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. 1984 Dec 1;3(12):2731–2736. doi: 10.1002/j.1460-2075.1984.tb02203.x

Initiation of translation of the cauliflower mosaic virus genome from a polycistronic mRNA: evidence from deletion mutagenesis

Linda K Dixon 1,1, Thomas Hohn 1
PMCID: PMC557760  PMID: 16453575

Abstract

Mutants with deletions in the open reading frame (ORF) VII to I region of the cauliflower mosaic virus genome were constructed in vitro and tested for infectivity by inoculation of plants. Sequences within ORF VII and the intergenomic region between ORFs VII and I are not required for viral infectivity. Nevertheless, the location of translation initiation and termination codons within this region governs the infectivity of the virus. Firstly, translation beginning at the initiation codon of ORF VII should reach an in-phase termination codon before the initiation codon of ORF I. Secondly, an initiation codon should be located in the vicinity of the sequence homologous to methionine tRNA, the proposed primer binding site for reverse transcription. Results suggest translation from a polycistronic mRNA by a `relay race' mechanism whereby ribosomes after passing a termination codon re-initiate protein synthesis at the nearest AUG codon.

Keywords: deletion mutagenesis, eukaryotic polycistronic mRNA, plant virus

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Selected References

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  1. Balàzs E., Guilley H., Jonard G., Richards K. Nucleotide sequence of DNA from an altered-virulence isolate D/H of the cauliflower mosaic virus. Gene. 1982 Oct;19(3):239–249. doi: 10.1016/0378-1119(82)90013-0. [DOI] [PubMed] [Google Scholar]
  2. Condit C., Meagher R. B. Multiple, discrete 35S transcripts of cauliflower mosaic virus. J Mol Appl Genet. 1983;2(3):301–314. [PubMed] [Google Scholar]
  3. Darlix J. L., Zuker M., Spahr P. F. Structure-function relationship of Rous sarcoma virus leader RNA. Nucleic Acids Res. 1982 Sep 11;10(17):5183–5196. doi: 10.1093/nar/10.17.5183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Daubert S., Shepherd R. J., Gardner R. C. Insertional mutagenesis of the cauliflower mosaic virus genome. Gene. 1983 Nov;25(2-3):201–208. doi: 10.1016/0378-1119(83)90224-x. [DOI] [PubMed] [Google Scholar]
  5. Dixon L. K., Koenig I., Hohn T. Mutagenesis of cauliflower mosaic virus. Gene. 1983 Nov;25(2-3):189–199. doi: 10.1016/s0378-1119(83)80001-8. [DOI] [PubMed] [Google Scholar]
  6. Franck A., Guilley H., Jonard G., Richards K., Hirth L. Nucleotide sequence of cauliflower mosaic virus DNA. Cell. 1980 Aug;21(1):285–294. doi: 10.1016/0092-8674(80)90136-1. [DOI] [PubMed] [Google Scholar]
  7. Gardner R. C., Howarth A. J., Hahn P., Brown-Luedi M., Shepherd R. J., Messing J. The complete nucleotide sequence of an infectious clone of cauliflower mosaic virus by M13mp7 shotgun sequencing. Nucleic Acids Res. 1981 Jun 25;9(12):2871–2888. doi: 10.1093/nar/9.12.2871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Givord L., Xiong C., Giband M., Koenig I., Hohn T., Lebeurier G., Hirth L. A second cauliflower mosaic virus gene product influences the structure of the viral inclusion body. EMBO J. 1984 Jun;3(6):1423–1427. doi: 10.1002/j.1460-2075.1984.tb01987.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Guilley H., Dudley R. K., Jonard G., Balàzs E., Richards K. E. Transcription of Cauliflower mosaic virus DNA: detection of promoter sequences, and characterization of transcripts. Cell. 1982 Oct;30(3):763–773. doi: 10.1016/0092-8674(82)90281-1. [DOI] [PubMed] [Google Scholar]
