Journal of Molecular Evolution

, Volume 20, Issue 2, pp 135–146 | Cite as

Divided genomes and intrinsic noise

  • J. Pressing
  • D. C. Reanney


Segmental genomes (i.e., genomes in which the genetic information is dispersed between two or more discrete molecules) are abundant in RNA viruses, but virtually absent in DNA viruses. It has been suggested that the division of information in RNA viruses expands the pool of variation available to natural selection by providing for the reassortment of modular RNAs from different genetic sources. This explanation is based on the apparent inability of related RNA molecules to undergo the kinds of physical recombination that generate variation among related DNA molecules. In this paper we propose a radically different hypothesis. Self-replicating RNA genomes have an error rate of about 10−3–10−4 substitutions per base per generation, whereas for DNA genomes the corresponding figure is 10−9–10−11. Thus the level of noise in the RNA copier process is five to eight orders of magnitude higher than that in the DNA process. Since a small module of information has a higher chance of passing undamaged through a noisy channel than does a large one, the division of RNA viral information among separate small units increases its overall chances of survival. The selective advantage of genome segmentation is most easily modelled for modular RNAs wrapped up in separate viral coats. If modular RNAs are brought together in a common viral coat, segmentation is advantageous only when interactions among the modular RNAs are selective enought to provide some degree of discrimination against miscopied sequences. This requirement is most clearly met by the reoviruses.

