Virus-associated small satellite RNAs and viroids display similarities in their replication strategies

Virology

Volumn 479-480, Issue , 2015, Pages 627-636

  Rao, A L N ^a   Kalantidis, Kriton ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF COMPUTER SCIENCE   (Greece)

Author keywords

BRP1; Host factors; Replication; Satellite RNAs; Viroid; Virp1

Indexed keywords

SATELLITE RNA;

GENETICS; PHYSIOLOGY; PLANT; VIROID; VIROLOGY; VIRUS REPLICATION;

PLANTS; RNA, SATELLITE; VIROIDS; VIRUS REPLICATION;

EID: 84937511422     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.02.018     Document Type: Review

References (104)

1. AbouHaidar M.G., Venkataraman S., Golshani A., Liu B., Ahmad T. Novel coding, translation, and gene expression of a replicating covalently closed circular RNA of 220 nt. Proc. Natl. Acad. Sci. USA 2014, 111(40):14542-14547.
2. Abraitiene A., Zhao Y., Hammond R. Nuclear targeting by fragmentation of the potato spindle tuber viroid genome. Biochem. Biophys. Res. Commun. 2008, 368(3):470-475.
3. Annamalai P., Rao A.L. Delivery and expression of functional viral RNA genomes in planta by agroinfiltration. Current Protocols in MIcrobiology 2006, Vol. Unit 16B:p2.1-2.15. John Wiley & Sons, New York.
4. Baumstark T., Schroder A.R., Riesner D. Viroid processing: switch from cleavage to ligation is driven by a change from a tetraloop to a loop E conformation. EMBO J. 1997, 16(3):599-610.
5. Branch A.D., Robertson H.D. A replication cycle for viroids and other small infectious RNA[U+05F3]s. Science 1984, 223(4635):450-455.
6. Bruening G., Passmore B.K., van Tol H., Buzayan J.M., Feldstein P.A. Replication of a plant virus satellite RNA: evidence favors transcription of circular templates of both polarities. Mol. Plant Microbe Interact. 1991, 4(3):219-225.
7. Burgyan J., Garcia-Arenal F. Template-independent repair of the 3' end of cucumber mosaic virus satellite RNA controlled by RNAs 1 and 2 of helper virus. J. Virol. 1998, 72(6):5061-5066.
8. Carpenter C.D., Simon A.E. In vivo repair of 3'-end deletions in a TCV satellite RNA may involve two abortive synthesis and priming events. Virology 1996, 226(2):153-160.
9. Carpenter C.D., Simon A.E. In vivo restoration of biologically active 3' ends of virus-associated RNAs by nonhomologous RNA recombination and replacement of a terminal motif. J. Virol. 1996, 70(1):478-486.
10. Carpenter C.D., Cascone P.J., Simon A.E. Formation of multimers of linear satellite RNAs. Virology 1991, 183(2):586-594.
11. Chaturvedi S., Kalantidis K., Rao A.L. A bromodomain-containing host protein mediates the nuclear importation of a satellite RNA of cucumber mosaic virus. J. Virol. 2014, 88(4):1890-1896.
12. Choi S.H., Seo J.K., Kwon S.J., Rao A.L. Helper virus-independent transcription and multimerization of a satellite RNA associated with cucumber mosaic virus. J. Virol. 2012, 86(9):4823-4832.
13. Collins R.F., Gellatly D.L., Sehgal O.P., Abouhaidar M.G. Self-cleaving circular RNA associated with rice yellow mottle virus is the smallest viroid-like RNA. Virology 1998, 241(2):269-275.
14. Dadami E., Boutla A., Vrettos N., Tzortzakaki S., Karakasilioti I., Kalantidis K. DICER-LIKE 4 but not DICER-LIKE 2 may have a positive effect on potato spindle tuber viroid accumulation in Nicotiana benthamiana. Mol. Plant 2013, 6(1):232-234.
15. Dalmay T., Russo M., Burgyan J. Repair in vivo of altered 3' terminus of cymbidium ringspot tombusvirus RNA. Virology 1993, 192(2):551-555.
16. Daros J.A., Flores R. A chloroplast protein binds a viroid RNA in vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J. 2002, 21(4):749-759.
17. Daros J.A., Marcos J.F., Hernandez C., Flores R. Replication of avocado sunblotch viroid: evidence for a symmetric pathway with two rolling circles and hammerhead ribozyme processing. Proc. Natl. Acad. Sci. USA 1994, 91(26):12813-12817.
