Viroid-specific small RNA in plant disease

RNA Biology

Volumn 9, Issue 6, 2012, Pages 809-819

  Hammann, Christian ^a,c   Steger, Gerhard ^b  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

Infection; Mechanisms of gene regulation; RNA interference; RNA mediated DNA methylation; Small RNA; Symptom; Target

Indexed keywords

DNA DIRECTED RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE II; MICRORNA; NUCLEOPLASMIN; RNA POLYMERASE; UNCLASSIFIED DRUG; VIROID SPECIFIC SMALL RNA; VIRUS RNA;

ARABIDOPSIS; AVOCADO SUN BLOTCH VIROID; AVSUNVIROIDAE; BARK; CHLOROPLAST; CITRUS EXOCORTIS VIROID; COCONUT; COCONUT CADANG CADANG VIROID; FRUIT DEVELOPMENT; HOP STUNT VIROID; NONHUMAN; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PEACH; PEACH LATENT MOSAIC VIROID; PLANT CELL; PLANT LEAF; POSPIVIROIDAE; REVIEW; RNA PROCESSING; RNA REPLICATION; RNA SEQUENCE; RNA SYNTHESIS; SEQUENCE ANALYSIS; STUNTING (PLANT); VIROID; VIROIDAL PLANT DISEASE; VIRUS ENTRY; VIRUS REPLICATION; VIRUS TRANSFORMATION;

AVSUNVIROIDAE; POSPIVIROIDAE; VIROIDS;

EID: 84863451242     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.19810     Document Type: Review

References (106)

1. Sanger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci USA 1976; 73:3852-6; PMID:1069269; http://dx.doi.org/10.1073/pnas.73.11.3852.
2. Ding B. Viroids: self-replicating, mobile and fast-evolving noncoding regulatory RNAs. Wiley Interdiscip Rev RNA 2010; 1:362-75; PMID:21956936; http://dx.doi.org/10.1002/wrna.22.
3. Daròs JA, Elena SF, Flores R. Viroids: an Ariadne's thread into the RNA labyrinth. EMBO Rep 2006; 7:593-8; PMID:16741503; http://dx.doi.org/10. 1038/sj.embor.7400706.
4. Flores R, Hernández C, Martínez de Alba AE, Daròs JA, Di Serio F. Viroids and viroid-host interactions. Annu Rev Phytopathol 2005; 43:117-39; PMID:16078879; http://dx.doi.org/10.1146/annurev.phyto.43.040204. 140243.
5. Tabler M, Tsagris M. Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci 2004; 9:339-48; PMID:15231279; http://dx.doi.org/10. 1016/j.tplants.2004.05.007.
6. Hadidi A, Flores R, Randles J, Semancik J. Viroids. CSIRO Publishing, Australia 2003.
7. Matoušek J, Riesner D, Steger G. Viroids: the smallest known infectious agents cause accumulation of viroid-specific small RNAs. In: Erdmann V, Barciszewski J, Eds. From Nucleic Acids Sequences to Molecular Medicine. New York, Berlin: Springer-Verlag 2012.
8. Schmitz M, Steger G. Potato spindle tuber viroid (PSTVd). Plant Viruses 2007; 1:106-15.
9. Flores R, Randles JW, Bar-Joseph M, Diener TO. A proposed scheme for viroid classification and nomenclature. Arch Virol 1998; 143:623-9; PMID:9572562; http://dx.doi.org/10.1007/s007050050318.
10. Rocheleau L, Pelchat M. The Subviral RNA Database: a toolbox for viroids, the hepatitis delta virus and satellite RNAs research. BMC Microbiol 2006; 6:24; PMID:16519798; http://dx.doi.org/10.1186/1471-2180-6-24.
11. Keese P, Symons RH. Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc Natl Acad Sci USA 1985; 82:4582-6; PMID:3860809; http://dx.doi.org/10.1073/pnas.82.14.4582.
