Skip to main content

Viroids: Small Noncoding Infectious RNAs with the Remarkable Ability of Autonomous Replication

  • Chapter
  • First Online:
Current Research Topics in Plant Virology

Abstract

Viroids are infectious agents of plants, constituted exclusively by a noncoding small (246–401 nucleotides) circular RNA molecule. When this RNA manages to enter a cell of an appropriate host plant, it moves to the subcellular replication site and replicates through an RNA-to-RNA rolling circle mechanism. Viroid progeny is then able to move cell-to-cell through plamodesmata and long distances through the phloem to invade distal parts of host plants. Two types of viroids exist, classified into the families Pospiviroidae and Avsunviroidae. They replicate in the nucleus (Pospiviroidae) and chloroplast (Avsunviroidae), hijacking host enzymes. Members of the family Pospiviroidae recruit host DNA-dependent RNA polymerase II, RNase III and DNA ligase 1, while members of the Avsunviroidae (which contain embedded hammerhead ribozymes for self-cleavage) use host nuclear-encoded chloroplastic RNA polymerase and the chloroplastic isoform of tRNA ligase. Viroids are mainly transmitted mechanically from plant to plant, and frequently exert a pathogenic effect on infected plants. Some symptoms in viroid infections are induced by the viroid-derived small RNAs produced by the host defensive RNA silencing machinery. Interestingly, viroids are targets of the host Dicer-like and RNA-dependent RNA polymerase enzymes, but are particularly resistant to the action of the RNA-induced silencing complex.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abelson J, Trotta CR, Li H (1998) tRNA splicing. J Biol Chem 273:12685–12688

    Article  CAS  PubMed  Google Scholar 

  • AbouHaidar MG, Venkataraman S, Golshani A, Liu B, Ahmad T (2014) Novel coding, translation, and gene expression of a replicating covalently closed circular RNA of 220 nt. Proc Natl Acad Sci U S A 111:14542–14547. doi:10.1073/pnas.1402814111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abraitiene A, Zhao Y, Hammond R (2008) Nuclear targeting by fragmentation of the potato spindle tuber viroid genome. Biochem Biophys Res Commun 368:470–475. doi:10.1016/j.bbrc.2008.01.043

    Article  CAS  PubMed  Google Scholar 

  • Adams I, Harrison C, Tomlinson J, Boonham N (2015) Microarray platform for the detection of a range of plant viruses and viroids. Methods Mol Biol 1302:273–282. doi:10.1007/978-1-4939-2620-6_20

    Article  PubMed  Google Scholar 

  • Antignus Y, Lachman O, Pearlsman M (2007) Spread of Tomato apical stunt viroid (TASVd) in greenhouse tomato crops is associated with seed transmission and bumble bee activity. Plant Dis 91:47–50. doi:10.1094/pd-91-0047

    Article  CAS  Google Scholar 

  • Bani-Hashemian SM, Pensabene-Bellavia G, Duran-Vila N, Serra P (2015) Phloem restriction of viroids in three citrus hosts is overcome by grafting with Etrog citron: potential involvement of a translocatable factor. J Gen Virol. doi:10.1099/vir.0.000154

    PubMed  Google Scholar 

  • Baumstark T, Schröder AR, Riesner D (1997) Viroid processing: switch from cleavage to ligation is driven by a change from a tetraloop to a loop E conformation. EMBO J 16:599–610. doi:10.1093/emboj/16.3.599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bojic T, Beeharry Y, da Zhang J, Pelchat M (2012) Tomato RNA polymerase II interacts with the rod-like conformation of the left terminal domain of the potato spindle tuber viroid positive RNA genome. J Gen Virol 93:1591–1600. doi:10.1099/vir.0.041574-0