18. Delgado S., Martinez de Alba A.E., Hernandez C., Flores R. A short double-stranded RNA motif of Peach latent mosaic viroid contains the initiation and the self-cleavage sites of both polarity strands. J. Virol. 2005, 79(20):12934-12943.
19. Denti M.A., Boutla A., Tsagris M., Tabler M. Short interfering RNAs specific for potato spindle tuber viroid are found in the cytoplasm but not in the nucleus. Plant J. 2004, 37(5):762-769.
20. Di Serio F., Martinez de Alba A.E., Navarro B., Gisel A., Flores R. RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. J. Virol. 2010, 84(5):2477-2489.
21. Diener T.O. Are viroids escaped introns?. Proc. Natl. Acad. Sci. USA 1981, 78(8):5014-5015.
22. Diener T.O. Viroid processing: a model involving the central conserved region and hairpin I. Proc. Natl. Acad. Sci. USA 1986, 83(1):58-62.
23. Diener T.O. Circular RNAs: relics of precellular evolution?. Proc. Natl. Acad. Sci. USA 1989, 86(23):9370-9374.
24. Diermann N., Matousek J., Junge M., Riesner D., Steger G. Characterization of plant miRNAs and small RNAs derived from potato spindle tuber viroid (PSTVd) in infected tomato. Biol. Chem. 2010, 391(12):1379-1390.
25. Ding B. The biology of viroid-host interactions. Ann. Rev. Phytopathol. 2009, 47:105-131.
26. Ding B. Viroids: self-replicating, mobile, and fast-evolving noncoding regulatory RNAs. Wiley Interdiscip. Rev. RNA 2010, 1(3):362-375.
27. Ding B., Itaya A. Viroid: a useful model for studying the basic principles of infection and RNA biology. Mol. Plant Microbe Interact. 2007, 20(1):7-20.
28. Ding S.W., Li H., Lu R., Li F., Li W.X. RNA silencing: a conserved antiviral immunity of plants and animals. Virus Res. 2004, 102(1):109-115.
29. Ding S.W., Lu R. Virus-derived siRNAs and piRNAs in immunity and pathogenesis. Curr. Opin. Virol. 2011, 1(6):533-544.
30. Flores R., Daros J.A., Hernandez C. Avsunviroidae family: viroids containing hammerhead ribozymes. Adv. Virus Res. 2000, 55:271-323.
31. Flores R., Gago-Zachert S., Serra P., Sanjuan R., Elena S.F. Viroids: survivors from the RNA world?. Annu. Rev. Microbiol. 2014, 68:395-414.
32. Flores R., Gas M.E., Molina-Serrano D., Nohales M.A., Carbonell A., Gago S., De la Pena M., Daros J.A. Viroid replication: rolling-circles, enzymes and ribozymes. Viruses 2009, 1(2):317-334.
33. Flores R., Grubb D., Elleuch A., Nohales M.A., Delgado S., Gago S. Rolling-circle replication of viroids, viroid-like satellite RNAs and hepatitis delta virus: variations on a theme. RNA Biol. 2011, 8(2):200-206.
34. Gas M.E., Hernandez C., Flores R., Daros J.A. Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Pathog. 2007, 3(11):e182.
35. Gerlach W.L., Buzayan J.M., Schneider I.R., Bruening G. Satellite tobacco ringspot virus RNA: biological activity of DNA clones and their in vitro transcripts. Virology 1986, 151:172-185.
36. Gomez G., Martinez G., Pallas V. Viroid-induced symptoms in Nicotiana benthamiana plants are dependent on RDR6 activity. Plant Physiol. 2008, 148(1):414-423.
37. Gomez G., Pallas V. Can the import of mRNA into chloroplasts be mediated by a secondary structure of a small non-coding RNA?. Plant Signal. Behav. 2010, 5(11):1517-1519.
38. Gomez G., Pallas V. Noncoding RNA mediated traffic of foreign mRNA into chloroplasts reveals a novel signaling mechanism in plants. PLoS One 2010, 5(8):e12269.
39. Gomez G., Pallas V. Studies on subcellular compartmentalization of plant pathogenic noncoding RNAs give new insights into the intracellular RNA-traffic mechanisms. Plant Physiol. 2012, 159(2):558-564.
40. Gozmanova M., Denti M.A., Minkov I.N., Tsagris M., Tabler M. Characterization of the RNA motif responsible for the specific interaction of potato spindle tuber viroid RNA (PSTVd) and the tomato protein Virp1. Nucleic Acids Res. 2003, 31(19):5534-5543.