12. Branch AD, Robertson HD. A replication cycle for viroids and other small infectious RNA's. Science 1984; 223:450-5; PMID:6197756; http://dx.doi.org/10. 1126/science.6197756.
13. Steger G, Riesner D. Properties of Viroids: Molecular characteristics. In: Hadidi A, Flores R, Randles J, Semancik J, Eds. Viroids: CSIRO Publishing, Australia 2003; 15-29.
14. Riesner D, Gross HJ. Viroids. Annu Rev Biochem 1985; 54:531-64; PMID:2411212; http://dx.doi.org/10.1146/annurev.bi.54.070185.002531.
15. Qi Y, Ding B. Differential subnuclear localization of RNA strands of opposite polarity derived from an autonomously replicating viroid. Plant Cell 2003; 15:2566-77; PMID:14555700; http://dx.doi.org/10.1105/tpc.016576.
16. Harders J, Lukács N, Robert-Nicoud M, Jovin TM, Riesner D. Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning microscopy. EMBO J 1989; 8:3941-9; PMID:2591366.
17. Schumacher J, Sänger HL, Riesner D. Subcellular localization of viroids in highly purified nuclei from tomato leaf tissue. EMBO J 1983; 2:1549-55; PMID:11892810.
18. Schindler IM, Mühlbach HP. Involvement of nuclear DNA-dependent RNA polymerases in potato spindle tuber viroid replication: a reevaluation. Plant Sci 1992; 84:221-9; http://dx.doi.org/10.1016/0168-9452(92)90138-C.
19. Warrilow D, Symons RH. Citrus exocortis viroid RNA is associated with the largest subunit of RNA polymerase II in tomato in vivo. Arch Virol 1999; 144:2367-75; PMID:10664390; http://dx.doi.org/10.1007/s007050050650.
20. Kolonko N, Bannach O, Aschermann K, Hu KH, Moors M, Schmitz M, et al. Transcription of potato spindle tuber viroid by RNA polymerase II starts in the left terminal loop. Virology 2006; 347:392-404; PMID:16406459; http://dx.doi.org/10.1016/j.virol.2005.11.039.
21. Baumstark T, Schröder AR, 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; 16:599-610; PMID:9034342; http://dx.doi.org/10.1093/ emboj/16.3.599.
22. Schrader O, Baumstark T, Riesner D. A mini-RNA containing the tetraloop, wobble-pair and loop E motifs of the central conserved region of potato spindle tuber viroid is processed into a minicircle. Nucleic Acids Res 2003; 31:988-98; PMID:12560495; http://dx.doi.org/10.1093/nar/gkg193.
23. Lima MI, Fonseca ME, Flores R, Kitajima EW. Detection of avocado sunblotch viroid in chloroplasts of avocado leaves by in situ hybridization. Arch Virol 1994; 138:385-90; PMID:7998844; http://dx.doi.org/10.1007/BF01379142.
24. Pelchat M, Coté F, Perreault JP. Study of the polymerization step of the rolling circle replication of peach latent mosaic viroid. Arch Virol 2001; 146:1753-63; PMID:11699960; http://dx.doi.org/10.1007/s007050170061.
25. Dubé A, Bolduc F, Bisaillon M, Perreault JP. Mapping studies of the Peach latent mosaic viroid reveal novel structural features. Mol Plant Pathol 2011; 12:688-701; PMID:21726370; http://dx.doi.org/10.1111/j.1364-3703. 2010.00703.x.
26. Navarro JA, 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; 19:2662-70; PMID:10835363; http://dx.doi.org/10.1093/ emboj/19.11.2662.
27. Navarro JA, Vera A, Flores R. A chloroplastic RNA polymerase resistant to tagetitoxin is involved in replication of avocado sunblotch viroid. Virology 2000; 268:218-25; PMID:10683343; http://dx.doi.org/10.1006/viro.1999.0161.