  10. Guilley H., Richards K. E., Jonard G. Observations concerning the discontinuous DNAs of cauliflower mosaic virus. EMBO J. 1983;2(2):277–282. doi: 10.1002/j.1460-2075.1983.tb01417.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kozak M. Selection of initiation sites by eucaryotic ribosomes: effect of inserting AUG triplets upstream from the coding sequence for preproinsulin. Nucleic Acids Res. 1984 May 11;12(9):3873–3893. doi: 10.1093/nar/12.9.3873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Krebbers E. T., Larrinua I. M., McIntosh L., Bogorad L. The maize chloroplast genes for the beta and epsilon subunits of the photosynthetic coupling factor CF1 are fused. Nucleic Acids Res. 1982 Aug 25;10(16):4985–5002. doi: 10.1093/nar/10.16.4985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lebeurier G., Hirth L., Hohn T., Hohn B. Infectivities of native and cloned DNA of cauliflower mosaic virus. Gene. 1980 Dec;12(1-2):139–146. doi: 10.1016/0378-1119(80)90024-4. [DOI] [PubMed] [Google Scholar]
  15. Liu C. C., Simonsen C. C., Levinson A. D. Initiation of translation at internal AUG codons in mammalian cells. Nature. 1984 May 3;309(5963):82–85. doi: 10.1038/309082a0. [DOI] [PubMed] [Google Scholar]
  16. Mertens P. P., Dobos P. Messenger RNA of infectious pancreatic necrosis virus is polycistronic. Nature. 1982 May 20;297(5863):243–246. doi: 10.1038/297243a0. [DOI] [PubMed] [Google Scholar]
  17. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  19. Ménissier J., de Murcia G., Lebeurier G., Hirth L. Electron microscopic studies of the different topological forms of the cauliflower mosaic virus DNA: knotted encapsidated DNA and nuclear minichromosome. EMBO J. 1983;2(7):1067–1071. doi: 10.1002/j.1460-2075.1983.tb01547.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Olszewski N., Hagen G., Guilfoyle T. J. A transcriptionally active, covalently closed minichromosome of cauliflower mosaic virus DNA isolated from infected turnip leaves. Cell. 1982 Jun;29(2):395–402. doi: 10.1016/0092-8674(82)90156-8. [DOI] [PubMed] [Google Scholar]
  21. Pfeiffer P., Hohn T. Involvement of reverse transcription in the replication of cauliflower mosaic virus: a detailed model and test of some aspects. Cell. 1983 Jul;33(3):781–789. doi: 10.1016/0092-8674(83)90020-x. [DOI] [PubMed] [Google Scholar]
  22. Richards K. E., Guilley H., Jonard G. Further characterization of the discontinuities in cauliflower mosaic virus DNA. FEBS Lett. 1981 Nov 2;134(1):67–70. doi: 10.1016/0014-5793(81)80552-2. [DOI] [PubMed] [Google Scholar]
  23. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Southern P. J., Berg P. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J Mol Appl Genet. 1982;1(4):327–341. [PubMed] [Google Scholar]
  25. Woolston C. J., Covey S. N., Penswick J. R., Davies J. W. Aphid transmission and a polypeptide are specified by a defined region of the cauliflower mosaic virus genome. Gene. 1983 Jul;23(1):15–23. doi: 10.1016/0378-1119(83)90212-3. [DOI] [PubMed] [Google Scholar]
  26. Xiong C., Muller S., Lebeurier G., Hirth L. Identification by immunoprecipitation of cauliflower mosaic virus in vitro major translation product with a specific serum against viroplasm protein. EMBO J. 1982;1(8):971–976. doi: 10.1002/j.1460-2075.1982.tb01280.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Zurawski G., Bottomley W., Whitfeld P. R. Structures of the genes for the beta and epsilon subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6260–6264. doi: 10.1073/pnas.79.20.6260. [DOI] [PMC free article] [PubMed] [Google Scholar]

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