1887

Abstract

A novel circular DNA virus sequence has been identified through next-generation sequencing and assembly of small RNAs of 21–24 nt from an apple tree grown in China. The virus genome was cloned using two independent approaches and sequenced. With a size of 2932 nt, it showed the same genomic structure and conserved origin of replication reported for members of the family . However, the low nucleotide and amino acid sequence identity with known geminiviruses indicated that it was a novel virus, for which the provisional name apple geminivirus (AGV) is proposed. Rolling circle amplification followed by RFLP analyses indicated that AGV was a virus with a monopartite DNA genome. This result was in line with bioassays showing that the cloned viral genome was infectious in several herbaceous plants (, and ), thus confirming it was complete and biologically active, although no symptoms were observed in these experimental hosts. AGV genome structure and phylogenetic analyses did not support the inclusion of this novel species in any of the established genera in the family . A survey of 165 apple trees grown in four Chinese provinces showed a prevalence of 7.2 % for AGV, confirming its presence in several cultivars and geographical areas in China, although no obvious relationship between virus infection and specific symptoms was found.

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2015-08-01
2024-04-20
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References

  1. Al Rwahnih M., Dave A., Anderson M.M., Rowhani A., Uyemoto J.K., Sudarshana M.R. 2013; Association of a DNA virus with grapevines affected by red blotch disease in California. Phytopathology 103:1069–1076 doi:10.1094/PHYTO-10-12-0253-R [PubMed] [CrossRef]
    [Google Scholar]
  2. Aliyari R., Wu Q., Li H.W., Wang X.H., Li F., Green L.D., Han C.S., Li W.X., Ding S.W. 2008; Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila . Cell Host Microbe 4:387–397 doi:10.1016/j.chom.2008.09.001 [PubMed] [CrossRef]
    [Google Scholar]
  3. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 doi:10.1016/S0022-2836(05)80360-2 [PubMed] [CrossRef]
    [Google Scholar]
  4. Aregger M., Borah B.K., Seguin J., Rajeswaran R., Gubaeva E.G., Zvereva A.S., Windels D., Vazquez F., Blevins T., other authors. 2012; Primary and secondary siRNAs in geminivirus-induced gene silencing. PLoS Pathog 8:e1002941 doi:10.1371/journal.ppat.1002941 [PubMed] [CrossRef]
    [Google Scholar]
  5. Argüello-Astorga G.R., Ruiz-Medrano R. 2001; An iteron-related domain is associated to Motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach. Arch Virol 146:1465–1485 doi:10.1007/s007050170072 [PubMed] [CrossRef]
    [Google Scholar]
  6. Bernardo P., Golden M., Akram M., Naimuddin, Nadarajan N., Fernandez E., Granier M., Rebelo A.G., Peterschmitt M., other authors. 2013; Identification and characterisation of a highly divergent geminivirus: evolutionary and taxonomic implications. Virus Res 177:35–45 doi:10.1016/j.virusres.2013.07.006 [PubMed] [CrossRef]
    [Google Scholar]
  7. Briddon R.W., Pinner M.S., Stanley J., Markham P.G. 1990; Geminivirus coat protein gene replacement alters insect specificity. Virology 177:85–94 doi:10.1016/0042-6822(90)90462-Z [PubMed] [CrossRef]
    [Google Scholar]
  8. Briddon R.W., Bull S.E., Mansoor S., Amin I., Markham P.G. 2002; Universal primers for the PCR-mediated amplification of DNA beta: a molecule associated with some monopartite begomoviruses. Mol Biotechnol 20:315–318 doi:10.1385/MB:20:3:315 [PubMed] [CrossRef]
    [Google Scholar]
  9. Brown J., Fauquet C., Briddon R., Zerbini M., Moriones E., Navas-Castillo J. 2012; Geminiviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses pp. 351–373 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. London: Academic Press;
    [Google Scholar]
  10. CABI 2012 Distribution maps of plant diseases, 2012, October, Map 1127 (edition 1) www.cabi.org/dmpd
  11. Carbonell A., Fahlgren N., Garcia-Ruiz H., Gilbert K.B., Montgomery T.A., Nguyen T., Cuperus J.T., Carrington J.C. 2012; Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 24:3613–3629 doi:10.1105/tpc.112.099945 [PubMed] [CrossRef]
    [Google Scholar]
  12. Coetzee B., Freeborough M.J., Maree H.J., Celton J.M., Rees D.J., Burger J.T. 2010; Deep sequencing analysis of viruses infecting grapevines: virome of a vineyard. Virology 400:157–163 doi:10.1016/j.virol.2010.01.023 [PubMed] [CrossRef]
