Tombusviridae

Tim L Sit, North Carolina State University, Raleigh, North Carolina, USA
Steven A Lommel, North Carolina State University, Raleigh, North Carolina, USA

Published online: April 2010

DOI: 10.1002/9780470015902.a0000756.pub2

The Tombusviridae is a relatively large and diverse family of soil-borne viruses that have single-stranded, positive-sense, RNA (ribonucleic acid) genomes and that share morphological, structural, molecular and genetic features. Their high titres, compact genomes and extremely stable virions lend to their attractiveness as research subjects. Indeed, the Tombusviridae are a particularly well-characterized family of viruses in the areas of virus structure, gene expression strategies, virus movement, the support of satellite viruses and defective-interfering RNAs as well as RNA recombination. Although the RNA-dependent RNA polymerases share a great deal of sequence identity, the capsid proteins can be separated by the presence (or absence) of a C-terminal protruding domain which gives the virions a bumpy appearance in electron micrographs. Transmission of several members by fungal zoospores in a species-specific manner has been reported. The virions of several members have been utilized for biotechnology purposes.

Key Concepts:

  • Virions are nonenveloped and extremely stable.
  • Tombusviridae species replicate to high titres within their host cells.
  • RNA genomes are small with a limited number of gene products that serve multiple functions.
  • RNA–RNA interactions control gene expression in several genera.
  • Viral-encoded suppressors of RNA silencing act at several different stages in the response cascade.
  • Several members transmitted through soil by specific fungal zoospores.

Keywords: RNA plant viruses; virus structure; satellites; soil and fungus transmission; gene expression strategies; RNA–RNA interactions

