Novel Betanucleorhabdoviruses Infecting Elderberry (Sambucus nigra L.): Genome Characterization and Genetic Variability
Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
LD15048
Ministry of Education, Youth and Sport (MEYS), Czech Republic
PubMed
38921743
PubMed Central
PMC11206775
DOI
10.3390/pathogens13060445
PII: pathogens13060445
Knihovny.cz E-resources
- Keywords
- genetic diversity, high-throughput sequencing, mixed infection, plant rhabdovirus,
- MeSH
- Sambucus nigra * MeSH
- Phylogeny * MeSH
- Genetic Variation * MeSH
- Genome, Viral * MeSH
- Plant Leaves virology MeSH
- Plant Diseases * virology MeSH
- Rhabdoviridae genetics isolation & purification classification MeSH
- RNA, Viral genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- RNA, Viral MeSH
The genus Betanucleorhabdovirus includes plant viruses with negative sense, non-segmented, single-stranded RNA genomes. Here, we characterized putative novel betanucleorhabdoviruses infecting a medically important plant, elderberry. Total RNA was purified from the leaves of several plants, ribodepleted and sequenced using the Illumina platform. Sequence data analysis led to the identification of thirteen contigs of approximately 13.5 kb, showing a genome structure (3'-N-P-P3-M-G-L-5') typical of plant rhabdoviruses. The detected isolates showed 69.4 to 98.9% pairwise nucleotide identity and had the highest identity among known viruses (64.7-65.9%) with tomato betanucleorhabdovirus 2. A detailed similarity analysis and a phylogenetic analysis allowed us to discriminate the elderberry isolates into five groups, each meeting the sequence-based ICTV demarcation criterion in the Betanucleorhabdovirus genus (lower than 75% identity for the complete genome). Hence, the detected viruses appear to represent five novel, closely related betanucleorhabdoviruses, tentatively named Sambucus betanucleorhabdovirus 1 to 5.
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Bejerman N., Dietzgen R.G., Debat H. Illuminating the plant rhabdovirus landscape through metatranscriptomics data. Viruses. 2021;13:1304. doi: 10.3390/v13071304. PubMed DOI PMC
Walker P.J., Freitas-Astúa J., Bejerman N., Blasdell K.R., Breyta R., Dietzgen R.G., Fooks A.R., Kondo H., Kurath G., Kuzmin I.V., et al. ICTV Virus Taxonomy Profile: 2022. J. Gen. Virol. 2022;103:001689. doi: 10.1099/jgv.0.001689. PubMed DOI
Kuhn J.H., Adkins S., Alioto D., Alkhovsky S.V., Amarasinghe G.K., Anthony S.J., Avsic-Zupanc T., Ayllon M.A., Bahl J., Balkema-Buschmann A., et al. 2020 taxonomic update for phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Arch. Virol. 2020;165:3023–3072. doi: 10.1007/s00705-020-04731-2. PubMed DOI PMC
Jackson A.O., Dietzgen R.G., Goodin M.M., Bragg J.N., Deng M. Biology of plant rhabdoviruses. Annu. Rev. Phytopathol. 2005;43:623–660. doi: 10.1146/annurev.phyto.43.011205.141136. PubMed DOI
Belete M.T., Igori D., Kim S.E., Lee S.H., Moon J.S. Complete genome sequence of cnidium virus 1, a novel betanucleorhabdovirus infecting Cnidium officinale. Arch. Virol. 2022;167:973–977. doi: 10.1007/s00705-021-05348-9. PubMed DOI
Kuhn J.H., Abe J., Adkins S., Alkhovsky S.V., Avsic-Zupanc T., Ayllón M.A., Bahl J., Balkema-Buschmann A., Ballinger M.J., Baranwal V.K., et al. Annual (2023) taxonomic update of RNA-directed RNA polymerase-encoding negative-sense RNA viruses (realm: Kingdom: Phylum) J. Gen. Virol. 2023;104:001864. doi: 10.1099/jgv.0.001864. PubMed DOI PMC
Sidharthan V.K., Baranwal V.K. Mining of the water hyssop (Bacopa monnieri) transcriptome reveals genome sequences of two putative novel rhabdoviruses and a solendovirus. Arch. Virol. 2021;166:1985–1990. doi: 10.1007/s00705-021-05061-7. PubMed DOI
Bhat A.I., Pamitha N.S., Naveen K.P., Biju C.N. Identification and characterization of cardamom vein clearing virus, a novel aphid-transmitted nucleorhabdovirus. Eur. J. Plant Pathol. 2020;156:1053–1062. doi: 10.1007/s10658-020-01958-2. DOI
