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Plant viral proteins and fibrillarin: the link to complete the infective cycle

Abstract

The interaction between viruses with the nucleolus is already a well-defined field of study in plant virology. This interaction is not restricted to those viruses that replicate in the nucleus, in fact, RNA viruses that replicate exclusively in the cytoplasm express proteins that localize in the nucleolus. Some positive single stranded RNA viruses from animals and plants have been reported to interact with the main nucleolar protein, Fibrillarin. Among nucleolar proteins, Fibrillarin is an essential protein that has been conserved in sequence and function throughout evolution. Fibrillarin is a methyltransferase protein with more than 100 methylation sites in the pre-ribosomal RNA, involved in multiple cellular processes, including initiation of transcription, oncogenesis, and apoptosis, among others. Recently, it was found that AtFib2 shows a ribonuclease activity. In plant viruses, Fibrillarin is involved in long-distance movement and cell-to-cell movement, being two highly different processes. The mechanism that Fibrillarin performs is still unknown. However, and despite belonging to very different viral families, the majority comply with the following. (1) They are positive single stranded RNA viruses; (2) encode different types of viral proteins that partially localize in the nucleolus; (3) interacts with Fibrillarin exporting it to the cytoplasm; (4) the viral protein-Fibrillarin interaction forms an RNP complex with the viral RNA and; (5) Fibrillarin depletion affects the infective cycle of the virus. Here we review the relationship of those plant viruses with Fibrillarin interaction, with special focus on the molecular processes of the virus to sequester Fibrillarin to complete its infective cycle.

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Fig. 1

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References

  1. Greco A (2009) Involvement of the nucleolus in replication of human viruses. Rev Med Virol 19:201–214

    Article  CAS  Google Scholar 

  2. Hiscox JA (2002) The nucleolus - a gateway to viral infection? Arch Virol 147:1077–1089. https://doi.org/10.1007/s00705-001-0792-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hiscox JA, Whitehouse A, Matthews DA (2010) Nucleolar proteomics and viral infection. Proteomics 10:4077–4086. https://doi.org/10.1002/pmic.201000251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Pederson T (2011) The nucleolus. Cold Spring Harb Perspect Biol 3:1–15. https://doi.org/10.1101/cshperspect.a000638

    Article  CAS  Google Scholar 

  5. Hiscox JA (2007) RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5:119–127. https://doi.org/10.1038/nrmicro1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Andersen JS, Lam YW, Leung AKL et al (2005) Nucleolar proteome dynamics. Nature 433:77–83. https://doi.org/10.1038/nature03207

    Article  CAS  PubMed  Google Scholar 

  7. Boisvert FM, Van Koningsbruggen S, Navascués J, Lamond AI (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8:574–585

    Article  CAS  Google Scholar 

  8. Hinsby AM, Kiemer L, Karlberg EO et al (2006) A wiring of the human nucleolus. Mol Cell 22:285–295. https://doi.org/10.1016/j.molcel.2006.03.012

    Article  CAS  PubMed  Google Scholar 

  9. Kressler D, Linder P, de la Cruz J (1999) Protein trans-acting factors involved in ribosome biogenesis in saccharomyces cerevisiae. Mol Cell Biol 19:7897–7912. https://doi.org/10.1128/mcb.19.12.7897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Shaw P, Brown J (2012) Nucleoli: composition, function, and dynamics. Plant Physiol 158:44–51. https://doi.org/10.1104/pp.111.188052

    Article  CAS  PubMed  Google Scholar 

  11. Ding Y, Lozano-Durán R (2020) The cajal body in plant-virus interactions. Viruses 12:21–28. https://doi.org/10.3390/v12020250

    Article  CAS  Google Scholar 

  12. Rodriguez-Corona U, Sobol M, Rodriguez-Zapata LC et al (2015) Fibrillarin from archaea to human. Biol Cell 107:159–174. https://doi.org/10.1111/boc.201400077

    Article  CAS  PubMed  Google Scholar 

  13. Ochs RL, Lischwe MA, Spohn WH, Busch H (1985) Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell 54:123–133. https://doi.org/10.1111/j.1768-322X.1985.tb00387.x

    Article  CAS  PubMed  Google Scholar 

  14. Sobol M, Yildirim S, Philimonenko VV et al (2013) UBF complexes with phosphatidylinositol 4,5-bisphosphate in nucleolar organizer regions regardless of ongoing RNA polymerase I activity. Nucl (United States). https://doi.org/10.4161/nucl.27154