28. Daròs JA, Marcos JF, Hernández 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; 91:12813-7; PMID:7809126; http://dx.doi.org/10.1073/pnas.91.26.12813.
29. Daròs JA, Flores R. A chloroplast protein binds a viroid RNA in vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J 2002; 21:749-59; PMID:11847122; http://dx.doi.org/10.1093/emboj/21.4.749.
30. Bajaj P, Steger G, Hammann C. Sequence elements outside the catalytic core of natural hairpin ribozymes modulate the reactions differentially. Biol Chem 2011; 392:593-600; PMID:21657980; http://dx.doi.org/10.1515/bc.2011.071.
31. Shepotinovskaya IV, Uhlenbeck OC. Catalytic diversity of extended hammerhead ribozymes. Biochemistry 2008; 47:7034-42; PMID:18543946; http://dx.doi.org/10.1021/bi7025358.
32. Przybilski R, Hammann C. The tolerance to exchanges of the Watson Crick base pair in the hammerhead ribozyme core is determined by surrounding elements. RNA 2007; 13:1625-30; PMID:17666711; http://dx.doi.org/10.1261/rna.631207.
33. Przybilski R, Hammann C. Idiosyncratic cleavage and ligation activity of individual hammerhead ribozymes and core sequence variants thereof. Biol Chem 2007; 388:737-41; PMID:17570826; http://dx.doi.org/10.1515/BC.2007.065.
34. Przybilski R, Gräf S, Lescoute A, Nellen W, Westhof E, Steger G, et al. Functional hammerhead ribozymes naturally encoded in the genome of Arabidopsis thaliana. Plant Cell 2005; 17:1877-85; PMID:15937227; http://dx.doi.org/10.1105/tpc.105.032730.
35. Daròs JA, Flores R. Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae. Proc Natl Acad Sci USA 2004; 101:6792-7; PMID:15096616; http://dx.doi.org/10.1073/pnas.0401090101.
36. Matoušek J, Orctová L, Steger G, Škopek J, Moors M, D di P, et al. Analysis of thermal stress-mediated PSTVd variation and biolistic inoculation of progeny of viroid "thermomutants" to tomato and Brassica species. Virology 2004; 323:9-23; PMID:15165815; http://dx.doi.org/10. 1016/j.virol.2004.02.010.
37. Palukaitis P. Potato spindle tuber viroid: Investigation of the long-distance, intra-plant transport route. Virology 1987; 158:239-41; PMID:18644563; http://dx.doi.org/10.1016/0042-6822(87)90260-1.
38. Zhu Y, Green L, Woo YM, Owens R, Ding B. Cellular basis of potato spindle tuber viroid systemic movement. Virology 2001; 279:69-77; PMID:11145890; http://dx.doi.org/10.1006/viro.2000.0724.
39. Ding B, Wang Y. Viroids: uniquely simple and tractable models to elucidate regulation of cell-to-cell trafficking of RNA. DNA Cell Biol 2009; 28:51-6; PMID:19105595; http://dx.doi.org/10.1089/dna.2008.0811.
40. Zhong X, Archual AJ, Amin AA, Ding B. A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 2008; 20:35-47; PMID:18178767; http://dx.doi.org/10.1105/tpc.107.056606.
41. Wang Y, Ding B. Viroids: small probes for exploring the vast universe of RNA trafficking in plants. J Integr Plant Biol 2010; 52:28-39; PMID:20074138; http://dx.doi.org/10.1111/j.1744-7909.2010.00900.x.
42. Gómez G, Pallás V. Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol Plant Microbe Interact 2001; 14:910-3; PMID:11437265; http://dx.doi.org/10.1094/MPMI.2001.14.7.910.
43. Owens RA, Blackburn M, Ding B. Possible involvement of the phloem lectin in long-distance viroid movement. Mol Plant Microbe Interact 2001; 14:905-9; PMID:11437264; http://dx.doi.org/10.1094/MPMI.2001.14.7.905.
