Skip to main content
SpringerLink
Log in

Exploring the tymovirales landscape through metatranscriptomics data

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Tymovirales is an order of viruses with positive-sense RNA genomes that mostly infect plants, but also fungi and insects. The number of genome sequences of viruses that could fit this taxon has been growing in the last few years with the extensive use of high-throughput sequencing. Here, we report the discovery of 31 novel viral genome sequences associated with 27 different host plant species, which were hidden in public databases. These viral sequences were identified through homology searches in more than 3,000 plant transcriptomes from the NCBI Sequence Read Archive (SRA) using known tymovirales sequences as queries. Identification, assembly, and curation of raw SRA reads resulted in 29 viral genome sequences with complete coding regions, and two representing partial genomes. Some of the obtained sequences highlight novel genome organizations for members of the order. Phylogenetic analysis showed that six of the novel viruses are related to alphaflexiviruses, 17 to betaflexiviruses, two to deltaflexiviruses, and six to tymovirids. These findings shed new light on the phylogenetic relationships and evolutionary landscape of this group of viruses. Furthermore, this study illustrates the complexity and genome diversity among members of the order and demonstrates that analyzing public SRA data provides an invaluable tool to accelerate virus discovery and refine virus taxonomy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The viral genome sequences have been deposited in the GenBank database under the accession numbers listed in Table 1.

References

  1. Gilbert KB, Holcomb EE, Allscheid RL, Carrington JC (2019) Hiding in plain sight: new virus genomes discovered via a systematic analysis of fungal public transcriptomes. PLoS ONE 14:e0219207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bejerman N, Roumagnac P, Nemchinov L (2020) High-Throughput Sequencing for Deciphering the Virome of Alfalfa (Medicago sativa .L). Front Microbiol 11:553109

    Article  PubMed  PubMed Central  Google Scholar 

  3. Debat HJ, Bejerman N (2019) Novel bird’s-foot trefoil RNA viruses provide insights into a clade of legume-associated enamoviruses and rhabdoviruses. Arch Virol 164:1419–1426

    Article  CAS  PubMed  Google Scholar 

  4. Goh C, Park D, Hahn Y (2020) Identification of Trichosanthes associated rhabdovirus 1, a novel member of the genus Cytorhabdovirus of the family Rhabdoviridae, in the Trichosanthes kirilowii transcriptome. Acta Virol 64:36–43

    Article  CAS  PubMed  Google Scholar 

  5. Jiang P, Shao J, Nemchinov LG (2019) Identification of emerging viral genomes in transcriptomic datasets of alfalfa (Medicago sativa L.). Virol J. 16:153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kim H, Park D, Hahn Y (2018) Identification a novel RNA viruses in alfalfa (Medicago sativa): an Alphapartitivirus, Deltapartitivirus, and a Marafivirus. Gene 638:7–12

    Article  CAS  PubMed  Google Scholar 

  7. Lauber C, Seifert M, Bartenschlager R, Seitz S (2019) Discovery of highly divergent lineages of plant-associated astro-like viruses sheds light on the emergence of potyviruses. Virus Res 260:38–48

    Article  CAS  PubMed  Google Scholar 

  8. Nibert ML, Vong M, Fugate KK, Debat HJ (2018) Evidence for contemporary plant mitoviruses. Virology 518:14–24

    Article  CAS  PubMed  Google Scholar 

  9. Sidharthan K, Baranwal V (2021) Mining of water hyssop (Bacopa monnieri) transcriptome revealed the genome sequences of two putative novel rhabdoviruses and a solendovirus. Arch Virol 166:1985–1990

    Article  CAS  PubMed  Google Scholar 

  10. Dolja VV, Krupovic M, Koonin EV (2020) Deep roots and splendid boughs of the global plant virome. Annu Rev Phytopathol 58:23–53

    Article  CAS  PubMed  Google Scholar 

  11. Lefeuvre P, Martin D, Elena SF, Shepherd DN, Roumagnac P, Varsani A (2019) Evolution and ecology of plant viruses. Nat Rev Microbiol 17:632–644