    Article  Google Scholar 

  15. Tessarz P, Santos-Rosa H, Robson SC et al (2014) Glutamine methylation in histone H2A is an RNA-polymerase-I-dedicated modification. Nature 505:564–568. https://doi.org/10.1038/nature12819

    Article  CAS  PubMed  Google Scholar 

  16. Loza-Muller L, Rodríguez-Corona U, Sobol M et al (2015) Fibrillarin methylates H2A in RNA polymerase I trans-active promoters in Brassica oleracea. Front Plant Sci 6:976. https://doi.org/10.3389/fpls.2015.00976

    Article  PubMed  PubMed Central  Google Scholar 

  17. Wang H, Boisvert D, Kim KK et al (2000) Crystal structure of a fibrillarin homologue from Methanococcus jannaschii, a hyperthermophile, at 1.6 Å resolution. EMBO J 19:317–323. https://doi.org/10.1093/emboj/19.3.317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Rakitina DV, Taliansky M, Brown JWS, Kalinina NO (2011) Two RNA-binding sites in plant fibrillarin provide interactions with various RNA substrates. Nucleic Acids Res 39:8869–8880. https://doi.org/10.1093/nar/gkr594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Rodriguez-Corona U, Pereira-Santana A, Sobol M et al (2017) Novel ribonuclease activity differs between fibrillarins from arabidopsis thaliana. Front Plant Sci 8:1–10. https://doi.org/10.3389/fpls.2017.01878

    Article  Google Scholar 

  20. Guillen-Chable F, Corona UR, Pereira-Santana A et al (2020) Fibrillarin ribonuclease activity is dependent on the GAR domain and modulated by phospholipids. Cells 9:1–22. https://doi.org/10.3390/cells9051143

    Article  CAS  Google Scholar 

  21. Taliansky ME, Robinson DJ (2003) Molecular biology of umbraviruses: phantom warriors. J Gen Virol 2:1951–1960. https://doi.org/10.1099/vir.0.19219-0

    Article  CAS  Google Scholar 

  22. Taliansky M, Roberts IM, Kalinina N et al (2003) An umbraviral protein involved in long-distance RNA movement, binds viral RNA and forms unique, protective ribonucleoprotein complexes. J Virol 77:3031–3040. https://doi.org/10.1128/JVI.77.5.3031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sang HK, MacFarlane S, Kalinina NO et al (2007) Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc Natl Acad Sci U S A 104:11115–11120. https://doi.org/10.1073/pnas.0704632104

    Article  CAS  Google Scholar 

  24. Kim SH, Ryabov EV, Kalinina NO et al (2007) Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO J 26:2169–2179. https://doi.org/10.1038/sj.emboj.7601674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rajamäki ML, Valkonen JPT (2009) Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like potato virus a in nicotiana species. Plant Cell 21:2485–2502. https://doi.org/10.1105/tpc.108.064147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. González I, Martínez L, Rakitina DV et al (2010) Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol Plant-Microbe Interact 23:294–303. https://doi.org/10.1094/MPMI-23-3-0294

    Article  CAS  PubMed  Google Scholar 

  27. Semashko MA, González I, Shaw J et al (2012) The extreme N-terminal domain of a hordeivirus TGB1 movement protein mediates its localization to the nucleolus and interaction with fibrillarin. Biochimie 94:1180–1188. https://doi.org/10.1016/j.biochi.2012.02.005

    Article  CAS  PubMed  Google Scholar 

  28. Wang X, Zhang Y, Xu J et al (2012) The R-rich motif of Beet black scorch virus P7a movement protein is important for the nuclear localization, nucleolar targeting and viral infectivity. Virus Res 167:207–218. https://doi.org/10.1016/j.virusres.2012.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zheng L, Du Z, Lin C et al (2015) Rice stripe tenuivirus p2 may recruit or manipulate nucleolar functions through an interaction with fibrillarin to promote virus systemic movement. Mol Plant Pathol 16:921–930. https://doi.org/10.1111/mpp.12220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chang CH, Hsu FC, Lee SC et al (2016) The nucleolar fibrillarin protein is required for helper virus-independent long-distance trafficking of a subviral satellite RNA in plants. Plant Cell 28:2586–2602. https://doi.org/10.1105/tpc.16.00071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Li Z, Zhang Y, Jiang Z et al (2018) Hijacking of the nucleolar protein fibrillarin by TGB1 is required for cell-to-cell movement of Barley stripe mosaic virus. Mol Plant Pathol 19:1222–1237. https://doi.org/10.1111/mpp.12612