Dietzgen R.G., Innes D.J., Bejerman N. Complete genome sequence and intracellular protein localization of Datura yellow vein nucleorhabdovirus. Virus Res. 2015;205:7–11. doi: 10.1016/j.virusres.2015.05.001. PubMed DOI
Debat H.J., Bejerman N. Novel bird’s-foot trefoil RNA viruses provide insights into a clade of legume-associated enamoviruses and rhabdoviruses. Arch. Virol. 2019;164:1419–1426. doi: 10.1007/s00705-019-04193-1. PubMed DOI
Baek D., Lim S., Ju H.J., Kim H.R., Lee S.H., Moon J.S. The complete genome sequence of apple rootstock virus A, a novel nucleorhabdovirus identified in apple rootstocks. Arch. Virol. 2019;164:2641–2644. doi: 10.1007/s00705-019-04348-0. PubMed DOI
Gaafar Y.Z.A., Richert-Poggeler K.R., Maass C., Vetten H.J., Ziebell H. Characterisation of a novel nucleorhabdovirus infecting alfalfa (Medicago sativa) Virol. J. 2019;16:55. doi: 10.1186/s12985-019-1147-3. PubMed DOI PMC
Rivarez M.P.S., Pecman A., Bacnik K., Maksimovic O., Vucurovic A., Seljak G., Mehle N., Gutiérrez-Aguirre I., Ravnikar M., Kutnjak D. In-depth study of tomato and weed viromes reveals undiscovered plant virus diversity in an agroecosystem. Microbiome. 2023;11:60. doi: 10.1186/s40168-023-01500-6. PubMed DOI PMC
Heaton L.A., Hillman B.I., Hunter B.G., Zuidema D., Jackson A.O. Physical map of the genome of sonchus yellow net virus, a plant rhabdovirus with 6 genes and conserved gene junction sequences. Proc. Natl. Acad. Sci. USA. 1989;86:8665–8668. doi: 10.1073/pnas.86.22.8665. PubMed DOI PMC
Wu L.P., Yang T., Liu H.W., Postman J., Li R. Molecular characterization of a novel rhabdovirus infecting blackcurrant identified by high-throughput sequencing. Arch. Virol. 2018;163:1363–1366. doi: 10.1007/s00705-018-3709-x. PubMed DOI
Stenger D.C., Burbank L.P., Wang R.Y., Stewart A.A., Mathias C., Goodin M.M. Lost and found: Rediscovery and genomic characterization of sowthistle yellow vein virus after a 30+year hiatus. Virus Res. 2020;284:197987. doi: 10.1016/j.virusres.2020.197987. PubMed DOI
Cao M.J., Zhang S., Li M., Liu Y.J., Dong P., Li S.R., Kuang M., Li R.H., Zhou Y. Discovery of four novel viruses associated with flower yellowing disease of Green sichuan pepper (Zanthoxylum armatum) by virome analysis. Viruses. 2019;11:696. doi: 10.3390/v11080696. PubMed DOI PMC
International Committee on Taxonomy of Viruses (ICTV) EC 55, Jena, Germany, August 2023. Email Ratification April 2024. 2024. [(accessed on 15 May 2024)]. Available online: https://ictv.global/msl.
Hu J.Y., Miao T.L., Que K.J., Rahman M.S., Zhang L., Dong X., Ji P.Z., Dong J.H. Identification, molecular characterization and phylogenetic analysis of a novel nucleorhabdovirus infecting Paris polyphylla var. yunnanensis. Sci. Rep. 2023;13:10040. doi: 10.1038/s41598-023-37022-2. PubMed DOI PMC
Atkinson M.D., Atkinson E. Sambucus nigra L. J. Ecol. 2002;90:895–923. doi: 10.1046/j.1365-2745.2002.00698.x. DOI
Plants of the World Online Royal Botanic Gardens, Kew. [(accessed on 16 April 2024)]. Available online: https://powo.science.kew.org/
Ferreira S.S., Martins-Gomes C., Nunes F.M., Silva A.M. Elderberry (Sambucus nigra L.) extracts promote anti-inflammatory and cellular antioxidant activity. Food Chem. X. 2022;15:100437. doi: 10.1016/j.fochx.2022.100437. PubMed DOI PMC
Mocanu M.L., Amariei S. Elderberries-A source of bioactive compounds with antiviral action. Plants. 2022;11:740. doi: 10.3390/plants11060740. PubMed DOI PMC
Dominguez R., Pateiro M., Munekata P.E.S., Santos Lopez E.M., Rodriguez J.A., Barros L., Lorenzo J.M. Potential use of elderberry (Sambucus nigra L.) as natural colorant and antioxidant in the food industry. A Review. Foods. 2021;10:2713. doi: 10.3390/foods10112713. PubMed DOI PMC
