Viroids: Survivors from the RNA world?

Annual Review of Microbiology

Volumn 68, Issue , 2014, Pages 395-414

  Flores, Ricardo ^a   Gago Zachert, Selma ^b   Serra, Pedro ^a   Sanjuán, Rafael ^c   Elena, Santiago F ^a,d  

^a Ciudad Politécnica de la Innovación   (Spain)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF VALENCIA   (Spain)

^d SANTA FE INSTITUTE   (United States)

Author keywords

Catalytic RNAs; Hammerhead ribozymes; Hepatitis virus; Small noncoding RNAs; Viroid like satellite RNAs

Indexed keywords

DNA; HAMMERHEAD RIBOZYME; PROTEIN; VIRUS RNA;

HEPATITIS VIRUS; NONHUMAN; REPLICON; REVIEW; RNA REPLICATION; RNA SEQUENCE; RNA STRUCTURE; VIROID; CHEMISTRY; CLASSIFICATION; GENETICS; METABOLISM; PHYSIOLOGY; VIRUS REPLICATION;

RNA, VIRAL; VIROIDS; VIRUS REPLICATION;

EID: 84907502470     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-091313-103416     Document Type: Review

References (147)

1. Allison LA, Simon LD, Maliga P. 1996. Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 15:2802-9
2. Ambr os S, Hernandez C, Flores R. 1999. Rapid generation of genetic heterogeneity in progenies from individual cDNA clones of peach latent mosaic viroid in its natural host. J. Gen. Virol. 80:2239-52
3. Atkins JF, Gesteland RF, Cech TR, eds. 2011. RNA Worlds: From Lifes Origins to Diversity in Gene Regulation. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
4. Beijerinck MW. 1898. Ueber ein Contagium vivum fluidum als Ursache der Fleckenkrankheit der Tabaksblatter. Verh. K. Akad. Wet. Amst. 65:3-21
5. Bernad L, Duran-Vila N, Elena SF. 2009. Effect of citrus hosts on the generation, maintenance and evolutionary fate of genetic variability of citrus exocortis viroid. J. Gen. Virol. 90:2040-9
6. Biebricher CK, Eigen M. 2006. What is a quasispecies? Curr. Top. Microbiol. Immunol. 299:1-31
7. Branch AD, RobertsonHD. 1984. A replication cycle for viroids and other small infectious RNAs. Science 223:450-4
8. Brazas R, GanemD. 1996. A cellular homolog of hepatitis delta antigen: implications for viral replication and evolution. Science 274:90-4
9. Briones C, Stich M, Manrubia SC. 2009. The dawn of the RNA world: toward functional complexity through ligation of random RNA oligomers. RNA 15:743-49
10. Bruening G, Passmore BK, van Tol H, Buzayan JM, Feldstein PA. 1991. Replication of a plant virus satellite RNA: Evidence favors transcription of circular templates of both polarities. Mol. Plant Microbe Interact. 4:219-25
11. Burch CL, Chao L. 1999. Evolution by small steps and rugged landscapes in the RNA virus φ6. Genetics 151:921-27
12. Buzayan JM, Gerlach WL, Bruening G. 1986. Non-enzymatic cleavage and ligation of RNAs complementary to a plant virus satellite RNA. Nature 323:349-53
13. Cech TR. 2000. The ribosome is a ribozyme. Science 289:878-79
14. Chela-Flores J. 1994. Are viroids molecular fossils of the RNA world? J. Theor. Biol. 166:163-66
15. Chen PJ, Kalpana G, Goldberg J, Mason W, Werner B, et al. 1986. Structure and replication of the genome of the hepatitis δ virus. Proc. Natl. Acad. Sci. USA 83:8774-78
16. Codoñer FM, Daros JA, Sole RV, Elena SF. 2006. The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens. PLoS Pathog. 2:1187-93
17. Cramer P, Armache KJ, Baumli S, Benkert S, Brueckner F, et al. 2008. Structure of eukaryotic RNA polymerases. Annu. Rev. Biophys. 37:337-52
18. Crick FH. 1968. The origin of the genetic code. J. Mol. Biol. 38:367-79
19. Daros JA, Flores R. 1995. Identification of a retroviroid-like element from plants. Proc. Natl. Acad. Sci. USA 92:6856-60
20. Daros JA, Flores R. 2002.Achloroplast protein binds a viroidRNAin vivo and facilitates its hammerheadmediated self-cleavage. EMBO J. 21:749-59