44. Flores R, Delgado S, Gas ME, Carbonell A, Molina D, Gago S, et al. Viroids: the minimal non-coding RNAs with autonomous replication. FEBS Lett 2004; 567:42-8; PMID:15165891; http://dx.doi.org/10.1016/j.febslet.2004.03.118.
45. Eiras M, Nohales MA, Kitajima EW, Flores R, Daròs JA. Ribosomal protein L5 and transcription factor IIIA from Arabidopsis thaliana bind in vitro specifically Potato spindle tuber viroid RNA. Arch Virol 2011; 156:529-33; PMID:21153748; http://dx.doi.org/10.1007/s00705-010-0867-x.
46. Martínez de Alba AE, Sägesser 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; 77:9685-94; PMID:12915580; http://dx.doi.org/10.1128/JVI.77.17.9685-94.2003.
47. Kalantidis K, Denti MA, 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; 81:12872-80; PMID:17898061; http://dx.doi.org/10.1128/JVI.00974-07.
48. Matoušek J, Orctová L, Ptácek J, Patzak J, Dedic P, Steger G, et al. Experimental transmission of pospiviroid populations to weed species characteristic of potato and hop fields. J Virol 2007; 81:11891-9; PMID:17715233; http://dx.doi.org/10.1128/JVI.01165-07.
49. Kawaguchi-Ito Y, Li SF, Tagawa M, Araki H, Goshono M, Yamamoto S, et al. Cultivated grapevines represent a symptomless reservoir for the transmission of hop stunt viroid to hop crops: 15 years of evolutionary analysis. PLoS One 2009; 4:8386; PMID:20041179; http://dx.doi.org/10.1371/journal.pone.0008386.
50. Verhoeven JTJ, Jansen C, Roenhorst JW. Epidemiological evidence that vegetatively propagated, solanaceous plant species act as sources of Potato spindle tuber viroid inoculum for tomato. Plant Pathol 2010; 59:3-12; http://dx.doi.org/10.1111/j.1365-3059.2009.02173.x.
51. Randles J. Economic impact of viroid dieseases. In: Hadidi A, Flores R, Randles J, Semancik J, Eds. Viroids: CSIRO Publishing, Australia 2003; 3-11.
52. Stark-Lorenzen P, Guitton MC, Werner R, Mühlbach HP. Detection and tissue distribution of potato spindle tuber viroid in infected tomato plants by tissue print hybridization. Arch Virol 1997; 142:1289-96; PMID:9267443; http://dx.doi.org/10.1007/s007050050160.
53. Matoušek J, Kozlová P, Orctová L, Schmitz A, Pešina K, Bannach O, et al. Accumulation of viroid-specific small RNAs and increase in nucleolytic activities linked to viroid-caused pathogenesis. Biol Chem 2007; 388:1-13; PMID:17214544; http://dx.doi.org/10.1515/BC.2007.001.
54. Schnölzer M, Haas B, Raam K, Hofmann H, Sänger HL. Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTV). EMBO J 1985; 4:2181-90; PMID:15938051.
55. Owens RA, Steger G, Hu Y, Fels A, Hammond RW, Riesner D. RNA structural features responsible for potato spindle tuber viroid pathogenicity. Virology 1996; 222:144-58; PMID:8806495; http://dx.doi.org/10.1006/viro.1996.0405.
56. Schmitz A, Riesner D. Correlation between bending of the VM region and pathogenicity of different Potato Spindle Tuber Viroid strains. RNA 1998; 4:1295-303; PMID:9769103; http://dx.doi.org/10.1017/S1355838298980815.
57. Sano T, Candresse T, Hammond RW, Diener TO, Owens RA. Identification of multiple structural domains regulating viroid pathogenicity. Proc Natl Acad Sci USA 1992; 89:10104-8; PMID:1332029; http://dx.doi.org/10.1073/pnas.89.21.10104.