Dominguez R., Zhang L., Rocchetti G., Lucini L., Pateiro M., Munekata P.E.S., Lorenzo J.M. Elderberry (Sambucus nigra L.) as potential source of antioxidants. Characterization, optimization of extraction parameters and bioactive properties. Food Chem. 2020;330:127266. doi: 10.1016/j.foodchem.2020.127266. PubMed DOI
Festa J., Hussain A., Hackney A., Desai U., Sahota T.S., Singh H., Da Boit M. Elderberry extract improves molecular markers of endothelial dysfunction linked to atherosclerosis. Food Sci. Nutr. 2023;11:4047–4059. doi: 10.1002/fsn3.3393. PubMed DOI PMC
Liu D., He X.Q., Wu D.T., Li H.B., Feng Y.B., Zou L., Gan R.Y. Elderberry (Sambucus nigra L.): Bioactive compounds, health functions, and applications. J. Agric. Food Chem. 2022;70:4202–4220. doi: 10.1021/acs.jafc.2c00010. PubMed DOI
Šafářová D., Vavroušková K., Candresse T., Navrátil M. Molecular characterization of a novel Aureusvirus infecting elderberry (Sambucus nigra L.) PLoS ONE. 2018;13:e0200506. doi: 10.1371/journal.pone.0200506. PubMed DOI PMC
Gentit P., Foissac X., Svanella-Dumas L., Peypelut M., Candresse T. Characterization of two different apricot latent virus variants associated with peach asteroid spot and peach sooty ringspot diseases. Arch. Virol. 2001;146:1453–1464. doi: 10.1007/s007050170071. PubMed DOI
Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC
Tamura K., Stecher G., Kumar S. MEGA11 Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021;38:3022–3027. doi: 10.1093/molbev/msab120. PubMed DOI PMC
Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–595. doi: 10.1093/genetics/123.3.585. PubMed DOI PMC
Martin D.P., Varsani A., Roumagnac P., Botha G., Maslamoney S., Schwab T., Kelz Z., Kumar V., Murrell B. RDP5: A computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol. 2021;7:veaa087. doi: 10.1093/ve/veaa087. PubMed DOI PMC
Nguyen Ba A.N., Pogoutse A., Provart N., Moses A.M. NLStradamus: A simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinform. 2009;10:202. doi: 10.1186/1471-2105-10-202. PubMed DOI PMC
Šafářová D., Candresse T., Navrátil M. Complete genome sequence of a novel cytorhabdovirus infecting elderberry (Sambucus nigra L.) in the Czech Republic. Arch. Virol. 2022;167:1589–1592. doi: 10.1007/s00705-022-05444-4. PubMed DOI
Šafářová D., Candresse T., Navrátil M. Complete genome sequence of a novel bromovirus infecting elderberry (Sambucus nigra L.) in the Czech Republic. Arch. Virol. 2018;163:567–570. doi: 10.1007/s00705-017-3629-1. PubMed DOI
Mlynarczyk K., Walkowiak-Tomczak D., Lysiak G.P. Bioactive properties of Sambucus nigra L. as a functional ingredient for food and pharmaceutical industry. J. Funct. Foods. 2018;40:377–390. doi: 10.1016/j.jff.2017.11.025. PubMed DOI PMC
Ho T., Quito-Avila D., Keller K.E., Postman J.D., Martin R.R., Tzanetakis I.E. Evidence of sympatric speciation of elderberry carlaviruses. Virus Res. 2016;215:72–75. doi: 10.1016/j.virusres.2016.01.017. PubMed DOI
Maree H.J., Fox A., Al Rwahnih M., Boonham N., Candresse T. Application of HTS for routine plant virus diagnostics: State of the art and challenges. Front. Plant Sci. 2018;9:1082. doi: 10.3389/fpls.2018.01082. PubMed DOI PMC
Vainio E.J., Rumbou A., Diez J.J., Büttner C. Forest tree virome as a source of tree diseases and biological control agents. Curr. For. Rep. 2024;10:153–174. doi: 10.1007/s40725-024-00214-8. DOI
Maliogka V.I., Minafra A., Saldarelli P., Ruiz-Garcia A.B., Glasa M., Katis N., Olmos A. Recent advances on detection and characterization of fruit tree viruses using high-throughput sequencing technologies. Viruses. 2018;10:436. doi: 10.3390/v10080436. PubMed DOI PMC
ICTV Taxonomy Release. 2024. [(accessed on 27 April 2024)]. Available online: https://ictv.global/taxonomy.
Thomas J.E., Dietzgen R.G. Characterization of Datura yellow vein virus, a newly described rhabdovirus from Australia. Ann. Appl. Biol. 1991;118:339–349. doi: 10.1111/j.1744-7348.1991.tb05634.x. DOI