1887

Journal of General Virology header logo

Volume 102, Issue 11

Novel circular DNA virus identified in () that codes for proteins with similarity to those of geminiviruses No Access

Abstract

Viral metagenomic studies have enabled the discovery of many unknown viruses and revealed that viral communities are much more diverse and ubiquitous than previously thought. Some viruses have multiple genome components that are encapsidated either in separate virions (multipartite viruses) or in the same virion (segmented viruses). In this study, we identify what is possibly a novel bipartite plant-associated circular single-stranded DNA virus in a wild prickly pear cactus, , that is endemic to the Chaco ecoregion in South America. Two ~1.8 kb virus-like circular DNA components were recovered, one encoding a replication-associated protein (Rep) and the other a capsid protein (CP). Both of the inferred protein sequences of the Rep and CP are homologous to those encoded by members of the family . These two putatively cognate components each have a nonanucleotide sequence within a likely hairpin structure that is homologous to the origins of rolling-circle replication (RCR), found in diverse circular single-stranded DNA viruses. In addition, the two components share similar putative replication-associated iterative sequences (iterons), which in circular single-stranded DNA viruses are important for Rep binding during the initiation of RCR. Such molecular features provide support for the possible bipartite nature of this virus, which we named utkilio virus (common name of the in South America) components A and B. In the infectivity assays conducted in plants, only the A component of utkilio virus, which encodes the Rep protein, was found to move and replicate systemically in . This was not true for component B, for which we did not detect replication, which may have been due to this being a defective molecule or because of the model plants () used for the infection assays. Future experiments need to be conducted with other plants, including , to understand more about the biology of these viral components.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Cressdnaviricota , Opuntia and ssDNA virus
© 2021 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001671
2021-11-02
2024-04-25
Loading full text...

Full text loading...

