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. 1994 Aug 11;22(15):2882–2886. doi: 10.1093/nar/22.15.2882

A histidine accepting tRNA-like fold at the 3'-end of satellite tobacco mosaic virus RNA.

B Felden 1, C Florentz 1, A McPherson 1, R Giegé 1
PMCID: PMC310250  PMID: 8065897

Abstract

A model of secondary structure is proposed for the 3'-terminal sequence of the satellite tobacco mosaic virus (STMV) RNA on the basis of phylogenetic comparisons with tobacco mosaic virus (TMV) genomic RNA. Sequence homologies and compensatory base changes found between the two related viral RNAs imply that the 3'-end of STMV RNA folds into a tRNA-like domain similar to that found in the TMV RNA. Accordingly, functional assays showed that STMV RNA can be aminoacylated in vitro with histidine by yeast histidyl-tRNA synthetase to plateaus reaching 30%. Histidylation properties of STMV RNA were compared to those of TMV RNA and of a canonical yeast tRNA(His) transcript which both are chargeable to nearly 100% plateau levels. Kinetic data indicate an excellent catalytic efficiency of STMV RNA charging expressed as Vmax/Km ratio, quasi-equivalent to that of TMV RNA, and only 17-fold reduced as compared to that of the yeast tRNAHis transcript. Biological implications of the structural mimicry between the tRNA-like regions of TMV and STMV RNAs are discussed in the light of the relationships of a satellite virus with its helper virus. This is the first report on a chargeable tRNA-like structure at the 3'-end of a satellite virus RNA.

