Abstract
The expression of the rice tungro bacilliform virus open reading frame I was studied in transiently transfected protoplasts. Expression occurs despite the presence of a long leader sequence and the absence of a proper ATG initiation codon. Translation is initiated at an ATT codon. The efficiency of initiation in rice protoplasts depends strongly on the mechanism by which ribosomes reach this codon. From the effects of scanning-inhibiting structures inserted into different leader regions, it can be deduced that this mechanism is related to the ribosome shunt described for cauliflower mosaic virus 35S RNA. The process delivers initiation-competent ribosomes to the region downstream of the leader and is so precise that only the second of two potential start codons only 12 nucleotides apart is recognized. The ATT codon that is used when it is present downstream of the leader is hardly recognized as a start codon by ribosomes that reach it by scanning.
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- Agol V. I. The 5'-untranslated region of picornaviral genomes. Adv Virus Res. 1991;40:103–180. doi: 10.1016/S0065-3527(08)60278-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bao Y., Hull R. Mapping the 5'-terminus of rice tungro bacilliform viral genomic RNA. Virology. 1993 Nov;197(1):445–448. doi: 10.1006/viro.1993.1609. [DOI] [PubMed] [Google Scholar]
- Beames B., Braunagel S., Summers M. D., Lanford R. E. Polyhedrin initiator codon altered to AUU yields unexpected fusion protein from a baculovirus vector. Biotechniques. 1991 Sep;11(3):378–383. [PubMed] [Google Scholar]
- Belsham G. J. Dual initiation sites of protein synthesis on foot-and-mouth disease virus RNA are selected following internal entry and scanning of ribosomes in vivo. EMBO J. 1992 Mar;11(3):1105–1110. doi: 10.1002/j.1460-2075.1992.tb05150.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bevan M. Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 1984 Nov 26;12(22):8711–8721. doi: 10.1093/nar/12.22.8711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boeck R., Kolakofsky D. Positions +5 and +6 can be major determinants of the efficiency of non-AUG initiation codons for protein synthesis. EMBO J. 1994 Aug 1;13(15):3608–3617. doi: 10.1002/j.1460-2075.1994.tb06668.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bonneville J. M., Sanfaçon H., Fütterer J., Hohn T. Posttranscriptional trans-activation in cauliflower mosaic virus. Cell. 1989 Dec 22;59(6):1135–1143. doi: 10.1016/0092-8674(89)90769-1. [DOI] [PubMed] [Google Scholar]
- Bouhida M., Lockhart B. E., Olszewski N. E. An analysis of the complete sequence of a sugarcane bacilliform virus genome infectious to banana and rice. J Gen Virol. 1993 Jan;74(Pt 1):15–22. doi: 10.1099/0022-1317-74-1-15. [DOI] [PubMed] [Google Scholar]
- Boyd L., Thummel C. S. Selection of CUG and AUG initiator codons for Drosophila E74A translation depends on downstream sequences. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9164–9167. doi: 10.1073/pnas.90.19.9164. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carroll R., Derse D. Translation of equine infectious anemia virus bicistronic tat-rev mRNA requires leaky ribosome scanning of the tat CTG initiation codon. J Virol. 1993 Mar;67(3):1433–1440. doi: 10.1128/jvi.67.3.1433-1440.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen G., Müller M., Potrykus I., Hohn T., Fütterer J. Rice tungro bacilliform virus: transcription and translation in protoplasts. Virology. 1994 Oct;204(1):91–100. doi: 10.1006/viro.1994.1513. [DOI] [PubMed] [Google Scholar]
