1887

Journal of General Virology header logo

Volume 93, Issue 12

Two distinct sites are essential for virulent infection and support of variant satellite RNA replication in spontaneous beet black scorch virus variants Free

Abstract

Spontaneous point mutations of virus genomes are important in RNA virus evolution and often result in modifications of their biological properties. Spontaneous variants of beet black scorch virus (BBSV) and its satellite (sat) RNA were generated from cDNA clones by serial propagation in and . Inoculation with recombinant RNAs synthesized revealed BBSV variants with divergent infectious phenotypes that affected either symptom expression or replication of satRNA variants. Sequence alignments showed a correlation between the phenotypes and distinct BBSV genomic loci in the 3′UTR or in the domain encoding the viral replicase. Comparative analysis between a virulent variant, BBSV-m294, and the wild-type (wt) BBSV by site-directed mutagenesis indicated that a single-nucleotide substitution of a uridine to a guanine at nt 3477 in the 3′UTR was responsible for significant increases in viral pathogenicity. Gain-of-function analyses demonstrated that the ability of the BBSV variants to support replication of variant satRNAs was mainly determined by aa 516 in the P82 replicase. In this case, an arginine substitution for a glutamine residue was essential for high levels of replication, and alterations of other residues surrounding position 516 in the wtBBSV isolate led to only minor phenotypic effects. These results provide evidence that divergence of virus functions affecting pathogenicity and supporting parasitic replication can be determined by a single genetic site, either a nucleotide or an amino acid. The results suggest that complex interactions occur between virus and associated satRNAs during virus evolution.

  • Received:
  • Accepted:
  • Published Online:
© 2012 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.045641-0
2012-12-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/12/2718.html?itemId=/content/journal/jgv/10.1099/vir.0.045641-0&mimeType=html&fmt=ahah