Figure 1. Electron micrograph of Red clover necrotic mosaic virus particles. (Copyright Tim L. Sit and Steven A. Lommel).
Figure 2. Structure and organization of the tomato bushy stunt virus particle. (a) Three-dimensional arrangement of the capsid protein (CP) domains. (b) Linear arrangement. The number of amino acid residues is indicated below each domain. R, RNA-binding domain; a, arm region; S, shell domain; h, hinge sequence and P, protruding domain. (c) Spatial arrangement of the CP subunits within the virus particle. A conformation, red; B conformation, blue and C conformation, green. Adapted with permission from Harrison (1999).
Figure 3. Genomic organization of representative members from each genus of the family Tombusviridae. Boxes represent known and predicted open reading frames with the sizes of the respective proteins (or readthrough products) indicated above or below. Colours indicate the proteins with extensive amino acid sequence conservation. Red boxes represent proteins involved in replication. Blue boxes represent capsid proteins (CPs) that are related to those of sobemoviruses. Green boxes represent tombusvirus-like capsid proteins which contain protruding domains. Black boxes represent viral movement proteins (MPs) analogous to that of TCV. RT, translational readthrough of termination codon and –1 FS, –1 ribosomal frameshifting event.
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 References
    Aramayo R, Merigoux C, Larquet E et al. (2005) Divalent ion-dependent swelling of tomato bushy stunt virus: a multi-approach study. Biochimica et Biophysica Acta 1724: 345–354.
    Basnayake VR, Sit TL and Lommel SA (2006) The genomic RNA packaging scheme of red clover necrotic mosaic virus. Virology 345: 532–539.
    Basnayake VR, Sit TL and Lommel SA (2009) The red clover necrotic mosaic virus origin of assembly is delimited to the RNA-2 trans-activator. Virology 384: 169–178.
    Bates HJ, Farjah M, Osman TA and Buck KW (1995) Isolation and characterization of an RNA-dependent RNA polymerase from Nicotiana clevelandii plants infected with red clover necrotic mosaic dianthovirus. Journal of General Virology 76: 1483–1491.
    Burgyan J, Rubino L and Russo M (1996) The 5¢-terminal region of a tombusvirus genome determines the origin of multivesicular bodies. Journal of General Virology 77(part 8): 1967–1974.
    Buzen FG Jr, Niblett CL, Hooper GR, Hubbard J and Newman MA (1984) Further characterization of panicum mosaic virus and its associated satellite virus. Phytopathology 74: 313–318.
    Cheng CP and Nagy PD (2003) Mechanism of RNA recombination in carmo- and tombusviruses: evidence for template switching by the RNA-dependent RNA polymerase in vitro. Journal of Virology 77: 12033–12047.
    Fabian MR and White KA (2006) Analysis of a 3¢-translation enhancer in a tombusvirus: a dynamic model for RNA–RNA interactions of mRNA termini. RNA (New York) 12: 1304–1314.
    book Harrison SC (1999) "The structure of spherical viruses". In: Branden C and Tooze J (eds) Introduction to Protein Structure, 2nd edn, pp. 325–372. New York: Garland Publishing, Inc.
    Hearne PQ, Knorr DA, Hillman BI and Morris TJ (1990) The complete genome structure and synthesis of infectious RNA from clones of tomato bushy stunt virus. Virology 177: 141–151.
    Heaton LA, Carrington JC and Morris TJ (1989) Turnip crinkle virus infection from RNA synthesized in vitro. Virology 170: 214–218.
    Hillman BI, Carrington JC and Morris TJ (1987) A defective interfering RNA that contains a mosaic of a plant virus genome. Cell 51: 427–433.
    Hogle JM, Maeda A and Harrison SC (1986) Structure and assembly of turnip crinkle virus. I. X-ray crystallographic structure analysis at 3.2 A resolution. Journal of Molecular Biology 191: 625–638.
    Iwakawa HO, Kaido M, Mise K and Okuno T (2007) cis-Acting core RNA elements required for negative-strand RNA synthesis and cap-independent translation are separated in the 3¢-untranslated region of red clover necrotic mosaic virus RNA1. Virology 369: 168–181.
    Jiang Y, Serviene E, Gal J, Panavas T and Nagy PD (2006) Identification of essential host factors affecting tombusvirus RNA replication based on the yeast Tet promoters Hughes Collection. Journal of Virology 80: 7394–7404.
    Joelson T, Akerblom L, Oxelfelt P et al. (1997) Presentation of a foreign peptide on the surface of tomato bushy stunt virus. Journal of General Virology 78(part 6): 1213–1217.
