1932

Abstract

Because RNA can be a carrier of genetic information and a biocatalyst, there is a consensus that it emerged before DNA and proteins, which eventually assumed these roles and relegated RNA to intermediate functions. If such a scenario—the so-called RNA world—existed, we might hope to find its relics in our present world. The properties of viroids that make them candidates for being survivors of the RNA world include those expected for primitive RNA replicons: () small size imposed by error-prone replication, () high G + C content to increase replication fidelity, () circular structure for assuring complete replication without genomic tags, () structural periodicity for modular assembly into enlarged genomes, () lack of protein-coding ability consistent with a ribosome-free habitat, and () replication mediated in some by ribozymes, the fingerprint of the RNA world. With the advent of DNA and proteins, those protoviroids lost some abilities and became the plant parasites we now know.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-091313-103416
2014-09-08
2024-04-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/68/1/annurev-micro-091313-103416.html?itemId=/content/journals/10.1146/annurev-micro-091313-103416&mimeType=html&fmt=ahah

Literature Cited

  1. Allison LA, Simon LD, Maliga P. 1.  1996. Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 15:2802–9 [Google Scholar]
  2. Ambrós S, Hernández C, Flores R. 2.  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 [Google Scholar]
  3. Atkins JF, Gesteland RF, Cech TR. 3.  2011. RNA Worlds: From Life's Origins to Diversity in Gene Regulation Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
  4. Beijerinck MW. 4.  1898. Ueber ein Contagium vivum fluidum als Ursache der Fleckenkrankheit der Tabaksblatter. Verh. K. Akad. Wet. Amst. 65:3–21 [Google Scholar]
  5. Bernad L, Duran-Vila N, Elena SF. 5.  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 [Google Scholar]
  6. Biebricher CK, Eigen M. 6.  2006. What is a quasispecies?. Curr. Top. Microbiol. Immunol. 299:1–31 [Google Scholar]
  7. Branch AD, Robertson HD. 7.  1984. A replication cycle for viroids and other small infectious RNAs. Science 223:450–4 [Google Scholar]
  8. Brazas R, Ganem D. 8.  1996. A cellular homolog of hepatitis delta antigen: implications for viral replication and evolution. Science 274:90–4 [Google Scholar]
  9. Briones C, Stich M, Manrubia SC. 9.  2009. The dawn of the RNA world: toward functional complexity through ligation of random RNA oligomers. RNA 15:743–49 [Google Scholar]
  10. Bruening G, Passmore BK, van Tol H, Buzayan JM, Feldstein PA. 10.  1991. Replication of a plant virus satellite RNA: Evidence favors transcription of circular templates of both polarities. Mol. Plant Microbe Interact. 4:219–25 [Google Scholar]
  11. Burch CL, Chao L. 11.  1999. Evolution by small steps and rugged landscapes in the RNA virus ϕ6. Genetics 151:921–27 [Google Scholar]
  12. Buzayan JM, Gerlach WL, Bruening G. 12.  1986. Non-enzymatic cleavage and ligation of RNAs complementary to a plant virus satellite RNA. Nature 323:349–53 [Google Scholar]
  13. Cech TR. 13.  2000. The ribosome is a ribozyme. Science 289:878–79 [Google Scholar]
  14. Chela-Flores J. 14.  1994. Are viroids molecular fossils of the RNA world?. J. Theor. Biol. 166:163–66 [Google Scholar]
  15. Chen PJ, Kalpana G, Goldberg J, Mason W, Werner B. 15.  et al. 1986. Structure and replication of the genome of the hepatitis δ virus. Proc. Natl. Acad. Sci. USA 83:8774–78 [Google Scholar]
  16. Codoñer FM, Daròs JA, Solé RV, Elena SF. 16.  2006. The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens. PLoS Pathog. 2:1187–93 [Google Scholar]
  17. Cramer P, Armache KJ, Baumli S, Benkert S, Brueckner F. 17.  et al. 2008. Structure of eukaryotic RNA polymerases. Annu. Rev. Biophys. 37:337–52 [Google Scholar]
  18. Crick FH. 18.  1968. The origin of the genetic code. J. Mol. Biol. 38:367–79 [Google Scholar]
