1887

Abstract

HCPro, the RNA-silencing suppressor (RSS) of viruses belonging to the genus in the family , is a multifunctional protein presumably involved in all essential steps of the viral infection cycle. Recent studies have shown that plum pox potyvirus (PPV) HCPro can be replaced successfully by cucumber vein yellowing ipomovirus P1b, a sequence-unrelated RSS from a virus of the same family. In order to gain insight into the requirement of a particular RSS to establish a successful potyviral infection, we tested the ability of different heterologous RSSs from both plant- and animal-infecting viruses to substitute for HCPro. Making use of engineered PPV chimeras, we show that PPV HCPro can be replaced functionally by some, but not all, unrelated RSSs, including the NS1 protein of the mammal-infecting influenza A virus. Interestingly, the capacity of a particular RSS to replace HCPro does not correlate strictly with its RNA silencing-suppression strength. Altogether, our results suggest that not all suppression strategies are equally suitable for efficient escape of PPV from the RNA-silencing machinery. The approach followed here, based on using PPV chimeras in which an under-consideration RSS substitutes for HCPro, could further help to study the function of diverse RSSs in a ‘highly sensitive’ RNA-silencing context, such as that taking place in plant cells during the process of a viral infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.042168-0
2012-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/7/1601.html?itemId=/content/journal/jgv/10.1099/vir.0.042168-0&mimeType=html&fmt=ahah

References

  1. Ala-Poikela M., Goytia E., Haikonen T., Rajamäki M.-L., Valkonen J. P. T. 2011; Helper component proteinase of the genus Potyvirus is an interaction partner of translation initiation factors eIF(iso)4E and eIF4E and contains a 4E binding motif. J Virol 85:6784–6794 [View Article][PubMed]
    [Google Scholar]
  2. Ambros V., Chen X. M. 2007; The regulation of genes and genomes by small RNAs. Development 134:1635–1641 [View Article][PubMed]
    [Google Scholar]
  3. Anandalakshmi R., Pruss G. J., Ge X., Marathe R., Mallory A. C., Smith T. H., Vance V. B. 1998; A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95:13079–13084 [View Article][PubMed]
    [Google Scholar]
  4. Anandalakshmi R., Marathe R., Ge X., Herr J. M. Jr, Mau C., Mallory A., Pruss G., Bowman L., Vance V. B. 2000; A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290:142–144 [View Article][PubMed]
    [Google Scholar]
  5. Ballut L., Drucker M., Pugnière M., Cambon F., Blanc S., Roquet F., Candresse T., Schmid H. P., Nicolas P. other authors 2005; HcPro, a multifunctional protein encoded by a plant RNA virus, targets the 20S proteasome and affects its enzymic activities. J Gen Virol 86:2595–2603 [View Article][PubMed]
    [Google Scholar]
  6. Baulcombe D. 2005; RNA silencing. Trends Biochem Sci 30:290–293 [View Article][PubMed]
    [Google Scholar]
  7. Bennasser Y., Le S. Y., Benkirane M., Jeang K. T. 2005; Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity 22:607–619 [View Article][PubMed]
    [Google Scholar]
  8. Blanc S., López-Moya J. J., Wang R. Y., García-Lampasona S., Thornbury D. W., Pirone T. P. 1997; A specific interaction between coat protein and helper component correlates with aphid transmission of a potyvirus. Virology 231:141–147 [View Article][PubMed]
    [Google Scholar]
  9. Brigneti G., Voinnet O., Li W. X., Ji L. H., Ding S. W., Baulcombe D. C. 1998; Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana . EMBO J 17:6739–6746 [View Article][PubMed]
    [Google Scholar]
  10. Bucher E., Hemmes H., de Haan P., Goldbach R., Prins M. 2004; The influenza A virus NS1 protein binds small interfering RNAs and suppresses RNA silencing in plants. J Gen Virol 85:983–991 [View Article][PubMed]
    [Google Scholar]
  11. Burgyán J., Havelda Z. 2011; Viral suppressors of RNA silencing. Trends Plant Sci 16:265–272 [View Article][PubMed]
