Skip to main content
SpringerLink
Log in

Isolation and characterization of a novel cripavirus, the first Dicistroviridae family member infecting the cotton mealybug Phenacoccus solenopsis

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

Abstract

A new virus belonging to the family Dicistroviridae was identified in the hibiscus-infesting cotton mealybug Phenacoccus solenopsis. Using high-throughput sequencing (HTS) on an Illumina HiSeq platform, a single contig of the complete genome sequence was assembled. The authenticity of the sequence obtained by HTS was validated by RT-PCR and Sanger sequencing of the amplicons, which was also employed for the 3’ untranslated region (UTR). The 5’ UTR was sequenced using a rapid amplification of cDNA ends kit. A large segment encompassing the whole genome was amplified by RT-PCR using viral RNA extracted from mealybugs. A whole-genome nucleotide sequence comparison showed 89% sequence identity to aphid lethal paralysis virus (ALPV), covering a short segment of 44 bp. Pairwise amino acid sequence comparisons of the protein encoded by open reading frame (ORF) 2 with its counterparts in the GenBank database, showed less than 40% identity to several members of the genus Cripavirus, including ALPV. Phylogenetic analysis based on the deduced amino acid sequence of the ORF 2 protein showed that the new virus grouped with members of the genus Cripavirus. The intergenic region (IGR) internal ribosome entry site (IRES) showed the conserved nucleotides of a type I IGR IRES and had two bulge sites, three pseudoknots, and two stem-loops. Virus morphology visualized by transmission electron microscopy demonstrated spherical particles with a diameter of ~30 nm. This virus was the only arthropod virus identified in the sampled mealybugs, and the purified virus was able to infect cotton mealybugs. To the best of our knowledge, this is the first report of a Dicistroviridae family member infecting P. solenopsis, and we have tentatively named this virus Phenacoccus solenopsis virus (PhSoV).

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

Similar content being viewed by others

Availability of data

All data generated or analyzed during this study are included in this published article.

References

  1. Bonning BC, Miller WA (2010) Dicistroviruses. Annu Rev Entomol 55:129–150

    Article  CAS  PubMed  Google Scholar 

  2. Valles S, Chen Y, Firth A, Guérin DA, Hashimoto Y, Herrero S, de Miranda J, Ryabov E, Consortium IR (2017) ICTV virus taxonomy profile: Dicistroviridae. J Gen Virol 98(3):355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Chen YP, Pettis JS, Corona M, Chen WP, Li CJ, Spivak M, Visscher PK, DeGrandi-Hoffman G, Boncristiani H, Zhao Y (2014) Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLoS Pathog 10(7):e1004261

    Article  PubMed  PubMed Central  Google Scholar 

  4. Gildow F, d’Arcy C (1988) Barley and oats as reservoirs for an aphid virus and the influence on barley yellow dwarf virus transmission. Phytopathology 78(6):811–816

    Article  Google Scholar 

  5. Reinganum C, O’Loughlin G, Hogan T (1970) A nonoccluded virus of the field crickets Teleogryllus oceanicus and T. commodus (Orthoptera: Gryllidae). Journal of Invertebrate Pathology 16(2):214–220

    Article  Google Scholar 

  6. Spodek M, Ben-Dov Y, Mondaca L, Protasov A, Erel E, Mendel Z (2018) The cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) in Israel: pest status, host plants and natural enemies. Phytoparasitica 46(1):45–55

    Article  Google Scholar 

  7. Saeed S, Ahmad M, Ahmad M, Kwon YJ (2007) Insecticidal control of the mealybug Phenacoccus gossypiphilous (Hemiptera: Pseudococcidae), a new pest of cotton in Pakistan. Entomol Res 37(2):76–80

    Article  Google Scholar 

  8. Saddiq B, Shad SA, Aslam M, Ijaz M, Abbas N (2015) Monitoring resistance of Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) to new chemical insecticides in Punjab, Pakistan. Crop Protection 74:24–29

    Article  CAS  Google Scholar 

  9. Saddiq B, Shad SA, Khan HAA, Aslam M, Ejaz M, Afzal MBS (2014) Resistance in the mealybug Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) in Pakistan to selected organophosphate and pyrethroid insecticides. Crop Protect 66:29–33

    Article  CAS  Google Scholar 

  10. Zhang P-J, Huang F, Zhang J-M, Wei J-N, Lu Y-B (2015) The mealybug Phenacoccus solenopsis suppresses plant defense responses by manipulating JA-SA crosstalk. Sci Rep 5:9354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Das U, Islam MS (2019) A review study on different plants in malvaceae family and their medicinal uses. Am J Biomed Sci Res 3(2):94–97

    Article  Google Scholar 

  12. Kapadia GJ (2003) Medicinal plants of the world. In: Ross IA (ed) Volume I: chemical constituents, traditional and modern uses. ACS Publications, Humana Press, Totawa

    Google Scholar 

  13. Calatayud P-A, Le Rü B (2006) Cassava and mealybugs. In: Cassava-Mealybug interactions. IRD Éditions, Marseille. https://doi.org/10.4000/books.irdeditions.9875

    Chapter  Google Scholar 

  14. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29(7):644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Coordinators NR (2017) Database resources of the national center for biotechnology information. Nucleic Acids Res 45(Database issue):D12

    Google Scholar 

  16. Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12(1):59

    Article  CAS  PubMed  Google Scholar 

  17. Zheng Y, Gao S, Padmanabhan C, Li R, Galvez M, Gutierrez D, Fuentes S, Ling K-S, Kreuze J, Fei Z (2017) VirusDetect: an automated pipeline for efficient virus discovery using deep sequencing of small RNAs. Virology 500:130–138