41. Gy I., Gasciolli V., Lauressergues D., Morel J.B., Gombert J., Proux F., Proux C., Vaucheret H., Mallory A.C. Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 2007, 19(11):3451-3461.
42. Hayes R.J., Tousch D., Jacquemond M., Pereira V.C., Buck K.W., Tepfer M. Complete replication of a satellite RNA in vitro by a purified RNA-dependent RNA polymerase. J. Gen. Virol. 1992, 73(Pt 6):1597-1600.
43. Hu C.-C., Hsu Y.-H., Lin N.-S. Satellite RNAs and satellite viruses of plants. Viruses 2009, 1:1325-1350.
44. Hutchins C.J., Rathjen P.D., Forster A.C., Symons R.H. Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res. 1986, 14(9):3627-3640.
45. Itaya A., Folimonov A., Matsuda Y., Nelson R.S., Ding B. Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol. Plant Microbe Interact. 2001, 14(11):1332-1334.
46. Itaya A., Zhong X., Bundschuh R., Qi Y., Wang Y., Takeda R., Harris A.R., Molina C., Nelson R.S., Ding B. A structured viroid RNA serves as a substrate for dicer-like cleavage to produce biologically active small RNAs but is resistant to RNA-induced silencing complex-mediated degradation. J. Virol. 2007, 81(6):2980-2994.
47. Jacquemond M. Cucumber mosaic virus. Adv. Virus Res. 2012, 84:439-504.
48. Jaegle M., Devic M., Longstaff M., Baulcombe D. Cucumber mosaic virus satellite RNA (Y strain): analysis of sequences which affect yellow mosaic symptoms on tobacco. J. Gen. Virol. 1990, 71(Pt 9):1905-1912.
49. Kalantidis K., Denti M.A., Tzortzakaki S., Marinou E., Tabler M., Tsagris M. Virp1 is a host protein with a major role in Potato spindle tuber viroid infection in Nicotiana plants. J. Virol. 2007, 81(23):12872-12880.
50. Kaper J.M., Waterworth H.E. Cucumber mosaic virus associated RNA 5: causal agent for tomato necrosis. Science 1977, 196(4288):429-431.
51. Kiefer M.C., Daubert S.D., Schneider I.R., Bruening G. Multimeric forms of satellite of tobacco ringspot virus RNA. Virology 1982, 121(2):262-273.
52. Kolonko N., Bannach O., Aschermann K., Hu K.H., Moors M., Schmitz M., Steger G., Riesner D. Transcription of potato spindle tuber viroid by RNA polymerase II starts in the left terminal loop. Virology 2006, 347(2):392-404.
53. Koonin E.V., Martin W. On the origin of genomes and cells within inorganic compartments. Trends Genet.: TIG 2005, 21(12):647-654.
54. Kuroda T., Natsuaki T., Wang W.Q., Okuda S. Formation of multimers of cucumber mosaic virus satellite RNA. J. .Gen. Virol. 1997, 78(Pt 4):941-946.
55. Kwon S.J., Chaturvedi S., Rao A.L. Repair of the 3' proximal and internal deletions of a satellite RNA associated with Cucumber mosaic virus is directed toward restoring structural integrity. Virology 2014, 450-451:222-232.
56. Landry P., Perreault J.P. Identification of a peach latent mosaic viroid hairpin able to act as a Dicer-like substrate. J. Virol. 2005, 79(10):6540-6543.
57. Linthorst H.J., Kaper J.M. Replication of peanut stunt virus and its associated RNA 5 in cowpea protoplasts. Virology 1984, 139(2):317-329.
58. Machida S., Yamahata N., Watanuki H., Owens R.A., Sano T. Successive accumulation of two size classes of viroid-specific small RNA in potato spindle tuber viroid-infected tomato plants. J. Gen. Virol. 2007, 88(Pt 12):3452-3457.
59. Maniataki E., Martinez de Alba A.E., Sagesser R., Tabler M., Tsagris M. Viroid RNA systemic spread may depend on the interaction of a 71-nucleotide bulged hairpin with the host protein VirP1. RNA 2003, 9(3):346-354.
60. Martinez de Alba A.E., Flores R., Hernandez C. Two chloroplastic viroids induce the accumulation of small RNAs associated with posttranscriptional gene silencing. J. Virol. 2002, 76(24):13094-13096.
61. Martinez de Alba A.E., Sagesser R., Tabler M., Tsagris M. A bromodomain-containing protein from tomato specifically binds potato spindle tuber viroid RNA in vitro and in vivo. J. Virol. 2003, 77(17):9685-9694.