    Article  CAS  PubMed  Google Scholar 

  32. Wang D, Sun S, Ren Y et al (2020) RepA promotes the nucleolar exclusion of the V2 protein of mulberry mosaic Dwarf-associated virus. Front Microbiol 11:1–12. https://doi.org/10.3389/fmicb.2020.01828

    Article  Google Scholar 

  33. Ogg SC, Lamond AI (2002) Cajal bodies and coilin - moving towards function. J Cell Biol 159:17–21

    Article  CAS  Google Scholar 

  34. Cioce M, Lamond AI (2005) Cajal bodies: a long history of discovery. Annu Rev Cell Dev Biol 21:105–131

    Article  CAS  Google Scholar 

  35. Ryabov EV, Kim SH, Taliansky M (2004) Identification of a nuclear localization signal and nuclear export signal of the umbraviral long-distance RNA movement protein. J Gen Virol 85:1329–1333. https://doi.org/10.1099/vir.0.79854-0

    Article  CAS  PubMed  Google Scholar 

  36. Hu CC, Hsu YH, Lin NS (2009) Satellite RNAs and satellite viruses of plants. Viruses 1:1325–1350

    Article  CAS  Google Scholar 

  37. Lin NS, Lin BY, Lo NW et al (1994) Nucleotide sequence of the genomic RNA of bamboo mosaic potexvirus. J Gen Virol 75:2513–2518. https://doi.org/10.1099/0022-1317-75-9-2513

    Article  CAS  PubMed  Google Scholar 

  38. Lin NS, Lee YS, Lin BY et al (1996) The open reading frame of bamboo mosaic potexvirus satellite RNA is not essential for its replication and can be replaced with a bacterial gene. Proc Natl Acad Sci U S A 93:3138–3142. https://doi.org/10.1073/pnas.93.7.3138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lin NS, Hsu YH (1994) A satellite RNA associated with bamboo mosaic potexvirus. Virology 202:707–714. https://doi.org/10.1006/viro.1994.1392

    Article  CAS  PubMed  Google Scholar 

  40. Tsai M-S, Hsu Y-H, Lin N-S (1999) Bamboo mosaic potexvirus satellite RNA (satBaMV RNA)-encoded P20 protein preferentially binds to satBaMV RNA. J Virol 73:3032–3039. https://doi.org/10.1128/jvi.73.4.3032-3039.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Donald RG, Lawrence DM, Jackson AO (1997) The barley stripe mosaic virus 58-kilodalton beta(b) protein is a multifunctional RNA binding protein. J Virol 71:1538–1546. https://doi.org/10.1128/jvi.71.2.1538-1546.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kalinina NO, Rakitina DV, Solovyev AG et al (2002) RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296:321–329. https://doi.org/10.1006/viro.2001.1328

    Article  CAS  PubMed  Google Scholar 

  43. Verchot-Lubicz J, Torrance L, Solovyev AG et al (2010) Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant-Microbe Interact 23:1231–1247

    Article  CAS  Google Scholar 

  44. Lim H-S, Bragg JN, Ganesan U et al (2008) Triple gene block protein interactions involved in movement of barley stripe mosaic virus. J Virol 82:4991–5006. https://doi.org/10.1128/jvi.02586-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Jackson AO, Lim HS, Bragg J et al (2009) Hordeivirus replication, movement, and pathogenesis. Annu Rev Phytopathol 47:385–422. https://doi.org/10.1146/annurev-phyto-080508-081733

    Article  CAS  PubMed  Google Scholar 

  46. Morozov SY, Solovyev AG (2003) Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366. https://doi.org/10.1099/vir.0.18922-0

    Article  CAS  PubMed  Google Scholar 

  47. Lough TJ, Shash K, Xoconostle-Ćzares B et al (1998) Molecular dissection of the mechanism by which potexvirus triple gene block proteins mediate cell-to-cell transport of infectious RNA. Mol Plant-Microbe Interact 11:801–814. https://doi.org/10.1094/MPMI.1998.11.8.801

    Article  CAS  Google Scholar 

  48. Yang Y, Ding B, Baulcombe DC, Verchot J (2000) Cell-to-cell movement of the 25K protein of Potato virus X is regulated by three other viral proteins. Mol Plant-Microbe Interact 13:599–605. https://doi.org/10.1094/MPMI.2000.13.6.599

