Skip to main content
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2005 Jun 9;1(4):485–493. doi: 10.1016/S0959-437X(05)80196-0

RNA viruses: genome structure and evolution

Ellen G Strauss 1, James H Strauss 1
PMCID: PMC7133357  PMID: 1822281

Abstract

The explosive pace of sequencing of RNA viruses is leading to rapid advances in our understanding of the evolution of these viruses and of the ways in which their genomes are organized and expressed. New insights are coming not only from genomic nucleotide sequence comparisons, but also from direct sequencing of transcribed mRNAs and of RNAs that serve as intermediates in replication.

Abbreviations: BSMV, barley stripe mosaic virus; L, large; Ldr, leader RNA; M, medium; NDV, Newcastle disease virus; NTR, non-translated region; ORF, open reading frame; PIV, parainfluenza virus; S, small; ssRNA, single-strand RNA; SV5, simian virus 5; TMV, tobacco mosaic virus; vc RNA, virus complementary RNA

References and recommended reading

  • 1.Strauss EG, Strauss JH. Replication Strategies of the Single Stranded RNA Viruses of Eukaryotes. Curr Topics Microbiol Immunol. 1983;105:1–98. doi: 10.1007/978-3-642-69159-1_1. [DOI] [PubMed] [Google Scholar]
  • 2.Kamer G, Argos P. Primary Structural Comparison of RNA-dependent Polymerases from Plant, Animal and Bacterial Viruses. Nucleic Acids Res. 1984;12:7269–7282. doi: 10.1093/nar/12.18.7269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Argos P. A Sequence Motif in Many Polymerases. Nucleic Acids Res. 1988;16:9909–9916. doi: 10.1093/nar/16.21.9909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Bruenn JA. Relationships Among the Positive Strand and Double-strand RNA Viruses as Viewed Through their RNA-dependent RNA Polymerases. Nucleic Acids Res. 1991;19:217–226. doi: 10.1093/nar/19.2.217. of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Sequences of 50 RNA-dependent RNA polymerases from 43 plus-strand viruses and seven double-strand viruses have been aligned, and phylogenetic trees constructed. A large number of these viruses form a single cluster whose only common characteristic is insect transmission.
  • 5.Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM. Two Related Superfamilies of Putative Helicases Involved in Replication, Repair, and Expression of DNA and RNA Genomes. Nucleic Acids Res. 1989;17:4713–4730. doi: 10.1093/nar/17.12.4713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Zimmern D. Evolution of RNA Viruses. In: Domingo E, Holland JJ, Ahlquist P, editors. RNA Genetics. CRC Press; Boca Raton Florida: 1988. pp. 211–240. [book] [Google Scholar]
  • 7.Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM. A Conserved nTP-Binding Motif in Putative Helicases. Nature. 1988;333:22. doi: 10.1038/333022a0. [DOI] [PubMed] [Google Scholar]
  • 8.Hardy WR, Strauss JH. Processing the Nonstructural Proteins of Sindbis Virus: Nonstructural Proteinase is in the C-Terminal Half of nsP2 and Functions Both in Cis and Trans. J Virol. 1989;63:4653–4664. doi: 10.1128/jvi.63.11.4653-4664.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Palmenberg AC. Sequence Alignments of Picornaviral Capsid Proteins. In: Semler B, Ehrenfeld E, editors. Molecular Aspects of Picornavirus Infection and Detection. American Society for Microbiology; Washington, DC: 1989. pp. 211–241. [book] [Google Scholar]
  • 10.King AMQ, Underwood BO, McCahon D, Newman JWI, Brown F. Biochemical Identification of Viruses Causing the 1981 Outbreaks of Foot-and-Mouth Disease in the UK. Nature. 1981;293:479–480. doi: 10.1038/293479a0. [DOI] [PubMed] [Google Scholar]
  • 11.Takeda N, Miyamura K, Ogino T, Natori K, Yamazaki S, Sakurai N, Nakazono N, Ishii K, Kono R. Evolution of Enterovirus Type 70: Oligonucleotide Mapping Analysis of RNA Genome. Virology. 1984;134:375–388. doi: 10.1016/0042-6822(84)90305-2. [DOI] [PubMed] [Google Scholar]