    [Google Scholar]
  13. de Andrade R.R., Vaslin M.F. 2014; SearchSmallRNA: a graphical interface tool for the assemblage of viral genomes using small RNA libraries data. Virol J 11:45 doi:10.1186/1743-422X-11-45 [PubMed] [CrossRef]
    [Google Scholar]
  14. Faruk M.I., Eusebio-Cope A., Suzuki N. 2008; A host factor involved in hypovirus symptom expression in the chestnut blight fungus, Cryphonectria parasitica . J Virol 82:740–754 doi:10.1128/JVI.02015-07 [PubMed] [CrossRef]
    [Google Scholar]
  15. Fauquet C.M., Briddon R.W., Brown J.K., Moriones E., Stanley J., Zerbini M., Zhou X. 2008; Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821 doi:10.1007/s00705-008-0037-6 [PubMed] [CrossRef]
    [Google Scholar]
  16. Finn R.D., Miller B.L., Clements J., Bateman A. 2014; iPfam: a database of protein family and domain interactions found in the Protein Data Bank. Nucleic Acids Res 42:(D1)D364–D373 doi:10.1093/nar/gkt1210 [PubMed] [CrossRef]
    [Google Scholar]
  17. Haible D., Kober S., Jeske H. 2006; Rolling circle amplification revolutionizes diagnosis and genomics of geminiviruses. J Virol Methods 135:9–16 doi:10.1016/j.jviromet.2006.01.017 [PubMed] [CrossRef]
    [Google Scholar]
  18. Hanley-Bowdoin L., Settlage S., Orozco B., Nagar S., Robertson D. 1999; Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Plant Sci 18:71–106 doi:10.1080/07352689991309162 [CrossRef]
    [Google Scholar]
  19. Hashimoto J., Koganezawa H. 1987; Nucleotide sequence and secondary structure of apple scar skin viroid. Nucleic Acids Res 15:7045–7052 doi:10.1093/nar/15.17.7045 [PubMed] [CrossRef]
    [Google Scholar]
  20. Ho T., Wang H., Pallett D., Dalmay T. 2007; Evidence for targeting common siRNA hotspots and GC preference by plant Dicer-like proteins. FEBS Lett 581:3267–3272 doi:10.1016/j.febslet.2007.06.022 [PubMed] [CrossRef]
    [Google Scholar]
  21. Ho T., Wang L., Huang L., Li Z., Pallett D.W., Dalmay T., Ohshima K., Walsh J.A., Wang H. 2010; Nucleotide bias of DCL and AGO in plant anti-virus gene silencing. Protein Cell 1:847–858 doi:10.1007/s13238-010-0100-4 [PubMed] [CrossRef]
    [Google Scholar]
  22. Inoue-Nagata A.K., Albuquerque L.C., Rocha W.B., Nagata T. 2004; A simple method for cloning the complete begomovirus genome using the bacteriophage phi29 DNA polymerase. J Virol Methods 116:209–211 doi:10.1016/j.jviromet.2003.11.015 [PubMed] [CrossRef]
    [Google Scholar]
  23. Ji Z., Zhao X., Duan H., Hu T., Wang S., Wang Y., Cao K. 2013; Multiplex RT-PCR detection and distribution of four apple viruses in China. Acta Virol 57:435–441 doi:10.4149/av_2013_04_435 [PubMed] [CrossRef]
    [Google Scholar]
  24. Krenz B., Thompson J.R., Fuchs M., Perry K.L. 2012; Complete genome sequence of a new circular DNA virus from grapevine. J Virol 86:7715 doi:10.1128/JVI.00943-12 [PubMed] [CrossRef]
    [Google Scholar]
  25. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., other authors. 2007; Clustal W Clustal X version 2.0. Bioinformatics 23:2947–2948 doi:10.1093/bioinformatics/btm404 [PubMed] [CrossRef]
    [Google Scholar]
  26. Loconsole G., Saldarelli P., Doddapaneni H., Savino V., Martelli G.P., Saponari M. 2012; Identification of a single-stranded DNA virus associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae . Virology 432:162–172 doi:10.1016/j.virol.2012.06.005 [PubMed] [CrossRef]
    [Google Scholar]
  27. Mallory A., Vaucheret H. 2010; Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22:3879–3889 doi:10.1105/tpc.110.080671 [PubMed] [CrossRef]
    [Google Scholar]
  28. Mason G., Caciagli P., Accotto G.P., Noris E. 2008; Real-time PCR for the quantitation of Tomato yellow leaf curl Sardinia virus in tomato plants and in Bemisia tabaci . J Virol Methods 147:282–289 doi:10.1016/j.jviromet.2007.09.015 [PubMed] [CrossRef]
    [Google Scholar]
  29. Minoia S., Carbonell A., Di Serio F., Gisel A., Carrington J.C., Navarro B., Flores R. 2014; Specific argonautes selectively bind small RNAs derived from potato spindle tuber viroid and attenuate viroid accumulation in vivo . J Virol 88:11933–11945 doi:10.1128/JVI.01404-14 [PubMed] [CrossRef]
    [Google Scholar]