    Article  CAS  PubMed  Google Scholar 

  49. Zhao X, Wang X, Dong K et al (2015) Phosphorylation of Beet black scorch virus coat protein by PKA is required for assembly and stability of virus particles. Sci Rep. https://doi.org/10.1038/srep11585

    Article  PubMed  PubMed Central  Google Scholar 

  50. Revers F, García JA (2015) Molecular biology of potyviruses, 1st ed. Elsevier Inc.

  51. Adams MJ, Antoniw JF, Beaudoin F (2005) Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol Plant Pathol 6:471–487

    Article  CAS  Google Scholar 

  52. Dougherty WG, Dawn Parks T (1991) Post-translational processing of the tobacco etch virus 49-kDa small nuclear inclusion polyprotein: identification of an internal cleavage site and delimitation of VPg and proteinase domains. Virology 183:449–456. https://doi.org/10.1016/0042-6822(91)90974-G

    Article  CAS  PubMed  Google Scholar 

  53. Anindya R, Savithri HS (2004) Potyviral NIa proteinase, a proteinase with novel deoxyribonuclease activity. J Biol Chem 279:32159–32169. https://doi.org/10.1074/jbc.M404135200

    Article  CAS  PubMed  Google Scholar 

  54. Elena SF, Rodrigo G (2012) Towards an integrated molecular model of plant-virus interactions. Curr Opin Virol 2:719–724

    Article  CAS  Google Scholar 

  55. Jiang J, Laliberté JF (2011) The genome-linked protein VPg of plant viruses - a protein with many partners. Curr Opin Virol 1:347–354

    Article  CAS  Google Scholar 

  56. Wang A, Krishnaswamy S (2012) Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol 13:795–803

    Article  CAS  Google Scholar 

  57. Huang TS, Wei T, Laliberté JF, Wang A (2010) A host RNA helicase-like protein, AtRH8, interacts with the potyviral genome-linked protein, VPg, associates with the virus accumulation complex, and is essential for infection. Plant Physiol 152:255–266. https://doi.org/10.1104/pp.109.147983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Beauchemin C, Laliberté J-F (2007) The poly(A) binding protein is internalized in virus-induced vesicles or redistributed to the nucleolus during turnip mosaic virus infection. J Virol 81:10905–10913. https://doi.org/10.1128/jvi.01243-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Oruetxebarria I, Guo D, Merits A et al (2001) Identification of the genome-linked protein in virions of potato virus A, with comparison to other members in genus potyvirus. Virus Res 73:103–112. https://doi.org/10.1016/S0168-1702(00)00216-1

    Article  CAS  PubMed  Google Scholar 

  60. Grzela R, Szolajska E, Ebel C et al (2008) Virulence factor of potato virus Y, genome-attached terminal protein VPg, is a highly disordered protein. J Biol Chem 283:213–221. https://doi.org/10.1074/jbc.M705666200

    Article  CAS  PubMed  Google Scholar 

  61. Rantalainen KI, Eskelin K, Tompa P, Makinen K (2011) Structural flexibility allows the functional diversity of potyvirus genome-linked protein VPg. J Virol 85:2449–2457. https://doi.org/10.1128/jvi.02051-10

    Article  CAS  PubMed  Google Scholar 

  62. Rantalainen KI, Uversky VN, Permi P et al (2008) Potato virus A genome-linked protein VPg is an intrinsically disordered molten globule-like protein with a hydrophobic core. Virology 377:280–288. https://doi.org/10.1016/j.virol.2008.04.025

    Article  CAS  PubMed  Google Scholar 

  63. Huang X, Yu R, Li W et al (2019) Identification and characterisation of a glycine-rich RNA-binding protein as an endogenous suppressor of RNA silencing from Nicotiana glutinosa. Planta 249:1811–1822. https://doi.org/10.1007/s00425-019-03122-5

    Article  CAS  PubMed  Google Scholar 

  64. Mallory AC, Reinhart BJ, Bartel D et al (2002) A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proc Natl Acad Sci U S A 99:15228–15233. https://doi.org/10.1073/pnas.232434999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Soitamo AJ, Jada B, Lehto K (2011) HC-Pro silencing suppressor significantly alters the gene expression profile in tobacco leaves and flowers. BMC Plant Biol 11:68. https://doi.org/10.1186/1471-2229-11-68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Hafrén A, Mäkinen K (2008) Purification of viral genome-linked protein VPg from potato virus A-infected plants reveals several post-translationally modified forms of the protein. J Gen Virol 89:1509–1518. https://doi.org/10.1099/vir.0.83649-0

