1887

Abstract

Triple gene block (TGB), a conserved gene module found in the genomes of many filamentous and rod-shaped plant viruses, encodes three proteins, TGB1, TGB2 and TGB3, required for viral cell-to-cell movement through plasmodesmata and systemic transport via the phloem. The genome of , the type species of the genus , includes TGB1 and TGB2 genes, but contains no canonical ORF for TGB3 protein. However, a TGB3-like protein-encoding sequence lacking an AUG initiator codon has been found in the shallot virus X (ShVX) genome in a position typical for TGB3 genes. This putative TGB3 gene is conserved in all allexiviruses. Here, we carried out sequence analysis to predict possible non-AUG initiator codons in the ShVX TGB3-encoding sequence. We further used an agroinfiltration assay in to confirm this prediction. Site-directed mutagenesis was used to demonstrate that the ShVX TGB3 could be translated on a bicistronic mRNA template via a leaky scanning mechanism.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000248
2015-10-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/10/3159.html?itemId=/content/journal/jgv/10.1099/jgv.0.000248&mimeType=html&fmt=ahah

References

  1. Arkhipov A.V. , Gushchin V.A. , Vishnichenko V.K. , Solovyev A.G. . ( 2013;). Accumulation of changes in the genome of shallot virus X persisting in vegetatively reproduced plants. Dokl Biochem Biophys 452: 237–240 [CrossRef] [PubMed].
    [Google Scholar]
  2. Castaño A. , Ruiz L. , Hernández C. . ( 2009;). Insights into the translational regulation of biologically active open reading frames of Pelargonium line pattern virus. Virology 386: 417–426 [CrossRef] [PubMed].
    [Google Scholar]
  3. Chen J. , Chen J. , Adams M.J. . ( 2001;). Molecular characterisation of a complex mixture of viruses in garlic with mosaic symptoms in China. Arch Virol 146: 1841–1853 [CrossRef] [PubMed].
    [Google Scholar]
  4. Dreher T.W. , Miller W.A. . ( 2006;). Translational control in positive strand RNA plant viruses. Virology 344: 185–197 [CrossRef] [PubMed].
    [Google Scholar]
  5. Firth A.E. , Brierley I. . ( 2012;). Non-canonical translation in RNA viruses. J Gen Virol 93: 1385–1409 [CrossRef] [PubMed].
    [Google Scholar]
  6. Gordon K. , Fütterer J. , Hohn T. . ( 1992;). Efficient initiation of translation at non-AUG triplets in plant cells. Plant J 2: 809–813 [PubMed].
    [Google Scholar]
  7. Jackson A.O. , Lim H.-S. , Bragg J. , Ganesan U. , Lee M.Y. . ( 2009;). Hordeivirus replication, movement, and pathogenesis. Annu Rev Phytopathol 47: 385–422 [CrossRef] [PubMed].
    [Google Scholar]
  8. Kanyuka K.V. , Vishnichenko V.K. , Levay K.E. , Kondrikov D.Y. , Ryabov E.V. , Zavriev S.K. . ( 1992;). Nucleotide sequence of shallot virus X RNA reveals a 5′-proximal cistron closely related to those of potexviruses and a unique arrangement of the 3′-proximal cistrons. J Gen Virol 73: 2553–2560 [CrossRef] [PubMed].
    [Google Scholar]
  9. Katis N.I. , Maliogka V.I. , Dovas C.I. . ( 2012;). Viruses of the genus Allium in the Mediterranean region. Adv Virus Res 84: 163–208 [CrossRef] [PubMed].
    [Google Scholar]
  10. Kozak M. . ( 1983;). Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev 47: 1–45 [PubMed].
    [Google Scholar]
  11. Kozak M. . ( 1989;). Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol Cell Biol 9: 5073–5080 [PubMed].[CrossRef]
    [Google Scholar]
  12. Kozak M. . ( 2002;). Pushing the limits of the scanning mechanism for initiation of translation. Gene 299: 1–34 [CrossRef] [PubMed].