58. Rodriguez MJ, Randles JW. Coconut cadang-cadang viroid (CCCVd) mutants associated with severe disease vary in both the pathogenicity domain and the central conserved region. Nucleic Acids Res 1993; 21:2771; PMID:8332477; http://dx.doi.org/10.1093/nar/21.11.2771.
59. Reanwarakorn K, Semancik JS. Regulation of pathogenicity in hop stunt viroid-related group II citrus viroids. J Gen Virol 1998; 79:3163-71; PMID:9880036.
60. Camacho Henriquez A, Sänger HL. Analysis of acid-extractable tomato leaf proteins after infection with a viroid, two viruses and a fungus and partial purification of the "pathogenesis-related" protein p 14. Arch Virol 1982; 74:181-96; PMID:6891893; http://dx.doi.org/10.1007/BF01314711.
61. Gadea J, Mayda ME, Conejero V, Vera P. Characterization of defense-related genes ectopically expressed in viroid-infected tomato plants. Mol Plant Microbe Interact 1996; 9:409-15; PMID:8672818; http://dx.doi.org/10. 1094/MPMI-9-0409.
62. López-Gresa MP, Maltese F, Bellés JM, Conejero V, Kim HK, Choi YH, et al. Metabolic response of tomato leaves upon different plant-pathogen interactions. Phytochem Anal 2010; 21:89-94; PMID:19866456; http://dx.doi.org/10.1002/pca.1179.
63. Itaya A, Matsuda Y, Gonzales RA, Nelson RS, Ding B. Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Mol Plant Microbe Interact 2002; 15:990-9; PMID:12437296; http://dx.doi.org/10.1094/MPMI.2002.15.10.990.
64. Hammond RW, Zhao Y. Modification of tobacco plant development by sense and antisense expression of the tomato viroid-induced AGC VIIIa protein kinase PKV suggests involvement in gibberellin signaling. BMC Plant Biol 2009; 9:108; PMID:19689802; http://dx.doi.org/10.1186/1471-2229-9-108.
65. Wolff P, Gilz R, Schumacher J, Riesner D. Complexes of viroids with histones and other proteins. Nucleic Acids Res 1985; 13:355-67; PMID:3889835; http://dx.doi.org/10.1093/nar/13.2.355.
66. Diener TO, Hammond RW, Black T, Katze MG. Mechanism of viroid pathogenesis: differential activation of the interferon-induced, double-stranded RNA-activated, M(r) 68,000 protein kinase by viroid strains of varying pathogenicity. Biochimie 1993; 75:533-8; PMID:7505621; http://dx.doi.org/10. 1016/0300-9084(93)90058-Z.
67. Werner R, Mühlbach HP, Guitton MC. Isolation of viroid-RNA-binding proteins from an expression library with nonradioactive-labeled RNA probes. Biotechniques 1995; 19:218-22; PMID:8527142.
68. Gozmanova M, Denti MA, Minkov IN, 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; 31:5534-43; PMID:14500815; http://dx.doi.org/10.1093/nar/gkg777.
69. Dickson E. A model for the involvement of viroids in RNA splicing. Virology 1981; 115:216-21; PMID:7292989; http://dx.doi.org/10.1016/0042-6822(81) 90104-5.
70. Haas B, Klanner A, Ramm K, Sänger HL. The 7S RNA from tomato leaf tissue resembles a signal recognition particle RNA and exhibits a remarkable sequence complementarity to viroids. EMBO J 1988; 7:4063-74; PMID:2468486.
71. Rodio ME, Delgado S, De Stradis A, Gómez MD, Flores R, Di Serio F. A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 2007; 19:3610-26; PMID:18055612; http://dx.doi.org/10.1105/tpc.106. 049775.
72. Aschermann M. Identifikation eines zellulären RNA- Wechselwirkungspartners von PSTVd in vitro und in vivo. Heinrich-Heine- Universität Düsseldorf 2001.