62. Masuta C., Takanami Y. Determination of sequence and structural requirements for pathogenicity of a cucumber mosaic virus satellite RNA (Y-satRNA). Plant Cell 1989, 1(12):1165-1173.
63. Minoia S., Carbonell A., Di Serio F., Gisel A., Carrington J.C., Navarro B., Flores R. Specific argonautes selectively bind small RNAs derived from potato spindle tuber viroid and attenuate viroid accumulation in vivo. J. Virol. 2014, 88(20):11933-11945.
64. Montasser M.S., Kaper J.M., Owens R.A. First report of potential biological control of potato spindle tuber viroid disease by virus-satellite combination. Plant Dis. 1991, 75:319.
65. Motard J., Bolduc F., Thompson D., Perreault J.P. The peach latent mosaic viroid replication initiation site is located at a universal position that appears to be defined by a conserved sequence. Virology 2008, 373(2):362-375.
66. Navarro B., Gisel A., Rodio M.E., Delgado S., Flores R., Di Serio F. Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host mRNA as predicted by RNA silencing. Plant J. 2012, 70(6):991-1003.
67. Navarro J.A., Flores R. Characterization of the initiation sites of both polarity strands of a viroid RNA reveals a motif conserved in sequence and structure. EMBO J. 2000, 19(11):2662-2670.
68. Ng T.F., Chen L.F., Zhou Y., Shapiro B., Stiller M., Heintzman P.D., Varsani A., Kondov N.O., Wong W., Deng X., Andrews T.D., Moorman B.J., Meulendyk T., MacKay G., Gilbertson R.L., Delwart E. Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. Proc. Natl. Acad. Sci. USA 2014.
69. Nohales M.A., Flores R., Daros J.A. Viroid RNA redirects host DNA ligase 1 to act as an RNA ligase. Proc. Natl. Acad. Sci. USA 2012, 109(34):13805-13810.
70. Nohales M.A., Molina-Serrano D., Flores R., Daros J.A. Involvement of the chloroplastic isoform of tRNA ligase in the replication of viroids belonging to the family Avsunviroidae. J. Virol. 2012, 86(15):8269-8276.
71. Palukaitis P. Pathogenicity regulation by satellite RNAs of cucumber mosaic virus: minor nucleotide sequence changes alter host responses. Mol. Plant-Microbe Interact.: MPMI 1988, 1(4):175-181.
72. Palukaitis P. What has been happening with viroids?. Virus Genes 2014, 49(2):175-184.
73. Palukaitis P., Garcia-Arenal F. Cucumoviruses. Adv. Virus Res. 2003, 62:241-323.
74. Papaefthimiou I., Hamilton A., Denti M., Baulcombe D., Tsagris M., Tabler M. Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res. 2001, 29(11):2395-2400.
75. Pelchat M., Grenier C., Perreault J.P. Characterization of a viroid-derived RNA promoter for the DNA-dependent RNA polymerase from Escherichia coli. Biochemistry 2002, 41(20):6561-6571.
76. Pelchat M., Perreault J.P. Binding site of Escherichia coli RNA polymerase to an RNA promoter. Biochem. Biophys. Res. Commun. 2004, 319(2):636-642.
77. Prody G.A., Bakos J.T., Buzayan J.M., Schneider I.R., Bruening G. Autolytic processing of dimeric plant virus satellite RNA. Science 1986, 231(4745):1577-1580.
78. Pruss G.J., Nester E.W., Vance V. Infiltration with Agrobacterium tumefaciens induces host defense and development-dependent responses in the infiltrated zone. Mol. Plant Microbe Interact. 2008, 21(12):1528-1538.
79. Quadt R., Jaspars E.M. Characterization of cucumber mosaic virus RNA-dependent RNA polymerase. FEBS Lett. 1991, 279(2):273-276.
80. Rodio M.E., Delgado S., De Stradis A., Gomez M.D., Flores R., Di Serio F. A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 2007, 19(11):3610-3626.
81. Schindler I., Muhlbach H.P. Involvement of nuclear DNA-dependent RNA polymerases in potato spindle tuber viroid replication- a reeavluation. Plant Sci. 1992, 84:221-229.
82. Seo J.K., Kwon S.J., Chaturvedi S., Ho Choi S., Rao A.L. Functional significance of a hepta nucleotide motif present at the junction of Cucumber mosaic virus satellite RNA multimers in helper-virus dependent replication. Virology 2013, 435(2):214-219.