21. Daros JA, Marcos JF, Hernandez C, Flores R. 1994. Replication of avocado sunblotch viroid: evidence for a symmetric pathway with two rolling circles and hammerhead ribozyme processing. Proc. Natl. Acad. Sci. USA 91:12813-17
22. de la Pena M, Garcia-Robles I. 2010 Ubiquitous presence of the hammerhead ribozyme motif along the tree of life RNA 16:1943-50
23. de la Pena M, Navarro B, Flores R. 1999. Mapping the molecular determinant of pathogenicity in a hammerhead viroid: a tetraloop within the in vivo branched RNA conformation. Proc. Natl. Acad. Sci. USA 96:9960-65
24. Delgado S, Martinez de Alba AE, Hernandez C, Flores R. 2005. 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. 79:12934-43
25. den Boon JA, Ahlquist P. 2010. Organelle-likemembrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 64:241-56
26. Diener TO. 1971. Potato spindle tuber "virus": IV. A replicating, low molecular weight RNA. Virology 45:411-28
27. Diener TO. 1972. Potato spindle tuber viroid: VIII. Correlation of infectivity with a UV-absorbing component and thermal denaturation properties of the RNA. Virology 50:606-9
28. Diener TO. 1981. Are viroids escaped introns? Proc. Natl. Acad. Sci. USA 78:5014-15
29. Diener TO. 1989. Circular RNAs: relics of precellular evolution? Proc. Natl. Acad. Sci. USA 86:9370-74
30. Diener TO. 2003. Discovering viroids: a personal perspective. Nat. Rev. Microbiol. 1:75-80
31. Ding B. 2009. The biology of viroid-host interactions. Annu. Rev. Phytopathol. 47:105-31
32. Ding B. 2010. Viroids: self-replicating, mobile, and fast-evolving noncoding regulatory RNAs. Wiley Interdiscip. Rev. RNA 1:362-75
33. Domingo E, Sabo D, Taniguchi T, Weissmann C. 1978. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735-44
34. Eigen M. 1971. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465-523
35. EigenM, Schuster P. 1978. The hypercycle. A principle of natural self-organization. Part C: the realistic hypercycle. Naturwissenschaften 65:341-69
36. Elena SF, Dopazo J, de la Pena M, Flores R, Diener TO, Moya A. 2001. Phylogenetic analysis of viroid and viroid-like satellite RNAs from plants: a reassessment. J. Mol. Evol. 53:155-59
37. Elena SF, Dopazo J, Flores R, Diener TO,Moya A. 1991. Phylogeny of viroids, viroidlike satellite RNAs, and the viroidlike domain of hepatitis δ virus RNA. Proc. Natl. Acad. Sci. USA 88:5631-34
38. Epstein LM, Gall JG. 1987. Self-cleaving transcripts of satellite DNA from the newt. Cell 48:535-43
39. Fadda Z, Daros JA, Fagoaga C, Flores R, Duran-Vila N. 2003. Eggplant latent viroid, the candidate type species for a new genus within the family Avsunviroidae (hammerhead viroids). J. Virol. 77:6528-32
40. Fedor MJ. 2000. Structure and function of the hairpin ribozyme. J. Mol. Biol. 297:269-91
41. Feix G, Pollet R,Weissmann C. 1968. Replication of viral RNA, XVI. Enzymatic synthesis of infectious viral RNA with noninfectious Q-beta minus strands as template. Proc. Natl. Acad. Sci. USA 59:145-52
42. Flores R, Di Serio F, Navarro B, Duran-Vila N, Owens RA. 2011. Viroids and viroid diseases of plants. In Studies in Viral Ecology, Vol. I: Microbial and BotanicalHost Systems, ed. CJ Hurst, pp. 311-46. Hoboken, NJ: JohnWiley & Sons
43. Flores R, Hernandez C, Martinez de Alba E, Daros JA, Di Serio F. 2005. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 43:117-39
44. Flores R, Semancik JS. 1982. Properties of a cell-free system for synthesis of citrus exocortis viroid. Proc. Natl. Acad. Sci. USA 79:6285-88
45. Flores R, Serra P, Minoia S, Di Serio F, Navarro B. 2012. Viroids: from genotype to phenotype just relying on RNA sequence and structural motifs. Front. Microbiol. 3:217