73. Stroeks P. Kontaktstellen zwischen dem Viroid PSTVd und der ribosomalen 5 S-RNA.: Heinrich-Heine-Universität Düsseldorf 2008.
74. Wassenegger M, Heimes S, Riedel L, Sänger HL. RNA-directed de novo methylation of genomic sequences in plants. Cell 1994; 76:567-76; PMID:8313476; http://dx.doi.org/10.1016/0092-8674(94)90119-8.
75. Girard A, Hannon GJ. Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 2008; 18:136-48; PMID:18282709; http://dx.doi.org/10. 1016/j.tcb.2008.01.004.
76. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391:806-11; PMID:9486653; http://dx.doi.org/10.1038/35888.
77. Riedmann LT, Schwentner R. miRNA, siRNA, piRNA and argonautes: news in small matters. RNA Biol 2010; 7:133-9; PMID:20200493; http://dx.doi.org/10.4161/ rna.7.2.11288.
78. 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; 29:2395-400; PMID:11376158; http://dx.doi.org/10.1093/ nar/29.11.2395.
79. Martínez de Alba AE, Flores R, Hernández C. Two chloroplastic viroids induce the accumulation of small RNAs associated with posttranscriptional gene silencing. J Virol 2002; 76:13094-6; PMID:12438638; http://dx.doi.org/10.1128/JVI.76.24.13094-6.2002.
80. Markarian N, Li HW, Ding SW, Semancik JS. RNA silencing as related to viroid induced symptom expression. Arch Virol 2004; 149:397-406; PMID:14745603; http://dx.doi.org/10.1007/s00705-003-0215-5.
81. Hammann C, Hartmann RK, Helm M, Klostermeier D, Marchfelder A, Suess B, et al. Regulatory RNAs and beyond. EMBO Rep 2011; 12:751-3; PMID:21760614; http://dx.doi.org/10.1038/embor.2011.150.
82. Hamilton A, Voinnet O, Chappell L, Baulcombe D. Two classes of short interfering RNA in RNA silencing. EMBO J 2002; 21:4671-9; PMID:12198169; http://dx.doi.org/10.1093/emboj/cdf464.
83. Itaya A, Folimonov A, Matsuda Y, Nelson RS, Ding B. Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol Plant Microbe Interact 2001; 14:1332-4; PMID:11763132; http://dx.doi.org/10.1094/MPMI.2001.14. 11.1332.
84. Machida S, Yamahata N, Watanuki H, Owens RA, 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; 88:3452-7; PMID:18024916; http://dx.doi.org/10.1099/vir.0.83228-0.
85. Diermann N, Matoušek 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; 391:1379-90; PMID:21087089; http://dx.doi.org/10.1515/bc.2010.148.
86. Wang Y, Shibuya M, Taneda A, Kurauchi T, Senda M, Owens RA, et al. Accumulation of Potato spindle tuber viroid-specific small RNAs is accompanied by specific changes in gene expression in two tomato cultivars. Virology 2011; 413:72-83; PMID:21353278; http://dx.doi.org/10.1016/j.virol.2011.01.021.
87. Di Serio F, Martínez de Alba AE, 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; 84:2477-89; PMID:20015979; http://dx.doi.org/10.1128/JVI.02336-09.
88. Itaya A, Zhong X, Bundschuh R, Qi Y, Wang Y, Takeda R, et al. 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; 81:2980-94; PMID:17202210; http://dx.doi.org/10.1128/JVI.02339-06.
89. Martín R, Arenas C, Daròs JA, Covarrubias A, Reyes JL, Chua NH. Characterization of small RNAs derived from Citrus exocortis viroid (CEVd) in infected tomato plants. Virology 2007; 367:135-46; PMID:17559901; http://dx.doi.org/10.1016/j.virol.2007.05.011.
