Abstract
The family Flaviviridae is composed of viruses with a positive-sense single-stranded RNA genome and includes viruses that are important veterinary and human pathogens. Most members of the family are arthropod- and vertebrate-infecting viruses, but more recently, divergent flavi-like viruses have been identified in marine invertebrate and vertebrate hosts. The striking discovery of gentian Kobu-sho-associated virus (GKaV), along with a recent report of a related virus from carrot, has expanded the known host range of flavi-like viruses to plants, suggesting they could be grouped in a proposed genus tentatively named “Koshovirus”. Here, we report the identification and characterization of two novel RNA viruses that show a genetic and evolutionary relationship to the previously identified “koshoviruses”. Their genome sequences were obtained from transcriptomic datasets of the flowering plants Coptis teeta and Sonchus asper. These two new viruses, which we have named "coptis flavi-like virus 1" (CopFLV1) and "sonchus flavi-like virus 1" (SonFLV1), are members of novel species characterized by the longest monopartite RNA genome observed so far among plant-associated RNA viruses, which is ca. 24 kb in size. Structural and functional annotations of the polyproteins of all koshoviruses resulted in the detection not only of the expected helicase and RNA-dependent RNA polymerase but also of several additional divergent domains, including AlkB oxygenase, trypsin-like serine protease, methyltransferase, and envelope E1 flavi-like domains. Phylogenetic analysis showed that CopFLV1, SonFLV1, GKaV, and the carrot flavi-like virus were grouped together in a monophyletic clade, strongly supporting the recent proposal for creation of the genus “Koshovirus” for the group of related plant-infecting flavi-like viruses.
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Data availability
Nucleotide sequence data reported are available in the Third Party Annotation Section of the DDBJ/ENA/GenBank databases under the accession numbers TPA: BK062902-BK062903.
References
Greninger AL (2018) A decade of RNA virus metagenomics is (not) enough. Virus Res 244:218–229. https://doi.org/10.1016/j.virusres.2017.10.014
Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI, Yutin N et al (2020) Global organization and proposed megataxonomy of the virus world. Microbiol Mol Biol Rev 84:1–33. https://doi.org/10.1128/mmbr.00061-19
Simmonds P, Adams MJ, Benko M, Breitbart M, Brister JR, Carstens EB et al (2017) Consensus statement: virus taxonomy in the age of metagenomics. Nat Rev Microbiol 15:161–168. https://doi.org/10.1038/nrmicro.2016.177
Bejerman N, Dietzgen RG, Debat H (2021) Illuminating the plant rhabdovirus landscape through metatranscriptomics data. Viruses 13:1304. https://doi.org/10.3390/v13071304
Mifsud J, Gallagher R, Holmes E, Geoghegan J (2022) Transcriptome mining expands knowledge of RNA viruses across the plant kingdom. J Virol 24:e0026022. https://doi.org/10.1128/jvi.00260-22
Lauber C, Seitz S (2022) Opportunities and challenges of data-driven virus discovery. Biomolecules 12:1073. https://doi.org/10.3390/biom12081073
Simmonds P, Becher P, Bukh J, Gould EA, Meyers G, Monath T, Muerhoff S, Pletnev A, Rico-Hesse R, Smith DB, Stapleton JT, Ictv Report C (2017) ICTV virus taxonomy profile: Flaviviridae. J Gen Virol 98:2–3. https://doi.org/10.1099/jgv.0.000672
Mifsud J, Costa V, Petrone M, Marzinelli E, Holmes E, Harvey E (2023) Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians. Virus Evol 9:veac124. https://doi.org/10.1093/ve/veac124
Parry R, Asgari S (2019) Discovery of novel crustacean and cephalopod flaviviruses: insights into the evolution and circulation of flaviviruses between marine invertebrate and vertebrate hosts. J Virol 93:e00432–e00419. https://doi.org/10.1128/jvi.00432-19
Kobayashi K, Atsumi G, Iwadate Y, Tomita R, Chiba K, Akasaka S, Nishihara M, Takahashi H, Yamaoka N, Nishiguchi M, Sekine KT (2013) Gentian Kobu-sho-associated virus: a tentative, novel double-stranded RNA virus that is relevant to gentian Kobu-sho syndrome. J Gen Plant Pathol 79:56–63. https://doi.org/10.1007/s10327-012-0423-5
Shaffer C, Michener DC, Vlasava NB, Botermans M, Starre J, Tzanetakis IE (2021) First report of gentian Kobu-sho-associated virus infecting peony in the United States and the Netherlands. Plant Dis. https://doi.org/10.1094/PDIS-06-21-1316-PDN
Dolja VV, Koonin EV (2018) Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res 244:36–52. https://doi.org/10.1016/j.virusres.2017.10.020
Schönegger D, Marais A, Faure C, Candresse T (2022) A new flavi-like virus identified in populations of wild carrots. Arch Virol 167:2407–2409. https://doi.org/10.1007/s00705-022-05544-1
Dahan J, Wolf YI, Orellana GE, Wenninger EJ, Koonin EV, Karasev AV (2022) A novel flavi-like virus in Alfalfa (Medicago sativa L.) crops along the Snake River Valley. Viruses 14(6):1320. https://doi.org/10.3390/v14061320
Bejerman N, Dietzgen RG, Debat H (2022) Unlocking the hidden genetic diversity of varicosaviruses, the neglected plant rhabdoviruses. Pathogens 11:1127. https://doi.org/10.3390/pathogens11101127
Debat H, Garcia ML, Bejerman N (2023) Expanding the repertoire of the plant infecting ophioviruses. bioRxiv. https://doi.org/10.1101/2023.01.27.525910.
Edgar RC, Taylor J, Lin V, Altman T, Barbera P, Meleshko D, Lohr D, Novakovsky G, Buchfink B, Al-Shayeb B et al (2022) Petabase-scale sequence alignment catalyses viral discovery. Nature 602:142–147. https://doi.org/10.1038/s41586-021-04332-2
Bushmanova E, Antipov D, Lapidus A, Prjibelski A (2019) rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data. GigaScience 8:GIZ100. https://doi.org/10.1093/gigascience/giz100
Bratlie MS, Drabl SF (2005) Bioinformatic map** of AlkB homology domains in viruses. BMC Genom 6:1. https://doi.org/10.1186/1471-2164-6-1
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
He SM, Liang YL, Cong K, Chen G, Zhao X, Zhao QM, Zhang JJ, Wang X, Dong Y, Yang JL et al (2018) Identification and characterization of genes involved in benzylisoquinoline alkaloid biosynthesis in Coptis species. Front Plant Sci 9:731. https://doi.org/10.3389/fpls.2018.00731
Jayasena AS, Fisher MF, Panero JL, Secco D, Bernath-Levin K, Berkowitz O, Taylor NL, Schilling EE, Whelan J, Mylne JS (2017) Stepwise evolution of a buried inhibitor peptide over 45 My. Mol Biol Evol 34:1505–1516. https://doi.org/10.1093/molbev/msx104
Acknowledgements
We would like to express sincere gratitude to the authors of the underlying data used for this work. By following open-access practices and making raw sequence data in public repositories available to the research community, they have promoted the generation of new knowledge and ideas.
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HD and NB contributed to the study conception and design and data analysis. The manuscript was written by both authors, who commented on and reviewed it. Both authors read and approved the final manuscript.
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Debat, H., Bejerman, N. Two novel flavi-like viruses shed light on the plant-infecting koshoviruses. Arch Virol 168, 184 (2023). https://doi.org/10.1007/s00705-023-05813-7
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DOI: https://doi.org/10.1007/s00705-023-05813-7