46. Forster AC, Symons RH. 1987. Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell 49:211-20
47. Forterre P. 2005. The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. Biochimie 87:793-803
48. Fraenkel-Conrat H. 1956. The role of the nucleic acid in the reconstitution of active tobacco mosaic virus. J. Am. Chem. Soc. 78:882-83
49. Freeland SJ, Knight RD, Landweber LF. 1999. Do proteins predate DNA? Science 286:690-92
50. Fresco JR, Alberts BM, Doty P. 1960. Some molecular details of the secondary structure of ribonucleic acid. Nature 188:98-101
51. Gago S, Elena SF, Flores R, Sanjuan R. 2009. Extremely high mutation rate of a hammerhead viroid. Science 323:1308
52. Gandia M, Duran-Vila N. 2004. Variability of the progeny of a sequence variant Citrus bent leaf viroid (CBLVd). Arch. Virol. 149:407-16
53. Gas ME, Hernandez C, Flores R, Daros JA. 2007. Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Pathog. 3:1813-26
54. Gesteland RF, Atkins JF, eds. 1993. The RNA World. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
55. Gierer A, SchrammG. 1956. Infectivity of ribonucleic acid from tobacco mosaic virus. Nature 177:702-3
56. GilbertW. 1986. Origin of life: the RNA world. Nature 319:618
57. G ora-Sochacka A, Kierzek A, Candresse T, Zag orski W. 1997. The genetic stability of potato spindle tuber viroid (PSTVd) molecular variants. RNA 3:68-74
58. Grill LK, Semancik JS. 1978. RNA sequences complementary to citrus exocortis viroid in nucleic acid preparations from infected Gynura aurantiaca. Proc. Natl. Acad. Sci. USA 75:896-900
59. Gross HJ, Domdey H, Lossow C, Jank P, Raba M, et al. 1978. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 273:203-8
60. Gudima S, Wu SY, Chiang CM, Moraleda G, Taylor J. 2000. Origin of hepatitis δ virusmRNA. J. Virol. 74:7204-10
61. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S. 1983. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849-57
62. Haag JR, Pikaard CS. 2011. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 12:483-92
63. Hadidi A. 1986. Relationship of viroids and certain other plant pathogenic nucleic acids to group I and II introns. Plant Mol. Biol. 7:129-42
64. Hajeri S, Ramadugu C, Manjunath K, Ng J, Lee R, Vidalakis G. 2011. In vivo generated Citrus exocortis viroid progeny variants display a range of phenotypes with altered levels of replication, systemic accumulation and pathogenicity. Virology 417:400-9
65. Hammann C, Luptak A, Perreault J, de la Pena M. 2012. The ubiquitous hammerhead ribozyme. RNA 18:871-85
66. Hammann C, Steger G. 2012. Viroid-specific small RNA in plant disease. RNA Biol. 9:809-19
67. Hammond R, Smith DR, Diener TO. 1989. Nucleotide sequence and proposed secondary structure of Columnea latent viroid: a natural mosaic of viroid sequences. Nucleic Acids Res. 17:10083-94
68. Haruna I, Spiegelman S. 1966. A search for an intermediate involving a complement during synchronous synthesis by a purified RNA replicase. Proc. Natl. Acad. Sci. USA 55:1256-63
69. Hegedus K, Dallmann G, Balazs E. 2004. The DNA form of a retroviroid-like element is involved in recombination events with itself and with the plant genome. Virology 325:277-86
70. Hernandez C, Daros JA, Elena SF, Moya A, Flores R. 1992. The strands of both polarities of a small circular RNA from carnation self-cleave in vitro through alternative double- and single-hammerhead structures. Nucleic Acids Res. 20:6323-29
71. Hernandez C, Flores R. 1992. Plus and minus RNAs of peach latent mosaic viroid self-cleave in vitro via hammerhead structures. Proc. Natl. Acad. Sci. USA 89:3711-15
72. Ho CK, Shuman S. 2002. Bacteriophage T4 RNA ligase 2 (gp24.1) exemplifies a family of RNA ligases found in all phylogenetic domains. Proc. Natl. Acad. Sci. USA 99:12709-14