  19. Daròs JA, Flores R. 19.  1995. Identification of a retroviroid-like element from plants. Proc. Natl. Acad. Sci. USA 92:6856–60 [Google Scholar]
  20. Daròs JA, Flores R. 20.  2002. A chloroplast protein binds a viroid RNA in vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J. 21:749–59 [Google Scholar]
  21. Daròs JA, Marcos JF, Hernández C, Flores R. 21.  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 [Google Scholar]
  22. de la Peña M, García-Robles I. 22.  2010. Ubiquitous presence of the hammerhead ribozyme motif along the tree of life. RNA 16:1943–50 [Google Scholar]
  23. de la Peña M, Navarro B, Flores R. 23.  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 [Google Scholar]
  24. Delgado S, Martínez de Alba AE, Hernández C, Flores R. 24.  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 [Google Scholar]
  25. den Boon JA, Ahlquist P. 25.  2010. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 64:241–56 [Google Scholar]
  26. Diener TO. 26.  1971. Potato spindle tuber “virus”: IV. A replicating, low molecular weight RNA. Virology 45:411–28 [Google Scholar]
  27. Diener TO. 27.  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 [Google Scholar]
  28. Diener TO. 28.  1981. Are viroids escaped introns?. Proc. Natl. Acad. Sci. USA 78:5014–15 [Google Scholar]
  29. Diener TO. 29.  1989. Circular RNAs: relics of precellular evolution?. Proc. Natl. Acad. Sci. USA 86:9370–74 [Google Scholar]
  30. Diener TO. 30.  2003. Discovering viroids: a personal perspective. Nat. Rev. Microbiol. 1:75–80 [Google Scholar]
  31. Ding B. 31.  2009. The biology of viroid-host interactions. Annu. Rev. Phytopathol. 47:105–31 [Google Scholar]
  32. Ding B. 32.  2010. Viroids: self-replicating, mobile, and fast-evolving noncoding regulatory RNAs. Wiley Interdiscip. Rev. RNA 1:362–75 [Google Scholar]
  33. Domingo E, Sabo D, Taniguchi T, Weissmann C. 33.  1978. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735–44 [Google Scholar]
  34. Eigen M. 34.  1971. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465–523 [Google Scholar]
  35. Eigen M, Schuster P. 35.  1978. The hypercycle. A principle of natural self-organization. Part C: the realistic hypercycle. Naturwissenschaften 65:341–69 [Google Scholar]
  36. Elena SF, Dopazo J, de la Peña M, Flores R, Diener TO, Moya A. 36.  2001. Phylogenetic analysis of viroid and viroid-like satellite RNAs from plants: a reassessment. J. Mol. Evol. 53:155–59 [Google Scholar]
  37. Elena SF, Dopazo J, Flores R, Diener TO, Moya A. 37.  1991. Phylogeny of viroids, viroidlike satellite RNAs, and the viroidlike domain of hepatitis δ virus RNA. Proc. Natl. Acad. Sci. USA 88:5631–34 [Google Scholar]
  38. Epstein LM, Gall JG. 38.  1987. Self-cleaving transcripts of satellite DNA from the newt. Cell 48:535–43 [Google Scholar]
  39. Fadda Z, Daròs JA, Fagoaga C, Flores R, Duran-Vila N. 39.  2003. Eggplant latent viroid, the candidate type species for a new genus within the family Avsunviroidae (hammerhead viroids). J. Virol. 77:6528–32 [Google Scholar]
  40. Fedor MJ. 40.  2000. Structure and function of the hairpin ribozyme. J. Mol. Biol. 297:269–91 [Google Scholar]
  41. Feix G, Pollet R, Weissmann C. 41.  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 [Google Scholar]
  42. Flores R, Di Serio F, Navarro B, Duran-Vila N, Owens RA. 42.  2011. Viroids and viroid diseases of plants. Studies in Viral Ecology I Microbial and Botanical Host Systems CJ Hurst 311–46 Hoboken, NJ: John Wiley & Sons [Google Scholar]
  43. Flores R, Hernández C, Martínez de Alba E, Daròs JA, Di Serio F. 43.  2005. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 43:117–39 [Google Scholar]
  44. Flores R, Semancik JS. 44.  1982. Properties of a cell-free system for synthesis of citrus exocortis viroid. Proc. Natl. Acad. Sci. USA 79:6285–88 [Google Scholar]
