RNA Plant and Animal Virus Replication

Abstract

RNA plant and animal viruses may have double‐stranded (ds) or single‐stranded messenger‐sense (+) or antimessenger‐sense (−) RNA genomes, which may be single‐ or multi‐component, and may be encapsidated in simple protein capsids, or complex membrane‐enveloped particles. The different types of viruses have a wide variety of different strategies for the replication of their genomes, and the production of infectious particles.

Keywords: RNA; virus; plant; animal; RdRp; replication

Figure 1.

Pathways of information flow for RNA viruses. Double‐stranded (dsRNA) viruses replicate conservatively via a full‐length RNA(+) which is transcribed from dsRNA by a virion‐associated virus‐specific RNA‐dependent RNA polymerase (RdRp). The RNA(+) then acts as messenger RNA (mRNA), for synthesis of viral proteins, then as a template for RNA(−) synthesis, to which it base pairs. Single‐stranded (ssRNA) (+) sense virus genomes initially act as mRNAs, and translate a RdRp component. The RNA(+) then replicates via a full‐length RNA(−), which is caught up in replicative complexes and is never free. This is used as template for mRNA transcription if this occurs, by the viral RdRp. Viruses with ssRNA(−) genomes replicate by means of a virion‐associated RdRp taken into the cell. This initially acts as a transcriptase, to make subgenomic mRNAs. The genome replicates via transcription of full‐length RNA(+). Translation is a cell‐specific process; all transcription and replication is done by virus‐specific RdRps.

Figure 2.

A scheme describing polyprotein translation and processing for picornaviruses (modelled on poliovirus; see Rueckert, ). Vpg, 5′‐genome‐linked protein; polyA, polyadenylate sequence at 3′ end. (a) Ribosomes initiate at the AUG start codon nearest the 5′ end of the single long open reading frame (ORF; shown in yellow), and translate until the termination codon at the end of the long ORF. Cotranslational proteolytic cleavages occur due to two viral proteases: the 2A and 3C proteins. The 2A activity begins autolytically in cis; it then acts in trans; the 3C cleavages are similar (shown by blue and yellow arrows respectively). The first 2A cleavage produces the P1 structural protein precursor, which is subsequently processed by the 3A protease.(b) Scheme showing the full extent of processing. Regulatory and structural proteins are shown. P1, P2, etc., polyprotein designations. ?, cleavage by unknown mechanism. P1 can assemble into pentamers: these are then processed via successive cleavages into VP0, VP3 and VP1, after which 12 pentamers may assemble into icosahedral procapsids. Complete assembly requires genomic RNA, and is accompanied by an apparently autolytic cleavage of VP0 into VP4 and VP2. Some of the P2 and other polyprotein processing accompanies replication: the RdRp may initially include a ‘3ABCD’ complex; initiation of new transcription on a nucleotide covalently bound to the 3B moiety is accompanied by its cleavage from the rest of the complex, to form the Vpg. The remainder of the replicase is capable only of elongation, and cannot initiate replication again.

Figure 3.

Depiction of the expression strategy of the Tobacco mosaic virus (TMV) genome. Red arrows indicate host‐dependent translation; blue arrows indicate transcription from an RNA(−) template. Solid boxes are open reading frames (ORFs); these are shown in different colours. Hatched boxes indicate proteins. The 5′ ends of the viral RNA and the mRNAs have a 7‐methylguanosine triphosphate (m7Gppp) cap structure; the 3′‐tRNA‐like sequence of all RNAs is shown as a cloverleaf structure.The ORF nearest the 5′ end of genomic RNA is translated into a 126‐kDa protein. A ‘leaky’ stop codon allows infrequent translational readthrough (1/10 times) to give a 183‐kDa protein product. These two proteins, together with (a) host protein(s) constitute the RdRp and replicase. This transcribes a full‐length RNA(−) from genomic RNA(+). The RdRp can also transcribe the RNA(−) into RNA(+), and, by recognition of two or more ‘RNA promoter’ sequences within the RNA(−) sequence, into at least two nested subgenomic mRNAs: all products of transcription from RNA(−) share the same 3′ terminus. Only the 5′‐proximal ORF of each mRNA is translated.

Figure 4.

Depiction of gene order and function and designations in viruses of the order Mononegavirales. The genomic 3′ end is a free –OH group; the 5′ end is phosphorylated but uncapped. The leader sequence is about 50 bases long and conserved in viruses in the same genus. Intergenic sequences are conserved within a virus, and include polyU sequences of 4–7 bases. The different open reading frames (ORFs) are shown in different colours. The gene order is conserved among viruses in the order, as is the function. N/NP are nucleoproteins which bind viral (−) and (+) sense RNA; NS proteins are nonstructural and involved in aspects of regulation; M or matrix protein is bound by assembled nucleocapsids and binds the cytoplasmic portion of the G/GP membrane glycoproteins, which span the cell‐derived envelope in the assembled virions; the L protein is the main component of the RdRp, and is incorporated into virions.

Figure 5.