  • 12.Burness AT, Pardoe I, Faragher SG, Vrati S, Dalgarno L. Genetic Stability of Ross River Virus During Epidemic Spread in Nonimmune Humans. Virology. 1988;167:639–643. [PubMed] [Google Scholar]
  • 13.Shirako Y, Niklasson B, Dalrymple JM, Strauss EG, Strauss JH. Structure of the Ockelbo Virus Genome and its Relationship to other Sindbis Viruses. Virology. 1991;182:753–764. doi: 10.1016/0042-6822(91)90616-j. of interest. [DOI] [PubMed] [Google Scholar]; Complete sequence of the genome of Ockelbo virus, a strain of Sindbis virus which causes epidemic disease in northern Europe. From sequence comparisons it was found that Ockelbo virus must have been transferred to northern Europe from South Africa.
  • 14.Thomas SM, Lamb RA, Paterson RG. Two mRNAs That Differ by Two Nontemplated Nucleotides Encode the Amino Coterminal Proteins P and V of the Paramyxovirus SV5. Cell. 1988;54:891–902. doi: 10.1016/S0092-8674(88)91285-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Cattaneo R, Kaelin K, Baczko K, Billeter MA. Measles Virus Editing Provides an Additional Cysteine-rich Protein. Cell. 1989;56:759–764. doi: 10.1016/0092-8674(89)90679-x. [DOI] [PubMed] [Google Scholar]
  • 16.Matsuoka Y, Curran J, Pelet T, Kolakovsky D, Ray R, Compans RW. The P gene of Human Parainfluenza Virus Type 1 Encodes P and C Proteins But not a Cysteine-rich V Protein. J Virol. 1991;65:3406–3410. doi: 10.1128/jvi.65.6.3406-3410.1991. of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Demonstration that PIV-1 does not need a cysteine-rich V protein, and that the addition of non-templated G residues is not essential for all paramyxo-viruses.
  • 17.Pelet T, Curran J, Kolakovsky D. The P Gene of Bovine Parainfluenza Virus 3 Expresses all Three Reading Frames From a Single mRNA Editing Site. EMBO J. 1991;10:443–448. doi: 10.1002/j.1460-2075.1991.tb07966.x. of outstanding interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; A comprehensive look at all of the mRNA transcripts and translated protein products of the P gene of PIV-3, illustrating that all three reading frames are used over a stretch of more than 300 nucleotides. This may be the first gene sequenced in which all three frames are used.
  • 18.Vidal S, Curran J, Kolakovsky D. Editing of the Sendai Virus P/C mRNA by G Insertion Occurs During mRNA Synthesis via a Virus-encoded Activity. J Virol. 1990;64:239–246. doi: 10.1128/jvi.64.1.239-246.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Southern JA, Precious B, Randall RE. Two Nontemplated Nucleotide Additions are Required to Generate the P mRNA of Parainfluenza Virus Type 2 Since the RNA Genome Encodes Protein V. Virology. 1990;177:388–390. doi: 10.1016/0042-6822(90)90497-f. of interest. [DOI] [PubMed] [Google Scholar]; To study the structure of the mRNAs from the PV gene, both genomic and mRNA sequences were amplified by PCR and sequenced.
  • 20.Kondo K, Bando H, Tsurudome M, Kawano M, Nishio M, Ito Y. Sequence Analysis of the Phosphoprotein (P) Genes of Human Parainfluenza Type 4A and 4B Viruses and RNA Editing at Transcript of the P Genes: the Number of G Residues Added is Imprecise. Virology. 1990;178:321–326. doi: 10.1016/0042-6822(90)90413-l. of interest. [DOI] [PubMed] [Google Scholar]; Proof that the number of G residues added to mRNAs of the P gene of PIV-4 is imprecise. The P gene products for nine paramyxoviruses are aligned to provide a phylogenetic dendrogram.
  • 21.Paterson RG, Lamb RA. RNA Editing by G-Nucleotide Insertion in Mumps Virus P-Gene mRNA Transcripts. J Virol. 1990;64:4137–4145. doi: 10.1128/jvi.64.9.4137-4145.1990. of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Demonstration that the unedited transcript encodes the cysteine-rich V protein and that variable numbers of inserted G's give transcripts for two other products.