References

  1. Briddon RW, Martin DP, Roumagnac P, Navas-Castillo J, Fiallo-Olivé E et al. Alphasatellitidae: A new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Arch Virol 2018; 163:2587–2600 [View Article] [PubMed]
     [Google Scholar]
  2. Fiallo-Olive E, Tovar R, Navas-Castillo J. Deciphering the biology of deltasatellites from the New World: maintenance by New World begomoviruses and whitefly transmission. New Phytol 2016; 212:680–692 [View Article] [PubMed]
     [Google Scholar]
  3. Gnanasekaran P, KishoreKumar R, Bhattacharyya D, Vinoth Kumar R, Chakraborty S. Multifaceted role of geminivirus associated betasatellite in pathogenesis. Mol Plant Pathol 2019; 20:1019–1033 [View Article] [PubMed]
     [Google Scholar]
  4. Adams MJ, Lefkowitz EJ, King AMQ, Harrach B, Harrison RL et al. Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Arch Virol 2017; 162:2505–2538 [View Article] [PubMed]
     [Google Scholar]
  5. Gronenborn B, Randles JW, Knierim D, Barrière Q, Vetten HJ et al. Analysis of DNAs associated with coconut foliar decay disease implicates a unique single-stranded dna virus representing a new taxon. Sci Rep 2018; 8:5698 [View Article] [PubMed]
     [Google Scholar]
  6. Li P, Wang S, Zhang L, Qiu D, Zhou X et al. A tripartite ssDNA mycovirus from a plant pathogenic fungus is infectious as cloned DNA and purified virions. Sci Adv 2020; 6:eaay9634 [View Article]
     [Google Scholar]
  7. Varsani A, Krupovic M. Sequence-based taxonomic framework for the classification of uncultured single-stranded DNA viruses of the family Genomoviridae. Virus Evol 2017; 3:vew037 [View Article] [PubMed]
     [Google Scholar]
  8. Krupovic M, Varsani A, Kazlauskas D, Breitbart M, Delwart E et al. Cressdnaviricota: a virus phylum unifying seven families of rep-encoding viruses with single-stranded, circular DNA genomes. J Virol 2020; 94:e00582–20 [View Article]
     [Google Scholar]
  9. Kraberger S, Cook CN, Schmidlin K, Fontenele RS, Bautista J et al. Diverse single-stranded DNA viruses associated with honey bees (Apis mellifera). Infect Genet Evol 2019; 71:179–188 [View Article] [PubMed]
     [Google Scholar]
  10. Male MF, Kraberger S, Stainton D, Kami V, Varsani A. Cycloviruses, gemycircularviruses and other novel replication-associated protein encoding circular viruses in Pacific flying fox (Pteropus tonganus) faeces. Infect Genet Evol 2016; 39:279–292 [View Article] [PubMed]
     [Google Scholar]
  11. Doyle JJ, Doyle JL. Isolation ofplant DNA from fresh tissue. Focus 1990; 12:39–40
     [Google Scholar]
  12. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  13. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  14. O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 2016; 44:D733–45 [View Article] [PubMed]
     [Google Scholar]
  15. Letunic I, Doerks T, Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 2012; 40:D302–305 [View Article] [PubMed]
     [Google Scholar]
  16. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  17. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164–1165 [View Article] [PubMed]
     [Google Scholar]
  18. Stover BC, Muller KF. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 2010; 11:7 [View Article] [PubMed]
     [Google Scholar]
  19. Ferro MMM, Ramos-Sobrinho R, Xavier CAD, Zerbini FM, Lima GSA et al. New approach for the construction of infectious clones of a circular DNA plant virus using Gibson Assembly. J Virol Methods 2019; 263:20–23 [View Article] [PubMed]
     [Google Scholar]
  20. Fontenele RS, Salywon AM, Majure LC, Cobb IN, Bhaskara A et al. New world cactaceae plants harbor diverse geminiviruses. Viruses 2021; 13:
     [Google Scholar]
  21. Claverie S, Bernardo P, Kraberger S, Hartnady P, Lefeuvre P et al. From spatial metagenomics to molecular characterization of plant viruses: a geminivirus case study. Adv Virus Res 2018; 101:55–83 [View Article] [PubMed]
     [Google Scholar]
  22. Hehnle S, Wege C, Jeske H. Interaction of DNA with the movement proteins of geminiviruses revisited. J Virol 2004; 78:7698–7706 [View Article] [PubMed]
     [Google Scholar]
  23. Boulton MI. Functions and interactions of mastrevirus gene products. Physiol Mol Plant Pathol 2002; 60:243–255 [View Article]
     [Google Scholar]
  24. Bernardo P, Golden M, Akram M, Naimuddin N, Nadarajan N et al. Identification and characterisation of a highly divergent geminivirus: evolutionary and taxonomic implications. Virus Res 2013; 177:35–45 [View Article] [PubMed]
     [Google Scholar]
  25. Van Wezel R, Liu H, Wu Z, Stanley J, Hong Y. Contribution of the zinc finger to zinc and DNA binding by a suppressor of posttranscriptional gene silencing. J Virol 2003; 77:696–700 [View Article] [PubMed]
