Skip to main content

Advertisement

SpringerLink
Log in

Characterization of siRNAs derived from cucumber mosaic virus in infected tobacco plants

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

This study characterized the viral small interfering RNAs (vsiRNAs) from Nicotiana tabacum cv. Samsun infected with a cucumber mosaic virus (CMV) 2b-deficient mutant. Most vsiRNAs were 21 -22 nucleotides in length and the 5′-terminal ends were dominated by A and U, respectively. The observed vsiRNAs were heterogeneously distributed throughout the CMV genome; however, most of the vsiRNAs were derived from sense strands, as opposed to antisense strands. These results demonstrate the conserved and specific function of Dicer-like (DCL), Argonaute (AGO) and RNA-dependent RNA polymerase (RDR) proteins in tobacco. Finally, it was revealed that vsiRNAs target abundant host genes, indicating complex roles for CMV vsiRNAs during the development of symptoms.

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

References

  1. Wang MB, Masuta C, Smith NA, Shimura H (2012) RNA silencing and plant viral diseases. Mol Plant Microbe Interact 25:1275–1285

    Article  CAS  PubMed  Google Scholar 

  2. Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130:413–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  CAS  PubMed  Google Scholar 

  4. Pattanayak D, Solanke AU, Kumar PA (2013) Plant RNA interference pathways: diversity in function, similarity in action. Plant Mol Biol Rep 31:493–506

    Article  CAS  Google Scholar 

  5. Ding SW (2010) RNA-based antiviral immunity. Nat Rev Immunol 10:632–644

    Article  CAS  PubMed  Google Scholar 

  6. Wang XB, Wu QF, Ito T, Cillo F, Li WX, Chen XM, Yu JL, Ding SW (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. PNAS 107:484–489

    Article  CAS  PubMed  Google Scholar 

  7. Sharma N, Sahu PP, Puranik S, Prasad M (2013) Recent Advances in plant-virus interaction with emphasis on small interfering RNAs (siRNAs). Mol Biotechnol 55:63–77

    Article  CAS  PubMed  Google Scholar 

  8. Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter—defence and counter-counter-defence. Nat Rev Microbiol 11:745–760

    Article  CAS  PubMed  Google Scholar 

  9. Burgyan J, Havelda Z (2011) Viral suppressors of RNA silencing. Trends Plant Sci 16:265–272

    Article  CAS  PubMed  Google Scholar 

  10. Smith NA, Eamens AL, Wang MB (2011) Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PloS Pathog 7:e1002022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Shimura H, Pantaleo V, Ishihara T, Myojo N, Inaba J, Sueda K, Burgyan J, Masuta C (2011) A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. Plos Pathog 7:e1002021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Shi B, Lin L, Wang S, Guo Q, Zhou H, Rong L, Li J, Peng J, Lu Y, Zheng H, Yang Y, Chen Z, Zhao J, Jiang T, Song B, Chen J, Yan F (2016) Identification and regulation of host genes related to Rice stripe virus symptom production. New Phytol 209:1106–1119

    Article  CAS  PubMed  Google Scholar 

  13. Hadidi A, Flores R, Candresse T, Barba M (2016) Next-generation sequencing and genome editing in plant virology. Front Microbiol 7:1325

    Article  PubMed  PubMed Central  Google Scholar 

  14. Palukaitis P, Garcia-Arenal F (2003) Cucumoviruses. Adv Virus Res 62:241–323

    Article  CAS  PubMed  Google Scholar 

  15. Mochizuki T, Ohki ST (2012) Cucumber mosaic virus: viral genes as virulence determinants. Mol Plant Pathol 13:217–225

    Article  CAS  PubMed  Google Scholar 

  16. Csorba T, Kontra L, Burgyan J (2015) viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence. Virology 479:85–103

    Article  PubMed  Google Scholar 

  17. Mochizuki T, Yamazaki R, Wada T, Ohki ST (2014) Coat protein mutations in an attenuated Cucumber mosaic virus encoding mutant 2b protein that lacks RNA silencing suppressor activity induces chlorosis with photosynthesis gene repression and chloroplast abnormalities in infected tobacco plants. Virology 456:292–299

    Article  PubMed  Google Scholar 

  18. Du ZY, Chen FF, Liao OS, Zhang HR, Cheni YF, Chen JS (2007) 2b ORFs encoded by subgroup IB strains of cucumber mosaic virus induce differential virulence on Nicotiana species. J Gen Virol 88:2596–2604