    Article  CAS  PubMed  Google Scholar 

  67. Rajamäki ML, Streng J, Valkonen JPT (2014) Silencing suppressor protein VPg of a potyvirus interacts with the plant silencing-related protein SGS3. Mol Plant-Microbe Interact 27:1199–1210. https://doi.org/10.1094/MPMI-04-14-0109-R

    Article  CAS  PubMed  Google Scholar 

  68. Cheng X, Wang A (2017) The POTYVIRUS silencing suppressor protein VPg mediates degradation of SGS3 via ubiquitination and autophagy patways. J Virol 91:e01478-e1516

    Article  CAS  Google Scholar 

  69. Anandalakshmi R, Marathe R, Ge X et al (2000) A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290:142–144. https://doi.org/10.1126/science.290.5489.142

    Article  CAS  PubMed  Google Scholar 

  70. Endres MW, Gregory BD, Gao Z et al (2010) Two plant viral suppressors of silencing require the ethylene-inducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000729

    Article  PubMed  PubMed Central  Google Scholar 

  71. Pontes O, Li CF, Nunes PC et al (2006) The arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126:79–92. https://doi.org/10.1016/j.cell.2006.05.031

    Article  CAS  PubMed  Google Scholar 

  72. Pontes O, Pikaard CS (2008) siRNA and miRNA processing: new functions for Cajal bodies. Curr Opin Genet Dev 18:197–203

    Article  CAS  Google Scholar 

  73. Brosnan CA, Mitter N, Christie M et al (2007) Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proc Natl Acad Sci U S A 104:14741–14746. https://doi.org/10.1073/pnas.0706701104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Wang D, Maule AJ (1995) Inhibition of host gene expression associated with plant virus replication. Science 267:229–231. https://doi.org/10.1126/science.267.5195.229

    Article  CAS  PubMed  Google Scholar 

  75. Hou WN, Duan CG, Fang RX et al (2011) Satellite RNA reduces expression of the 2b suppressor protein resulting in the attenuation of symptoms caused by Cucumber mosaic virus infection. Mol Plant Pathol 12:595–605. https://doi.org/10.1111/j.1364-3703.2010.00696.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lewsey M, Surette M, Robertson FC et al (2009) The role of the Cucumber mosaic virus 2b protein in viral movement and symptom induction. Mol Plant Microbe Interact 22:642–654. https://doi.org/10.1094/MPMI-22-6-0642

    Article  CAS  PubMed  Google Scholar 

  77. Netsu O, Hiratsuka K, Kuwata S et al (2008) Peanut stunt virus 2b cistron plays a role in viral local and systemic accumulation and virulence in Nicotiana benthamiana. Arch Virol 153:1731–1735. https://doi.org/10.1007/s00705-008-0166-y

    Article  CAS  PubMed  Google Scholar 

  78. Soards AJ, Murphy AM, Palukaitis P, Carr JP (2002) Virulence and differential local and systemic spread of Cucumber mosaic virus in tobacco are affected by the CMV 2b protein. Mol Plant-Microbe Interact 15:647–653. https://doi.org/10.1094/MPMI.2002.15.7.647

    Article  CAS  PubMed  Google Scholar 

  79. Wang Y, Tzfira T, Gaba V et al (2004) Functional analysis of the Cucumber mosaic virus 2b protein: pathogenicity and nuclear localization. J Gen Virol 85:3135–3147. https://doi.org/10.1099/vir.0.80250-0

    Article  CAS  PubMed  Google Scholar 

  80. Qi Y, Zhong X, Itaya A, Ding B (2004) Dissecting RNA silencing in protoplasts uncovers novel effects of viral suppressors on the silencing pathway at the cellular level. Nucleic Acids Res. https://doi.org/10.1093/nar/gnh180

    Article  PubMed  PubMed Central  Google Scholar 

  81. Diaz-Pendon JA, Li F, Li WX, Ding SW (2007) Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19:2053–2063. https://doi.org/10.1105/tpc.106.047449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Zhang X, Yuan YR, Pei Y et al (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20:3255–3268. https://doi.org/10.1101/gad.1495506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Hamera S, Yan Y, Song X et al (2016) Expression of Cucumber mosaic virus suppressor 2b alters FWA methylation and its siRNA accumulation in Arabidopsis thaliana. Biol Open 5:1727–1734. https://doi.org/10.1242/bio.017244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Du Z, Chen A, Chen W et al (2014) Nuclear-cytoplasmic partitioning of cucumber mosaic virus protein 2b determines the balance between its roles as a virulence determinant and an RNA-silencing suppressor. J Virol 88:5228–5241. https://doi.org/10.1128/jvi.00284-14