73. Hutchins CJ, Keese P, Visvader JE, Rathjen PD, McInnes JL, Symons RH. 1985. Comparison of multimeric plus and minus forms of viroids and virusoids. Plant Mol. Biol. 4:293-304
74. Hutchins CJ, Rathjen PD, Forster AC, Symons RH. 1986. Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res. 14:3627-40
75. Ivica NA, Obermayer B, Campbell GW, Rajamani S, Gerland U, Chen IA. 2013. The paradox of dual roles in the RNA world: resolving the conflict between stable folding and templating ability. J. Mol. Evol. 77:55-63
76. JenkinsGM, WoelkCH, Rambaut A,Holmes EC. 2000. Testing the extent of sequence similarity among viroids, satellite RNAs, and the hepatitis delta virus. J. Mol. Evol. 50:98-102
77. JohnstonWK, Unrau PJ, LawrenceMS, GlasnerME, Bartel DP. 2001. RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension. Science 292:1319-25
78. Juhasz A, Hegyi H, Solymosy F. 1988. A novel aspect of the information content of viroids. Biochim. Biophys. Acta 950:455-58
79. KieferMC,Owens RA,DienerTO. 1983. Structural similarities between viroids and transposable genetic elements. Proc. Natl. Acad. Sci. USA 80:6234-38
80. Kolonko N, Bannach O, Aschermann K, Hu KH, MoorsM, et al. 2006. Transcription of potato spindle tuber viroid by RNA polymerase II starts in the left terminal loop. Virology 347:392-404
81. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR. 1982. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31:147-57
82. KuoMY, Goldberg J, Coates L, MasonW, Gerin J, Taylor J. 1988. Molecular cloning of hepatitis delta virus RNA from an infected woodchuck liver: sequence, structure, and applications. J. Virol. 62:1855-61
83. Kuo MY, Sharmeen L, Dinter-Gottlieb G, Taylor J. 1988. Characterization of self-cleaving RNA sequences on the genome and antigenome of human hepatitis delta virus. J. Virol. 62:4439-44
84. Lauring AS, Andino R. 2010. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog. 6:e1001005
85. Lazcano A, Guerrero R, Margulis L, Oro J. 1988. The evolutionary transition from RNA to DNA in early cells. J. Mol. Evol. 27:283-90
86. Lima MI, Fonseca MEN, Flores R, Kitajima EW. 1994. Detection of avocado sunblotch viroid in chloroplasts of avocado leaves by in situ hybridization. Arch. Virol. 138:385-90
87. Lincoln TA, Joyce GF. 2009. Self-sustained replication of an RNA enzyme. Science 323:1229-32
88. Manrubia SC, Briones C. 2007. Modular evolution and increase of functional complexity in replicating RNA molecules. RNA 13:97-107
89. Margulis L. 1993. Symbiosis in Cell Evolution. New York:W.H. Freeman. 2nd ed.
90. McInnes JL, Symons RH. 1991. Comparative structure of viroids and their rapid detection using radioactive and nonradioactive nucleic acid probes. In Viroids and Satellites: Molecular Parasites at the Frontier of Life, ed. K Maramorosch, pp. 21-58. Boca Raton, FL: CRC
91. Moelling K. 2013. What contemporary viruses tell us about evolution: a personal view. Arch. Virol. 158:1833-48
92. Muhlbach HP, Sänger HL. 1979. Viroid replication is inhibited by α-amanitin. Nature 278:185-88
93. Navarro B, Flores R. 1997. Chrysanthemum chlorotic mottle viroid: unusual structural properties of a subgroup of viroids with hammerhead ribozymes. Proc. Natl. Acad. Sci. USA 94:11262-67
94. Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F. 2012. 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. 70:991-1003
95. Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F. 2012. Viroids: how to infect a host and cause disease without encoding proteins. Biochimie 94:1474-80
96. Navarro JA, Flores R. 2000. Characterization of the initiation sites of both polarity strands of a viroid RNA reveals a motif conserved in sequence and structure. EMBO J. 19:2662-70