    Article  CAS  PubMed  Google Scholar 

  18. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321

    Article  CAS  PubMed  Google Scholar 

  20. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PloS One 9(9):1–8

    Article  Google Scholar 

  21. Luria N, Reingold V, Lachman O, Dombrovsky A (2013) Full-genome sequence of hibiscus chlorotic ringspot virus from Israel. Genome Announc 1(6):e01050–e01053

    Article  PubMed  PubMed Central  Google Scholar 

  22. Jan E (2006) Divergent IRES elements in invertebrates. Virus Res 119(1):16–28

    Article  CAS  PubMed  Google Scholar 

  23. van Rij RP, Andino R (2006) The silent treatment: RNAi as a defense against virus infection in mammals. Trends Biotechnol 24(4):186–193

    Article  PubMed  Google Scholar 

  24. Nayak A, Berry B, Tassetto M, Kunitomi M, Acevedo A, Deng C, Krutchinsky A, Gross J, Antoniewski C, Andino R (2010) Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nat Struct Mol Biol 17(5):547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. St Johnston D, Brown NH, Gall JG, Jantsch M (1992) A conserved double-stranded RNA-binding domain. Proc Natl Acad Sci 89(22):10979–10983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hahn H, Palmenberg AC (1996) Mutational analysis of the encephalomyocarditis virus primary cleavage. J Virol 70(10):6870–6875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Scotti PD, Christian PD (2008) Small RNA viruses of invertebrates. In: Capinera JL (ed) Encyclopedia of entomology. Springer Netherlands, Dordrecht, pp 3422–3426. https://doi.org/10.1007/978-1-4020-6359-6_4235

    Chapter  Google Scholar 

  28. Kanamori Y, Nakashima N (2001) A tertiary structure model of the internal ribosome entry site (IRES) for methionine-independent initiation of translation. Rna 7(2):266–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nakashima N, Uchiumi T (2009) Functional analysis of structural motifs in dicistroviruses. Virus Res 139(2):137–147

    Article  CAS  PubMed  Google Scholar 

  30. Pfingsten JS, Castile AE, Kieft JS (2010) Mechanistic role of structurally dynamic regions in Dicistroviridae IGR IRESs. J Mol Biol 395(1):205–217

    Article  CAS  PubMed  Google Scholar 

  31. Ren Q, Au HH, Wang QS, Lee S, Jan E (2014) Structural determinants of an internal ribosome entry site that direct translational reading frame selection. Nucleic Acids Res 42(14):9366–9382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Shin YC, Bischof GF, Lauer WA, Desrosiers RC (2015) Importance of codon usage for the temporal regulation of viral gene expression. Proc Natl Acad Sci 112(45):14030–14035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Velazquez-Salinas L, Zarate S, Eschbaumer M, Lobo FP, Gladue DP, Arzt J, Novella IS, Rodriguez LL (2016) Selective factors associated with the evolution of codon usage in natural populations of arboviruses. PloS One 11(7):1–17

    Article  Google Scholar 

  34. Zhou Z, Dang Y, Zhou M, Li L, Yu C-h, Fu J, Chen S, Liu Y (2016) Codon usage is an important determinant of gene expression levels largely through its effects on transcription. Proc Natl Acad Sci 113(41):E6117–E6125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Förstemann K, Horwich MD, Wee L, Tomari Y, Zamore PD (2007) Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 130(2):287–297

    Article  PubMed  PubMed Central  Google Scholar 

  36. Podgwaite J, Mazzone H (1986) Latency of insect viruses. Adv Virus Res 31:293–320

    Article  CAS  PubMed  Google Scholar 

  37. Dombrovsky A, Luria N (2013) The Nerium oleander aphid Aphis nerii is tolerant to a local isolate of Aphid lethal paralysis virus (ALPV). Virus Genes 46(2):354–361

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

For A.D from the Israeli Agriculture chief scientist and Ministry of Economy and Industry for the ‘Kendel project’ - Development of microbial control agents for agriculture industry (grand number: 20-13-0027).

Author information

Authors and Affiliations

  1. Department of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion, 7505101, Israel

    Neta Luria, Elisheva Smith, Oded Lachman, Noa Sela & Aviv Dombrovsky

  2. Israel Institute for Biological Research (IIBR), Ness-Ziona, 74100, Israel

    Orly Laskar

Authors
  1. Neta Luria
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisheva Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Oded Lachman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Orly Laskar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Noa Sela
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aviv Dombrovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N. L., experimental work and data analysis; E.S., data analysis and manuscript preparation; O.L., assistance in experimental work; N.S., bioinformatics and A.D. research design and supervising the project, data analysis and manuscript preparation.

Corresponding author

Correspondence to Aviv Dombrovsky.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: T. K. Frey.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (AB1 301 kb)

Supplementary material 2 (AB1 296 kb)

Supplementary material 3 (AB1 295 kb)

Supplementary material 4 (AB1 302 kb)

705_2020_4702_MOESM5_ESM.pdf

Hibiscus rosa-sinensis plants infested by cotton mealybugs (Phenacoccus solenopsis). (a, b) Hibiscus plants infested by cotton mealybugs. (c, d) Individual cotton mealybugs. (d) Hibiscus leaves infested with cotton mealybugs for inoculation studies (PDF 176 kb)

Supplementary material 6 (PDF 365 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luria, N., Smith, E., Lachman, O. et al. Isolation and characterization of a novel cripavirus, the first Dicistroviridae family member infecting the cotton mealybug Phenacoccus solenopsis. Arch Virol 165, 1987–1994 (2020). https://doi.org/10.1007/s00705-020-04702-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-020-04702-7

Search

Navigation