References

  1. Andriessen M., Meulewaeter F., Cornelissen M. 1995; Expression of tobacco necrosis virus open reading frames 1 and 2 is sufficient for the replication of satellite tobacco necrosis virus. Virology 212:222–224 [View Article][PubMed]
     [Google Scholar]
  2. Aranda M. A., Fraile A., Dopazo J., Malpica J. M., García-Arenal F. 1997; Contribution of mutation and RNA recombination to the evolution of a plant pathogenic RNA. J Mol Evol 44:81–88 [View Article][PubMed]
     [Google Scholar]
  3. Argos P. 1988; A sequence motif in many polymerases. Nucleic Acids Res 16:9909–9916 [View Article][PubMed]
     [Google Scholar]
  4. Barlow J. J., Mathias A. P., Williamson R., Gammack D. B. 1963; A simple method for the quantitative isolation of undegraded high molecular weight ribonucleic acid. Biochem Biophys Res Commun 13:61–66 [View Article][PubMed]
     [Google Scholar]
  5. Bo Y. X., Cai Z. N., Ding Q., Yu J. L., Liu Y. 1996; Characterization of beet black scorch virus RNA, partial cDNA cloning and sequencing of the small component. Chin J Agric Biotechnol 4:269–276
     [Google Scholar]
  6. Cai Z. N., Chen D. H., Wu M. S., Cui X. M., Yu J. L., Liu Y. 1993; Identification of pathogenic virus of beet black scorch disease and detection by synthesized cDNA probes. J Beijing Agric Univ 19:112
     [Google Scholar]
  7. Cao Y. H., Cai Z. N., Ding Q., Li D. W., Han C. G., Yu J. L., Liu Y. 2002; The complete nucleotide sequence of Beet black scorch virus (BBSV), a new member of the genus Necrovirus . Arch Virol 147:2431–2435 [View Article][PubMed]
     [Google Scholar]
  8. Cao Y. H., Yuan X. F., Wang X. X., Guo L. H., Cai Z. N., Han C. G., Li D. W., Yu J. L. 2006; Effect of beet black scorch virus coat protein on viral pathogenicity. Prog Biochem Biophys 33:127–134
     [Google Scholar]
  9. Célix A., Burgyán J., Rodríguez-Cerezo E. 1999; Interactions between tombusviruses and satellite RNAs of tomato bushy stunt virus: a defect in sat RNA B1 replication maps to ORF1 of a helper virus. Virology 262:129–138 [View Article][PubMed]
     [Google Scholar]
  10. Choi K. H., Groarke J. M., Young D. C., Kuhn R. J., Smith J. L., Pevear D. C., Rossmann M. G. 2004; The structure of the RNA-dependent RNA polymerase from bovine viral diarrhea virus establishes the role of GTP in de novo initiation. Proc Natl Acad Sci U S A 101:4425–4430 [View Article][PubMed]
     [Google Scholar]
  11. Choi K. H., Gallei A., Becher P., Rossmann M. G. 2006; The structure of bovine viral diarrhea virus RNA-dependent RNA polymerase and its amino-terminal domain. Structure 14:1107–1113 [View Article][PubMed]
     [Google Scholar]
  12. Coutts R. H., Rigden J. E., Slabas A. R., Lomonossoff G. P., Wise P. J. 1991; The complete nucleotide sequence of tobacco necrosis virus strain D. J Gen Virol 72:1521–1529 [View Article][PubMed]
     [Google Scholar]
  13. de Assis Filho F. M., Paguio O. R., Sherwood J. L., Deom C. M. 2002; Symptom induction by Cowpea chlorotic mottle virus on Vigna unguiculata is determined by amino acid residue 151 in the coat protein. J Gen Virol 83:879–883[PubMed]
     [Google Scholar]
  14. Du Z. Y., Chen F. F., Liao Q. S., Zhang H. R., Chen Y. F., Chen J. S. 2007; 2b ORFs encoded by subgroup IB strains of cucumber mosaic virus induce differential virulence on Nicotiana species. J Gen Virol 88:2596–2604 [View Article][PubMed]
     [Google Scholar]
  15. Fraile A., García-Arenal F. 1991; Secondary structure as a constraint on the evolution of a plant viral satellite RNA. J Mol Biol 221:1065–1069[PubMed] [CrossRef]
     [Google Scholar]
  16. Gal-On A. 2000; A point mutation in the FRNK motif of the potyvirus helper component-protease gene alters symptom expression in cucurbits and elicits protection against the severe homologous virus. Phytopathology 90:467–473 [View Article][PubMed]
     [Google Scholar]
  17. Geier G. E., Modrich P. 1979; Recognition sequence of the dam methylase of Escherichia coli K12 and mode of cleavage of Dpn I endonuclease. J Biol Chem 254:1408–1413[PubMed]
     [Google Scholar]
  18. Gellatly D. L., Mirhadi K., Venkataraman S., AbouHaidar M. G. 2011; Structural and sequence integrity are essential for the replication of the viroid-like satellite RNA of lucerne transient streak virus. J Gen Virol 92:1475–1481 [View Article][PubMed]
     [Google Scholar]
  19. González-Vázquez M., Ayala J., García-Arenal F., Fraile A. 2009; Occurrence of beet black scorch virus infecting sugar beet in Europe. Plant Dis 93:21–24 [View Article]
     [Google Scholar]
  20. Gu H., Ghabrial S. A. 2005; The bean pod mottle virus proteinase cofactor and putative helicase are symptom severity determinants. Virology 333:271–283 [View Article][PubMed]
     [Google Scholar]
