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Melandrium yellow fleck bromovirus infects Arabidopsis thaliana and has genomic RNA sequence characteristics that are unique among bromoviruses

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Abstract

Melandrium yellow fleck bromovirus (MYFV) systemically infected Arabidopsis thaliana, although the susceptibility of several A. thaliana accessions to MYFV differed from their susceptibility to the other two bromoviruses infecting A. thaliana. We constructed full-length cDNA clones of MYFV genomic RNAs 1, 2, and 3 and determined their complete nucleotide sequences. Similar to Broad bean mottle bromovirus, (1) the 5′-terminal nucleotide of the MYFV genomic RNAs was adenine, and (2) the “D-arm” was absent from the tRNA-like structure in the 3′ untranslated regions (UTRs) of MYFV RNAs. As unique characteristics, MYFV RNA3 lacked the poly(A) tract in the intercistronic region and contained a directly repeated sequence of about 200 nucleotides and polypyrimidine tracts of heterogeneous lengths in the 5′ UTR. Co-infection experiments using RNA3 clones with or without the duplicated sequence demonstrated that the duplication contributed to the competitive fitness of the virus in Nicotiana benthamiana.

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References

  1. Ahlquist P, Dasgupta R, Kaesberg P (1981) Near identity of 3′ RNA secondary structure in bromoviruses and cucumber mosaic virus. Cell 23:183–189

    Article  PubMed  CAS  Google Scholar 

  2. Ahlquist P, Luckow V, Kaesberg P (1981) Complete nucleotide sequence of brome mosaic virus RNA3. J Mol Biol 153:23–38

    Article  PubMed  CAS  Google Scholar 

  3. Ahlquist P, Dasgupta R, Kaesberg P (1984) Nucleotide sequence of the brome mosaic virus genome and its implications for viral replication. J Mol Biol 172:369–383

    Article  PubMed  CAS  Google Scholar 

  4. Ahlquist P, French R, Janda M, Loesch-Fries LS (1984) Multicomponent RNA plant virus infection derived from cloned viral cDNA. Proc Natl Acad Sci USA 81:7066–7070

    Article  PubMed  CAS  Google Scholar 

  5. Ahola T, den Boon JA, Ahlquist P (2000) Helicase and capping enzyme active site mutations in brome mosaic virus protein 1a cause defects in template recruitment, negative-strand RNA synthesis, and viral RNA capping. J Virol 74:8803–8811

    Article  PubMed  CAS  Google Scholar 

  6. Allison RF, Janda M, Ahlquist P (1988) Infectious in vitro transcripts from cowpea chlorotic mottle virus cDNA clones and exchange of individual RNA components with brome mosaic virus. J Virol 62:3581–3588

    PubMed  CAS  Google Scholar 

  7. Allison RF, Janda M, Ahlquist P (1989) Sequence of cowpea chlorotic mottle virus RNAs 2 and 3 and evidence of a recombination event during bromovirus evolution. Virology 172:321–330

    Article  PubMed  CAS  Google Scholar 

  8. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805

    Article  PubMed  CAS  Google Scholar 

  9. Damayanti TA, Nagano H, Mise K, Furusawa I, Okuno T (1999) Brome mosaic virus defective RNAs generated during infection of barley plants. J Gen Virol 80:2511–2518

    PubMed  CAS  Google Scholar 

  10. Duggal R, Lahser FC, Hall TC (1994) cis-Acting sequences in the replication of plant viruses with plus-sense RNA genomes. Annu Rev Phytopathol 32:287–309

    Article  CAS  Google Scholar 

  11. Dzianott AM, Bujarski JJ (1991) The nucleotide sequence and genome organization of the RNA-1 segment in two bromoviruses: broad bean mottle virus and cowpea chlorotic mottle virus. Virology 185:553–562

    Article  PubMed  CAS  Google Scholar 

  12. French R, Ahlquist P (1987) Intercistronic as well as terminal sequences are required for efficient amplification of brome mosaic virus RNA3. J Virol 61:1457–1465

    PubMed  CAS  Google Scholar 

  13. French R, Ahlquist P (1988) Characterization and engineering of sequences controlling in vivo synthesis of brome mosaic virus subgenomic RNA. J Virol 62:2411–2420

    PubMed  CAS  Google Scholar 

  14. Frohman MA (1990) RACE: Rapid amplification of cDNA ends In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. Academic Press, San Diego, pp 28–38