    [Google Scholar]
  13. Lauber E. , Jonard G. , Richards K. , Guilley H. . ( 2005;). Nonregulated expression of TGBp3 of hordei-like viruses but not of potex-like viruses inhibits beet necrotic yellow vein virus cell-to-cell movement. Arch Virol 150: 1459–1467 [CrossRef] [PubMed].
    [Google Scholar]
  14. Lim H.-S. , Bragg J.N. , Ganesan U. , Ruzin S. , Schichnes D. , Lee M.Y. , Vaira A.M. , Ryu K.H. , Hammond J. , Jackson A.O. . ( 2009;). Subcellular localization of the barley stripe mosaic virus triple gene block proteins. J Virol 83: 9432–9448 [CrossRef] [PubMed].
    [Google Scholar]
  15. Ling R. , Pate A.E. , Carr J.P. , Firth A.E. . ( 2013;). An essential fifth coding ORF in the sobemoviruses. Virology 446: 397–408 [CrossRef] [PubMed].
    [Google Scholar]
  16. Lukhovitskaya N.I. , Solovieva A.D. , Boddeti S.K. , Thaduri S. , Solovyev A.G. , Savenkov E.I. . ( 2013;). An RNA virus-encoded zinc-finger protein acts as a plant transcription factor and induces a regulator of cell size and proliferation in two tobacco species. Plant Cell 25: 960–973 [CrossRef] [PubMed].
    [Google Scholar]
  17. Lukhovitskaya N.I. , Vetukuri R.R. , Sama I. , Thaduri S. , Solovyev A.G. , Savenkov E.I. . ( 2014;). A viral transcription factor exhibits antiviral RNA silencing suppression activity independent of its nuclear localization. J Gen Virol 95: 2831–2837 [CrossRef] [PubMed].
    [Google Scholar]
  18. Memelink J. , van der Vlugt C.I.M. , Linthorst H.J.M. , Derks A.F.L.M. , Asjes C.J. , Bol J.F. . ( 1990;). Homologies between the genomes of a carlavirus (lily symptomless virus) and a potexvirus (lily virus X) from lily plants. J Gen Virol 71: 917–924 [CrossRef] [PubMed].
    [Google Scholar]
  19. Morozov S.Y. , Solovyev A.G. . ( 2003;). Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84: 1351–1366 [CrossRef] [PubMed].
    [Google Scholar]
  20. Morozov S.Y. , Solovyev A.G. . ( 2012;). Did silencing suppression counter-defensive strategy contribute to origin and evolution of the triple gene block coding for plant virus movement proteins?. Front Plant Sci 3: 136 [CrossRef] [PubMed].
    [Google Scholar]
  21. Morozov S.Y. , Solovyev A.G. . ( 2015;). Phylogenetic relationship of some ‘accessory’ helicases of plant positive-stranded RNA viruses: toward understanding the evolution of triple gene block. Front Microbiol 6: 1–8 [CrossRef] [PubMed].
    [Google Scholar]
  22. Morozov S.Y. , Miroshnichenko N.A. , Solovyev A.G. , Fedorkin O.N. , Zelenina D.A. , Lukasheva L.I. , Karasev A.V. , Dolja V.V. , Atabekov J.G. . ( 1991;). Expression strategy of the potato virus X triple gene block. J Gen Virol 72: 2039–2042 [CrossRef] [PubMed].
    [Google Scholar]
  23. Schepetilnikov M.V. , Manske U. , Solovyev A.G. , Zamyatnin A.A Jr , Schiemann J. , Morozov S.Y. . ( 2005;). The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J Gen Virol 86: 2379–2391 [CrossRef] [PubMed].
    [Google Scholar]
  24. Shemyakina E.A. , Erokhina T.N. , Gorshkova E.N. , Schiemann J. , Solovyev A.G. , Morozov S.Y. . ( 2011;). Formation of protein complexes containing plant virus movement protein TGBp3 is necessary for its intracellular trafficking. Biochimie 93: 742–748 [CrossRef] [PubMed].