97. Navarro JA, Vera A, Flores R. 2000. A chloroplastic RNA polymerase resistant to tagetitoxin is involved in replication of Avocado sunblotch viroid. Virology 268:218-25
98. Nohales MA, Flores R, Daros JA. 2012. A viroid RNA redirects host DNA ligase 1 to act as an RNA ligase. Proc. Natl. Acad. Sci. USA 109:13805-10
99. NohalesMA, Molina-Serrano D, Flores R, Daros JA. 2012. Involvement of the chloroplastic isoform of tRNA ligase in the replication of the viroids belonging to the family Avsunviroidae. J. Virol. 86:8269-76
100. Ojosnegros S, Perales C,Mas A, Domingo E. 2011. Quasispecies as a matter of fact: viruses and beyond. Virus Res. 162:203-15
101. Orgel LE. 1968. Evolution of the genetic apparatus. J. Mol. Biol. 38:381-93
102. Pascal JM. 2008.DNAandRNAligases: Structural variations and sharedmechanisms. Curr. Opin. Struct. Biol. 18:96-105
103. Pascal JM, OBrien PJ, Tomkinson AE, Ellenberger T. 2004. Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature 432:473-78
104. Poole AM, Logan DT. 2005. Modern mRNA proofreading and repair: clues that the last universal common ancestor possessed an RNA genome? Mol. Biol. Evol. 22:1444-55
105. Powner MW, Gerland B, Sutherland JD. 2009. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459:239-42
106. Prody GA, Bakos JT, Buzayan JM, Schneider IR, Bruening G. 1986. Autolytic processing of dimeric plant virus satellite RNA. Science 231:1577-80
107. Reanney D. 1984. Genetic noise in evolution? Nature 307:318-19
108. Rezaian MA. 1990. Australian grapevine viroid-evidence for extensive recombination between viroids. Nucleic Acids Res. 18:1813-18
109. RiesnerD,Henco K, Rokohl U, KlotzG,KleinschmidtAK, et al. 1979. Structure and structure formation of viroids. J. Mol. Biol. 133:85-115
110. Rizzetto M, Canese MG, Aric o J, Crivelli O, Trepo C, et al. 1977. Immunofluorescence detection of a new antigen-antibody system (δ/anti-δ) associated to the hepatitis B virus in the liver and in the serum of HBsAg carriers. Gut 18:997-1003
111. Rizzetto M, Hoyer B, Canese MG, Shih JW, Purcell RH, Gerin JL. 1980. δ agent: association of δ antigen with hepatitis B surface antigen and RNA in serum of δ-infected chimpanzees. Proc. Natl. Acad. Sci. USA 77:6124-28
112. Robertson HD. 1996. How did replicating and coding RNAs first get together? Science 274:66-67
113. Rodio ME, Delgado S, de Stradis AE, Gomez MD, Flores R, Di Serio F. 2007. A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 19:3610-26
114. Roossinck MJ, Sleat D, Palukaitis P. 1992. Satellite RNAs of plant viruses: structures and biological effects. Microbiol. Rev. 56:265-79
115. Sanjuan R, Cuevas JM, Furi o V, Holmes EC, Moya A. 2007. Selection for robustness in mutagenized RNA viruses. PLoS Genet. 3:939-46
116. Sanjuan R, Forment J, Elena SF. 2006. In silico predicted robustness of viroid RNA secondary structures. II. Interaction between mutation pairs. Mol. Biol. Evol. 23:2123-30
117. Sanjuan R, Forment J,Elena SF. 2006. In silico predicted robustness of viroidsRNAsecondary structures. I. The effect of single mutations. Mol. Biol. Evol. 23:1427-36
118. Schiebel W, Pelissier T, Riedel L, Thalmeir S, Schiebel R, et al. 1998. Isolation of an RNA-directed RNA polymerase-specific cDNA clone from tomato. Plant Cell 10:2087-101
119. Schindler IM,Muhlbach HP. 1992. Involvement of nuclear DNA-dependentRNApolymerases in potato spindle tuber viroid replication: a reevaluation. Plant Sci. 84:221-29
120. Schneider R. 1969. Satellite-like particle of tobacco ringspot virus that resembles tobacco ringspot virus. Science 166:1627-29