  15. Fujisaki K, Hagihara F, Kaido M, Mise K, Okuno T (2003) Complete nucleotide sequence of spring beauty latent virus, a bromovirus infectious to Arabidopsis thaliana. Arch Virol 148:165–175

    Article  PubMed  CAS  Google Scholar 

  16. Fujisaki K, Hagihara F, Kaido M, Mise K, Okuno T (2004) Identification and characterization of the SSB1 locus involved in symptom development by Spring beauty latent virus infection in Arabidopsis thaliana. Mol Plant Microbe Interact 17:967–975

    Article  PubMed  CAS  Google Scholar 

  17. Fujisaki K, Iwahashi F, Kaido M, Okuno T, Mise K (2009) Genetic analysis of a host determination mechanism of bromoviruses in Arabidopsis thaliana. Virus Res 140:103–111

    Article  PubMed  CAS  Google Scholar 

  18. Gubler U, Hoffman BJ (1983) A simple and very efficient method for generating cDNA libraries. Gene 25:263–269

    Article  PubMed  CAS  Google Scholar 

  19. Hollings M, Horváth J (1981) Melandrium yellow fleck virus. In: CMI/AAB Descriptions of Plant Viruses. Holywell Press, Oxford, No. 236

  20. Iwahashi F, Fujisaki K, Kaido M, Okuno T, Mise K (2005) Synthesis of infectious in vitro transcripts from Cassia yellow blotch bromovirus cDNA clones and a reassortment analysis with other bromoviruses in protoplasts. Arch Virol 150:1301–1314

    Article  PubMed  CAS  Google Scholar 

  21. Iwamoto T, Mise K, Mori K, Arimoto M, Nakai T, Okuno T (2001) Establishment of an infectious RNA transcription system for Striped jack nervous necrosis virus, the type species of the betanodaviruses. J Gen Virol 82:2653–2662

    PubMed  CAS  Google Scholar 

  22. Janda M, French R, Ahlquist P (1987) High efficiency T7 polymerase synthesis of infectious RNA from cloned brome mosaic virus cDNA and effects of 5′ extensions on transcript infectivity. Virology 158:259–262

    Article  PubMed  CAS  Google Scholar 

  23. Jayasena KW, Randles JW (2004) A short insert in the leader sequence of RNA 3L, a long variant of Alfalfa mosaic virus RNA3, introduces two unidentified reading frames. Virus Genes 29:311–316

    Article  PubMed  CAS  Google Scholar 

  24. Kroner P, Richards D, Traynor P, Ahlquist P (1989) Defined mutations in a small region of the brome mosaic virus 2 gene cause diverse temperature-sensitive RNA replication phenotypes. J Virol 63:5302–5309

    PubMed  CAS  Google Scholar 

  25. Kroner PA, Young BM, Ahlquist P (1990) Analysis of the role of brome mosaic virus 1a protein domains in RNA replication, using linker insertion mutagenesis. J Virol 64:6110–6120

    PubMed  CAS  Google Scholar 

  26. Kroner P, Ahlquist P (1992) RNA-based viruses In: Gurr SJ, McPherson MJ, Bowles DJ (eds) Molecular plant pathology; a practical approach vol 1. Oxford University Press, New York, pp 23–34

  27. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  28. Lane LC (1981) Bromoviruses In: Kurstak E (ed) Handbook of plant virus infections and comparative diagnosis. Elsevier, North-Holland, Biomedical Press, New York, pp 333–376

  29. Langereis K, Mugnier MA, Cornelissen BJ, Pinck L, Bol JF (1986) Variable repeats and poly (A)-stretches in the leader sequence of alfalfa mosaic virus RNA 3. Virology 154:409–414

    Article  PubMed  CAS  Google Scholar 

  30. Mise K, Allison RF, Janda M, Ahlquist P (1993) Bromovirus movement protein genes play a crucial role in host specificity. J Virol 67:2815–2823

    PubMed  CAS  Google Scholar 

  31. Navas-Castillo J, Albiach-Martí MR, Gowda S, Hilf ME, Garnsey SM, Dawson WO (1997) Kinetics of accumulation of citrus tristeza virus RNAs. Virology 228:92–97

    Article  PubMed  CAS  Google Scholar 

  32. Pacha RF, Allison RF, Ahlquist P (1990) cis-Acting sequences required for in vivo amplification of genomic RNA3 are organized differently in related bromoviruses. Virology 174:436–443