    [Google Scholar]
  25. Smirnova E. , Firth A.E. , Miller W.A. , Scheidecker D. , Brault V. , Reinbold C. , Rakotondrafara A.M. , Chung B.Y.-W. , Ziegler-Graff V. . ( 2015;). Discovery of a small non-AUG-initiated ORF in Poleroviruses and Luteoviruses that is required for long-distance movement. PLoS Pathog 11: e1004868 [CrossRef] [PubMed].
    [Google Scholar]
  26. Solovyev A.G. , Schiemann J. , Morozov S.Y. . ( 2012;). Microscopic analysis of severe structural rearrangements of the plant endoplasmic reticulum and Golgi caused by overexpression of Poa semilatent virus movement protein. ScientificWorldJournal 2012: 416076 [CrossRef] [PubMed].
    [Google Scholar]
  27. Solovyev A.G. , Minina E.A. , Makarova S.S. , Erokhina T.N. , Makarov V.V. , Kaplan I.B. , Kopertekh L. , Schiemann J. , Richert-Pöggeler K.R. , Morozov S.Y. . ( 2013;). Subcellular localization and self-interaction of plant-specific Nt-4/1 protein. Biochimie 95: 1360–1370 [CrossRef] [PubMed].
    [Google Scholar]
  28. Song S.I. , Song J.T. , Kim C.H. , Lee J.S. , Choi Y.D. . ( 1998;). Molecular characterization of the garlic virus X genome. J Gen Virol 79: 155–159 [PubMed].[CrossRef]
    [Google Scholar]
  29. Sumi S. , Tsuneyoshi T. , Furutani H. . ( 1993;). Novel rod-shaped viruses isolated from garlic, Allium sativum, possessing a unique genome organization. J Gen Virol 74: 1879–1885 [CrossRef] [PubMed].
    [Google Scholar]
  30. Sumi S. , Matsumi T. , Tsuneyoshi T. . ( 1999;). Complete nucleotide sequences of garlic viruses A and C, members of the newly ratified genus Allexivirus. Arch Virol 144: 1819–1826 [CrossRef] [PubMed].
    [Google Scholar]
  31. Tamai A. , Meshi T. . ( 2001;). Cell-to-cell movement of Potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block. Mol Plant Microbe Interact 14: 1158–1167 [CrossRef] [PubMed].
    [Google Scholar]
  32. Turina M. , Maruoka M. , Monis J. , Jackson A.O. , Scholthof K.B. . ( 1998;). Nucleotide sequence and infectivity of a full-length cDNA clone of panicum mosaic virus. Virology 241: 141–155 [CrossRef] [PubMed].
    [Google Scholar]
  33. Verchot-Lubicz J. , Torrance L. , Solovyev A.G. , Morozov S.Y. , Jackson A.O. , Gilmer D. . ( 2010;). Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 23: 1231–1247 [CrossRef] [PubMed].
    [Google Scholar]
  34. Vishnichenko V.K. , Konareva T.N. , Zavriev S.K. . ( 1993;). A new filamentous virus in shallot. Plant Pathol 42: 121–126 [CrossRef].
    [Google Scholar]
  35. Zavriev S.K. , Vishnichenko V.K. . ( 2000;). Allexiviruses. . In Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses, pp. 981–984. Edited by van Regenmortel M. H. V. , Fauquet C. M. , Bishop D. H. L. , Carsten E. B. , Estes M. K. , Lemon S. M. , Maniloff J. , Mayo M. A. , McGeoch D. J. , other editors . San Diego, CA: Academic Press;.
    [Google Scholar]
  36. Zhou H. , Jackson A.O. . ( 1996;). Expression of the barley stripe mosaic virus RNA beta triple gene block. Virology 216: 367–379 [CrossRef] [PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000248
Loading
/content/journal/jgv/10.1099/jgv.0.000248
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error