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Front Plant Sci. 2015 Apr 24;6:281. doi: 10.3389/fpls.2015.00281. eCollection 2015.

Satellite RNAs interfere with the function of viral RNA silencing suppressors.

Frontiers in plant science

Wan-Xia Shen, Phil Chi Khang Au, Bu-Jun Shi, Neil A Smith, Elizabeth S Dennis, Hui-Shan Guo, Chang-Yong Zhou, Ming-Bo Wang

Affiliations

  1. National Citrus Engineering Research Center, Citrus Research Institute, Southwest University Chongqing, China ; Commonwealth Scientific and Industrial Research Organisation Plant Industry Canberra, ACT, Australia.
  2. Commonwealth Scientific and Industrial Research Organisation Plant Industry Canberra, ACT, Australia.
  3. Department of Plant Science, Waite Institute, Adelaide University Glen Osmond, SA, Australia.
  4. State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences Beijing, China.
  5. National Citrus Engineering Research Center, Citrus Research Institute, Southwest University Chongqing, China.

PMID: 25964791 PMCID: PMC4408847 DOI: 10.3389/fpls.2015.00281

Abstract

Viral satellite RNAs (satRNAs) are small subviral RNAs and depend on the helper virus for replication and spread. satRNAs can attenuate helper virus-induced symptoms, the mechanism of which remains unclear. Here, we show that two virus-encoded suppressors of RNA silencing (VSRs), Cucumber mosaic virus (CMV) 2b and Tombusvirus P19, suppress hairpin RNA (hpRNA)-induced silencing of a β-glucuronidase (GUS) gene in Nicotiana benthamiana. This suppression can be overcome by CMV Y-satellite RNA (Y-Sat) via the Y-Sat-derived small interfering RNAs (siRNAs), which bind to the VSRs and displace the bound hpGUS-derived siRNAs. We also show that microRNA target gene expression in N. tabacum was elevated by CMV infection, presumably due to function of the 2b VSR, but this upregulation of microRNA target genes was reversed in the presence of Y-Sat. These results suggest that satRNA infection minimizes the effect of VSRs on host siRNA and microRNA-directed silencing. Our results suggest that the high abundance of satRNA-derived siRNAs contributes to symptom attenuation by binding helper virus-encoded VSRs, minimizing the capacity of the VSRs to bind host siRNA and miRNA and interfere with their function.

Keywords: RNA silencing; microRNA expression; satellite RNA; symptom attenuation; virus-encoded suppressor

References

  1. Plant Cell. 1989 Dec;1(12):1165-73 - PubMed
  2. Annu Rev Plant Biol. 2009;60:485-510 - PubMed
  3. Mol Plant Pathol. 2011 Aug;12(6):595-605 - PubMed
  4. J Virol. 2014 May;88(10):5228-41 - PubMed
  5. Plant J. 2012 Jan;69(1):104-15 - PubMed
  6. Nat Rev Microbiol. 2013 Nov;11(11):745-60 - PubMed
  7. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7470-4 - PubMed
  8. Cell Host Microbe. 2008 Oct 16;4(4):387-97 - PubMed
  9. Cell. 2009 Feb 20;136(4):669-87 - PubMed
  10. J Virol. 2005 Jan;79(1):450-7 - PubMed
  11. Biosci Biotechnol Biochem. 2009 Jan;73(1):47-52 - PubMed
  12. FEBS Lett. 2009 Jan 5;583(1):101-6 - PubMed
  13. RNA. 2009 Apr;15(4):724-31 - PubMed
  14. Virology. 1981 Feb;109(1):120-6 - PubMed
  15. J Gen Virol. 1994 Nov;75 ( Pt 11):3185-91 - PubMed
  16. Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3275-80 - PubMed
  17. Mol Plant Microbe Interact. 2002 Jul;15(7):647-53 - PubMed
  18. Microbiol Rev. 1992 Jun;56(2):265-79 - PubMed
  19. Dev Cell. 2003 Feb;4(2):205-17 - PubMed
  20. Virology. 1982 Oct 15;122(1):147-57 - PubMed
  21. Plant Mol Biol. 2000 May;43(1):67-82 - PubMed
  22. Trends Biochem Sci. 2004 Jun;29(6):279-81 - PubMed
  23. Nat Struct Biol. 2001 Sep;8(9):746-50 - PubMed
  24. Biochim Biophys Acta. 2011 Nov-Dec;1809(11-12):601-12 - PubMed
  25. Annu Rev Phytopathol. 2004;42:415-37 - PubMed
  26. Genes Dev. 2004 May 15;18(10):1179-86 - PubMed
  27. Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14147-52 - PubMed
  28. Adv Virus Res. 1992;41:281-348 - PubMed
  29. Curr Top Microbiol Immunol. 1999;239:37-63 - PubMed
  30. Viruses. 2009 Dec;1(3):1325-50 - PubMed
  31. PLoS Pathog. 2011 May;7(5):e1002035 - PubMed
  32. Res Virol. 1995 Jan-Feb;146(1):61-7 - PubMed
  33. Plant J. 2007 Apr;50(2):240-52 - PubMed
  34. RNA. 2008 May;14 (5):903-13 - PubMed
  35. Plant Cell. 2012 Jan;24(1):259-74 - PubMed
  36. EMBO J. 1998 Nov 16;17(22):6739-46 - PubMed
  37. Cell. 2003 Dec 26;115(7):799-811 - PubMed
  38. Genes Dev. 2006 Dec 1;20(23):3255-68 - PubMed
  39. Mol Plant Microbe Interact. 2002 Sep;15(9):947-55 - PubMed
  40. Plant Biotechnol J. 2009 Dec;7(9):914-24 - PubMed
  41. PLoS Pathog. 2011 May;7(5):e1002021 - PubMed
  42. J Virol. 2006 Mar;80(6):3000-8 - PubMed
  43. EMBO J. 2006 Jun 21;25(12):2768-80 - PubMed
  44. RNA. 2012 Apr;18(4):771-82 - PubMed
  45. PLoS Pathog. 2011 May;7(5):e1002022 - PubMed
  46. RNA. 2001 Jan;7(1):16-28 - PubMed
  47. Virology. 1992 Feb;186(2):475-80 - PubMed
  48. J Virol Methods. 2002 Sep;105(2):343-8 - PubMed

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