  • 22.Stec DA, Hill MAI, Collins PL. Sequence Analysis of the Polymerase L Gene of Human Respiratory Syncytial Virus and Predicted Phylogeny of Nonsegmented Negative-strand Viruses. Virology. 1991;183:273–287. doi: 10.1016/0042-6822(91)90140-7. of outstanding interest. [DOI] [PubMed] [Google Scholar]; The complete sequence of the polymerase gene of RSV is presented and compared with the L genes of Rhabdoviridae and Paramyxoviridae. Comprehensive phylogenetic trees are shown.
  • 23.Sethna PB, Hung S-L, Brian DA. Vol. 86. 1989. Coronavirus Subgenomic Minus-strand RNAs and the Potential for mRNA Replicons; pp. 5626–5630. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Lai MMC. Coronavirus: Organization, Replication and Expression of Genome. Annu Rev Microbiol. 1990;44:303–333. doi: 10.1146/annurev.mi.44.100190.001511. [DOI] [PubMed] [Google Scholar]
  • 25.Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM. Coronavirus Genome: Prediction of Putative Functional Domains in the Non-structural Polyprotein by Comparative Amino Acid Sequence Analysis. Nucleic Acids Res. 1989;17:4847–4861. doi: 10.1093/nar/17.12.4847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Baker SC, Shieh C-K, Soe LH, Chang M-F, Vannier DM, Lai MMC. Identification of a Domain Required for Autoproteolytic Cleavage of Murine Coronavirus Gene A Polyprotein. J Virol. 1989;63:3693–3699. doi: 10.1128/jvi.63.9.3693-3699.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Vlasak R, Luytjes W, Leider W, Spaan W, Palese P. The E3 Protein of Bovine Coronavirus is a Receptor-destroying Enzyme With Acetyl-esterase Activity. J Virol. 1988;62:4686–4690. doi: 10.1128/jvi.62.12.4686-4690.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Lai MMC. Coronavirus Leader-RNA-primed Transcription: an Alternative Mechanism to RNA Splicing. Bioessays. 1986;5:257–260. doi: 10.1002/bies.950050606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Sawicki SG, Sawicki DL. Coronavirus Transcription: Subgenomic Mouse Hepatitis Virus Replicative Intermediates Function in RNA Synthesis. J Virol. 1990;64:1050–1056. doi: 10.1128/jvi.64.3.1050-1056.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Hofmann MA, Sethna PB, Brian DA. Bovine Coronavirus mRNA Replication Continues Throughout Persistent Infection in Cell Culture. J Virol. 1990;64:4108–4114. doi: 10.1128/jvi.64.9.4108-4114.1990. of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Quantitation of the amount of minus strands corresponding to the nested set of mRNAs made during persistent infection. Suggests that replication of mRNAs is not a rare or unimportant event.
  • 31.Sethna PB, Hofmann MA, Brian DA. Minus-strand Copies of Replicating Coronavirus mRNAs Contain Antileaders. J Virol. 1991;65:320–325. doi: 10.1128/jvi.65.1.320-325.1991. of outstanding interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Direct sequencing of minus strands corresponding to coronavirus mRNAs to show that they are exactly complementary to the mRNAs.
  • 32.Snijder EJ, Den Boon JA, Horzinek MC, Spaan WJM. Comparison of the Genome Organization of Toro- and Coronaviruses: Evidence for Two Nonhomologous RNA Recombination Events During Berne Virus Evolution. Virology. 1991;180:448–452. doi: 10.1016/0042-6822(91)90056-H. of outstanding interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Sequence analysis to suggest that coronaviruses and toroviruses are related and that recombination has played a role in their evolution.
  • 33.Mahy BWJ, editor. Related Viruses of Plants and Animals. Vol. 2. 1991. pp. 1–77. (Seminars in Virology). of interest. [Google Scholar]; A collection of brief reviews that summarizes the know facts about related plant and animal viruses.