90. Gómez G, Martínez G, Pallás V. Viroid-induced symptoms in Nicotiana benthamiana plants are dependent on RDR6 activity. Plant Physiol 2008; 148:414-23; PMID:18599649; http://dx.doi.org/10.1104/pp.108. 120808.
91. Navarro B, Pantaleo V, Gisel A, Moxon S, Dalmay T, Bisztray G, et al. Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant-viroid interaction. PLoS One 2009; 4:7686; PMID:19890399; http://dx.doi.org/10.1371/journal.pone.0007686.
92. Martinez G, Donaire L, Llave C, Pallás V, Gómez G. High-throughput sequencing of Hop stunt viroid-derived small RNAs from cucumber leaves and phloem. Mol Plant Pathol 2010; 11:347-59; PMID:20447283; http://dx.doi.org/10.1111/j.1364-3703.2009.00608.x.
93. Di Serio F, Gisel A, Navarro B, Delgado S, Martínez de Alba AE, Donvito G, et al. Deep sequencing of the small RNAs derived from two symptomatic variants of a chloroplastic viroid: implications for their genesis and for pathogenesis. PLoS One 2009; 4:7539; PMID:19847296; http://dx.doi.org/10.1371/ journal.pone.0007539.
94. Bolduc F, Hoareau C, St-Pierre P, Perreault JP. In-depth sequencing of the siRNAs associated with peach latent mosaic viroid infection. BMC Mol Biol 2010; 11:16; PMID:20158907; http://dx.doi.org/10.1186/1471-2199-11-6.
95. Hammann C. Protein Interactions with Double Stranded RNA in Eukaryotic Cells. In: Nellen W, Hammann C, Eds. Small RNAs: analysis and regulatory functions. Berlin: Springer Verlag 2005; 91-118.
96. Nellen W, Hammann C, Eds. Small RNAs: Analysis and Regulatory Functions. Berlin: Springer Verlag 2005.
97. Ramachandran V, Chen X. Small RNA metabolism in Arabidopsis. Trends Plant Sci 2008; 13:368-74; PMID:18501663; http://dx.doi.org/10.1016/j.tplants.2008. 03.008.
98. Landry P, Perreault JP. Identification of a peach latent mosaic viroid hairpin able to act as a Dicer-like substrate. J Virol 2005; 79:6540-3; PMID:15858039; http://dx.doi.org/10.1128/JVI.79.10.6540-3.2005.
99. Teune JH, Steger G. NOVOMIR: De Novo Prediction of MicroRNA-Coding Regions in a Single Plant-Genome. J Nucleic Acids 2010; 2010:495904; PMID:20871826; http://dx.doi.org/10.4061/2010/495904.
100. Denti MA, 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; 37:762-9; PMID:14871315; http://dx.doi.org/10.1111/j. 1365-313X.2004.02001.x.
101. Wassenegger M, Krczal G. Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci 2006; 11:142-51; PMID:16473542; http://dx.doi.org/10.1016/j.tplants.2006.01.003.
102. Moissiard G, Parizotto EA, Himber C, Voinnet O. Transitivity in Arabidopsis can be primed, requires the redundant action of the antiviral Dicer-like 4 and Dicer-like 2, and is compromised by viral-encoded suppressor proteins. RNA 2007; 13:1268-78; PMID:17592042; http://dx.doi.org/10.1261/rna. 541307.
103. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, et al. Small RNA duplexes function as mobile silencing signals between plant cells. Science 2010; 328:912-6; PMID:20413458; http://dx.doi.org/10.1126/science. 1185880.
104. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 2010; 328:872-5; PMID:20413459; http://dx.doi.org/10. 1126/science.1187959.
105. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, et al. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 2004; 303:672-6; PMID:14704433; http://dx.doi.org/10.1126/science.1093686.
106. Diermann N, Matoušek 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; 391:1379-90; PMID:21087089; http://dx.doi.org/10.1515/bc.2010.148.