Key words

RNA viruses Divided genomes Copying fidelity Intrinsic selection pressure 


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  1. Ahmed R, Fields BN (1981) Reassortment of genome segments between reovirus defective interfering particles and infectious virus: construction of temperature sensitive and attenuated viruses by rescue of mutations from DI particles. Virology 111:351–363CrossRefPubMedGoogle Scholar
  2. Bancroft JB (1972) A virus made from parts of the genomes of brome mosaic and cowpea chlorotic mottle viruses. J Gen Virol 14:223–228Google Scholar
  3. Both GW, Bellamy AR, Street JE, Siegman LJ (1982) A general strategy for cloning double-stranded RNA: nucleotide sequence of the Simian-II rotavirus gene. Nucleic Acids Res 10:7075–7087PubMedGoogle Scholar
  4. Bromley PA, Barry RD (1973) Characterisation of the RNA of fowl plague virus. Arch Gesamte Virusforsch 42:182–196CrossRefPubMedGoogle Scholar
  5. Domingo E, Sabo D, Taniguchi T, Weissman C (1978) Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735–744CrossRefPubMedGoogle Scholar
  6. Drake JW (1974) The role of mutation in microbial evolution. Soc Gen Microbiol Symp (Cambridge) 24:41–58Google Scholar
  7. Eigen M Schuster P (1977) The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercele. Naturwissenschaften 64:541–565CrossRefPubMedGoogle Scholar
  8. Greenberg HB, Wyatt RG, Kapikian AZ, Kalica AR, Flores J, Jones R (1982) Rescue and serotypic characterisation of noncultivable human rotavirus by gene reassortment. Infect Immun 37:104–109PubMedGoogle Scholar
  9. Haber S, Ikegami M, Bajet NB Goodman RM (1981) Evidence for a divided genome in bean golden mosaic virus, a geminivirus. Nature 289:324–326CrossRefGoogle Scholar
  10. Habili N, Francki RIB (1974) Comparative studies on tomato aspermy and cucumber mosaic viruses. III. Further studies on the relationship and construction of a virus from parts of the two viral genomes. Virology 61:443–449CrossRefPubMedGoogle Scholar
  11. Holland J, Spindler K, Horodyski F, Grabau, E, Nichol S, Vande Pol S (1982) Rapid evolution of RNA genomes. Science 215:1577–1585Google Scholar
  12. Inoue T, Orgel LE (1983) A non-enzymatic RNA polymerase model. Science 219:859–862PubMedGoogle Scholar
  13. Jaspers EMJ (1974) Plant viruses with a multipartite genome. Adv Virus Res 19:37–149PubMedGoogle Scholar
  14. Joklik W (1974) Evolution in viruses. Soc Gen Microbiol (Cambridge) 42:293–320Google Scholar
  15. Joklik W (1981) Structure and function of the reovirus genome. Microbiol Rev 45:483–501PubMedGoogle Scholar
  16. Kornberg A (1980) DNA replication. WH Freeman and Co, San Francisco, p 724Google Scholar
  17. Lane LC (1979) The RNAs of multipartite and satellite viruses of plants. In: Hall TC, Davies JW (eds) Nucleic acids in plants, vol 2. CRC Press, Boca Raton, pp 65–110Google Scholar
  18. Loeb AA, Kunkel TA (1982) Fidelity of DNA synthesis. Annu Rev Biochem 51:429–457CrossRefPubMedGoogle Scholar
  19. Matthews REF (1979) Classification and nomenclature of viruses. Intervirology 12:129–296PubMedGoogle Scholar
  20. Maynard-Smith J (1978) The evolution of sex. Cambridge University Press. Cambridge, England, chapter 1Google Scholar
  21. Min Jou W, Haegeman G, Ysebaert M, Fiers W (1972) Nucleotide sequences of the gene coding for the bacteriophage MS2 coat protein. Nature 237:82–88CrossRefPubMedGoogle Scholar
  22. Nahmias AJ, Reanney DC (1977) The evolution of viruses. Annu Rev Ecol Systematics 8:29–49CrossRefGoogle Scholar
  23. Palese P, Schulman JL (1976) Differences in RNA patterns of influenza A viruses. J Virol 17:876–884PubMedGoogle Scholar
  24. Palese P, Young JF (1982) Variation of influenza A, B and C viruses. Science 215:1468–1473PubMedGoogle Scholar
  25. Portner A, Webster RG, Bean WJ (1980) Similar frequencies of antigenic variants in Sendai, vesicular stomatitis and influenza A viruses. Virology 104:235–238CrossRefPubMedGoogle Scholar
  26. Prabhakar BS, Haspel MV, McClintock PR, Notkins AL (1982). High frequency of antigenic variants among naturally occurring human Coxsackie B4 virus isolates identified by monoclonal antibodies. Nature 300:374–376CrossRefPubMedGoogle Scholar
  27. Reanney DC (1982) The evolution of RNA viruses. Annu Rev Microbiol 36:47–73CrossRefPubMedGoogle Scholar
  28. Reanney DC, Pressing J (1983) Heat as a determinative factor in the evolution of genetic systems. J Mol Evol, submittedGoogle Scholar
  29. Reanney DC (1984) Genetic noise in evolution? Nature 307:318–319CrossRefPubMedGoogle Scholar
  30. Reanney DC (1984) The molecular evolution of RNA viruses. Soc Gen Microbiol Symp (Cambridge) 35:175–196Google Scholar
  31. Reijnders L (1978) The origin of multicomponent small ribonucleoprotein viruses. Adv Virus Res 23:79–102PubMedGoogle Scholar
  32. Rogers J, Wall R (1980) A mechanism for RNA splicing. Proc Natl Acad Sci USA 77:1877–1879PubMedGoogle Scholar
  33. Rose M, Doolittle WF (1983) Parasitic DNA—the origin of species and sex. New Scientist 16:787–789Google Scholar
  34. Shannon CE (1949) The mathematical theory of communication. In: Shannon CE, Weaver W (eds) The mathematical theory of communication. University of Illinois Press, Urbana, IllinoisGoogle Scholar
  35. Shatkin AJ, Sipe JD, Loh P (1968) Separation of ten reovirus genome segments by polyacrylamide gel electrophoresis. J Virol 2:986–991PubMedGoogle Scholar
  36. Silverstein SC, Christman JK, Acs G (1976) The reovirus replicative cycle. Annu Rev Biochem 45:375–408CrossRefPubMedGoogle Scholar
  37. Tinoco I, Uhlenbeck O, Levine M (1971) Estimation of secondary structure in ribonucleic acids. Nature 230:362–367CrossRefPubMedGoogle Scholar
  38. Webster RB, Granoff A (1974) The evolution of orthomyxoviruses. In: Kurstak E, Maramorosch K (eds) Viruses, evolution and cancer. Academic Press, New York, pp 625–647Google Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • J. Pressing
    • 1
  • D. C. Reanney
    • 1
  1. 1.Department of MicrobiologyLa Trobe UniversityBundooraAustralia

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