121. Schuster P, Swetina J. 1988. Stationary mutant distributions and evolutionary optimization. Bull. Math. Biol. 50:635-60
122. Semancik JS, Szychowski JA, Rakowski AG, Symons RH. 1993. Isolates of citrus exocortis viroid recovered by host and tissue selection. J. Gen. Virol. 74:2427-36
123. Shuman S, Lima CD. 2004. The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltransferases. Curr. Opin. Struct. Biol. 14:757-64
124. Sogo JM,KollerT,DienerTO. 1973. Potato spindle tuber viroid. X: Visualization and size determination by electron microscopy. Virology 55:70-80
125. Sugiura M. 1992. The chloroplast genome. Plant Mol. Biol. 19:149-68
126. Symons RH. 1981. Avocado sunblotch viroid: primary sequence and proposed secondary structure. Nucleic Acids Res. 9:6527-37
127. Symons RH, Randles JW. 1999. Encapsidated circular viroidlike satellite RNAs (virusoids) of plants. Curr. Top. Microbiol. Immunol. 239:81-105
128. Tabler M, Tsagris M. 2004. Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci. 9:339-48
129. Taylor JM. 2009. Replication of the hepatitis delta virus RNA genome. Adv. Virus Res. 74:103-21
130. Taylor JM, Pelchat M. 2010. Origin of hepatitis δ virus. Future Microbiol. 5:393-402
131. Tessitori M, Rizza S, Reina A, Causarano G, Di Serio F. 2013. The genetic diversity of Citrus dwarfing viroid populations is mainly dependent on the infected host species. J. Gen. Virol. 94:687-93
132. TsagrisEM, Martinez de Alba AE,Gozmanova M, KalantidisK. 2008. Viroids. CellMicrobiol. 10:2168-79
133. Verhoeven JT,Meekes ET, Roenhorst JW, Flores R, Serra P. 2013. Dahlia latent viroid: a recombinant new species of the family Pospiviroidae posing intriguing questions about its origin and classification. J. Gen. Virol. 94:711-19
134. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344-48
135. Visvader JE, Symons RH. 1985. Eleven new sequence variants of citrus exocortis viroid and the correlation of sequence with pathogenicity. Nucleic Acids Res. 13:2907-20
136. Wang KS, Choo QL, Weiner AJ, Ou JH, Najarian RC, et al. 1986. Structure, sequence and expression of the hepatitis delta (δ) viral genome. Nature 323:508-14. Corrigendum. 1987. Nature 328:456
137. Wang LK, Schwer B, Shuman S. 2006. Structure-guided mutational analysis of T4 RNA ligase 1. RNA 12:2126-34
138. Wassenegger M, Krczal G. 2006. Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci. 11:142-51
139. Wassenegger M, Spieker RL, Thalmeir S, Gast FU, Riedel L, Sänger HL. 1996. A single nucleotide substitution converts potato spindle tuber viroid (PSTVd) from a noninfectious to an infectious RNA for Nicotiana tabacum. Virology 226:191-97
140. Webb C-HT, Riccitelli NJ, Ruminski DJ, Luptak A. 2009. Widespread occurrence of self-cleaving ribozymes. Science 326:953
141. Wilke CO, Wang JL, Ofria C, Lenski RE, Adami C. 2001. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412:331-33
142. Wochner A, Attwater J, Coulson A, Holliger P. 2011. Ribozyme-catalyzed transcription of an active ribozyme. Science 332:209-12
143. Woese CR. 1967. The Genetic Code: The Molecular Basis for Genetic Expression. New York: Harper and Row
144. Wu Q, Wang Y, Cao M, Pantaleo V, Burgyan J, et al. 2012. Homology-independent discovery of replicating pathogenic circular RNAs by deep sequencing and a new computational algorithm. Proc. Natl. Acad. Sci. USA 109:3938-43
145. Xiong Y, Eickbush TH. 1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9:3353-62
146. Zhang ZX, Chen SS, Qi SS, Ding SW,WuQF, Li SF. 2013. Identification of new viroid-like circular RNAs from grapevine and apple plants. Presented at Int. Workshop on Viroids and Satell. RNAs. Beijing
147. Zhong X, Archual AJ, Amin AA, Ding B. 2008. A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 20:35-47