  45. Flores R, Serra P, Minoia S, Di Serio F, Navarro B. 45.  2012. Viroids: from genotype to phenotype just relying on RNA sequence and structural motifs. Front. Microbiol. 3:217 [Google Scholar]
  46. Forster AC, Symons RH. 46.  1987. Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell 49:211–20 [Google Scholar]
  47. Forterre P. 47.  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 [Google Scholar]
  48. Fraenkel-Conrat H. 48.  1956. The role of the nucleic acid in the reconstitution of active tobacco mosaic virus. J. Am. Chem. Soc. 78:882–83 [Google Scholar]
  49. Freeland SJ, Knight RD, Landweber LF. 49.  1999. Do proteins predate DNA?. Science 286:690–92 [Google Scholar]
  50. Fresco JR, Alberts BM, Doty P. 50.  1960. Some molecular details of the secondary structure of ribonucleic acid. Nature 188:98–101 [Google Scholar]
  51. Gago S, Elena SF, Flores R, Sanjuán R. 51.  2009. Extremely high mutation rate of a hammerhead viroid. Science 323:1308 [Google Scholar]
  52. Gandía M, Duran-Vila N. 52.  2004. Variability of the progeny of a sequence variant Citrus bent leaf viroid (CBLVd). Arch. Virol. 149:407–16 [Google Scholar]
  53. Gas ME, Hernández C, Flores R, Daròs JA. 53.  2007. Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Pathog. 3:1813–26 [Google Scholar]
  54. Gesteland RF, Atkins JF. 54.  1993. The RNA World Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
  55. Gierer A, Schramm G. 55.  1956. Infectivity of ribonucleic acid from tobacco mosaic virus. Nature 177:702–3 [Google Scholar]
  56. Gilbert W. 56.  1986. Origin of life: the RNA world. Nature 319:618 [Google Scholar]
  57. Góra-Sochacka A, Kierzek A, Candresse T, Zagórski W. 57.  1997. The genetic stability of potato spindle tuber viroid (PSTVd) molecular variants. RNA 3:68–74 [Google Scholar]
  58. Grill LK, Semancik JS. 58.  1978. RNA sequences complementary to citrus exocortis viroid in nucleic acid preparations from infected Gynura aurantiaca. Proc. Natl. Acad. Sci. USA 75:896–900 [Google Scholar]
  59. Gross HJ, Domdey H, Lossow C, Jank P, Raba M. 59.  et al. 1978. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 273:203–8 [Google Scholar]
  60. Gudima S, Wu SY, Chiang CM, Moraleda G, Taylor J. 60.  2000. Origin of hepatitis δ virus mRNA. J. Virol. 74:7204–10 [Google Scholar]
  61. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S. 61.  1983. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–57 [Google Scholar]
  62. Haag JR, Pikaard CS. 62.  2011. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 12:483–92 [Google Scholar]
  63. Hadidi A. 63.  1986. Relationship of viroids and certain other plant pathogenic nucleic acids to group I and II introns. Plant Mol. Biol. 7:129–42 [Google Scholar]
  64. Hajeri S, Ramadugu C, Manjunath K, Ng J, Lee R, Vidalakis G. 64.  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 [Google Scholar]
  65. Hammann C, Luptak A, Perreault J, de la Peña M. 65.  2012. The ubiquitous hammerhead ribozyme. RNA 18:871–85 [Google Scholar]
  66. Hammann C, Steger G. 66.  2012. Viroid-specific small RNA in plant disease. RNA Biol. 9:809–19 [Google Scholar]
  67. Hammond R, Smith DR, Diener TO. 67.  1989. Nucleotide sequence and proposed secondary structure of Columnea latent viroid: a natural mosaic of viroid sequences. Nucleic Acids Res. 17:10083–94 [Google Scholar]
  68. Haruna I, Spiegelman S. 68.  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 [Google Scholar]
  69. Hegedus K, Dallmann G, Balazs E. 69.  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 [Google Scholar]
  70. Hernández C, Daròs JA, Elena SF, Moya A, Flores R. 70.  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 [Google Scholar]
  71. Hernández C, Flores R. 71.  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 [Google Scholar]
  72. Ho CK, Shuman S. 72.  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 [Google Scholar]
