Cited by 66Plant Virus Research StudiesPlant and Fungal Interactions ResearchRNA Research and Splicing

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A complex network of RNA–RNA interactions controls subgenomic mRNA transcription in a tombusvirus

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Lin, Han‐Xin, White, K Andrew·2004·The EMBO Journal

Abstract

Eukaryotic (+)-strand RNA viruses utilize a wide variety of gene expression strategies to achieve regulated production of their viral proteins. A common mechanism used by many is to transcribe viral subgenomic (sg) mRNAs. Transcription of sg mRNA2 in tombusviruses allows for expression of the p19 suppressor of gene silencing and p22 movement proteins. We have investigated the mechanism of transcription of this sg mRNA in Tomato bushy stunt virus and have determined that this process is facilitated by no less than three different RNA modules that are located throughout the viral genome. These RNA units perform distinct tasks and function via long-distance RNA-RNA interactions. Systematic deconstruction of the RNA network and analysis of related RNA promoter elements allowed us to identify fundamental properties necessary for productive sg mRNA2 transcription. Collectively, our results (i) establish specific roles for the different RNA components of a multipartite RNA-based control system, (ii) support a premature termination mechanism for tombusvirus sg mRNA transcription and (iii) reveal a close mechanistic relationship between sg mRNA transcription, viral RNA replication and RNA recombination.

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Research works printed but not linked: 40

  1. Buck KW (1996) Comparison of the replication of positive‐stranded RNA viruses of plants and animals. Adv Virus Res 47: 159–251 · DOI
  2. Choi IR, Ostrovsky M, Zhang G, White KA (2001) Regulatory activity of distal and core RNA elements in tombusvirus subgenomic mRNA2 transcription. J Biol Chem 276: 41761–41768 · DOI
  3. Choi IR, White KA (2002) An RNA activator of subgenomic mRNA1 transcription in tomato bushy stunt virus. J Biol Chem 277: 3760–3766 · DOI
  4. Eckerle LD, Albarino CG, Ball LA (2003) Flock house virus subgenomic RNA3 is replicated and its replication correlates with transactivation of RNA2. Virology 317: 95–108 · DOI
  5. Fabian MR, White KA (2004) 5′–3′ RNA–RNA interaction facilitates cap‐ and poly(A) tail‐independent translation of tomato bushy stunt virus mRNA: a potential common mechanism for tombusviridae. J Biol Chem 279: 28862–28872 · DOI
  6. Gowda S, Satyanarayana T, Ayllon MA, Albiach‐Marti MR, Mawassi M, Rabindran S, Garnsey SM, Dawson WO (2001) Characterization of the cis‐acting elements controlling subgenomic mRNAs of citrus tristeza virus: production of positive‐ and negative‐stranded 3′‐terminal and positive‐stranded 5′‐terminal RNAs. Virology 286: 134–151 · DOI
  7. Haasnoot PCJ, Brederode FT, Olsthoorn RCL, Bol JF (2000) A conserved hairpin structure in Alfamovirus and Bromovirus subgenomic promoters is required for efficient RNA synthesis in vitro. RNA 6: 708–716 · DOI
  8. Hearne PQ, Knorr DA, Hillman BI, Morris TJ (1990) The complete genome structure and synthesis of infectious RNA from clones of tomato bushy stunt virus. Virology 177: 141–151 · DOI
  9. Hillman BI, Hearne P, Rochon D, Morris TJ (1989) Organization of tomato bushy stunt virus genome: characterization of the coat protein gene and the 3′ terminus. Virology 169: 42–50 · DOI
  10. Joost Haasnoot PC, Olsthoorn RC, Bol JF (2002) The Brome mosaic virus subgenomic promoter hairpin is structurally similar to the iron‐responsive element and functionally equivalent to the minus‐strand core promoter stem–loop C. RNA 8: 110–122 · DOI
  11. Lindenbach BD, Sgro JY, Ahlquist P (2002) Long‐distance base pairing in Flock House virus RNA1 regulates subgenomic RNA3 synthesis and RNA2 replication. J Virol 76: 3905–3919 · DOI
  12. Liu X, Gorovsky MA (1993) Mapping the 5′ and 3′ ends of Tetrahymena thermophila mRNAs using RNA ligase mediated amplification of cDNA ends (RLM‐RACE). Nucleic Acids Res 21: 4954–4960 · DOI
  13. Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters provides robust prediction of RNA secondary structure. J Mol Biol 288: 911–940 · DOI · Paper page
  14. Miller WA, Dreher TW, Hall TC (1985) Synthesis of brome mosaic virus subgenomic RNA in vitro by internal initiation on (−)‐sense genome RNA. Nature 313: 68–70 · DOI
  15. Miller WA, Koev G (2000) Synthesis of subgenomic RNAs by positive‐strand RNA viruses. Virology 273: 1–8 · DOI
  16. Nagaswamy U, Larios‐Sanz M, Hury J, Collins S, Zhang Z, Zhao Q, Fox GE (2002) NCIR: a database of non‐canonical interactions in known RNA structures. Nucleic Acids Res 30: 395–397 · DOI
  17. Olsthoorn RC, Haasnoot PC, Bol JF (2004) Similarities and differences between the subgenomic and minus‐strand promoters of an RNA plant virus. J Virol 78: 4048–4053 · DOI
  18. Oster SK, Wu B, White KA (1998) Uncoupled expression of p33 and p92 permits amplification of tomato bushy stunt virus RNAs. J Virol 72: 5845–5851 · DOI
  19. Panavas T, Pogany J, Nagy PD (2002) Analysis of minimal promoter sequences for plus‐strand synthesis by the Cucumber necrosis virus RNA‐dependent RNA polymerase. Virology 296: 263–274 · DOI
  20. Pasternak AO, van den Born E, Spaan WJ, Snijder EJ (2001) Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J 20: 7220–7228 · DOI
  21. Price BD, Roeder M, Ahlquist P (2000) DNA‐directed expression of functional flock house virus RNA1 derivatives in Saccharomyces cerevisiae, heterologous gene expression, and selective effects on subgenomic mRNA synthesis. J Virol 74: 11724–11733 · DOI
  22. Ray D, Wu B, White KA (2003) A second functional RNA domain in the 5′ UTR of the Tomato bushy stunt virus genome: intra‐ and interdomain interactions mediate viral RNA replication. RNA 9: 1232–1245 · DOI
  23. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edn Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
  24. Sawicki SG, Sawicki DL (1998) A new model for coronavirus transcription. Adv Exp Med Biol 440: 215–219 · DOI
  25. Scholthof HB, Scholthof KB, Kikkert M, 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 · DOI
  26. Sit TL, Vaewhongs AA, Lommel SA (1998) RNA‐mediated trans‐activation of transcription from a viral RNA. Science 281: 829–832 · DOI
  27. Sivakumaran K, Choi SK, Hema M, Kao CC (2004) Requirements for brome mosaic virus subgenomic RNA synthesis in vivo and replicase‐core promoter interactions in vitro. J Virol 78: 6091–6101 · DOI
  28. van Marle G, Dobbe JC, Gultyaev AP, Luytjes W, Spaan WJ, Snijder EJ (1999) Arterivirus discontinuous mRNA transcription is guided by base pairing between sense and antisense transcription‐regulating sequences. Proc Natl Acad Sci USA 96: 12056–12061 · DOI
  29. van Vliet AL, Smits SL, Rottier PJ, de Groot RJ (2002) Discontinuous and non‐discontinuous subgenomic RNA transcription in a nidovirus. EMBO J 21: 6571–6580 · DOI
  30. Voinnet O, Pinto YM, Baulcombe DC (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci USA 96: 14147–14152 · DOI
  31. White KA (1996) Formation and evolution of tombusvirus defective interfering RNAs. Semin Virol 7: 409–416 · DOI
  32. White KA (2002) The premature termination model: a possible third mechanism for subgenomic mRNA transcription in (+)‐strand RNA viruses. Virology 304: 147–154 · DOI
  33. White KA, Morris TJ (1995) RNA determinants of junction site selection in RNA virus recombinants and defective interfering RNAs. RNA 1: 1029–1040
  34. White KA, Nagy PD (2004) Advances in the molecular biology of tombusviruses: gene expression, genome replication and recombination. Prog Nucleic Acids Res Mol Biol 78: 187–226 · DOI
  35. Wu B, Vanti WB, White KA (2001) An RNA domain within the 5′ untranslated region of the tomato bushy stunt virus genome modulates viral RNA replication. J Mol Biol 305: 741–756 · DOI
  36. Wu B, White KA (1998) Formation and amplification of a novel tombusvirus defective RNA which lacks the 5′ nontranslated region of the viral genome. J Virol 72: 9897–9905 · DOI
  37. Ye K, Malinina L, Patel DJ (2003) Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 426: 874–878 · DOI
  38. Zhang G, Slowinski V, White KA (1999) Subgenomic mRNA regulation by a distal RNA element in a (+)‐strand RNA virus. RNA 5: 550–561 · DOI
  39. Zhong W, Rueckert RR (1993) Flock house virus: down‐regulation of subgenomic RNA3 synthesis does not involve coat protein and is targeted to synthesis of its positive strand. J Virol 67: 2716–2722 · DOI
  40. Zuker M, Mathews DH, Turner DH (1999) Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In RNA Biochemistry and Bio/Technology, Barciszewski J, Clark BFC (eds) pp 11–43. Dordrecht/Norwell, MA: Kluwer Academic Publishers · DOI

