Archives of Virology

, Volume 163, Issue 6, pp 1419–1427 | Cite as

Allexiviruses may have acquired inserted sequences between the CP and CRP genes to change the translation reinitiation strategy of CRP

Original Article

Abstract

Allexiviruses are economically important garlic viruses that are involved in garlic mosaic diseases. In this study, we characterized the allexivirus cysteine-rich protein (CRP) gene located just downstream of the coat protein (CP) gene in the viral genome. We determined the nucleotide sequences of the CP and CRP genes from numerous allexivirus isolates and performed a phylogenetic analysis. According to the resulting phylogenetic tree, we found that allexiviruses were clearly divided into two major groups (group I and group II) based on the sequences of the CP and CRP genes. In addition, the allexiviruses in group II had distinct sequences just before the CRP gene, while group I isolates did not. The inserted sequence between the CP and CRP genes was partially complementary to garlic 18S rRNA. Using a potato virus X vector, we showed that the CRPs affected viral accumulation and symptom induction in Nicotiana benthamiana, suggesting that the allexivirus CRP is a pathogenicity determinant. We assume that the inserted sequences before the CRP gene may have been generated during viral evolution to alter the termination-reinitiation mechanism for coupled translation of CP and CRP.

Notes

Acknowledgements

We thank Dr. David Baulcombe for providing the PVX vector. We are also grateful to Dr. Katsunori Murota for his technical assistance in the in vitro translation experiment.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

705_2018_3749_MOESM1_ESM.pptx (90 kb)
Supplementary material 1 (PPTX 89 kb)
705_2018_3749_MOESM2_ESM.xlsx (40 kb)
Supplementary material 2 (XLSX 39 kb)