  73. Hutchins CJ, Keese P, Visvader JE, Rathjen PD, McInnes JL, Symons RH. 73.  1985. Comparison of multimeric plus and minus forms of viroids and virusoids. Plant Mol. Biol. 4:293–304 [Google Scholar]
  74. Hutchins CJ, Rathjen PD, Forster AC, Symons RH. 74.  1986. Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res. 14:3627–40 [Google Scholar]
  75. Ivica NA, Obermayer B, Campbell GW, Rajamani S, Gerland U, Chen IA. 75.  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 [Google Scholar]
  76. Jenkins GM, Woelk CH, Rambaut A, Holmes EC. 76.  2000. Testing the extent of sequence similarity among viroids, satellite RNAs, and the hepatitis delta virus. J. Mol. Evol. 50:98–102 [Google Scholar]
  77. Johnston WK, Unrau PJ, Lawrence MS, Glasner ME, Bartel DP. 77.  2001. RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension. Science 292:1319–25 [Google Scholar]
  78. Juhasz A, Hegyi H, Solymosy F. 78.  1988. A novel aspect of the information content of viroids. Biochim. Biophys. Acta 950:455–58 [Google Scholar]
  79. Kiefer MC, Owens RA, Diener TO. 79.  1983. Structural similarities between viroids and transposable genetic elements. Proc. Natl. Acad. Sci. USA 80:6234–38 [Google Scholar]
  80. Kolonko N, Bannach O, Aschermann K, Hu KH, Moors M. 80.  et al. 2006. Transcription of potato spindle tuber viroid by RNA polymerase II starts in the left terminal loop. Virology 347:392–404 [Google Scholar]
  81. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR. 81.  1982. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31:147–57 [Google Scholar]
  82. Kuo MY, Goldberg J, Coates L, Mason W, Gerin J, Taylor J. 82.  1988. Molecular cloning of hepatitis delta virus RNA from an infected woodchuck liver: sequence, structure, and applications. J. Virol. 62:1855–61 [Google Scholar]
  83. Kuo MY, Sharmeen L, Dinter-Gottlieb G, Taylor J. 83.  1988. Characterization of self-cleaving RNA sequences on the genome and antigenome of human hepatitis delta virus. J. Virol. 62:4439–44 [Google Scholar]
  84. Lauring AS, Andino R. 84.  2010. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog.6:e1001005
  85. Lazcano A, Guerrero R, Margulis L, Oro J. 85.  1988. The evolutionary transition from RNA to DNA in early cells. J. Mol. Evol. 27:283–90 [Google Scholar]
  86. Lima MI, Fonseca MEN, Flores R, Kitajima EW. 86.  1994. Detection of avocado sunblotch viroid in chloroplasts of avocado leaves by in situ hybridization. Arch. Virol. 138:385–90 [Google Scholar]
  87. Lincoln TA, Joyce GF. 87.  2009. Self-sustained replication of an RNA enzyme. Science 323:1229–32 [Google Scholar]
  88. Manrubia SC, Briones C. 88.  2007. Modular evolution and increase of functional complexity in replicating RNA molecules. RNA 13:97–107 [Google Scholar]
  89. Margulis L. 89.  1993. Symbiosis in Cell Evolution New York: W.H. Freeman, 2nd ed..
  90. McInnes JL, Symons RH. 90.  1991. Comparative structure of viroids and their rapid detection using radioactive and nonradioactive nucleic acid probes. Viroids and Satellites: Molecular Parasites at the Frontier of Life K Maramorosch 21–58 Boca Raton, FL: CRC [Google Scholar]
  91. Moelling K. 91.  2013. What contemporary viruses tell us about evolution: a personal view. Arch. Virol. 158:1833–48 [Google Scholar]
  92. Mühlbach HP, Sänger HL. 92.  1979. Viroid replication is inhibited by α-amanitin. Nature 278:185–88 [Google Scholar]
  93. Navarro B, Flores R. 93.  1997. Chrysanthemum chlorotic mottle viroid: unusual structural properties of a subgroup of viroids with hammerhead ribozymes. Proc. Natl. Acad. Sci. USA 94:11262–67 [Google Scholar]
  94. Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F. 94.  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 [Google Scholar]
  95. Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F. 95.  2012. Viroids: how to infect a host and cause disease without encoding proteins. Biochimie 94:1474–80 [Google Scholar]
  96. Navarro JA, Flores R. 96.  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 [Google Scholar]