  • 34.Haseloff J, Goelet P, Zimmern D, Ahlquist P, Dasgluta R, Kaesberg P. Vol. 81. 1984. Striking Similarities in Amino Acid Sequence Among Nonstructural Proteins Encoded by RNA Viruses that have Dissimilar Genomic Organization; pp. 4358–4362. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Ahlquist P, Strauss EG, Rice CM, Strauss JH, Haseloff J, Zimmern D. Sindbis Virus Proteins nsP1 and nsP2 Contain Homology to Nonstructural Proteins from Several RNA Plant Viruses. J Virol. 1985;53:536–542. doi: 10.1128/jvi.53.2.536-542.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Franssen H, Leunissen J, Goldbach R, Lomonossoff G, Zimmern D. Homologous Sequences in Non-structural Proteins from Cowpea Mosaic Virus and Picomavirus. EMBO J. 1984;3:855–861. doi: 10.1002/j.1460-2075.1984.tb01896.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Argos P, Kamer G, Nicklin MJH, Wimmer E. Similarity in Gene Organization and Homology Between Protein of Animal Picornaviruses and a Plant Comovirus Suggest Common Ancestry of these Virus Families. Nucleic Acids Res. 1984;12:7251–7267. doi: 10.1093/nar/12.18.7251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Dreher TW, Hall TC. Mutational Analysis of the Sequence and Structural Requirements in Brome Mosaic Virus RNA for Minus Strand Promoter Activity. J Mol Biol. 1988;201:31–40. doi: 10.1016/0022-2836(88)90436-6. [DOI] [PubMed] [Google Scholar]
  • 39.Pleij CWA, Abrahams JP, van Belkum A, Pietveld K, Bosch L. The Spatial Folding of the 3′ Noncoding Region of Aminoacylatable Plant Viral RNAs. In: Brinton MA, Rueckert RR, editors. Positive Strand RNA Viruses. Alan R Liss Inc.; New York: 1987. pp. 299–316. [book] [Google Scholar]
  • 40.Gallie DR, Walbot V. RNA Pseudoknot Domain of Tobacco Mosaic Virus can Functionally Substitute for a Poly(A) Tail in Plant and Animal Cells. Genes Dev. 1990;4:1149–1157. doi: 10.1101/gad.4.7.1149. of outstanding interest. [DOI] [PubMed] [Google Scholar]; An extremely interesting dissection of the functions of various domains in the 3′-NTR of a plant virus.
  • 41.Petty ITD, French R, Jones RW, Jackson AO. Identification of Barley Stripe Mosaic Virus Genes Involved in Viral RNA Replication and Systemic Movement. EMBO J. 1990;9:3453–3457. doi: 10.1002/j.1460-2075.1990.tb07553.x. of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; An excellent synthesis of all that is known about BSMV, the functions of the various genes, and the heterogeneity of RNA 3 within a population of genomes.
  • 42.Jackson AO, Hunter BG, Gustafson GD. Hordeivirus Relationships and Genome Organization. Annu Rev Phytopathol. 1989;27:95–121. [Google Scholar]
  • 43.Simons JF, Hellman U, Pettersson RF. Uukuniemi Virus Segment S: Ambisense Coding Strategy, Packaging of Complementary Strands into Virions and Homology to Members of the Genus Phlebovirus. J Virol. 1990;64:247–255. doi: 10.1128/jvi.64.1.247-255.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.de Haan P, Wagemakers L, Peters D, Goldbach R. The S RNA Segment of Tomato Spotted Wilt Virus has an Ambisense Character. J Gen Virol. 1990;71:1001–1007. doi: 10.1099/0022-1317-71-5-1001. of outstanding interest. [DOI] [PubMed] [Google Scholar]; Cogent arguments for the inclusion of tomato spotted wilt virus with the family Bunyaviridae.
  • 45.Kakutani T, Hayano Y, Hayashi T, Minobe Y. Ambisense Segment 4 of Rice Stripe Virus: Possible Evolutionary Relationship with Phleboviruses and Uukuviruses (Bunyaviridae) J Gen Virol. 1990;71:1427–1432. doi: 10.1099/0022-1317-71-7-1427. of interest. [DOI] [PubMed] [Google Scholar]; Sequence analysis to show that the terminal sequences are self-complementary and very similar to those of phleboviruses and uukuviruses.
  • 46.Kakutani T, Hayano Y, Hayashi T, Minobe Y. Ambisense Segment 3 of Rice Stripe Virus: the First Instance of a Virus Containing Two Ambisense Segments. J Gen Virol. 1991;72:465–468. doi: 10.1099/0022-1317-72-2-465. of outstanding interest. [DOI] [PubMed] [Google Scholar]; First description of a virus with two ambisense segments.

Articles from Current Opinion in Genetics & Development are provided here courtesy of Elsevier

RESOURCES