  30. Miozzi L., Pantaleo V., Burgyán J., Accotto G.P., Noris E. 2013; Analysis of small RNAs derived from tomato yellow leaf curl Sardinia virus reveals a cross reaction between the major viral hotspot and the plant host genome. Virus Res 178:287–296 doi:10.1016/j.virusres.2013.09.029 [PubMed] [CrossRef]
    [Google Scholar]
  31. Moffat A. 1999; Geminiviruses emerge as serious crop threat. Science 286:1835 doi:10.1126/science.286.5446.1835 [CrossRef]
    [Google Scholar]
  32. Murray M.G., Thompson W.F. 1980; Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326 doi:10.1093/nar/8.19.4321 [PubMed] [CrossRef]
    [Google Scholar]
  33. Nash T.E., Dallas M.B., Reyes M.I., Buhrman G.K., Ascencio-Ibañez J.T., Hanley-Bowdoin L. 2011; Functional analysis of a novel motif conserved across geminivirus Rep proteins. J Virol 85:1182–1192 doi:10.1128/JVI.02143-10 [PubMed] [CrossRef]
    [Google Scholar]
  34. Navarro B., Gisel A., Rodio M.E., Delgado S., Flores R., Di Serio F. 2012; Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host mRNA as predicted by RNA silencing. Plant J 70:991–1003 doi:10.1111/j.1365-313X.2012.04940.x [PubMed] [CrossRef]
    [Google Scholar]
  35. Padidam M., Beachy R.N., Fauquet C.M. 1995; Classification and identification of geminiviruses using sequence comparisons. J Gen Virol 76:249–263 doi:10.1099/0022-1317-76-2-249 [PubMed] [CrossRef]
    [Google Scholar]
  36. Polston J.E., Londoño M.A., Capobianco H. 2014; The complete genome sequence of New World jatropha mosaic virus. Arch Virol 159:3131–3136 doi:10.1007/s00705-014-2132-1 [PubMed] [CrossRef]
    [Google Scholar]
  37. Poojari S., Alabi O.J., Fofanov V.Y., Naidu R.A. 2013; A leafhopper-transmissible DNA virus with novel evolutionary lineage in the family Geminiviridae implicated in grapevine redleaf disease by next-generation sequencing. PLoS One 8:e64194 doi:10.1371/journal.pone.0064194 [PubMed] [CrossRef]
    [Google Scholar]
  38. Rojas M., Gilbertson R., Russel D., Maxwell D. 1993; Use of degenarate primers in polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Dis 77:340–347 doi:10.1094/PD-77-0340 [CrossRef]
    [Google Scholar]
  39. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  40. Seguin J., Rajeswaran R., Malpica-López N., Martin R.R., Kasschau K., Dolja V.V., Otten P., Farinelli L., Pooggin M.M. 2014; De novo reconstruction of consensus master genomes of plant RNA and DNA viruses from siRNAs. PLoS One 9:e88513 doi:10.1371/journal.pone.0088513 [PubMed] [CrossRef]
    [Google Scholar]
  41. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 doi:10.1093/molbev/mst197 [PubMed] [CrossRef]
    [Google Scholar]
  42. Varma A., Malathi V.G. 2003; Emerging geminivirus problems: a serious threat to crop production. Ann Appl Biol 142:145–164 [CrossRef]
    [Google Scholar]
  43. Varsani A., Navas-Castillo J., Moriones E., Hernández-Zepeda C., Idris A., Brown J.K., Murilo Zerbini F., Martin D.P. 2014; Establishment of three new genera in the family Geminiviridae: Becurtovirus Eragrovirus Turncurtovirus . Arch Virol 159:2193–2203 doi:10.1007/s00705-014-2050-2 [PubMed] [CrossRef]
    [Google Scholar]
  44. Wu Q., Wang Y., Cao M., Pantaleo V., Burgyan J., Li W.X., Ding S.W. 2012; Homology-independent discovery of replicating pathogenic circular RNAs by deep sequencing and a new computational algorithm. Proc Natl Acad Sci U S A 109:3938–3943 doi:10.1073/pnas.1117815109 [PubMed] [CrossRef]
    [Google Scholar]
  45. Yang X., Wang Y., Guo W., Xie Y., Xie Q., Fan L., Zhou X. 2011; Characterization of small interfering RNAs derived from the geminivirus/betasatellite complex using deep sequencing. PLoS One 6:e16928 doi:10.1371/journal.pone.0016928 [PubMed] [CrossRef]
    [Google Scholar]
  46. Zerbino D.R., Birney E. 2008; Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829 doi:10.1101/gr.074492.107 [PubMed] [CrossRef]
    [Google Scholar]
  47. Zhang Z., Qi S., Tang N., Zhang X., Chen S., Zhu P., Ma L., Cheng J., Xu Y., other authors. 2014; Discovery of replicating circular RNAs by RNA-seq and computational algorithms. PLoS Pathog 10:e1004553 doi:10.1371/journal.ppat.1004553 [PubMed] [CrossRef]
    [Google Scholar]
  48. Zhou X., Liu Y., Robinson D.J., Harrison B.D. 1998; Four DNA-A variants among Pakistani isolates of cotton leaf curl virus and their affinities to DNA-A of geminivirus isolates from okra. J Gen Virol 79:915–923[PubMed] [CrossRef]
    [Google Scholar]
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