83. Sheikh A.H., Raghuram B., Eschen-Lippold L., Scheel D., Lee J., Sinha A.K. Agroinfiltration by Cytokinin-Producing Agrobacterium sp. Strain GV3101 Primes Defense Responses in Nicotiana tabacum. Mol. Plant Microbe Interact. 2014, 27(11):1175-1185.
84. Shimura H., Pantaleo V., Ishihara T., Myojo N., Inaba J., Sueda K., Burgyan J., Masuta C. A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog. 2011, 7(5):e1002021.
85. Sivanandam V., Varady E., Rao A.L.N. Heterologous replicase driven 3' end repair of Cucumber mosaic virus satellite RNA. Virology 2015, 478:18-26.
86. Sleat D.E., Palukaitis P. A single nucleotide change within a plant virus satellite RNA alters the host specificity of disease induction. Plant J.: Cell Mol. Biol. 1992, 2(1):43-49.
87. Smith N.A., Eamens A.L., Wang M.B. Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathog. 2011, 7(5):e1002022.
88. Song S.I., Miller W.A. Cis and trans requirements for rolling circle replication of a satellite RNA. J. Virol. 2004, 78(6):3072-3082.
89. Symons R.H., Randles J.W. Encapsidated circular viroid-like satellite RNAs (virusoids) of plants. Curr. Top. Microbiol. Immunol. 1999, 239:81-105.
90. Tabler M., Tsagris M. Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci. 2004, 9(7):339-348.
91. Takanami Y. A striking change in symptoms on cucumber mosaic virus-infected tobacco plants induced by a satellite RNA. Virology 1981, 109(1):120-126.
92. Vashist S., Urena L., Chaudhry Y., Goodfellow I. Identification of RNA-protein interaction networks involved in the norovirus life cycle. J. Virol. 2012, 86(22):11977-11990.
93. Vogt U., Pelissier T., Putz A., Razvi F., Fischer R., Wassenegger M. Viroid-induced RNA silencing of GFP-viroid fusion transgenes does not induce extensive spreading of methylation or transitive silencing. Plant J. 2004, 38(1):107-118.
94. Voinnet O., Lederer C., Baulcombe D.C. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 2000, 103(1):157-167.
95. Wang M.B., Bian X.Y., Wu L.M., Liu L.X., Smith N.A., Isenegger D., Wu R.M., Masuta C., Vance V.B., Watson J.M., Rezaian A., Dennis E.S., Waterhouse P.M. On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc. Natl. Acad. Sci. USA 2004, 101(9):3275-3280.
96. Wang M.B., Wesley S.V., Finnegan E.J., Smith N.A., Waterhouse P.M. Replicating satellite RNA induces sequence-specific DNA methylation and truncated transcripts in plants. RNA 2001, 7(1):16-28.
97. Wang X.B., Wu Q., Ito T., Cillo F., Li W.X., Chen X., Yu J.L., Ding S.W. RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2010, 107(1):484-489.
98. Wassenegger M., Spieker R.L., Thalmeir S., Gast F.U., Riedel L., Sanger H.L. A single nucleotide substitution converts potato spindle tuber viroid (PSTVd) from a noninfectious to an infectious RNA for Nicotiana tabacum. Virology 1996, 226(2):191-197.
99. Yang X., Kang L., Po T. Resistance of tomato infected with cucumber mosaic virus satellite RNA to potato spindle tuber viroid. Ann. Appl. Biol. 1996, 130:207-215.
100. Yang X.J. Lysine acetylation and the bromodomain: a new partnership for signaling. BioEssays: News Rev. Mol. Cell. Dev. Biol. 2004, 26(10):1076-1087.
101. Zhang J., Zhang G., McCormack J.C., Simon A.E. Evolution of virus-derived sequences for high-level replication of a subviral RNA. Virology 2006, 351(2):476-488.
102. Zhao Y., Owens R.A., Hammond R.W. Use of a vector based on Potato virus X in a whole plant assay to demonstrate nuclear targeting of Potato spindle tuber viroid. J. Gen. Virol. 2001, 82(Pt 6):1491-1497.
103. Zimmern D. Do viroids and RNA viruses derive from a system that exchanges genetic information between eukaryotioc cells?. Trends Biochem. Sci. 1982, 7:205-207.
104. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31(13):3406-3415.