References

  1. 1.
    Marais A, Faure C, Mustafayev E, Candresse T (2015) Characterization of new isolates of Apricot vein clearing-associated virus and of a new prunus-infecting virus: evidence for recombination as a driving force in Betaflexiviridae evolution. PLoS One 10:e0129469.  https://doi.org/10.1371/journal.pone.0129469 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Senshu H, Yamaji Y, Minato N, Shiraishi T, Maejima K, Hashimoto M, Miura C, Neriya Y, Namba S (2011) A dual strategy for the suppression of host antiviral silencing: two distinct suppressors for viral replication and viral movement encoded by potato virus M. J Virol 85:10269–10278.  https://doi.org/10.1128/JVI.05273-11 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Zhou ZS, Dell’Orco M, Saldarelli P, Turturo C, Minafra A, Martelli GP (2006) Identification of an RNA-silencing suppressor in the genome of Grapevine virus A. J Gen Virol 87:2387–2395CrossRefPubMedGoogle Scholar
  4. 4.
    Lukhovitskaya NI, Solovieva AD, Boddeti SK, Thaduri S, Solovyev AG, Savenkov EI (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 25:960–973CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Lukhovitskaya NI, Vetukuri RR, Sama I, Thaduri S, Solovyev AG, Savenkov EI (2014) A viral transcription factor exhibits antiviral RNA silencing suppression activity independent of its nuclear localization. J Gen Virol 95:2831–2837CrossRefPubMedGoogle Scholar
  6. 6.
    Lukhovitskaya NI, Yelina NE, Zamyatnin AA Jr, Schepetilnikov MV, Solovyev AG, Sandgren M, Morozov SY, Valkonen JP, Savenkov EI (2005) Expression, localization and effects on virulence of the cysteine-rich 8 kDa protein of Potato mop-top virus. J Gen Virol 86:2879–2889CrossRefPubMedGoogle Scholar
  7. 7.
    Arkhipov AV, Solovyev AG, Vishnichenko VK (2013) Reproduction of Shallot virus X in absence of its own active suppressor protein of RNA silencing. Russ Agri Sci 39:218–221CrossRefGoogle Scholar
  8. 8.
    Adams MJ, Antoniw JF, Bar-Joseph M, Brunt AA, Candresse T, Foster GD, Martelli GP, Milne RG, Zavriev SK, Fauquet CM (2004) The new plant virus family Flexiviridae and assessment of molecular criteria for species demarcation. Arch Virol 149:1045–1060PubMedGoogle Scholar
  9. 9.
    Wylie SJ, Li H, Saqib M, Jones MGK (2014) The global trade in fresh produce and the vagility of plant viruses: a case study in garlic. PLoS One 9:e105044CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Bereda M, Paduch-Cichal E, Dąbrowskaet E (2017) Occurrence and phylogenetic analysis of allexiviruses identified on garlic from China, Spain and Poland commercially available on the polish retail market. Eur J Plant Pathol 149:227–237CrossRefGoogle Scholar
  11. 11.
    Chen J, Zheng HY, Antoniw JF, Adams MJ, Chen JP, Lin L (2004) Detection and classification of allexiviruses from garlic in China. Arch Virol 149:435–445CrossRefPubMedGoogle Scholar
  12. 12.
    Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program from Windows 95/98/NT. Nucleic Acids Symp 41:95–98Google Scholar
  13. 13.
    Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  14. 14.
    Rambaut A, Suchard MA, Drummond AJ (2013) Tracer version 1.6. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 28 Feb 2014
  15. 15.
    Rambaut A (2012) FigTree version 1.4. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 28 Feb 2014
  16. 16.
    Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921.  https://doi.org/10.1111/j.1755-0998.2011.03021.x CrossRefPubMedGoogle Scholar
  17. 17.
    Yoshida N, Shimura H, Yamashita K, Suzuki M, Masuta C (2012) Variability in the P1 gene helps to refine phylogenetic relationships among leek yellow stripe virus isolates from garlic. Arch Virol 157:147–153CrossRefPubMedGoogle Scholar
  18. 18.
    Gramstat A, Prüfer D, Rohde W (1994) The nucleic acid-binding zinc finger protein of potato virus M is translated by internal initiation as well as by ribosomal frameshifting involving a shifty stop codon and a novel mechanism of P-site slippage. Nucleic Acids Res 22:3911–3917CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Malygin AA, Kossinova OA, Shatsky IN, Karpova GG (2013) HCV IRES interacts with the 18S rRNA to activate the 40S ribosome for subsequent steps of translation initiation. Nucleic Acids Res 41:8706–8714CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Luttermann C, Meyers G (2007) A bipartite sequence motif induces translation reinitiation in feline calicivirus RNA. J Biol Chem 282:7056–7065CrossRefPubMedGoogle Scholar
  21. 21.
    Powell ML, Napthine S, Jackson RJ, Brierley I, Brown TD (2008) Characterization of the termination–reinitiation strategy employed in the expression of influenza B virus BM2 protein. RNA 14:2394–2406.  https://doi.org/10.1261/rna.1231008 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Guo LH, Sun L, Chiba S, Araki H, Suzuki N (2009) Coupled termination/reinitiation for translation of the downstream open reading frame B of the prototypic hypovirus CHV1-EP713. Nucleic Acids Res 37:3645–3659.  https://doi.org/10.1093/nar/gkp224 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Akbergenov RZh, Zhanybekova SSh, Kryldakov RV, Zhigailov A, Polimbetova NS, Hohn T, Iskakov BK (2004) ARC-1, a sequence element complementary to an internal 18S rRNA segment, enhances translation efficiency in plants when present in the leader or intercistronic region of mRNAs. Nucleic Acids Res 32:239–247CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Lukhovitskaya NI, Ignatovich IV, Savenkov EI, Schiemann J, Morozov SY, Solovyev AG (2009) Role of the zinc-finger and basic motifs of chrysanthemum virus B p12 protein in nucleic acid binding, protein localization and induction of a hypersensitive response upon expression from a viral vector. J Gen Virol 90:723–733.  https://doi.org/10.1099/vir.0.005025-0 CrossRefPubMedGoogle Scholar
  25. 25.
    Fujita N, Komatsu K, Ayukawa Y, Matsuo Y, Hashimoto M, Netsu O, Teraoka T, Yamaji Y, Namba S, Arie T (2017) N-terminal region of cysteine-rich protein (CRP) in carlaviruses is involved in the determination of symptom types. Mol Plant Pathol.  https://doi.org/10.1111/mpp.12513 PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Graduate School of AgricultureHokkaido UniversitySapporoJapan

Personalised recommendations