  97. Navarro JA, Vera A, Flores R. 97.  2000. A chloroplastic RNA polymerase resistant to tagetitoxin is involved in replication of Avocado sunblotch viroid. Virology 268:218–25 [Google Scholar]
  98. Nohales MA, Flores R, Daròs JA. 98.  2012. A viroid RNA redirects host DNA ligase 1 to act as an RNA ligase. Proc. Natl. Acad. Sci. USA 109:13805–10 [Google Scholar]
  99. Nohales MA, Molina-Serrano D, Flores R, Daròs JA. 99.  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 [Google Scholar]
  100. Ojosnegros S, Perales C, Mas A, Domingo E. 100.  2011. Quasispecies as a matter of fact: viruses and beyond. Virus Res. 162:203–15 [Google Scholar]
  101. Orgel LE. 101.  1968. Evolution of the genetic apparatus. J. Mol. Biol. 38:381–93 [Google Scholar]
  102. Pascal JM. 102.  2008. DNA and RNA ligases: Structural variations and shared mechanisms. Curr. Opin. Struct. Biol. 18:96–105 [Google Scholar]
  103. Pascal JM, O’Brien PJ, Tomkinson AE, Ellenberger T. 103.  2004. Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature 432:473–78 [Google Scholar]
  104. Poole AM, Logan DT. 104.  2005. Modern mRNA proofreading and repair: clues that the last universal common ancestor possessed an RNA genome?. Mol. Biol. Evol. 22:1444–55 [Google Scholar]
  105. Powner MW, Gerland B, Sutherland JD. 105.  2009. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459:239–42 [Google Scholar]
  106. Prody GA, Bakos JT, Buzayan JM, Schneider IR, Bruening G. 106.  1986. Autolytic processing of dimeric plant virus satellite RNA. Science 231:1577–80 [Google Scholar]
  107. Reanney D. 107.  1984. Genetic noise in evolution?. Nature 307:318–19 [Google Scholar]
  108. Rezaian MA. 108.  1990. Australian grapevine viroid—evidence for extensive recombination between viroids. Nucleic Acids Res. 18:1813–18 [Google Scholar]
  109. Riesner D, Henco K, Rokohl U, Klotz G, Kleinschmidt AK. 109.  et al. 1979. Structure and structure formation of viroids. J. Mol. Biol. 133:85–115 [Google Scholar]
  110. Rizzetto M, Canese MG, Aricò J, Crivelli O, Trepo C. 110.  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 [Google Scholar]
  111. Rizzetto M, Hoyer B, Canese MG, Shih JW, Purcell RH, Gerin JL. 111.  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 [Google Scholar]
  112. Robertson HD. 112.  1996. How did replicating and coding RNAs first get together?. Science 274:66–67 [Google Scholar]
  113. Rodio ME, Delgado S, de Stradis AE, Gómez MD, Flores R, Di Serio F. 113.  2007. A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 19:3610–26 [Google Scholar]
  114. Roossinck MJ, Sleat D, Palukaitis P. 114.  1992. Satellite RNAs of plant viruses: structures and biological effects. Microbiol. Rev. 56:265–79 [Google Scholar]
  115. Sanjuán R, Cuevas JM, Furió V, Holmes EC, Moya A. 115.  2007. Selection for robustness in mutagenized RNA viruses. PLoS Genet. 3:939–46 [Google Scholar]
  116. Sanjuán R, Forment J, Elena SF. 116.  2006. In silico predicted robustness of viroid RNA secondary structures. II. Interaction between mutation pairs. Mol. Biol. Evol. 23:2123–30 [Google Scholar]
  117. Sanjuán R, Forment J, Elena SF. 117.  2006. In silico predicted robustness of viroids RNA secondary structures. I. The effect of single mutations. Mol. Biol. Evol. 23:1427–36 [Google Scholar]
  118. Schiebel W, Pélissier T, Riedel L, Thalmeir S, Schiebel R. 118.  et al. 1998. Isolation of an RNA-directed RNA polymerase–specific cDNA clone from tomato. Plant Cell 10:2087–101 [Google Scholar]
  119. Schindler IM, Mühlbach HP. 119.  1992. Involvement of nuclear DNA-dependent RNA polymerases in potato spindle tuber viroid replication: a reevaluation. Plant Sci. 84:221–29 [Google Scholar]
  120. Schneider R. 120.  1969. Satellite-like particle of tobacco ringspot virus that resembles tobacco ringspot virus. Science 166:1627–29 [Google Scholar]
  121. Schuster P, Swetina J. 121.  1988. Stationary mutant distributions and evolutionary optimization. Bull. Math. Biol. 50:635–60 [Google Scholar]