     [Google Scholar]
  26. van WR, Dong X, Liu H, Tien P, Stanley J et al. Mutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression. Mol Plant Microbe Interact 2002; 15:203–208 [View Article] [PubMed]
     [Google Scholar]
  27. Jeske H, Lutgemeier M, Preiss W. DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J 2001; 20:6158–6167 [View Article] [PubMed]
     [Google Scholar]
  28. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 2013; 11:777–788 [View Article] [PubMed]
     [Google Scholar]
  29. Arguello-Astorga GR, Ruiz-Medrano R. An iteron-related domain is associated to Motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach. Arch Virol 2001; 146:1465–1485 [View Article] [PubMed]
     [Google Scholar]
  30. Koonin EV. A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication. Nucleic Acids Res 1993; 21:2541–2547 [View Article] [PubMed]
     [Google Scholar]
  31. Koonin EV, Ilyina TV. Computer-assisted dissection of rolling circle DNA replication. Biosystems 1993; 30:241–268 [View Article] [PubMed]
     [Google Scholar]
  32. Gorbalenya AE, Koonin EV. Helicases: amino acid sequence comparisons and structure-function relationships. Curr Opin Struct Bio 1993; 3:419–429 [View Article]
     [Google Scholar]
  33. Gorbalenya AE, Koonin EV, Wolf YI. A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett 1990; 262:145–148 [View Article] [PubMed]
     [Google Scholar]
  34. Nash TE, Dallas MB, Reyes MI, Buhrman GK, Ascencio-Ibañez JT et al. Functional analysis of a novel motif conserved across Geminivirus rep proteins. J Virol 2011; 85:1182–1192 [View Article] [PubMed]
     [Google Scholar]
  35. Hasanvand V, Heydanejad J, Massumi H, Kleinow T, Jeske H et al. Isolation and characterization of a novel geminivirus from parsley. Virus Res 2020; 286:198056 [View Article] [PubMed]
     [Google Scholar]
  36. Roumagnac P, Varsani A, Martin DP, Lett J-. M. Approved Proposals - Plant Viruses; 2020 https://talk.ictvonline.org/files/ictv_official_taxonomy_updates_since_the_8th_report/m/plant-official/11081 accessed h 1 Mar 21
  37. Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM et al. Changes to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021). Arch Virol 2021; 166:2633–2648 [View Article] [PubMed]
     [Google Scholar]
  38. Chakraborty S, Pandey PK, Banerjee MK, Kalloo G, Fauquet CM. Tomato leaf curl Gujarat virus, a New Begomovirus Species Causing a Severe Leaf Curl Disease of Tomato in Varanasi, India. Phytopathology 2003; 93:1485–1495 [View Article] [PubMed]
     [Google Scholar]
  39. Galvao RM, Mariano AC, Luz DF, Alfenas PF, Andrade EC et al. A naturally occurring recombinant DNA-A of a typical bipartite begomovirus does not require the cognate DNA-B to infect Nicotiana benthamiana systemically. J Gen Virol 2003; 84:715–726 [View Article] [PubMed]
     [Google Scholar]
  40. Evans D, Jeske H. DNA B facilitates, but is not essential for, the spread of abutilon mosaic virus in agroinoculated Nicotiana benthamiana. Virology 1993; 194:752–757 [View Article] [PubMed]
     [Google Scholar]
  41. Hou Y-M, Paplomatas EJ, Gilbertson RL. Host adaptation and replication properties of two bipartite geminiviruses and their pseudorecombinants. MPMI 1998; 11:208–217 [View Article]
     [Google Scholar]
  42. Klinkenberg FA, Stanley J. Encapsidation and spread of African cassava mosaic virus DNA A in the absence of DNA B when agroinoculated to Nicotiana benthamiana. J Gen Virol 1990; 71:1409–1412 [View Article]
     [Google Scholar]
  43. Weigel K, Pohl JO, Wege C, Jeske H. A population genetics perspective on geminivirus infection. J Virol 2015; 89:11926–11934 [View Article] [PubMed]
     [Google Scholar]
  44. Saunders K, Salim N, Mali VR, Malathi VG, Briddon R et al. Characterisation of Sri Lankan cassava mosaic virus and Indian cassava mosaic virus: evidence for acquisition of a DNA B component by a monopartite begomovirus. Virology 2002; 293:63–74 [View Article] [PubMed]
     [Google Scholar]
  45. Rochester DE, Kositratana W, Beachy RN. Systemic movement and symptom production following agroinoculation with a single DNA of tomato yellow leaf curl geminivirus (Thailand). Virology 1990; 178:520–526 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001671
Loading
Novel circular DNA virus identified in Opuntia discolor (Cactaceae) that codes for proteins with similarity to those of geminiviruses
J. Gen. Virol. 102, 001671 (2021); https://doi.org/10.1099/jgv.0.001671
/content/journal/jgv/10.1099/jgv.0.001671
/content/journal/jgv/10.1099/jgv.0.001671
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error