    Article  PubMed  PubMed Central  Google Scholar 

  85. Zheng L, He J, Ding Z et al (2018) Identification of functional domain(s) of fibrillarin interacted with p2 of rice stripe virus. Can J Infect Dis Med Microbiol. https://doi.org/10.1155/2018/8402839

    Article  PubMed  PubMed Central  Google Scholar 

  86. Dalmay T, Hamilton A, Rudd S et al (2000) An RNA-dependent RNA polymerase gene in arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543–553. https://doi.org/10.1016/S0092-8674(00)80864-8

    Article  CAS  PubMed  Google Scholar 

  87. Fukunaga R, Doudna JA (2009) dsRNA with 5′ overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J 28:545–555. https://doi.org/10.1038/emboj.2009.2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Glick E, Zrachya A, Levy Y et al (2008) Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci U S A 105:157–161. https://doi.org/10.1073/pnas.0709036105

    Article  PubMed  Google Scholar 

  89. Mourrain P, Béclin C, Elmayan T et al (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542. https://doi.org/10.1016/S0092-8674(00)80863-6

    Article  CAS  PubMed  Google Scholar 

  90. Muangsan N, Beclin C, Vaucheret H, Robertson D (2004) Geminivirus VIGS of endogenous genes requires SGS2/SDE1 and SGS3 and defines a new branch in the genetic pathway for silencing in plants. Plant J 38:1004–1014. https://doi.org/10.1111/j.1365-313X.2004.02103.x

    Article  CAS  PubMed  Google Scholar 

  91. Du Z, Xiao D, Wu J et al (2011) p2 of Rice stripe virus (RSV) interacts with OsSGS3 and is a silencing suppressor. Mol Plant Pathol 12:808–814. https://doi.org/10.1111/j.1364-3703.2011.00716.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Yang X, Ren Y, Sun S et al (2018) Identification of the potential virulence factors and RNA silencing suppressors of mulberry mosaic Dwarf-associated geminivirus. Viruses 10:472. https://doi.org/10.3390/v10090472

    Article  CAS  PubMed Central  Google Scholar 

  93. Ma Y, Navarro B, Zhang Z et al (2015) Identification and molecular characterization of a novel monopartite geminivirus associated with mulberry mosaic dwarf disease. J Gen Virol 96:2421–2434. https://doi.org/10.1099/vir.0.000175

    Article  CAS  PubMed  Google Scholar 

  94. Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510. https://doi.org/10.1146/annurev.arplant.043008.092111

    Article  CAS  PubMed  Google Scholar 

  95. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408

    Article  CAS  Google Scholar 

  96. Wang L, Ding Y, He L et al (2019) A virus-encoded protein suppresses methylation of the viral genome in the Cajal body through its interaction with AGO4. bioRxiv. https://doi.org/10.1101/811091

    Article  Google Scholar 

  97. Makarov VV, Makarova SS, Makhotenko AV et al (2015) In vitro properties of hordeivirus TGB1 protein forming ribonucleoprotein complexes. J Gen Virol 96:3422–3431. https://doi.org/10.1099/jgv.0.000252

    Article  CAS  PubMed  Google Scholar 

  98. Rajamäki ML, Valkonen JPT (2003) Localization of a potyvirus and the viral genome-linked protein in wild potato leaves at an early stage of systemic infection. Mol Plant-Microbe Interact 16:25–34 . https://doi.org/10.1094/MPMI.2003.16.1.25

    Article  PubMed  Google Scholar 

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Funding

This research was funded by CONACYT project FC 1572 and CB-2016-286730-Z-0142.

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Stefano Decle, contributed with the writing and research for the review.

Dr. Luis Carlos Contributed with the editing and managing.

Dr. Enrique Castano Defined the subject rewrite and overall management of the review and defined the model.

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Correspondence to Enrique Castano.

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Decle-Carrasco, S., Rodríguez-Zapata, L.C. & Castano, E. Plant viral proteins and fibrillarin: the link to complete the infective cycle. Mol Biol Rep 48, 4677–4686 (2021). https://doi.org/10.1007/s11033-021-06401-1

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  • DOI: https://doi.org/10.1007/s11033-021-06401-1

Keywords

  • GAR domain
  • Long-distance movement
  • Cell-to-cell movement
  • Fibrillarin
  • Nucleolus
  • Plant viruses