J.R. (eds). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1982, pp. 561–606.

  11. Berghöfer B., Kröckel L., Körtner C., Truss M., Schallenberg J., and Klein A., Nucleic Acids Res16 8113–8128, 1988.

    Google Scholar 

  12. Leffers H., Gropp F., Lottspeich F., Zillig W., and Garrett R.A., J Mol Biol206 1–17, 1989.

    Google Scholar 

  13. Puhler G., Leffers H., Gropp F., Palm P., Klenk H.-P., Lottspeich F., Garrett R.A., and Zillig W., Proc Natl Acad Sci USA86 4569–4573, 1989.

    Google Scholar 

  14. Allison L.A., Moyle M., Shales M., and Ingles C.J., Cell42 599–610, 1985.

    Google Scholar 

  15. Jokerst R.S., Weeks J.R., Zehring W.A., and Grenleaf A.L., Mol Gen Genet215 166–175, 1989.

    Google Scholar 

  16. Mémet S., Saurin W., and Sentenac A., J Biol Chem263 2830–2839, 1988.

    Google Scholar 

  17. Cornelissen A.W., Evers R., and Kock J., Oxf Surv Eukaryot Genes5 91–131, 1988.

    Google Scholar 

  18. Falkenburg D., Dworniczak B., Faust D.M., and Bautz E.K.F., J Mol Biol195 929–937, 1987.

    Google Scholar 

  19. Sweetser D., Nonet M., and Young R.A., Proc Natl Acad Sci USA84 1192–1196, 1987.

    Google Scholar 

  20. James P., Whelen S., and Hall B.D., J Biol Chem266 5616–5624, 1991.

    Google Scholar 

  21. Sawadago M. and Sentenac A., Annu Rev Biochem59 711–754, 1990.

    Google Scholar 

  22. Borukhov S., Lee J., and Goldfarb A., J Biol Chem266 23932–23935, 1991.

    Google Scholar 

  23. Grachev M.A., Luchtanov E.A., Mustaev A.A., Zaychikov E.F., Abdukayumov M.N., Rabinov I.V., Richter V.I., Skoblov Y.S., and Christyakov P.G., Eur J Biochem180 577–585, 1989.

    Google Scholar 

  24. Mustaev A., Kashlev M., Lee J., Polyakov A., Lebedev A., Zalenskaya K., Grachev M., Goldfarb A., and Nikiforov V., J Biol Chem266 23927–23931, 1991.