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Selected References

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  1. Chen J. M., Hall T. C. Comparison of tyrosyl transfer ribonucleic acid and brome mosaic virus tyrosyl ribonucleic acid as amino acid donors in protein synthesis. Biochemistry. 1973 Nov 6;12(23):4570–4574. doi: 10.1021/bi00747a004. [DOI] [PubMed] [Google Scholar]
  2. Coutts R. H., Rigden J. E., Slabas A. R., Lomonossoff G. P., Wise P. J. The complete nucleotide sequence of tobacco necrosis virus strain D. J Gen Virol. 1991 Jul;72(Pt 7):1521–1529. doi: 10.1099/0022-1317-72-7-1521. [DOI] [PubMed] [Google Scholar]
  3. Danthinne X., Seurinck J., Van Montagu M., Pleij C. W., van Emmelo J. Structural similarities between the RNAs of two satellites of tobacco necrosis virus. Virology. 1991 Dec;185(2):605–614. doi: 10.1016/0042-6822(91)90531-f. [DOI] [PubMed] [Google Scholar]
  4. Dreher T. W., Hall T. C. Mutational analysis of the sequence and structural requirements in brome mosaic virus RNA for minus strand promoter activity. J Mol Biol. 1988 May 5;201(1):31–40. doi: 10.1016/0022-2836(88)90436-6. [DOI] [PubMed] [Google Scholar]
  5. Dreher T. W., Tsai C. H., Florentz C., Giegé R. Specific valylation of turnip yellow mosaic virus RNA by wheat germ valyl-tRNA synthetase determined by three anticodon loop nucleotides. Biochemistry. 1992 Sep 29;31(38):9183–9189. doi: 10.1021/bi00153a010. [DOI] [PubMed] [Google Scholar]
  6. Dumas P., Moras D., Florentz C., Giegé R., Verlaan P., Van Belkum A., Pleij C. W. 3-D graphics modelling of the tRNA-like 3'-end of turnip yellow mosaic virus RNA: structural and functional implications. J Biomol Struct Dyn. 1987 Apr;4(5):707–728. doi: 10.1080/07391102.1987.10507674. [DOI] [PubMed] [Google Scholar]
  7. Felden B., Florentz C., Giegé R., Westhof E. Solution structure of the 3'-end of brome mosaic virus genomic RNAs. Conformational mimicry with canonical tRNAs. J Mol Biol. 1994 Jan 14;235(2):508–531. doi: 10.1006/jmbi.1994.1010. [DOI] [PubMed] [Google Scholar]
  8. Francklyn C., Schimmel P. Enzymatic aminoacylation of an eight-base-pair microhelix with histidine. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8655–8659. doi: 10.1073/pnas.87.21.8655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gallie D. R., Feder J. N., Schimke R. T., Walbot V. Functional analysis of the tobacco mosaic virus tRNA-like structure in cytoplasmic gene regulation. Nucleic Acids Res. 1991 Sep 25;19(18):5031–5036. doi: 10.1093/nar/19.18.5031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Goelet P., Lomonossoff G. P., Butler P. J., Akam M. E., Gait M. J., Karn J. Nucleotide sequence of tobacco mosaic virus RNA. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5818–5822. doi: 10.1073/pnas.79.19.5818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gordon K. H., Symons R. H. Satellite RNA of cucumber mosaic virus forms a secondary structure with partial 3'-terminal homology to genomal RNAs. Nucleic Acids Res. 1983 Feb 25;11(4):947–960. doi: 10.1093/nar/11.4.947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Haenni A. L., Joshi S., Chapeville F. tRNA-like structures in the genomes of RNA viruses. Prog Nucleic Acid Res Mol Biol. 1982;27:85–104. doi: 10.1016/s0079-6603(08)60598-x. [DOI] [PubMed] [Google Scholar]
  13. Himeno H., Hasegawa T., Ueda T., Watanabe K., Miura K., Shimizu M. Role of the extra G-C pair at the end of the acceptor stem of tRNA(His) in aminoacylation. Nucleic Acids Res. 1989 Oct 11;17(19):7855–7863. doi: 10.1093/nar/17.19.7855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Joshi R. L., Joshi S., Chapeville F., Haenni A. L. tRNA-like structures of plant viral RNAs: conformational requirements for adenylation and aminoacylation. EMBO J. 1983;2(7):1123–1127. doi: 10.1002/j.1460-2075.1983.tb01556.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Larson S. B., Koszelak S., Day J., Greenwood A., Dodds J. A., McPherson A. Double-helical RNA in satellite tobacco mosaic virus. Nature. 1993 Jan 14;361(6408):179–182. doi: 10.1038/361179a0. [DOI] [PubMed] [Google Scholar]
  16. Larson S. B., Koszelak S., Day J., Greenwood A., Dodds J. A., McPherson A. Three-dimensional structure of satellite tobacco mosaic virus at 2.9 A resolution. J Mol Biol. 1993 May 20;231(2):375–391. doi: 10.1006/jmbi.1993.1289. [DOI] [PubMed] [Google Scholar]
  17. Leathers V., Tanguay R., Kobayashi M., Gallie D. R. A phylogenetically conserved sequence within viral 3' untranslated RNA pseudoknots regulates translation. Mol Cell Biol. 1993 Sep;13(9):5331–5347. doi: 10.1128/mcb.13.9.5331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mans R. M., Pleij C. W., Bosch L. tRNA-like structures. Structure, function and evolutionary significance. Eur J Biochem. 1991 Oct 15;201(2):303–324. doi: 10.1111/j.1432-1033.1991.tb16288.x. [DOI] [PubMed] [Google Scholar]
  19. Miller W. A., Bujarski J. J., Dreher T. W., Hall T. C. Minus-strand initiation by brome mosaic virus replicase within the 3' tRNA-like structure of native and modified RNA templates. J Mol Biol. 1986 Feb 20;187(4):537–546. doi: 10.1016/0022-2836(86)90332-3. [DOI] [PubMed] [Google Scholar]
  20. Mirkov T. E., Mathews D. M., Du Plessis D. H., Dodds J. A. Nucleotide sequence and translation of satellite tobacco mosaic virus RNA. Virology. 1989 May;170(1):139–146. doi: 10.1016/0042-6822(89)90361-9. [DOI] [PubMed] [Google Scholar]
  21. Oberg B., Philipson L. Binding of histidine to tobacco mosaic virus RNA. Biochem Biophys Res Commun. 1972 Aug 21;48(4):927–932. doi: 10.1016/0006-291x(72)90697-3. [DOI] [PubMed] [Google Scholar]
  22. Rao A. L., Dreher T. W., Marsh L. E., Hall T. C. Telomeric function of the tRNA-like structure of brome mosaic virus RNA. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5335–5339. doi: 10.1073/pnas.86.14.5335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rietveld K., Linschooten K., Pleij C. W., Bosch L. The three-dimensional folding of the tRNA-like structure of tobacco mosaic virus RNA. A new building principle applied twice. EMBO J. 1984 Nov;3(11):2613–2619. doi: 10.1002/j.1460-2075.1984.tb02182.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rietveld K., Pleij C. W., Bosch L. Three-dimensional models of the tRNA-like 3' termini of some plant viral RNAs. EMBO J. 1983;2(7):1079–1085. doi: 10.1002/j.1460-2075.1983.tb01549.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roossinck M. J., Sleat D., Palukaitis P. Satellite RNAs of plant viruses: structures and biological effects. Microbiol Rev. 1992 Jun;56(2):265–279. doi: 10.1128/mr.56.2.265-279.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rudinger J., Florentz C., Dreher T., Giegé R. Efficient mischarging of a viral tRNA-like structure and aminoacylation of a minihelix containing a pseudoknot: histidinylation of turnip yellow mosaic virus RNA. Nucleic Acids Res. 1992 Apr 25;20(8):1865–1870. doi: 10.1093/nar/20.8.1865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Simon A. E., Howell S. H. The virulent satellite RNA of turnip crinkle virus has a major domain homologous to the 3' end of the helper virus genome. EMBO J. 1986 Dec 20;5(13):3423–3428. doi: 10.1002/j.1460-2075.1986.tb04664.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Solis I., Garcia-Arenal F. The complete nucleotide sequence of the genomic RNA of the tobamovirus tobacco mild green mosaic virus. Virology. 1990 Aug;177(2):553–558. doi: 10.1016/0042-6822(90)90520-2. [DOI] [PubMed] [Google Scholar]
  29. Tsai C. H., Dreher T. W. Turnip yellow mosaic virus RNAs with anticodon loop substitutions that result in decreased valylation fail to replicate efficiently. J Virol. 1991 Jun;65(6):3060–3067. doi: 10.1128/jvi.65.6.3060-3067.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weiner A. M., Maizels N. tRNA-like structures tag the 3' ends of genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7383–7387. doi: 10.1073/pnas.84.21.7383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wyatt J. R., Chastain M., Puglisi J. D. Synthesis and purification of large amounts of RNA oligonucleotides. Biotechniques. 1991 Dec;11(6):764–769. [PubMed] [Google Scholar]
  32. Ysebaert M., van Emmelo J., Fiers W. Total nucleotide sequence of a nearly full-size DNA copy of satellite tobacco necrosis virus RNA. J Mol Biol. 1980 Nov 5;143(3):273–287. doi: 10.1016/0022-2836(80)90190-4. [DOI] [PubMed] [Google Scholar]
  33. van Belkum A., Abrahams J. P., Pleij C. W., Bosch L. Five pseudoknots are present at the 204 nucleotides long 3' noncoding region of tobacco mosaic virus RNA. Nucleic Acids Res. 1985 Nov 11;13(21):7673–7686. doi: 10.1093/nar/13.21.7673. [DOI] [PMC free article] [PubMed] [Google Scholar]

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