    Article  CAS  PubMed  Google Scholar 

  12. Roossinck MJ, Martin D, Roumagnac P (2015) Plant virus metagenomics: advances in virus discovery. Phytopathol 105:716–727

    Article  CAS  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. Dutilh E, Varsani A, Tong Y, Simmonds P, Sabanadzovic S et al (2021) Perspective on taxonomic classification of uncultivated viruses. Curr Opinion Virol 51:207–215

    Article  CAS  Google Scholar 

  16. Adams MJ, Candresse T, Hammond J, Kreuze JF, Martelli GP et al (2012) Family Betaflexiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, London, pp 920–941

    Google Scholar 

  17. Kreuze JF, Vaira AM, Menzel W, Candresse T, Zavriev SK et al (2020) ICTV virus taxonomy profile: Alphaflexiviridae. J GenVirol 101:699

    CAS  Google Scholar 

  18. Chen X, He H, Yang X, Zeng H, Qiu D, Guo L (2016) The complete genome sequence of a novel Fusarium graminearum RNA virus in a new proposed family within the order Tymovirales. Arch Virol 161:2899–2903

    Article  CAS  PubMed  Google Scholar 

  19. Li K, Zheng D, Cheng J, Chen T, Fu Y, Jiang D, Xie J (2016) Characterization of a novel Sclerotinia sclerotiorum RNA virus as the prototype of a new proposed family within the order Tymovirales. Virus Res 219:92–99

    Article  CAS  PubMed  Google Scholar 

  20. Rizwan Hamid MR, Xie J, Wu S, Maria SK, Zheng D, Assane HA et al (2018) A novel deltaflexivirus that infects the plant fungal pathogen, Sclerotinia sclerotiorum, can be transmitted among host vegetative incompatible strains. Viruses 10:E295

    Article  CAS  Google Scholar 

  21. Dreher TW, Edwards MC, Gibbs AJ, Haenni AL, Hammond RW et al (2012) Tymovirus. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, London, pp 946–952

    Google Scholar 

  22. de Miranda JR, Cornman RS, Evans JD, Semberg E, Haddad N, Neumann P et al (2015) Genome characterization, prevalence and distribution of a macula-like virus from Apis mellifera and Varroa destructor. Viruses 7:3586–3602

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Li P, Lin Y, Zhang H, Wang S, Qiu D, Guo L (2016) Molecular characterization of a novel mycovirus of the family Tymoviridae isolated from the plant pathogenic fungus Fusarium graminearum. Virology 489:86–94

    Article  CAS  PubMed  Google Scholar 

  24. Wang L, Lu X, Zhai Y, Fu S, Wang D, Rayner S et al (2012) Genomic characterization of a novel virus of the family Tymoviridae isolated from mosquitoes. PLoS ONE 7:e39845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Martin DP, Varsani A, Roumagnac P, Botha G, Maslamoney S et al (2020) RDP5: a computer program for analysing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol. 7:veaa087

    Article  PubMed  PubMed Central  Google Scholar 

  27. Francois S, Antoine-Lorquin A, Kulikowski M, Frayssinet M, Filloux D, Fernandez E et al (2021) Characterisation of the viral community associated with the alfalfa weevil (Hypera postica) and its host plant, alfalfa (Medicago sativa). Viruses 13:791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Li Z, Wang G, Zhao R, Zhang Z, Xia Z, Zhai J, Huang X (2020) Complete genome sequence of a novel capillovirus infecting Hevea brasiliensis in China. Arch Virol 165:249–252

    Article  CAS  PubMed  Google Scholar 

  29. Luo Q, Hu S, Lin Q, Xu F, Peng J et al (2021) Complete genome sequence of a novel foveavirus isolated from Allium sativum L. in China. Arch Virol 166:983–986