Depiction of genome components and expression strategy of bunyaviruses. All viruses have three genomic ssRNA(−) components: these are L, M and S, coding for polymerase (L), glycoproteins (G1, G2) and nonstructural (NSm), and nucleoprotein (N) and nonstructural (NSs) proteins, respectively. Different open reading frames (ORFs) are shown in different colours. Genus‐specific ORFs are indicated: only bunyaviruses have an extra NSs (small nonstructural protein) ORF internal to the N ORF; tospoviruses and phleboviruses have an ambisense (both (+) and (−) sense ORFs) S component, with an mRNA being transcribed off the RNA(+) form of the genome. Tospoviruses in addition have an ambisense M component, with the extra 5′‐ORF coding for a host‐derived movement protein (MP).

close

References

Bessarab IN, Liu HW, Ip CF and Tai JH (2000) The complete cDNA sequence of a type II Trichomonas vaginalis virus. Virology 267: 350–359.

Ghabrial SA (1998) Origin, adaptation and evolutionary pathways of fungal viruses. Virus Genes 16: 119–131.

Gibbs MJ, Koga R, Moriyama H, Pfeiffer P and Fukuhara T (2000) Phylogenetic analysis of some large double‐stranded RNA replicons from plants suggests they evolved from a defective single‐stranded RNA virus. Journal of General Virology 81: 227–233.

Harrison H, Wiley DC and Skehel JJ (1996) Virus structure. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 59–100. New York: Lippincott‐Raven.

Lamb RA and Kolakofsky D (1996) Paramyxoviridae: the viruses and their replication. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 1177–1204. New York: Lippincott‐Raven.

Lamb RA and Krug RM (1996) Orthomyxoviridae: the viruses and their replication. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 1353–1396. New York: Lippincott‐Raven.

Lewandowski DJ and Dawson WO (2000) Functions of the 126‐ and 183‐kDa proteins of tobacco mosaic virus. Virology 271: 90–98.

Melcher U (2000) The ‘30K’ superfamily of viral movement proteins. Journal of General Virology 81: 257–266.

Murphy FA (1996) Virus taxonomy. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 15–57. New York: Lippincott‐Raven.

Nibert ML, Schiff LA and Fields BN (1996) Reoviruses and their replication. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn. pp. 1557–1596. New York: Lippincott‐Raven.

Pringle CR (1999) Virus taxonomy – 1999. Archives of Virology 144: 421–429.

Roner MR (1999) Rescue systems for dsRNA viruses of higher organisms. In: Maramorosch K, Murphy FA and Shatkin AJ (eds) Advances in Virus Research, pp. 355–367. San Diego: Academic Press.

Rueckert RR (1996) Picornaviridae: the viruses and their replication. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 609–654. New York: Lippincott‐Raven.

Schmaljohn CS (1996) Bunyaviridae: the viruses and their replication. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 1447–1472. New York: Lippincott‐Raven.

Smart CD, Yuan W, Foglia R, Nuss DL, Fulbright DW and Hillman BI (1999) Cryphonectria hypovirus 3, a virus species in the family hypoviridae with a single open reading frame. Virology 265: 66–73.

Southern PJ (1996) Arenaviridae: the viruses and their replication. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 1505–1520. New York: Lippincott‐Raven.

Strauss EE, Lakshman DK and Tavantzis SM (2000) Molecular characterization of the genome of a partitivirus from the basidiomycete Rhizoctonia solani. Journal of General Virology 81: 549–555.

Strauss EG, Strauss JH and Levine AJ (1996) Virus evolution. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 153–172. New York: Lippincott‐Raven.

Wagner RR and Rose JK (1996) Rhabdoviridae: the viruses and their replication. In: Fields BN, Knipe DM and Howley PM (eds) Fields Virology, 2nd edn, pp. 1121–1136. New York: Lippincott‐Raven.

Further Reading

Agol VI, Paul AV and Wimmer E (1999) Paradoxes of the replication of picornaviral genomes. Virus Research 62: 129–147.

Gubareva LV, Kaiser L and Hayden FG (2000) Influenza virus neuraminidase inhibitors. Lancet 355: 827–835.

Jaspars EM (1999) Genome activation in alfamo‐ and ilarviruses. Archives of Virology 144: 843–863.

Neumann G and Kawaoka Y (1999) Genetic engineering of influenza and other negative‐strand RNA viruses containing segmented genomes. Advances in Virus Research 53: 265–300.

Portela A, Zurcher T, Nieto A and Ortin J (1999) Replication of orthomyxoviruses. Advances in Virus Research 54: 319–348.

Rijnbrand RC and Lemon SM (2000) Internal ribosome entry site‐mediated translation in hepatitis C virus replication. Current Topics in Microbiology and Immunology 242: 85–116.

Roberts A and Rose JK (1999) Redesign and genetic dissection of the rhabdoviruses. Advances in Virus Research 53: 301–319.

Suzuki R, Suzuki T, Ishii K, Matsuura Y and Miyamura T (1999) Processing and functions of Hepatitis C virus proteins. Intervirology 42: 145–152.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Rybicki, Edward P(Jul 2003) RNA Plant and Animal Virus Replication. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0001086]