    Johnston JC and Rochon DM (1996) Both codon context and leader length contribute to efficient expression of two overlapping open reading frames of a cucumber necrosis virus bifunctional subgenomic mRNA. Virology 221: 232–239.
    Kakani K, Sgro JY and Rochon D (2001) Identification of specific cucumber necrosis virus coat protein amino acids affecting fungus transmission and zoospore attachment. Journal of Virology 75: 5576–5583.
    Katpally U, Kakani K, Reade R et al. (2007) Structures of T=1 and T=3 particles of cucumber necrosis virus: evidence of internal scaffolding. Journal of Molecular Biology 365: 502–512.
    Kozak M (1992) Regulation of translation in eukaryotic systems. Annual Review of Cell Biology 8: 197–225.
    Kumar S, Ochoa W, Singh P et al. (2009) Tomato bushy stunt virus (TBSV), a versatile platform for polyvalent display of antigenic epitopes and vaccine design. Virology 388: 185–190.
    Lakatos L, Szittya G, Silhavy D and Burgyan J (2004) Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO Journal 23: 876–884.
    Li WZ, Qu F and Morris TJ (1998) Cell-to-cell movement of turnip crinkle virus is controlled by two small open reading frames that function in trans. Virology 244: 405–416.
    Lin HX, Xu W and White KA (2007) A multicomponent RNA-based control system regulates subgenomic mRNA transcription in a tombusvirus. Journal of Virology 81: 2429–2439.
    Loo L, Guenther RH, Lommel SA and Franzen S (2008) Infusion of dye molecules into red clover necrotic mosaic virus. Chemical Communications (Cambridge, England) 2008: 88–90.
    Mizumoto H, Tatsuta M, Kaido M, Mise K and Okuno T (2003) Cap-independent translational enhancement by the 3¢ untranslated region of red clover necrotic mosaic virus RNA1. Journal of Virology 77: 12113–12121.
    Morgunova E, Dauter Z, Fry E et al. (1994) The atomic structure of Carnation mottle virus capsid protein. FEBS Letters 338: 267–271.
    Nutter RC, Scheets K, Panganiban LC and Lommel SA (1989) The complete nucleotide sequence of the maize chlorotic mottle virus genome. Nucleic Acids Research 17: 3163–3177.
    Oda Y, Saeki K, Takahashi Y et al. (2000) Crystal structure of tobacco necrosis virus at 2.25 A resolution. Journal of Molecular Biology 300: 153–169.
    Olson AJ, Bricogne G and Harrison SC (1983) Structure of tomato busy stunt virus IV. The virus particle at 2.9 A resolution. Journal of Molecular Biology 171: 61–93.
    Panavas T and Nagy PD (2003) Yeast as a model host to study replication and recombination of defective interfering RNA of tomato bushy stunt virus. Virology 314: 315–325.
    Panavas T, Serviene E, Brasher J and Nagy PD (2005) Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proceedings of the National Academy of Sciences of the USA 102: 7326–7331.
    Pantaleo V, Rubino L and Russo M (2003) Replication of Carnation Italian ringspot virus defective interfering RNA in Saccharomyces cerevisiae. Journal of Virology 77: 2116–2123.
    Powers JG, Sit TL, Heinsohn C et al. (2008) The red clover necrotic mosaic virus RNA-2 encoded movement protein is a second suppressor of RNA silencing. Virology 381: 277–286.
    Qu F and Morris TJ (1997) Encapsidation of turnip crinkle virus is defined by a specific packaging signal and RNA size. Journal of Virology 71: 1428–1435.
    Qu F, Ren T and Morris TJ (2003) The coat protein of turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. Journal of Virology 77: 511–522.
    Reichmann ME (1964) The satellite tobacco necrosis virus: a single protein and its genetic code. Proceedings of the National Academy of Sciences of the USA 52: 1009–1017.
    Ren Y, Wong SM and Lim LY (2007) Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin. Bioconjugate Chemistry 18: 836–843.
    Russo M, Burgyan J and Martelli GP (1994) Molecular biology of tombusviridae. Advances in Virus Research 44: 381–428.
    Sarawaneeyaruk S, Iwakawa HO, Mizumoto H et al. (2009) Host-dependent roles of the viral 5¢ untranslated region (UTR) in RNA stabilization and cap-independent translational enhancement mediated by the 3¢ UTR of red clover necrotic mosaic virus RNA1. Virology 391: 107–118.
    Scholthof HB, Scholthof KB and Jackson AO (1996) Plant virus gene vectors for transient expression of foreign proteins in plants. Annual Review of Phytopathology 34: 299–323.
    Scholthof HB, Scholthof KB, Kikkert M and Jackson AO (1995) Tomato bushy stunt virus spread is regulated by two nested genes that function in cell-to-cell movement and host-dependent systemic invasion. Virology 213: 425–438.
