Archives of Virology

, Volume 164, Issue 5, pp 1419–1426 | Cite as

Novel bird’s-foot trefoil RNA viruses provide insights into a clade of legume-associated enamoviruses and rhabdoviruses

  • Humberto J. DebatEmail author
  • Nicolas BejermanEmail author
Brief Report


Here, we report the identification and characterization of two novel viruses associated with bird’s-foot trefoil. Virus sequences related to those of enamoviruses (ssRNA (+); Luteoviridae; Enamovirus) and nucleorhabdoviruses (ssRNA (-); Rhabdoviridae; Nucleorhabdovirus) were detected in Lotus corniculatus transcriptome data. The genome of the tentatively named “bird’s-foot trefoil-associated virus 1” (BFTV-1) is a 13,626-nt-long negative-sense ssRNA. BFTV-1 encodes six predicted gene products in the antigenome orientation in the canonical order 3′-N-P-P3-M-G-L-5′. The genome of the proposed “bird’s-foot trefoil-associated virus 2” (BFTV-2) is 5,736 nt long with a typical 5΄-PO-P1-2-IGS-P3-P5-3′ enamovirus genome structure. Phylogenetic analysis indicated that BFTV-1 is closely related to datura yellow vein nucleorhabdovirus and that BFTV-2 clusters into a monophyletic lineage of legume-associated enamoviruses. This subclade of highly related and co-divergent legume-associated viruses provides insights into the evolutionary history of the enamoviruses.



We would like to express sincere gratitude to the generators of the underlying data used for this work: Dr. Ying Wang and Dr. Zhezhi Wang. By following open access practices and making accessible raw sequence data in public repositories available to the research community, they have promoted the generation of new knowledge and ideas.


This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sector.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict 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_2019_4193_MOESM1_ESM.docx (1.5 mb)
Supplementary material 1 (DOCX 1549 kb)
705_2019_4193_MOESM2_ESM.docx (535 kb)
Supplementary material 2 (DOCX 535 kb)
705_2019_4193_MOESM3_ESM.docx (386 kb)
Supplementary material 3 (DOCX 386 kb)
705_2019_4193_MOESM4_ESM.docx (564 kb)
Supplementary material 4 (DOCX 563 kb)
705_2019_4193_MOESM5_ESM.docx (18 kb)
Supplementary material 5 (DOCX 17 kb)
705_2019_4193_MOESM6_ESM.docx (14 kb)
Supplementary material 6 (DOCX 14 kb)
705_2019_4193_MOESM7_ESM.docx (17 kb)
Supplementary material 7 (DOCX 16 kb)
705_2019_4193_MOESM8_ESM.docx (19 kb)
Supplementary material 8 (DOCX 18 kb)
705_2019_4193_MOESM9_ESM.bam (1 mb)
Supplementary material 9 (BAM 1057 kb)
705_2019_4193_MOESM10_ESM.bam (4.7 mb)
Supplementary material 10 (BAM 4841 kb)