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Metadata

Authors
Lin, H., & White, K. A.
Affiliations
York University (CA)
Corresponding author
White, K Andrew
Venue
The EMBO Journal
Published
2004-07-29
Volume
23
Issue
16
Pages
3365-3374
ISSN
  • 0261-4189 (ISSN-L)
  • 1460-2075
OpenAlex
W2136046332
Cited by
66
References
0
Citations by year
2026: 1 · 2024: 3 · 2023: 2 · 2021: 3 · 2020: 2 · 2018: 1 · 2017: 2 · 2016: 2 · 2015: 4 · 2014: 4 · 2013: 5 · 2012: 3
FWCI
6.93
Type
journal article
Language
en
Open access
Locations
  • The EMBO Journal (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
Natural Sciences and Engineering Research Council of Canada
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Virus Research Studies
  • Life Sciences › Immunology and Microbiology › Virology › Plant and Fungal Interactions Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords
tombusvirus, tomato bushy stunt virus, RNA-RNA interactions, early termination, viral RNA replication, RNA recombination, positive-strand RNA viruses
MeSH terms
Base Sequence, Genetic Engineering, Molecular Sequence Data, Promoter Regions, Genetic, RNA, Messenger, RNA, Viral, Transcription, Genetic, Virus Replication, Down-Regulation, Gene Expression Regulation, Viral, Genome, Viral, Tombusvirus, Base Pairing, RNA Stability

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CoChat. (2026). Citation check: A complex network of RNA–RNA interactions controls subgenomic mRNA transcription in a tombusvirus. https://app.cochat.ai/papers/10.1038/sj.emboj.7600336
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Lin, H., & White, K. A. (2004). A complex network of RNA–RNA interactions controls subgenomic mRNA transcription in a tombusvirus. The EMBO Journal. https://doi.org/10.1038/sj.emboj.7600336