    [Google Scholar]
  12. Carbonell A., Dujovny G., García J. A., Valli A. 2012; The Cucumber vein yellowing virus silencing suppressor P1b can functionally replace HCPro in Plum pox virus infection in a host-specific manner. Mol Plant Microbe Interact 25:151–164 [View Article][PubMed]
    [Google Scholar]
  13. Carrington J. C., Cary S. M., Parks T. D., Dougherty W. G. 1989; A second proteinase encoded by a plant potyvirus genome. EMBO J 8:365–370[PubMed]
    [Google Scholar]
  14. Cheng Y. Q., Liu Z. M., Xu J., Zhou T., Wang M., Chen Y. T., Li H. F., Fan Z. F. 2008; HC-Pro protein of sugar cane mosaic virus interacts specifically with maize ferredoxin-5 in vitro and in planta . J Gen Virol 89:2046–2054 [View Article][PubMed]
    [Google Scholar]
  15. Choi I. R., Stenger D. C., French R. 2000; Multiple interactions among proteins encoded by the mite-transmitted wheat streak mosaic tritimovirus. Virology 267:185–198 [View Article][PubMed]
    [Google Scholar]
  16. Cuellar W. J., Kreuze J. F., Rajamäki M. L., Cruzado K. R., Untiveros M., Valkonen J. P. 2009; Elimination of antiviral defense by viral RNase III. Proc Natl Acad Sci U S A 106:10354–10358 [View Article][PubMed]
    [Google Scholar]
  17. Delgadillo M. O., Sáenz P., Salvador B., García J. A., Simón-Mateo C. 2004; Human influenza virus NS1 protein enhances viral pathogenicity and acts as an RNA silencing suppressor in plants. J Gen Virol 85:993–999 [View Article][PubMed]
    [Google Scholar]
  18. Dielen A. S., Sassaki F. T., Walter J., Michon T., Ménard G., Pagny G., Krause-Sakate R., Maia I. G., Badaoui S. other authors 2011; The 20S proteasome α5 subunit of Arabidopsis thaliana carries an RNase activity and interacts in planta with the Lettuce mosaic potyvirus HcPro protein. Mol Plant Pathol 12:137–150 [View Article][PubMed]
    [Google Scholar]
  19. Ding S. W. 2010; RNA-based antiviral immunity. Nat Rev Immunol 10:632–644 [View Article][PubMed]
    [Google Scholar]
  20. Ding S.-W., Li W.-X., Symons R. H. 1995; A novel naturally occurring hybrid gene encoded by a plant RNA virus facilitates long distance virus movement. EMBO J 14:5762–5772[PubMed]
    [Google Scholar]
  21. Dunoyer P., Voinnet O. 2005; The complex interplay between plant viruses and host RNA-silencing pathways. Curr Opin Plant Biol 8:415–423 [View Article][PubMed]
    [Google Scholar]
  22. Endres M. W., Gregory B. D., Gao Z., Foreman A. W., Mlotshwa S., Ge X., Pruss G. J., Ecker J. R., Bowman L. H., Vance V. 2010; Two plant viral suppressors of silencing require the ethylene-inducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog 6:e1000729 [View Article][PubMed]
    [Google Scholar]
  23. Garcia-Ruiz H., Takeda A., Chapman E. J., Sullivan C. M., Fahlgren N., Brempelis K. J., Carrington J. C. 2010; Arabidopsis RNA-dependent RNA polymerases and Dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22:481–496 [View Article][PubMed]
    [Google Scholar]
  24. Gazzani S., Lawrenson T., Woodward C., Headon D., Sablowski R. 2004; A link between mRNA turnover and RNA interference in Arabidopsis . Science 306:1046–1048 [View Article][PubMed]
    [Google Scholar]
  25. Giner A., Lakatos L., García-Chapa M., López-Moya J. J., Burgyán J. 2010; Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog 6:e1000996 [View Article][PubMed]
    [Google Scholar]
  26. Guo D. Y., Rajamäki M. L., Saarma M., Valkonen J. P. T. 2001; Towards a protein interaction map of potyviruses: protein interaction matrixes of two potyviruses based on the yeast two-hybrid system. J Gen Virol 82:935–939[PubMed]
    [Google Scholar]
  27. Guo D., Spetz C., Saarma M., Valkonen J. P. 2003; Two potato proteins, including a novel RING finger protein (HIP1), interact with the potyviral multifunctional protein HCpro. Mol Plant Microbe Interact 16:405–410 [View Article][PubMed]
    [Google Scholar]
  28. Haas G., Azevedo J., Moissiard G., Geldreich A., Himber C., Bureau M., Fukuhara T., Keller M., Voinnet O. 2008; Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J 27:2102–2112 [View Article][PubMed]