    Article  PubMed  CAS  Google Scholar 

  33. Pacha RF, Ahlquist P (1992) Substantial portions of the 5′ and intercistronic noncoding regions of cowpea chlorotic mottle virus RNA3 are dispensable for systemic infection but influence viral competitiveness and infection pathology. Virology 187:298–307

    Article  PubMed  CAS  Google Scholar 

  34. Pogany J, Hung Q, Romero J, Nagy PD, Bujarski JJ (1994) Infectious transcripts from PCR-amplified broad bean mottle bromovirus cDNA clones and variable nature of leader regions in RNA3 segment. J Gen Virol 75:693–699

    Article  PubMed  CAS  Google Scholar 

  35. Pogue GP, Marsh LE, Hall TC (1990) Point mutations in the ICR2 motif of brome mosaic virus RNAs debilitate in the (+)-strand replication. Virology 188:742–753

    Article  Google Scholar 

  36. Pogue GP, Hall TC (1992) The requirement for a 5′ stem-structure in brome mosaic virus replication supports a new model for viral positive-strand RNA initiation. J Virol 66:674–684

    PubMed  CAS  Google Scholar 

  37. Romero J, Dzianott AM, Bujarski JJ (1992) The nucleotide sequence and genome organization of the RNA2 and RNA3 segments in broad bean mottle virus. Virology 187:671–681

    Article  PubMed  CAS  Google Scholar 

  38. Roossinck MJ, Bujarski J, Ding SW, Hajimorad R, Hanada K, Scott S, Tousignant M (2005) Family Bromoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy. Elsevier Academic Press, San Diego, pp 1049–1058

  39. Sacher R, Ahlquist P (1989) Effects of deletions in the N-terminal basic arm of brome mosaic virus coat protein on RNA packaging and systemic infection. J Virol 63:4545–4552

    PubMed  CAS  Google Scholar 

  40. Sasaki N, Fujita Y, Mise K, Furusawa I (2001) Site-specific single amino acid changes to Lys or Arg in the central region of the movement protein of a hybrid bromovirus are required for adaptation to a nonhost. Virology 279:47–57

    Article  PubMed  CAS  Google Scholar 

  41. Schmitz I, Rao ALN (1996) Molecular study on bromovirus capsid protein; I Characterization of cell-to-cell movement-defective RNA3 variants of brome mosaic virus. Virology 226:281–293

    Article  PubMed  CAS  Google Scholar 

  42. Sullivan ML, Ahlquist P (1999) A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo. J Virol 73:2622–2632

    PubMed  CAS  Google Scholar 

  43. Smirnyagina E, Hsu YH, Chua N, Ahlquist P (1994) Second-site mutations in the brome mosaic virus RNA3 intercistronic region partially suppress a defect in coat protein mRNA transcription. Virology 198:427–436

    Article  PubMed  CAS  Google Scholar 

  44. Valverde RA (1985) Spring beauty latent bromovirus: a new member of the bromovirus group. Phytopathology 75:395–398

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Rodrigo A. Valverde for MYFV-infected leaves of Nicotiana clevelandii and Dr. Yoshihiko Yonezawa for Melandrium album seeds. This work was supported in part by a Grant-in-Aid (19380027) for Scientific Research (B) and a Grant-in-Aid (18208004) for Scientific Research (A) from the Japan Society for the Promotion of Science.

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Author notes

  1. Fukumatsu Iwahashi

    Present address: Sumitomo Chemicals Co., Ltd., Takarazuka, Hyogo, 665-8555, Japan

Authors and Affiliations

  1. Laboratory of Plant Pathology, Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Taiki Narabayashi, Fukumatsu Iwahashi, Masanori Kaido, Tetsuro Okuno & Kazuyuki Mise

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  1. Taiki Narabayashi
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  2. Fukumatsu Iwahashi
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  3. Masanori Kaido
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  5. Kazuyuki Mise
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Corresponding author

Correspondence to Kazuyuki Mise.

Additional information

The DDBJ/EMBL/GenBank accession nos of MYFV RNA1, MYFV RNA2 and MYFV RNA3 determined in this study are AB444583, AB444584 and AB444585, respectively.

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Narabayashi, T., Iwahashi, F., Kaido, M. et al. Melandrium yellow fleck bromovirus infects Arabidopsis thaliana and has genomic RNA sequence characteristics that are unique among bromoviruses. Arch Virol 154, 1381–1389 (2009). https://doi.org/10.1007/s00705-009-0449-y

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