  21. Guo L. H., Cao Y. H., Li D. W., Niu S. N., Cai Z. N., Han C. G., Zhai Y. F., Yu J. L. 2005; Analysis of nucleotide sequences and multimeric forms of a novel satellite RNA associated with beet black scorch virus. J Virol 79:3664–3674 [View Article][PubMed]
     [Google Scholar]
  22. Hagiwara K., Ichiki T. U., Ogawa Y., Omura T., Tsuda S. 2002; A single amino acid substitution in 126-kDa protein of Pepper mild mottle virus associates with symptom attenuation in pepper; the complete nucleotide sequence of an attenuated strain, C-1421. Arch Virol 147:833–840 [View Article][PubMed]
     [Google Scholar]
  23. Hirata H., Lu X., Yamaji Y., Kagiwada S., Ugaki M., Namba S. 2003; A single silent substitution in the genome of Apple stem grooving virus causes symptom attenuation. J Gen Virol 84:2579–2583 [View Article][PubMed]
     [Google Scholar]
  24. Hu C. C., Sanger M., Ghabrial S. A. 1998; Production of infectious RNA transcripts from full-length cDNA clones representing two subgroups of peanut stunt virus strains: mapping satellite RNA support to RNA1. J Gen Virol 79:2013–2021[PubMed]
     [Google Scholar]
  25. Huang Y. W., Hu C. C., Lin N. S., Hsu Y. H. 2010; Mimicry of molecular pretenders: the terminal structures of satellites associated with plant RNA viruses. RNA Biol 7:162–171 [View Article][PubMed]
     [Google Scholar]
  26. Koenig R., Valizadeh J. 2008; Molecular and serological characterization of an Iranian isolate of Beet black scorch virus . Arch Virol 153:1397–1400 [View Article][PubMed]
     [Google Scholar]
  27. Lim H. S., Vaira A. M., Reinsel M. D., Bae H., Bailey B. A., Domier L. L., Hammond J. 2010; Pathogenicity of Alternanthera mosaic virus is affected by determinants in RNA-dependent RNA polymerase and by reduced efficacy of silencing suppression in a movement-competent TGB1. J Gen Virol 91:277–287 [View Article][PubMed]
     [Google Scholar]
  28. Mehrvar M., Bragard C. 2008; Distribution and characterization of Iranian Beet black scorch virus . In Proceedings of the Seventh Symposium of the International Working Group on Plant Viruses with Fungal Vectors, Quedlinburg, Germany, 1–4 September 2008 http://www.iwgpvfv.ethz.ch/pdf/2008_Proceedings.pdf
     [Google Scholar]
  29. Meulewaeter F., Seurinck J., Van Emmelo J. 1990; Genome structure of tobacco necrosis virus strain A. Virology 177:699–709 [View Article][PubMed]
     [Google Scholar]
  30. Miller W. A., White K. A. 2006; Long-distance RNA–RNA interactions in plant virus gene expression and replication. Annu Rev Phytopathol 44:447–467 [View Article][PubMed]
     [Google Scholar]
  31. Miller W. A., Wang Z., Treder K. 2007; The amazing diversity of cap-independent translation elements in the 3′-untranslated regions of plant viral RNAs. Biochem Soc Trans 35:1629–1633 [View Article][PubMed]
     [Google Scholar]
  32. Ochman H., Gerber A. S., Hartl D. L. 1988; Genetic applications of an inverse polymerase chain reaction. Genetics 120:621–623[PubMed]
     [Google Scholar]
  33. Ramìrez B. C., Barbier P., Seron K., Haenni A. L., Bernardi F. 1995; Molecular mechanisms of point mutation in RNA viruses. In Molecular Basis of Virus Evolution pp. 105–118 Edited by Gibbs A. J., Calisher C. H., García-Arenal F. Cambridge, UK: Cambridge University Press; [View Article]
     [Google Scholar]
  34. Rasochová L., Passmore B. K., Falk B. W., Miller W. A. 1997; The satellite RNA of barley yellow dwarf virus-RPV is supported by beet western yellows virus in dicotyledonous protoplasts and plants. Virology 231:182–191 [View Article][PubMed]
     [Google Scholar]
  35. Rochon D., Lommel S., Martelli G. P., Rubino L., Russo M. 2011; Genus Necrovirus . In Virus Taxonomy: Ninth report of the International Committee on Taxonomy of Viruses pp. 1129–1131 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. San Diego: Elsevier Academic Press;
     [Google Scholar]
  36. Roossinck M. J. (editor) ( 2008 Plant Virus Evolution Heidelberg: Springer; [View Article]
     [Google Scholar]
  37. Roossinck M. J., Kaplan I., Palukaitis P. 1997; Support of a cucumber mosaic virus satellite RNA maps to a single amino acid proximal to the helicase domain of the helper virus. J Virol 71:608–612[PubMed]
     [Google Scholar]
  38. Routh G., Yassi M. N. A., Rao A. L. N., Mirkov T. E., Dodds J. A. 1997; Replication of wild-type and mutant clones of satellite tobacco mosaic virus in Nicotiana benthamiana protoplasts. J Gen Virol 78:1271–1275[PubMed]
     [Google Scholar]
  39. Shen R., Miller W. A. 2004; The 3′ untranslated region of tobacco necrosis virus RNA contains a barley yellow dwarf virus-like cap-independent translation element. J Virol 78:4655–4664 [View Article][PubMed]
     [Google Scholar]