    [Google Scholar]
  29. Haasnoot J., de Vries W., Geutjes E. J., Prins M., de Haan P., Berkhout B. 2007; The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathog 3:e86 [View Article][PubMed]
    [Google Scholar]
  30. Havelda Z., Hornyik C., Crescenzi A., Burgyán J. 2003; In situ characterization of Cymbidium ringspot tombusvirus infection-induced posttranscriptional gene silencing in Nicotiana benthamiana . J Virol 77:6082–6086 [View Article][PubMed]
    [Google Scholar]
  31. Janssen D., Martín G., Velasco L., Gómez P., Segundo E., Ruiz L., Cuadrado I. M. 2005; Absence of a coding region for the helper component-proteinase in the genome of cucumber vein yellowing virus, a whitefly-transmitted member of the Potyviridae . Arch Virol 150:1439–1447 [View Article][PubMed]
    [Google Scholar]
  32. Jin Y. S., Ma D. Y., Dong J. L., Jin J. C., Li D. F., Deng C. W., Wang T. 2007a; HC-Pro protein of Potato virus Y can interact with three Arabidopsis 20S proteasome subunits in planta. J Virol 81:12881–12888 [View Article][PubMed]
    [Google Scholar]
  33. Jin Y. S., Ma D. Y., Dong J. L., Li D. F., Deng C. W., Jin J. C., Wang T. 2007b; The HC-pro protein of potato virus Y interacts with NtMinD of tobacco. Mol Plant Microbe Interact 20:1505–1511 [View Article][PubMed]
    [Google Scholar]
  34. Kasschau K. D., Carrington J. C. 1995; Requirement for HC-Pro processing during genome amplification of tobacco etch potyvirus. Virology 209:268–273 [View Article][PubMed]
    [Google Scholar]
  35. Kasschau K. D., Carrington J. C. 1998; A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95:461–470 [View Article][PubMed]
    [Google Scholar]
  36. Kasschau K. D., Carrington J. C. 2001; Long-distance movement and replication maintenance functions correlate with silencing suppression activity of potyviral HC-Pro. Virology 285:71–81 [View Article][PubMed]
    [Google Scholar]
  37. Kasschau K. D., Xie Z. X., Allen E., Llave C., Chapman E. J., Krizan K. A., Carrington J. C. 2003; P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217 [View Article][PubMed]
    [Google Scholar]
  38. Lakatos L., Csorba T., Pantaleo V., Chapman E. J., Carrington J. C., Liu Y. P., Dolja V. V., Calvino L. F., López-Moya J. J., Burgyán J. 2006; Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J 25:2768–2780 [View Article][PubMed]
    [Google Scholar]
  39. Lecellier C.-H., Dunoyer P., Arar K., Lehmann-Che J., Eyquem S., Himber C., Saïb A., Voinnet O. 2005; A cellular microRNA mediates antiviral defense in human cells. Science 308:557–560 [View Article][PubMed]
    [Google Scholar]
  40. Li W. X., Li H., Lu R., Li F., Dus M., Atkinson P., Brydon E. W., Johnson K. L., García-Sastre A. other authors 2004; Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc Natl Acad Sci U S A 101:1350–1355 [View Article][PubMed]
    [Google Scholar]
  41. Love A. J., Laird J., Holt J., Hamilton A. J., Sadanandom A., Milner J. J. 2007; Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. J Gen Virol 88:3439–3444 [View Article][PubMed]
    [Google Scholar]
  42. Maia I. G., Haenni A.-L., Bernardi F. 1996; Potyviral HC-Pro: a multifunctional protein. J Gen Virol 77:1335–1341 [View Article][PubMed]
    [Google Scholar]
  43. Merits A., Guo D. Y., Järvekülg L., Saarma M. 1999; Biochemical and genetic evidence for interactions between potato A potyvirus-encoded proteins P1 and P3 and proteins of the putative replication complex. Virology 263:15–22 [View Article][PubMed]
    [Google Scholar]
  44. Qian S., Zhong X., Yu L., Ding B., de Haan P., Boris-Lawrie K. 2009; HIV-1 Tat RNA silencing suppressor activity is conserved across kingdoms and counteracts translational repression of HIV-1. Proc Natl Acad Sci U S A 106:605–610 [View Article][PubMed]
    [Google Scholar]
  45. Qiu W. P., Park J. W., Scholthof H. B. 2002; Tombusvirus P19-mediated suppression of virus-induced gene silencing is controlled by genetic and dosage features that influence pathogenicity. Mol Plant Microbe Interact 15:269–280 [View Article][PubMed]