    Article  CAS  PubMed  Google Scholar 

  30. Marais A, Faure C, Theil S, Candresse T (2018) Molecular characterization of a novel species of capillovirus from Japanese apricot (Prunus mume). Viruses 10:144

    Article  PubMed Central  CAS  Google Scholar 

  31. Thekke-Veetil T, Ho T, Postman JD, Martin RR, Tzanetakis IE (2018) A virus in American Blackcurrant (Ribes americanum) with distinct genome features reshapes classification in the tymovirales. Viruses 10:406

    Article  PubMed Central  CAS  Google Scholar 

  32. Veerakone S, Liefting L, Khan S, Pal C, Tang J, Ward L (2021) Partial biological and molecular characterization of a novel citrivirus from Nandina domestica. Arch Virol 166:1395–1399

    Article  CAS  PubMed  Google Scholar 

  33. Zheng L, Chen M, Li R (2020) Camellia ringspot-associated virus 4, a proposed new foveavirus from Camellia japonica. Arch Virol 165:1707–1710

    Article  CAS  PubMed  Google Scholar 

  34. Goh C, Park D, Kim H, Sebastiani F, Hahn Y (2018) Novel Divavirus (the family Betaflexiviridae) and Mitovirus (the family Narnaviridae) species identified in basil (Ocimum basilicum). Acta Virol 62:304–309

    Article  CAS  PubMed  Google Scholar 

  35. Goh C, Park D, Lee J, Davey P, Pernice M et al (2019) Zostera virus T-a novel virus of the genus Tepovirus identified in the eelgrass. Zostera muelleri. Acta Virol. 63:366–372

    Article  CAS  PubMed  Google Scholar 

  36. Goh C, Park D, Hahn Y (2021) A novel tepovirus, Agave virus T, identified by the analysis of the transcriptome data of blue agave (Agave tequilana). Acta Virol 65:68–71

    Article  CAS  PubMed  Google Scholar 

  37. Maachi A, Nagata T, Silva JMF (2020) Date palm virus A: first plant virus found in date palm trees. Virus Genes 56:792–795

    Article  PubMed  CAS  Google Scholar 

  38. Park D, Zhang M, Hahn Y (2019) Novel Foveavirus (the family Betaflexiviridae) species identified in ginseng (Panax ginseng). Acta Virol 63:155–161

    Article  CAS  PubMed  Google Scholar 

  39. Park D, Goh C, Lee J, Sebastiani F, Hahn Y (2020) Identification of Pistacia-associated flexivirus 1, a putative mycovirus of the family Gammaflexiviridae, in the mastic tree (Pistacia lentiscus) transcriptome. Acta Virol 64:28–35

    Article  PubMed  CAS  Google Scholar 

  40. Sidharthan K, Kalaivanan N, Baranwal V (2021) Discovery of putative novel viruses in the transcriptomes of endangered plant species native to India and China. Gene 786:145626

    Article  CAS  PubMed  Google Scholar 

  41. Martelli GP, Adams MJ, Kreuze JF, Dolja VV (2007) Family Flexiviridae: a case study in virion and genome plasticity. Annu Rev Phytopathol 45:73–100

    Article  CAS  PubMed  Google Scholar 

  42. Nery FMB, Melo FL, Boiteux LS, Ribeiro SG, Resende RO et al (2020) Molecular characterization of Hovenia Dulcis-Associated Virus 1 (HDaV1) and 2 (HDaV2): new tentative species within the order Picornavirales. Viruses 12:950

    Article  CAS  PubMed Central  Google Scholar 

  43. Malandrakis E, Dadali O, Kavouras M, Danis T, Panagiotaki P et al (2017) Identification of the abiotic stress-related transcription in little Neptune grass Cymodocea nodosa with RNA-seq. Mar Genom 34:47–56

    Article  CAS  Google Scholar 

  44. Zinkgraf M, Gerttula S, Groover A (2017) Transcript profiling of a novel plant meristem, the monocot cambium. J Integr Plant Biol 59:436–449