    Article  CAS  PubMed  Google Scholar 

  19. Axtell MJ (2014) Butter: High-precision genomic alignment of small RNA-seq data. BioRxiv.doi:10.1101/007427

    Google Scholar 

  20. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lin KY, Cheng CP, Chang BC, Wang WC, Huang YW, Lee YS, Huang HD, Hsu YH, Lin NS (2010) Global analyses of small interfering RNAs derived from Bamboo mosaic virus and its associated satellite RNAs in different plants. PLoS One 5:e11928

    Article  PubMed  PubMed Central  Google Scholar 

  22. Margaria P, Miozzi L, Ciuffo M, Rosa C, Axtell MJ, Pappu HR, Turina M (2016) Comparison of small RNA profiles in Nicotiana benthamiana and Solanum lycopersicum infected by polygonum ringspot tospovirus reveals host-specific responses to viral infection. Virus Res 211:38–45

    Article  CAS  PubMed  Google Scholar 

  23. Yan F, Zhang H, Adams MJ, Yang J, Peng J, Antoniw JF, Zhou Y, Chen J (2010) Characterization of siRNAs derived from rice stripe virus in infected rice plants by deep sequencing. Arch Virol 155:935–940

    Article  CAS  Google Scholar 

  24. Li Y, Deng C, Shang Q, Zhao X, Liu X, Zhou Q (2016) Characterization of siRNAs derived from cucumber green mottle mosaic virus in infected cucumber plants. Arch Virol 161:455–458

    Article  CAS  PubMed  Google Scholar 

  25. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896

    Article  CAS  PubMed  Google Scholar 

  26. Wassenegger M, Krczal G (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci 11:142–151

    Article  CAS  PubMed  Google Scholar 

  27. Seo JK, Wu JG, Lii YF, Li Y, Jin HL (2013) Contribution of small RNA pathway components in plant immunity. Mol Plant Microbe Interact 26:617–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wang XB, Jovel J, Udomporn P, Wang Y, Wu QF, Li WX, Gasciolli V, Vaucheret H, Ding SW (2011) The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23:1625–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Margaria P, Miozzi L, Rosa C, Axtell MJ, Pappu HR, Turina M (2015) Small RNA profiles of wild-type and silencing suppressor-deficient tomato spotted wilt virus infected Nicotiana benthamiana. Virus Res 208:30–38

    Article  CAS  PubMed  Google Scholar 

  30. Xu Y, Huang L, Fu S, Wu J, Zhou X (2012) Population diversity of rice stripe virus-derived siRNAs in three different hosts and RNAi-based antiviral immunity in Laodelphgax striatellus. PLoS One 7:e46238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5’ terminal nucleotide. Cell 133:116–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ogwok E, Ilyas M, Alicai T, Rey ME, Taylor NJ (2016) Comparative analysis of virus-derived small RNAs within cassava (Manihot esculenta Crantz) infected with cassava brown streak viruses. Virus Res 215:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Donaire L, Wang Y, Gonzalez-Ibeas D, Mayer KF, Aranda MA, Llave C (2009) Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392:203–214

    Article  CAS  PubMed  Google Scholar 

  34. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucl Acids Res 32:277–280

    Article  Google Scholar 

  36. Lu J, Du ZX, Kong J, Chen LN, Qiu YH, Li GF, Meng XH, Zhu SF (2012) Transcriptome analysis of Nicotiana tabacum infected by cucumber mosaic virus during systemic symptom development. PloS One 7:e43447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program (2016YFC1200600).

Author information

Authors and Affiliations

  1. Institute of Plant Quarantine, Chinese Academy of Inspection and Quarantine, Ronghua South Street No. 11, Beijing, 100176, People’s Republic of China

    Yanhong Qiu, Yongjiang Zhang & Shuifang Zhu

  2. China Agricultural University, Yuanmingyuan West Street No. 2, Beijing, 100129, People’s Republic of China

    Fan Hu

Authors
  1. Yanhong Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongjiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fan Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuifang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shuifang Zhu.

Ethics declarations

Funding

This work was supported by the National Key Research and Development Program (2016YFC1200600).

Conflict of interest

The 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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qiu, Y., Zhang, Y., Hu, F. et al. Characterization of siRNAs derived from cucumber mosaic virus in infected tobacco plants. Arch Virol 162, 2077–2082 (2017). https://doi.org/10.1007/s00705-017-3335-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3335-z

Keywords

Search

Navigation