    [Google Scholar]
  46. Roth B. M., Pruss G. J., Vance V. B. 2004; Plant viral suppressors of RNA silencing. Virus Res 102:97–108 [View Article][PubMed]
    [Google Scholar]
  47. Roudet-Tavert G., German-Retana S., Delaunay T., Delécolle B., Candresse T., Le Gall O. 2002; Interaction between potyvirus helper component-proteinase and capsid protein in infected plants. J Gen Virol 83:1765–1770[PubMed]
    [Google Scholar]
  48. Roudet-Tavert G., Michon T., Walter J., Delaunay T., Redondo E., Le Gall O. 2007; Central domain of a potyvirus VPg is involved in the interaction with the host translation initiation factor eIF4E and the viral protein HcPro. J Gen Virol 88:1029–1033 [View Article][PubMed]
    [Google Scholar]
  49. Sáenz P., Salvador B., Simón-Mateo C., Kasschau K. D., Carrington J. C., García J. A. 2002; Host-specific involvement of the HC protein in the long-distance movement of potyviruses. J Virol 76:1922–1931 [View Article][PubMed]
    [Google Scholar]
  50. Shimura H., Pantaleo V. 2011; Viral induction and suppression of RNA silencing in plants. Biochim Biophys Acta 1809:601–612[PubMed] [CrossRef]
    [Google Scholar]
  51. Silhavy D., Molnár A., Lucioli A., Szittya G., Hornyik C., Tavazza M., Burgyán J. 2002; A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21:3070–3080 [View Article][PubMed]
    [Google Scholar]
  52. Stenger D. C., French R., Gildow F. E. 2005; Complete deletion of Wheat streak mosaic virus HC-Pro: a null mutant is viable for systemic infection. J Virol 79:12077–12080 [View Article][PubMed]
    [Google Scholar]
  53. Syller J. 2005; The roles and mechanisms of helper component proteins encoded by potyviruses and caulimoviruses. Physiol Mol Plant Pathol 67:119–130 [View Article]
    [Google Scholar]
  54. Valli A., Martín-Hernández A. M., López-Moya J. J., García J. A. 2006; RNA silencing suppression by a second copy of the P1 serine protease of Cucumber vein yellowing ipomovirus, a member of the family Potyviridae that lacks the cysteine protease HCPro. J Virol 80:10055–10063 [View Article][PubMed]
    [Google Scholar]
  55. Valli A., López-Moya J. J., García J. A. 2009; RNA silencing and its suppressors in the plant–virus interplay. In: Encyclopedia of Life Sciences (ELS). Chichester: Wiley http://www.els.net/WileyCDA/ doi:10.1002/9780470015902.a9780470021261
  56. Valli A., Oliveros J. C., Molnar A., Baulcombe D., García J. A. 2011; The specific binding to 21-nt double-stranded RNAs is crucial for the anti-silencing activity of Cucumber vein yellowing virus P1b and perturbs endogenous small RNA populations. RNA 17:1148–1158 [View Article][PubMed]
    [Google Scholar]
  57. Vargason J. M., Szittya G., Burgyán J., Hall T. M. 2003; Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115:799–811 [View Article][PubMed]
    [Google Scholar]
  58. Voinnet O., Pinto Y. M., Baulcombe D. C. 1999; Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96:14147–14152 [View Article][PubMed]
    [Google Scholar]
  59. Yambao M. L., Masuta C., Nakahara K., Uyeda I. 2003; The central and C-terminal domains of VPg of Clover yellow vein virus are important for VPg–HCPro and VPg–VPg interactions. J Gen Virol 84:2861–2869 [View Article][PubMed]
    [Google Scholar]
  60. Young B. A., Stenger D. C., Qu F., Morris T. J., Tatineni S., French R. 2012; Tritimovirus P1 functions as a suppressor of RNA silencing and an enhancer of disease symptoms. Virus Res 163:672–677 [View Article][PubMed]
    [Google Scholar]
  61. Zilian E., Maiss E. 2011; Detection of plum pox potyviral protein–protein interactions in planta using an optimized mRFP-based bimolecular fluorescence complementation system. J Gen Virol 92:2711–2723 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.042168-0
Loading
/content/journal/jgv/10.1099/vir.0.042168-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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