    Article  CAS  PubMed  Google Scholar 

  45. Hua W, Kong W, Cao XY, Chen C, Liu Q, Li X, Wang Z (2017) Transcriptome analysis of Dioscorea zingiberensis identified genes involved in diosgenin biosynthesis. Genes Genomics 39:509–520

    Article  CAS  Google Scholar 

  46. Liu XF, Ma H, Li TQ, Li ZH, Wan YM, Liu XX et al (2018) Development of novel EST-SSR markers for Phyllanthus emblica (Phyllanthaceae) and cross-amplification in two related species. Appl Plant Sci. 6:e1169

    Article  Google Scholar 

  47. Amini H, Naghavi MR, Shen T, Wang Y, Nasiri J et al (2019) Tissue-specific transcriptome analysis reveals candidate genes for terpenoid and phenylpropanoid metabolism in the medicinal plant ferula assafoetida. G3. 9:807–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Gross SM, Martin JA, Simpson J, Abraham-Juarez MJ, Wang Z, Visel A (2013) De novo transcriptome assembly of drought tolerant CAM plants, Agave deserti and Agave tequilana. BMC Genomics 14:563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Liquin L, Bo S, Deng WJ, Wang Y, Wei Y et al (2019) Avocado fruit pulp transcriptomes in the after-ripening process. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 47:308–319

    Google Scholar 

  50. Ling LZ, Zhang S, Zhao F, Yang JL, Song WH et al (2017) Transcriptome-wide identification and prediction of miRNAs and their targets in Paris polyphylla var. yunnanensis by high-throughput sequencing analysis. Int J Mol Sci 18:E219

    Article  PubMed  CAS  Google Scholar 

  51. Zhang L, Xu P, Cai Y, Ma L, Zhang C, Gao Q et al (2017) The draft genome assembly of Rhododendron delavayi Franch. var. delavayi. Gigascience 6:1–11

    Article  PubMed  PubMed Central  Google Scholar 

  52. Laricchia KM, Johnson MG, Ragone D, Williams EW, Zerega NJ, Wickett NJ (2018) A transcriptome screen for positive selection in domesticated breadfruit and its wild relatives (Artocarpus spp.). Am J Bot 105:915–926

    Article  CAS  PubMed  Google Scholar 

  53. Kavas M, Kizildogan AK, Balik HI (2019) Gene expression analysis of bud burst process in European hazelnut (Corylus avellana L.) using RNA-Seq. Physiol Mol Biol Pla 25:13–29

    Article  CAS  Google Scholar 

  54. Fan ZP, Gao YK, Liu R, Wang XZ, Guo YC, Zhang QX (2020) The major gene and polygene effects of ornamental traits in bearded iris (Iris germanica) using joint segregation analysis. Scientia Hort 260:108882

    Article  CAS  Google Scholar 

  55. Torrens-Spence MP, Pluskal T, Li FS, Carballo V, Weng JK (2018) Complete pathway elucidation and heterologous reconstitution of Rhodiola salidroside biosynthesis. Mol Plant 11:205–217

    Article  CAS  PubMed  Google Scholar 

  56. Cegan R, Hudzieczek V, Hobza R (2017) De novo transcriptome assembly of heavy metal tolerant Silene dioica. Genom Data 11:118–119

    Article  PubMed  PubMed Central  Google Scholar 

  57. Diray-Arce J, Clement M, Gul B, Khan AM, Nielsen BL (2015) Transcriptome assembly, profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance. BMC Genom 16:353

    Article  CAS  Google Scholar 

  58. Zhang S, Liu Q, Lyu C, Chen J, Xiao R, Chen J, Yang Y, Zhang H, Hou K, Wu W (2020) Characterizing glycosyltransferases by a combination of sequencing platforms applied to the leaf tissues of Stevia rebaudiana. BMC Genom 21:794