    Shen R and Miller WA (2004) The 3¢ untranslated region of tobacco necrosis virus RNA contains a barley yellow dwarf virus-like cap-independent translation element. Journal of Virology 78: 4655–4664.
    Sherman MB, Guenther RH, Tama F et al. (2006) Removal of divalent cations induces structural transitions in red clover necrotic mosaic virus, revealing a potential mechanism for RNA release. Journal of Virology 80: 10395–10406.
    Simon AE, Roossinck MJ and Havelda Z (2004) Plant virus satellite and defective interfering RNAs: new paradigms for a new century. Annual Review of Phytopathology 42: 415–437.
    Sit TL, Vaewhongs AA and Lommel SA (1998) RNA-mediated trans-activation of transcription from a viral RNA. Science (New York) 281: 829–832.
    Song C and Simon AE (1994) RNA-dependent RNA polymerase from plants infected with turnip crinkle virus can transcribe (+)- and (–)-strands of virus-associated RNAs. Proceedings of the National Academy of Sciences of the USA 91: 8792–8796.
    Stockley PG, Kirsh AL, Chow EP, Smart JE and Harrison SC (1986) Structure of turnip crinkle virus. III. Identification of a unique coat protein dimer. Journal of Molecular Biology 191: 721–725.
    Takeda A, Tsukuda M, Mizumoto H et al. (2005) A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO Journal 24: 3147–3157.
    Turina M, Desvoyes B and Scholthof KB (2000) A gene cluster encoded by panicum mosaic virus is associated with virus movement. Virology 266: 120–128.
    Wang J and Simon AE (1997) Analysis of the two subgenomic RNA promoters for turnip crinkle virus in vivo and in vitro. Virology 232: 174–186.
    White KA (2002) The premature termination model: a possible third mechanism for subgenomic mRNA transcription in (+)-strand RNA viruses. Virology 304: 147–154.
    Wu B, Pogany J, Na H et al. (2009) A discontinuous RNA platform mediates RNA virus replication: building an integrated model for RNA-based regulation of viral processes. PLoS Pathogens 5: e1000323.
    Wu B and White KA (1999) A primary determinant of cap-independent translation is located in the 3¢-proximal region of the tomato bushy stunt virus genome. Journal of Virology 73: 8982–8988.
    Xiong Z, Kim KH, Giesman-Cookmeyer D and Lommel SA (1993a) The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology 192: 27–32.
    Xiong Z, Kim KH, Kendall TL and Lommel SA (1993b) Synthesis of the putative red clover necrotic mosaic virus RNA polymerase by ribosomal frameshifting in vitro. Virology 193: 213–221.
    Xiong Z and Lommel SA (1989) The complete nucleotide sequence and genome organization of red clover necrotic mosaic virus RNA-1. Virology 171: 543–554.
    Zhang G, Leung C, Murdin L, Rovinski B and White KA (2000) In planta expression of HIV-1 p24 protein using an RNA plant virus-based expression vector. Molecular Biotechnology 14: 99–107.
 Further Reading
    Kneller EL, Rakotondrafara AM and Miller WA (2006) Cap-independent translation of plant viral RNAs. Virus Research 119: 63–75.
    Lee KK and Johnson JE (2003) Complementary approaches to structure determination of icosahedral viruses. Current Opinion in Structural Biology 13: 558–569.
    book Lommel SA, Martelli GP, Rubino L and Russo M (2005) "Tombusviridae". In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U and Ball LA (eds) Virus Taxonomy. 8th Report of the International Committee on the Taxonomy of Viruses, pp. 907–936. San Diego: Elsevier Academic Press.
    Miller WA and White KA (2006) Long-distance RNA–RNA interactions in plant virus gene expression and replication. Annual Review of Phytopathology 44: 447–467.
    Nagy PD and Pogany J (2006) Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology 344: 211–220.
    Rochon D, Kakani K, Robbins M and Reade R (2004) Molecular aspects of plant virus transmission by olpidium and plasmodiophorid vectors. Annual Review of Phytopathology 42: 211–241.
    Silhavy D and Burgyan J (2004) Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends in Plant Science 9: 76–83.
    Simon AE and Gehrke L (2009) RNA conformational changes in the life cycles of RNA viruses, viroids, and virus-associated RNAs. Biochimica et Biophysica Acta 1789: 571–583.
    White KA and Nagy PD (2004) Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Progress in Nucleic Acid Research and Molecular Biology 78: 187–226.

Related Sub-Topics:

Viruses Infecting Plants | RNA Viruses | Plant Disease
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Article Title: Tombusviridae
 
How to Cite close
Sit, Tim L, and Lommel, Steven A(Apr 2010) Tombusviridae. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000756.pub2]