- Chen X., Chamorro M., Lee S. I., Shen L. X., Hines J. V., Tinoco I., Jr, Varmus H. E. Structural and functional studies of retroviral RNA pseudoknots involved in ribosomal frameshifting: nucleotides at the junction of the two stems are important for efficient ribosomal frameshifting. EMBO J. 1995 Feb 15;14(4):842–852. doi: 10.1002/j.1460-2075.1995.tb07062.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clements J. M., Laz T. M., Sherman F. Efficiency of translation initiation by non-AUG codons in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Oct;8(10):4533–4536. doi: 10.1128/mcb.8.10.4533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dasgupta I., Hull R., Eastop S., Poggi-Pollini C., Blakebrough M., Boulton M. I., Davies J. W. Rice tungro bacilliform virus DNA independently infects rice after Agrobacterium-mediated transfer. J Gen Virol. 1991 Jun;72(Pt 6):1215–1221. doi: 10.1099/0022-1317-72-6-1215. [DOI] [PubMed] [Google Scholar]
- Davies M. V., Kaufman R. J. The sequence context of the initiation codon in the encephalomyocarditis virus leader modulates efficiency of internal translation initiation. J Virol. 1992 Apr;66(4):1924–1932. doi: 10.1128/jvi.66.4.1924-1932.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fütterer J., Gordon K., Bonneville J. M., Sanfaçon H., Pisan B., Penswick J., Hohn T. The leading sequence of caulimovirus large RNA can be folded into a large stem-loop structure. Nucleic Acids Res. 1988 Sep 12;16(17):8377–8390. doi: 10.1093/nar/16.17.8377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fütterer J., Gordon K., Pfeiffer P., Sanfaçon H., Pisan B., Bonneville J. M., Hohn T. Differential inhibition of downstream gene expression by the cauliflower mosaic virus 35S RNA leader. Virus Genes. 1989 Sep;3(1):45–55. doi: 10.1007/BF00301986. [DOI] [PubMed] [Google Scholar]
- Fütterer J., Gordon K., Sanfaçon H., Bonneville J. M., Hohn T. Positive and negative control of translation by the leader sequence of cauliflower mosaic virus pregenomic 35S RNA. EMBO J. 1990 Jun;9(6):1697–1707. doi: 10.1002/j.1460-2075.1990.tb08293.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fütterer J., Hohn T. Role of an upstream open reading frame in the translation of polycistronic mRNAs in plant cells. Nucleic Acids Res. 1992 Aug 11;20(15):3851–3857. doi: 10.1093/nar/20.15.3851. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fütterer J., Hohn T. Translation of a polycistronic mRNA in the presence of the cauliflower mosaic virus transactivator protein. EMBO J. 1991 Dec;10(12):3887–3896. doi: 10.1002/j.1460-2075.1991.tb04958.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fütterer J., Kiss-László Z., Hohn T. Nonlinear ribosome migration on cauliflower mosaic virus 35S RNA. Cell. 1993 May 21;73(4):789–802. doi: 10.1016/0092-8674(93)90257-q. [DOI] [PubMed] [Google Scholar]
- Fütterer J., Potrykus I., Valles Brau M. P., Dasgupta I., Hull R., Hohn T. Splicing in a plant pararetrovirus. Virology. 1994 Feb;198(2):663–670. doi: 10.1006/viro.1994.1078. [DOI] [PubMed] [Google Scholar]
- Gordon K., Fütterer J., Hohn T. Efficient initiation of translation at non-AUG triplets in plant cells. Plant J. 1992 Sep;2(5):809–813. [PubMed] [Google Scholar]
- Gowda S., Scholthof H. B., Wu F. C., Shepherd R. J. Requirement of gene VII in cis for the expression of downstream genes on the major transcript of figwort mosaic virus. Virology. 1991 Dec;185(2):867–871. doi: 10.1016/0042-6822(91)90561-o. [DOI] [PubMed] [Google Scholar]
- Gowda S., Wu F. C., Scholthof H. B., Shepherd R. J. Gene VI of figwort mosaic virus (caulimovirus group) functions in posttranscriptional expression of genes on the full-length RNA transcript. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9203–9207. doi: 10.1073/pnas.86.23.9203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grünert S., Jackson R. J. The immediate downstream codon strongly influences the efficiency of utilization of eukaryotic translation initiation codons. EMBO J. 1994 Aug 1;13(15):3618–3630. doi: 10.1002/j.1460-2075.1994.tb06669.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hagen L. S., Jacquemond M., Lepingle A., Lot H., Tepfer M. Nucleotide sequence and genomic organization of cacao swollen shoot virus. Virology. 1993 Oct;196(2):619–628. doi: 10.1006/viro.1993.1518. [DOI] [PubMed] [Google Scholar]
- Hann S. R., Sloan-Brown K., Spotts G. D. Translational activation of the non-AUG-initiated c-myc 1 protein at high cell densities due to methionine deprivation. Genes Dev. 1992 Jul;6(7):1229–1240. doi: 10.1101/gad.6.7.1229. [DOI] [PubMed] [Google Scholar]