    Article  CAS  Google Scholar 

  59. Feng G, Huang S, Liu Y, Xiao F, Liu J et al (2018) The transcriptome analyses of Tagetes erecta provides novel insights into secondary metabolite biosynthesis during flower development. Gene 660:18–27

    Article  CAS  PubMed  Google Scholar 

  60. Piñeiro-Fernández L, Byers KJ, Cai J, Sedeek KE, Kellenberger RT, Russo A et al (2019) A phylogenomic analysis of the floral transcriptomes of sexually deceptive and rewarding European orchids, Ophrys and Gymnadenia. Front Plant Sci 10:1553

    Article  PubMed  PubMed Central  Google Scholar 

  61. Kado T, Innan H (2018) Horizontal gene transfer in five parasite plant species in Orobanchaceae. Genome Biol Evol 10:3196–3210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Karinho-Betancourt E, Hernández-Soto P, Rendón-Anaya M, Calderón-Cortés N, Oyama K (2019) Differential expression of genes associated with phenolic compounds in galls of Quercus castanea induced by Amphibolips michoacaensis. J Plant Interact 14:177–186

    Article  CAS  Google Scholar 

  63. Zhang H, Wei L, Miao H, Zhang T, Wang C (2012) Development and validation of genic-SSR markers in sesame by RNA-seq. BMC Genom 13:316

    Article  CAS  Google Scholar 

  64. Yang H, Zhou C, Li G, Wang J, Gao P et al (2019) RNA data from multiple tissues of Davidia involucrate. Sci Data. 6:181

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Voutsina N, Payne AC, Hancock RD, Clarkson GJJ, Rothwell SD (2016) Characterization of the watercress (Nasturtium officinale R. Br; Brassicaceae) transcriptome using RNASeq and identification of candidate genes for important phytonutrient traits linked to human health. BMC Genom 17:378

    Article  CAS  Google Scholar 

  66. Pluskal T, Torrens-Spence MP, Fallon TR, De Abreu A, Shi CH, Weng J-K (2019) The biosynthetic origin of psychoactive kavalactones in kava. Nat Plants 5:867–878

    Article  PubMed  Google Scholar 

  67. Wang Y, Wang X, Wang C, Wang R, Peng F, Xiao X, Zeng J, Fan X, Kang H, Sha L, Zhang H, Zhou Y (2016) Proteomic profiling of the interactions of Cd/Zn in the roots of dwarf polish wheat (Triticum polonicum L.). Front Plant Sci 7:1378

    PubMed  PubMed Central  Google Scholar 

  68. Zinkgraf M, Zhao S, Canning C, Gerttula S, Lu M et al (2020) Evolutionary network genomics of wood formation in a phylogenetic survey of angiosperm forest trees. New Phytol 228:1811–1823

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to express our sincere gratitude to the authors of the primary data used for this work, who are cited in Table 1. By following open access practices and supporting accessible raw sequence data in public repositories available to the research community, they have promoted the generation of new knowledge and ideas. We also thank the editor, whose valuable and insightful comments helped to improve this manuscript.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Instituto de Patología Vegetal, Centro de Investigaciones Agropecuarias, Instituto Nacional de Tecnología Agropecuaria (IPAVE-CIAP-INTA), Camino 60 Cuadras Km 5,5 (X5020ICA), Córdoba, Argentina

    Nicolás Bejerman & Humberto Debat

  2. Consejo Nacional de Investigaciones Científicas y Técnicas. Unidad de Fitopatología y Modelización Agrícola, Camino 60 Cuadras Km 5,5 (X5020ICA), Córdoba, Argentina

    Nicolás Bejerman & Humberto Debat

Authors
  1. Nicolás Bejerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Humberto Debat
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Nicolás Bejerman.

Ethics declarations

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.

Additional information

Handling Editor: Sead Sabanadzovic.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 816 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bejerman, N., Debat, H. Exploring the tymovirales landscape through metatranscriptomics data. Arch Virol 167, 1785–1803 (2022). https://doi.org/10.1007/s00705-022-05493-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-022-05493-9

Search

Navigation