  1. 1.
    Barry JK, Miller WA (2002) A − 1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proc Natl Acad Sci USA 99:11133–11138CrossRefGoogle Scholar
  2. 2.
    Bejerman N, Giolitti F, de Breuil S, Trucco V, Dietzgen RG, Lenardon S (2016) Complete genome sequence of a new enamovirus from Argentina infecting alfalfa plants showing dwarfism symptoms. Arch Virol 161:2029–2032CrossRefGoogle Scholar
  3. 3.
    Brown CM, Dinesh-Kumar SP, Miller WA (1996) Local and distant sequences are required for efficient readthrough of the barley yellow dwarf virus PAV coat protein gene stop codon. J Virol 70:5884–5892Google Scholar
  4. 4.
    Debat HJ (2017) An RNA virome associated to the Golden orb-weaver Spider Nephila clavipes. Front Microbiol 8:2097CrossRefGoogle Scholar
  5. 5.
    Demler SA, De Zoeten GA (1991) The nucleotide sequence and luteovirus-like nature of RNA 1 of an aphid non-transmissible strain of pea enation mosaic virus. J Gen Virol 72:1819–1834CrossRefGoogle Scholar
  6. 6.
    Dietzgen RG, Innes DJ, Bejerman N (2015) Complete genome sequence and intracellular protein localization of Datura yellow vein nucleorhabdovirus. Virus Res 205:7–11CrossRefGoogle Scholar
  7. 7.
    Dietzgen RG, Kondo H, Goodin MM, Kurath G, Vasilakis N (2017) The family Rhabdoviridae: mono-and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins. Virus Res 227:158–170CrossRefGoogle Scholar
  8. 8.
    Domier LL (2012) Family Luteoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy, ninth report of the international committee on taxonomy of viruses. Elsevier, Oxford, pp 1045–1053Google Scholar
  9. 9.
    Escaray FJ, Menendez AB, Garriz A, Pieckenstain FL, Estrella MJ, Castagno LN, Carrasco P, Sanjuan J, Ruiz OA (2012) Ecological and agronomic importance of the plant genus Lotus. Its application in grassland sustainability and the amelioration of constrained and contaminated soils. Plant Science 182:121e133Google Scholar
  10. 10.
    Firth AE, Brierley I (2012) Non-canonical translation in RNA viruses. J Gen Virol 93:1385–1409CrossRefGoogle Scholar
  11. 11.
    Fusaro AF, Correa RL, Nakasugi K, Jackson C, Kawchuk L, Vaslin MF, Waterhouse PM (2012) The Enamovirus P0 protein is a silencing suppressor which inhibits local and systemic RNA silencing. Virol 426:178–187CrossRefGoogle Scholar
  12. 12.
    Goodin MM, Austin J, Tobias R, Fujita M, Morales C, Jackson AO (2001) Interactions and nuclear import of the N and P proteins of sonchus yellow net virus, a plant nucleorhabdovirus. J Virol 75:9393–9406CrossRefGoogle Scholar
  13. 13.
    Hannaway DB, Myers D (2004) Birdsfoot trefoil (Lotus corniculatus L.). Species selection information system. Oregon State University, CorvallisGoogle Scholar
  14. 14.
    Heaton LA, Hillman BI, Hunter BG, Zuidema D, Jackson AO (1989) Physical map of the genome of sonchus yellow net virus, a plant rhabdovirus with six genes and conserved gene junction sequences. Proc Natl Acad Sci USA 86:8665–8668CrossRefGoogle Scholar
  15. 15.
    Kim H, Park D, Hahn Y (2018) Identification of novel RNA viruses in alfalfa (Medicago sativa): an alphapartitivirus, a deltapartitivirus, and a marafivirus. Gene 638:7–12CrossRefGoogle Scholar
  16. 16.
    McDonald JG, Susuki M (1983) Occurrence of alfalfa mosaic virus in Prince Edward Island. Canadian Plant Disease Survey 63:47–50Google Scholar
  17. 17.
    Nibert ML, Vong M, Fugate KK, Debat HJ (2018) Evidence for contemporary plant mitoviruses. Virol 518:14–24CrossRefGoogle Scholar
  18. 18.
    Roossinck MJ, Martin DP, Roumagnac P (2015) Plant virus metagenomics: advances in virus discovery. Phytopathol 105:716–727CrossRefGoogle Scholar
  19. 19.
    Silva JMF, Al Rwahnih M, Blawid R, Nagata T, Fajardo TVM (2017) Discovery and molecular characterization of a novel enamovirus, Grapevine enamovirus-1. Virus Genes 53:667–671CrossRefGoogle Scholar
  20. 20.
    Simmonds P, Adams MJ, Benkő M, Breitbart M, Brister JR, Carstens EB, Hull R (2017) Consensus statement: virus taxonomy in the age of metagenomics. Nat Rev Microbiol 15:161CrossRefGoogle Scholar
  21. 21.
    Singh KS, Beadle K, Troczka BJ, Field L, Davies E, Williamson M, Bass C (2018) Extension of partial gene transcripts by iterative mapping of RNA-Seq raw reads. IEEE/ACM Trans Comput Biol Bioinform.
  22. 22.
    Vives MC, Velázquez K, Pina JA, Moreno P, Guerri J, Navarro L (2013) Identification of a new enamovirus associated with citrus vein enation disease by deep sequencing of small RNAs. Phytopathol 103:1077–1086CrossRefGoogle Scholar
  23. 23.
    Wang Y, Hua W, Wang J, Hannoufa A, Xu Z, Wang Z (2013) Deep sequencing of Lotus corniculatus L. reveals key enzymes and potential transcription factors related to the flavonoid biosynthesis pathway. Mol Genet Genom 288:131–139CrossRefGoogle Scholar
  24. 24.
    Wu LP, Yang T, Liu HW, Postman J, Li R (2018) Molecular characterization of a novel rhabdovirus infecting blackcurrant identified by high-throughput sequencing. Arch Virol 162:2493–2494Google Scholar
  25. 25.
    Xu Y, Ju HJ, DeBlasio S, Carino EJ, Johnson R, MacCoss M, Heck MC, Miller WA, Gray SM (2018) A stem-loop structure in Potato leafroll virus ORF5 that is essential for read through translation of the coat protein ORF stop codon 700 bases upstream. J Virol 92:e01544-17CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Instituto de Patología Vegetal, Centro de Investigaciones AgropecuariasInstituto Nacional de Tecnología Agropecuaria (IPAVE-CIAP-INTA)CórdobaArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina

Personalised recommendations