    Google Scholar 

  25. Riva M., Carles C., Sentenac A., Grachev M.A., Mustaev A.A., and Zaychikov E.F., J Biol Chem265 16498–16503, 1990.

    Google Scholar 

  26. Chamberlin M.J.,Harvey Lectures, Series 88. Wiley-Liss, New York, 1994, pp. 1–22.

    Google Scholar 

  27. Nudler E., Goldfarb A., and Kashlev M., Science265 793–796, 1994.

    Google Scholar 

  28. Kashlev M., Lee J., Zalenskaya K., Nikiforov, and Goldfarb A., Science248 1006–1009, 1990.

    Google Scholar 

  29. Lee J., Kashlev M., Borukhov S., and Goldfarb A., Proc Natl Acad Sci USA88 6018–6022, 1991.

    Google Scholar 

  30. Sagitov V., Nikiforov V., and Goldfarb, A., J Biol Chem268 2195–2202, 1993.

    Google Scholar 

  31. Jin D.J. and Turnbough C.L. Jr., J Mol Biol236 72–80, 1994.

    Google Scholar 

  32. Jin D. and Gross C., J Biol Chem266 14478–14485, 1991.

    Google Scholar 

  33. Severinov K. and Goldfarb A., J Biol Chem269 31701–31705, 1994.

    Google Scholar 

  34. Dieci G., Hermann-Le Denmat S., Lukhtanov E., Thuriaux P., Werner M., and Sentenac A., EMBO J14 3766–3776, 1995.

    Google Scholar 

  35. Bonner G., Lafer E.M., and Sousa R., J Biol Chem269 25120–25128, 1994.

    Google Scholar 

  36. Landick R., Stewart J., and Lee D.N. Genes Dev4 1623–1636, 1990.

    Google Scholar 

  37. Weilbaecher R., Hebron C., Feng G., and Landick R., Genes Dev8 2913–2927, 1994.

    Google Scholar 

  38. Shaaban S.A., Krupp B.M., and Hall B.J., Moll Cell Biol15 1467–1478, 1995.

    Google Scholar 

  39. Archambault J. and Friesen J.D., Microbiol Rev57 703–724, 1993.

    Google Scholar 

  40. Kolodziej P. and Young R.A., Mol Cell Biol10 1915–1920, 1989.

    Google Scholar 

  41. Mann C., Buhler J.-M., Treich I., and Sentenac A., Cell48 627–637, 1987.

    Google Scholar 

  42. Dequart-Chablat M., Riva M., Carles C., and Sentenac A., J Biol Chem266 15300–13507, 1991.

    Google Scholar 

  43. Woychik N.A., Liao S.-M., Kolodziej P.A., and Young R.A., Genes Dev4 313–323, 1990.

    Google Scholar 

  44. Horikoshi M., Wang C.K., Fuji H., Cromlish J.A., Weil P.A., and Roeder R.G., Nature341 299–303, 1989.

    Google Scholar 

  45. Sopta M., Burton Z.F., and Greenblatt J., Nature341 410–414, 1989.

    Google Scholar 

  46. Lesley S.A. and Burgess R.R., Biochemistry28 7728–7734, 1989.

    Google Scholar 

  47. McCracken S. and Greenblatt J., Science253 900–902, 1990.

    Google Scholar 

  48. Ha I., Lane W.S., and Reinberg D., Nature352 689–695, 1991.

    Google Scholar 

  49. Ohkuma Y., Sumimoto H., Hoffmann A., Shimasaki S., Horikoshi M., and Roeder R.G., Nature354 398–401, 1991.

    Google Scholar 

  50. Moss B., Ann Rev Biochem59 661–688, 1990.

    Google Scholar 

  51. Kates J.R. and McAuslan B., Proc Natl Acad Sci USA57 315–320, 1967.

    Google Scholar 

  52. Munyon W., Poaletti E., and Grace J.T., Proc Natl Acad Sci USA58 2280–2287, 1967.

    Google Scholar 

  53. Moss B., Ahn B.-Y., Amegadzie B., Gershon P.D., and Keck J.G., J Biol Chem266 1355–1358, 1991.

    Google Scholar 

  54. Kuznar J., Salas M.L., and Vinuela E., Virology101 169–175, 1980.

    Google Scholar 

  55. Jones E.V., Puckett C., and Moss B., J Virol61 1765–1771, 1987.

    Google Scholar 

  56. Amegadzie B.Y., Ahn B.-Y., and Moss B., Biol Chem266 13712–13718, 1991.

    Google Scholar 

  57. Broyles S. and Moss B., Proc Natl Acad Sci USA83 3141–3145, 1986.

    Google Scholar 

  58. Goebel S.J., Johnson G.P., Perkus M.E., Davis S.W., Winslow J.P., and Paoletti E., Virology179 247–266, 1990.

    Google Scholar 

  59. Goebel S.J., Johnson G.P., Perkus M.E., Davis S.W., Winslow J.P., and Paoletti E., Virology179 517–563, 1990.

    Google Scholar 

  60. Shelkunov S.N., Blinov V.M., Totmenin A.V., Marennikova S.S., Kolykhalov A.A., Frolov I.V., Chizikov V.E., Gytorov V.V., Gashikov P.V., Belanov E.F., Belavin P.A., Resenchuk S.M., Andzhaparidze O.G., and Sandhakchiev L.S., Virus Res27 25–35, 1993.