  40. Shen R., Miller W. A. 2007; Structures required for poly(A) tail-independent translation overlap with, but are distinct from, cap-independent translation and RNA replication signals at the 3′ end of Tobacco necrosis virus RNA. Virology 358:448–458 [View Article][PubMed]
     [Google Scholar]
  41. Suzuki M., Kuwata S., Masuta C., Takanami Y. 1995; Point mutations in the coat protein of cucumber mosaic virus affect symptom expression and virion accumulation in tobacco. J Gen Virol 76:1791–1799 [View Article][PubMed]
     [Google Scholar]
  42. Szittya G., Silhavy D., Molnár A., Havelda Z., Lovas A., Lakatos L., Bánfalvi Z., Burgyán J. 2003; Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:633–640 [View Article][PubMed]
     [Google Scholar]
  43. Sztuba-Solińska J., Urbanowicz A., Figlerowicz M., Bujarski J. J. 2011; RNA–RNA recombination in plant virus replication and evolution. Annu Rev Phytopathol 49:415–443 [View Article][PubMed]
     [Google Scholar]
  44. Terribilini M., Lee J. H., Yan C., Jernigan R. L., Honavar V., Dobbs D. 2006; Prediction of RNA binding sites in proteins from amino acid sequence. RNA 12:1450–1462 [View Article][PubMed]
     [Google Scholar]
  45. Tsai C. H., Dreher T. W. 1993; Increased viral yield and symptom severity result from a single amino acid substitution in the turnip yellow mosaic virus movement protein. Mol Plant Microbe Interact 6:268–273 [View Article][PubMed]
     [Google Scholar]
  46. van der Vossen E. A. G., Neeleman L., Bol J. F. 1996; The 5′ terminal sequence of alfalfa mosaic virus RNA 3 is dispensable for replication and contains a determinant for symptom formation. Virology 221:271–280 [View Article][PubMed]
     [Google Scholar]
  47. Wang Z., Kraft J. J., Hui A. Y., Miller W. A. 2010; Structural plasticity of barley yellow dwarf virus-like cap-independent translation elements in four genera of plant viral RNAs. Virology 402:177–186 [View Article][PubMed]
     [Google Scholar]
  48. Weiland J. J., Larson R. L., Freeman T. P., Edwards M. C. 2006; First report of beet black scorch virus in the United States. Plant Dis 90:828 [View Article]
     [Google Scholar]
  49. Weiland J. J., Van Winkle D., Edwards M. C., Larson R. L., Shelver W. L., Freeman T. P., Liu H. Y. 2007; Characterization of a U.S. isolate of Beet black scorch virus . Phytopathology 97:1245–1254 [View Article][PubMed]
     [Google Scholar]
  50. Xi D. H., Cao Y. H., Guo L. H., Yuan X. F., Cai Z. N., Han C. G., Li D. W., Yu J. L. 2006; Sequence analysis and construction of infectious cDNA clone of beet black scorch virus Xinjiang isolate. Chin J Virol 22:309–313
     [Google Scholar]
  51. Xi D. H., Li J., Cao C., Han C. G., Li D. W., Yu J. L., Zhou X. P. 2007; Characterization of tobacco necrosis virus A, an isolate infecting soybean (Glycine max). Acta Phytopathol Sin 37:595–603
     [Google Scholar]
  52. Yamaguchi N., Seshimo Y., Yoshimoto E., Ahn H. I., Ryu K. H., Choi J. K., Masuta C. 2005; Genetic mapping of the compatibility between a lily isolate of Cucumber mosaic virus and a satellite RNA. J Gen Virol 86:2359–2369 [View Article][PubMed]
     [Google Scholar]
  53. Yambao M. L., Yagihashi H., Sekiguchi H., Sekiguchi T., Sasaki T., Sato M., Atsumi G., Tacahashi Y., Nakahara K. S., Uyeda I. 2008; Point mutations in helper component protease of clover yellow vein virus are associated with the attenuation of RNA-silencing suppression activity and symptom expression in broad bean. Arch Virol 153:105–115 [View Article][PubMed]
     [Google Scholar]
  54. Yuan X. F., Cao Y. H., Xi D. H., Guo L. H., Han C. G., Li D. W., Zhai Y. F., Yu J. L. 2006; Analysis of the subgenomic RNAs and the small open reading frames of Beet black scorch virus . J Gen Virol 87:3077–3086 [View Article][PubMed]
     [Google Scholar]
  55. Zhang Y. L., Li J., Pu H., Jin J., Zhang X. F., Chen M. K., Wang B., Han C. G., Yu J. L., Li D. 2010; Development of Tobacco necrosis virus A as a vector for efficient and stable expression of FMDV VP1 peptides. Plant Biotechnol J 8:506–523 [View Article][PubMed]
     [Google Scholar]
  56. Zhang Y. J., Zhang X. F., Niu S. F., Han C. G., Yu J. L., Li D. W. 2011; Nuclear localization of Beet black scorch virus capsid protein and its interaction with importin α. Virus Res 155:307–315 [View Article][PubMed]
     [Google Scholar]
  57. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.045641-0
Loading
Two distinct sites are essential for virulent infection and support of variant satellite RNA replication in spontaneous beet black scorch virus variants
J. Gen. Virol. 93, 2718 (2012); https://doi.org/10.1099/vir.0.045641-0
/content/journal/jgv/10.1099/vir.0.045641-0
/content/journal/jgv/10.1099/vir.0.045641-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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