- Hatfield D. L., Levin J. G., Rein A., Oroszlan S. Translational suppression in retroviral gene expression. Adv Virus Res. 1992;41:193–239. doi: 10.1016/S0065-3527(08)60037-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hay J. M., Jones M. C., Blakebrough M. L., Dasgupta I., Davies J. W., Hull R. An analysis of the sequence of an infectious clone of rice tungro bacilliform virus, a plant pararetrovirus. Nucleic Acids Res. 1991 May 25;19(10):2615–2621. doi: 10.1093/nar/19.10.2615. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hay J., Grieco F., Druka A., Pinner M., Lee S. C., Hull R. Detection of rice tungro bacilliform virus gene products in vivo. Virology. 1994 Dec;205(2):430–437. doi: 10.1006/viro.1994.1663. [DOI] [PubMed] [Google Scholar]
- Hellen C. U., Pestova T. V., Wimmer E. Effect of mutations downstream of the internal ribosome entry site on initiation of poliovirus protein synthesis. J Virol. 1994 Oct;68(10):6312–6322. doi: 10.1128/jvi.68.10.6312-6322.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hohn T., Fütterer J. Transcriptional and translational control of gene expression in cauliflower mosaic virus. Curr Opin Genet Dev. 1992 Feb;2(1):90–96. doi: 10.1016/s0959-437x(05)80328-4. [DOI] [PubMed] [Google Scholar]
- Hsiao K. A fast and simple procedure for sequencing double stranded DNA with sequenase. Nucleic Acids Res. 1991 May 25;19(10):2787–2787. doi: 10.1093/nar/19.10.2787. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hunt S. L., Kaminski A., Jackson R. J. The influence of viral coding sequences on the efficiency of internal initiation of translation of cardiovirus RNAs. Virology. 1993 Dec;197(2):801–807. doi: 10.1006/viro.1993.1661. [DOI] [PubMed] [Google Scholar]
- Jang S. K., Pestova T. V., Hellen C. U., Witherell G. W., Wimmer E. Cap-independent translation of picornavirus RNAs: structure and function of the internal ribosomal entry site. Enzyme. 1990;44(1-4):292–309. doi: 10.1159/000468766. [DOI] [PubMed] [Google Scholar]
- Kaminski A., Belsham G. J., Jackson R. J. Translation of encephalomyocarditis virus RNA: parameters influencing the selection of the internal initiation site. EMBO J. 1994 Apr 1;13(7):1673–1681. doi: 10.1002/j.1460-2075.1994.tb06431.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaminski A., Howell M. T., Jackson R. J. Initiation of encephalomyocarditis virus RNA translation: the authentic initiation site is not selected by a scanning mechanism. EMBO J. 1990 Nov;9(11):3753–3759. doi: 10.1002/j.1460-2075.1990.tb07588.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaminski A., Hunt S. L., Gibbs C. L., Jackson R. J. Internal initiation of mRNA translation in eukaryotes. Genet Eng (N Y) 1994;16:115–155. [PubMed] [Google Scholar]
- Kozak M. Circumstances and mechanisms of inhibition of translation by secondary structure in eucaryotic mRNAs. Mol Cell Biol. 1989 Nov;9(11):5134–5142. doi: 10.1128/mcb.9.11.5134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kozak M. Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol Cell Biol. 1989 Nov;9(11):5073–5080. doi: 10.1128/mcb.9.11.5073. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kozak M. Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8301–8305. doi: 10.1073/pnas.87.21.8301. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. doi: 10.1016/0092-8674(86)90762-2. [DOI] [PubMed] [Google Scholar]
- Kozak M. Regulation of translation in eukaryotic systems. Annu Rev Cell Biol. 1992;8:197–225. doi: 10.1146/annurev.cb.08.110192.001213. [DOI] [PubMed] [Google Scholar]