    Google Scholar 

  61. Massung R.F., Liu L.-L., Qi J., Knight J.C., Yuran T.E., Kerlavage A.R., Parsons J.M., Venter J.C., and Esposito J.J., Virology201 215–240, 1994.

    Google Scholar 

  62. Schnitzler P., Sonntag K.-C., Müller M., Janssen W., Bugert J.J., Koonin E.V., and Darai J., Gen Virol75 1557–1567, 1994.

    Google Scholar 

  63. Müller M., Schnitzler P., Koonin E.V., and Darai G., J Gen Virol76 1099–1107, 1995.

    Google Scholar 

  64. Sonntag K.-C., Clauer U., Bugert J.J., Schnitzler P., and Darai G., Virology210 471–478, 1995.

    Google Scholar 

  65. García-Beato R., Salas M.L., Vinuela E., and Salas J., Virology188 637–649, 1992.

    Google Scholar 

  66. Salas M.L., Kuznar J., and Vinuela E., Virology113 484–491, 1981.

    Google Scholar 

  67. Salas M.L., Kuznar J., and Vinuela E., Arch Virol77 77–80, 1983.

    Google Scholar 

  68. Rogríguez J.M., Salas M.L., and Vinuela E., Virology186 40–52, 1992.

    Google Scholar 

  69. Pena L., Yánez R.J., Revilla Y., Vnuela E., and Salas M.L., Virology193 319–328, 1993.

    Google Scholar 

  70. Yanez R.J., Boursnell M., Nogal M.L., Yuste L., and Vinuela E., Nucleic Acids Res21 2423–2427, 1993.

    Google Scholar 

  71. Goorha R., Murti G., Granoff A., and Tirey R., Virology84 32–50, 1978.

    Google Scholar 

  72. Allison L.A., Wong K.C., Fitzpatrick V.D., Moyle M., and Ingles C.J., Mol Cell Biol8 321–329, 1988.

    Google Scholar 

  73. Bartolomei M.S. and Corden J.L., Mol Cell Biol7 586–594, 1987.

    Google Scholar 

  74. Azuma T., Masahiro M., Ushima R., and Ishihama A., Nucleic Acids Res19 461–468, 1991.

    Google Scholar 

  75. Kontermann R.E., Liu Z., Schulze R.A., Sommer K.A., Queitsch I., Dübel S., Kipriyanov S.M., Breitling F., and Bautz E.K.F., Biol Chem Hoppe Seyler376 473–481, 1995.

    Google Scholar 

  76. Krämer A. and Bautz E.K.F., Eur J Biochem117 449–455, 1981.

    Google Scholar 

  77. Dingwall C. and Laskey R.A., Trends Biochem Sci16 478–481, 1991.

    Google Scholar 

  78. Woese C.R., Microbiol Rev51 221–271, 1987.

    Google Scholar 

  79. Iwabe N., Kuma K., Kishino H., Hasegawa M., and Miyata T., J Mol Evol32 70–78, 1991.

    Google Scholar 

  80. Iwabe H., Kuma K., Hasegawa M., Osawa S., and Miyata T., Proc Natl Acad Sci USA86 9355–9359, 1989.

    Google Scholar 

  81. Sonntag K.-C., Schnitzler P., Koonin E.V., and Darai G., Virus Genes8 151–158, 1994.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Medizinische Virologie der Universität Heidelberg, Im Neuenheimer Feld 324, 69120, Heidelberg, Germany

    Kai-Christian Sonntag & Gholamreza Darai

Authors
  1. Kai-Christian Sonntag
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gholamreza Darai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gholamreza Darai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sonntag, KC., Darai, G. Evolution of viral DNA-dependent RNA polymerases. Virus Genes 11, 271–284 (1995). https://doi.org/10.1007/BF01728665

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01728665

Key words

Search

Navigation