  122. Semancik JS, Szychowski JA, Rakowski AG, Symons RH. 122.  1993. Isolates of citrus exocortis viroid recovered by host and tissue selection. J. Gen. Virol. 74:2427–36 [Google Scholar]
  123. Shuman S, Lima CD. 123.  2004. The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltransferases. Curr. Opin. Struct. Biol. 14:757–64 [Google Scholar]
  124. Sogo JM, Koller T, Diener TO. 124.  1973. Potato spindle tuber viroid. X: Visualization and size determination by electron microscopy. Virology 55:70–80 [Google Scholar]
  125. Sugiura M. 125.  1992. The chloroplast genome. Plant Mol. Biol. 19:149–68 [Google Scholar]
  126. Symons RH. 126.  1981. Avocado sunblotch viroid: primary sequence and proposed secondary structure. Nucleic Acids Res. 9:6527–37 [Google Scholar]
  127. Symons RH, Randles JW. 127.  1999. Encapsidated circular viroidlike satellite RNAs (virusoids) of plants. Curr. Top. Microbiol. Immunol. 239:81–105 [Google Scholar]
  128. Tabler M, Tsagris M. 128.  2004. Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci. 9:339–48 [Google Scholar]
  129. Taylor JM. 129.  2009. Replication of the hepatitis delta virus RNA genome. Adv. Virus Res. 74:103–21 [Google Scholar]
  130. Taylor JM, Pelchat M. 130.  2010. Origin of hepatitis δ virus. Future Microbiol. 5:393–402 [Google Scholar]
  131. Tessitori M, Rizza S, Reina A, Causarano G, Di Serio F. 131.  2013. The genetic diversity of Citrus dwarfing viroid populations is mainly dependent on the infected host species. J. Gen. Virol. 94:687–93 [Google Scholar]
  132. Tsagris EM, Martínez de Alba AE, Gozmanova M, Kalantidis K. 132.  2008. Viroids. Cell Microbiol. 10:2168–79 [Google Scholar]
  133. Verhoeven JT, Meekes ET, Roenhorst JW, Flores R, Serra P. 133.  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 [Google Scholar]
  134. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 134.  2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–48 [Google Scholar]
  135. Visvader JE, Symons RH. 135.  1985. Eleven new sequence variants of citrus exocortis viroid and the correlation of sequence with pathogenicity. Nucleic Acids Res. 13:2907–20 [Google Scholar]
  136. Wang KS, Choo QL, Weiner AJ, Ou JH, Najarian RC. 136.  et al. 1986. Structure, sequence and expression of the hepatitis delta (δ) viral genome. Nature 323:508–14Corrigendum 1987. Nature 328:456 [Google Scholar]
  137. Wang LK, Schwer B, Shuman S. 137.  2006. Structure-guided mutational analysis of T4 RNA ligase 1. RNA 12:2126–34 [Google Scholar]
  138. Wassenegger M, Krczal G. 138.  2006. Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci. 11:142–51 [Google Scholar]
  139. Wassenegger M, Spieker RL, Thalmeir S, Gast FU, Riedel L, Sänger HL. 139.  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 [Google Scholar]
  140. Webb C-HT, Riccitelli NJ, Ruminski DJ, Lupták A. 140.  2009. Widespread occurrence of self-cleaving ribozymes. Science 326:953 [Google Scholar]
  141. Wilke CO, Wang JL, Ofria C, Lenski RE, Adami C. 141.  2001. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412:331–33 [Google Scholar]
  142. Wochner A, Attwater J, Coulson A, Holliger P. 142.  2011. Ribozyme-catalyzed transcription of an active ribozyme. Science 332:209–12 [Google Scholar]
  143. Woese CR. 143.  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. 144.  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 [Google Scholar]
  145. Xiong Y, Eickbush TH. 145.  1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9:3353–62 [Google Scholar]
  146. Zhang ZX, Chen SS, Qi SS, Ding SW, Wu QF, Li SF. 146.  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. 147.  2008. A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 20:35–47 [Google Scholar]
/content/journals/10.1146/annurev-micro-091313-103416
Loading
/content/journals/10.1146/annurev-micro-091313-103416
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error