- Kozak M. The scanning model for translation: an update. J Cell Biol. 1989 Feb;108(2):229–241. doi: 10.1083/jcb.108.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- La Teana A., Pon C. L., Gualerzi C. O. Translation of mRNAs with degenerate initiation triplet AUU displays high initiation factor 2 dependence and is subject to initiation factor 3 repression. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4161–4165. doi: 10.1073/pnas.90.9.4161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lütcke H. A., Chow K. C., Mickel F. S., Moss K. A., Kern H. F., Scheele G. A. Selection of AUG initiation codons differs in plants and animals. EMBO J. 1987 Jan;6(1):43–48. doi: 10.1002/j.1460-2075.1987.tb04716.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Medberry S. L., Lockhart B. E., Olszewski N. E. Properties of Commelina yellow mottle virus's complete DNA sequence, genomic discontinuities and transcript suggest that it is a pararetrovirus. Nucleic Acids Res. 1990 Sep 25;18(18):5505–5513. doi: 10.1093/nar/18.18.5505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mehdi H., Ono E., Gupta K. C. Initiation of translation at CUG, GUG, and ACG codons in mammalian cells. Gene. 1990 Jul 16;91(2):173–178. doi: 10.1016/0378-1119(90)90085-6. [DOI] [PubMed] [Google Scholar]
- Nivinskas R., Vaiskunaite R., Raudonikiene A. An internal AUU codon initiates a smaller peptide encoded by bacteriophage T4 baseplate gene 26. Mol Gen Genet. 1992 Mar;232(2):257–261. doi: 10.1007/BF00280004. [DOI] [PubMed] [Google Scholar]
- Peabody D. S. Translation initiation at non-AUG triplets in mammalian cells. J Biol Chem. 1989 Mar 25;264(9):5031–5035. [PubMed] [Google Scholar]
- Pelletier J., Sonenberg N. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature. 1988 Jul 28;334(6180):320–325. doi: 10.1038/334320a0. [DOI] [PubMed] [Google Scholar]
- Qu R. D., Bhattacharyya M., Laco G. S., De Kochko A., Rao B. L., Kaniewska M. B., Elmer J. S., Rochester D. E., Smith C. E., Beachy R. N. Characterization of the genome of rice tungro bacilliform virus: comparison with Commelina yellow mottle virus and caulimoviruses. Virology. 1991 Nov;185(1):354–364. doi: 10.1016/0042-6822(91)90783-8. [DOI] [PubMed] [Google Scholar]
- Rohde W., Gramstat A., Schmitz J., Tacke E., Prüfer D. Plant viruses as model systems for the study of non-canonical translation mechanisms in higher plants. J Gen Virol. 1994 Sep;75(Pt 9):2141–2149. doi: 10.1099/0022-1317-75-9-2141. [DOI] [PubMed] [Google Scholar]
- Rothnie H. M., Chapdelaine Y., Hohn T. Pararetroviruses and retroviruses: a comparative review of viral structure and gene expression strategies. Adv Virus Res. 1994;44:1–67. doi: 10.1016/s0065-3527(08)60327-9. [DOI] [PubMed] [Google Scholar]
- Sacerdot C., Fayat G., Dessen P., Springer M., Plumbridge J. A., Grunberg-Manago M., Blanquet S. Sequence of a 1.26-kb DNA fragment containing the structural gene for E.coli initiation factor IF3: presence of an AUU initiator codon. EMBO J. 1982;1(3):311–315. doi: 10.1002/j.1460-2075.1982.tb01166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scheper G. C., Voorma H. O., Thomas A. A. Basepairing with 18S ribosomal RNA in internal initiation of translation. FEBS Lett. 1994 Oct 3;352(3):271–275. doi: 10.1016/0014-5793(94)00975-9. [DOI] [PubMed] [Google Scholar]
- Scholthof H. B., Gowda S., Wu F. C., Shepherd R. J. The full-length transcript of a caulimovirus is a polycistronic mRNA whose genes are trans activated by the product of gene VI. J Virol. 1992 May;66(5):3131–3139. doi: 10.1128/jvi.66.5.3131-3139.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scholthof H. B., Wu F. C., Gowda S., Shepherd R. J. Regulation of caulimovirus gene expression and the involvement of cis-acting elements on both viral transcripts. Virology. 1992 Sep;190(1):403–412. doi: 10.1016/0042-6822(92)91226-k. [DOI] [PubMed] [Google Scholar]
- Yin Y., Beachy R. N. The regulatory regions of the rice tungro bacilliform virus promoter and interacting nuclear factors in rice (Oryza sativa L.). Plant J. 1995 Jun;7(6):969–980. doi: 10.1046/j.1365-313x.1995.07060969.x. [DOI] [PubMed] [Google Scholar]
- Zijlstra C., Hohn T. Cauliflower Mosaic Virus Gene VI Controls Translation from Dicistronic Expression Units in Transgenic Arabidopsis Plants. Plant Cell. 1992 Dec;4(12):1471–1484. doi: 10.1105/tpc.4.12.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]