    Article  CAS  PubMed  Google Scholar 

  • Bolduc F, Hoareau C, St-Pierre P, Perreault JP (2010) In-depth sequencing of the siRNAs associated with peach latent mosaic viroid infection. BMC Mol Biol 11:16. doi:10.1186/1471-2199-11-16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonfiglioli RG, McFadden GI, Symons RH (1994) In-situ hybridization localizes avocado aunblotch viroid on chloroplast thylakoid membranes and coconut cadang cadang viroid in the nucleus. Plant J 6:99–103

    Article  Google Scholar 

  • Botermans M, van de Vossenberg BT, Verhoeven JT, Roenhorst JW, Hooftman M, Dekter R, Meekes ET (2013) Development and validation of a real-time RT-PCR assay for generic detection of pospiviroids. J Virol Methods 187:43–50. doi:10.1016/j.jviromet.2012.09.004

    Article  CAS  PubMed  Google Scholar 

  • Branch AD, Robertson HD (1984) A replication cycle for viroids and other small infectious RNAs. Science 223:450–455

    Article  CAS  PubMed  Google Scholar 

  • Branch AD, Benenfeld BJ, Robertson HD (1988) Evidence for a single rolling circle in the replication of potato spindle tuber viroid. Proc Natl Acad Sci U S A 85:9128–9132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bussière F, Lehoux J, Thompson DA, Skrzeczkowski LJ, Perreault J (1999) Subcellular localization and rolling circle replication of peach latent mosaic viroid: hallmarks of group A viroids. J Virol 73:6353–6360

    PubMed  PubMed Central  Google Scholar 

  • Carbonell A, De la Peña M, Flores R, Gago S (2006) Effects of the trinucleotide preceding the self-cleavage site on eggplant latent viroid hammerheads: differences in co- and post-transcriptional self-cleavage may explain the lack of trinucleotide AUC in most natural hammerheads. Nucleic Acids Res 34:5613–5622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carbonell A, Martínez de Alba AE, Flores R, Gago S (2008) Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families. Virology 371:44–53. doi:10.1016/j.virol.2007.09.031

    Article  CAS  PubMed  Google Scholar 

  • Chaturvedi S, Kalantidis K, Rao AL (2014) A bromodomain-containing host protein mediates the nuclear importation of a satellite RNA of Cucumber mosaic virus. J Virol 88:1890–1896. doi:10.1128/JVI.03082-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chiumenti M, Torchetti EM, Di Serio F, Minafra A (2014) Identification and characterization of a viroid resembling apple dimple fruit viroid in fig (Ficus carica L.) by next generation sequencing of small RNAs. Virus Res 188:54–59. doi:10.1016/j.virusres.2014.03.026

    Article  CAS  PubMed  Google Scholar 

  • Dalakouras A, Dadami E, Wassenegger M (2013) Viroid-induced DNA methylation in plants. Biomol Concepts 4:557–565. doi:10.1515/bmc-2013-0030

    Article  CAS  PubMed  Google Scholar 

  • Dalakouras A, Dadami E, Bassler A, Zwiebel M, Krczal G, Wassenegger M (2015) Replicating Potato spindle tuber viroid mediates de novo methylation of an intronic viroid sequence but no cleavage of the corresponding pre-mRNA. RNA Biol 12:268–275. doi:10.1080/15476286.2015.1017216

    Article  PubMed  PubMed Central  Google Scholar 

  • Daròs JA, Flores R (1995) Identification of a retroviroid-like element from plants. Proc Natl Acad Sci U S A 92:6856–6860

    Article  PubMed  PubMed Central  Google Scholar 

  • Daròs JA, Flores R (2002) A chloroplast protein binds a viroid RNA in vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J 21:749–759

    Article  PubMed  PubMed Central  Google Scholar 

  • Daròs JA, Flores R (2004) Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae. Proc Natl Acad Sci U S A 101:6792–6797. doi:10.1073/pnas.0401090101

    Article  PubMed  PubMed Central  Google Scholar 

  • Daròs JA, Marcos JF, Hernández 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 U S A 91:12813–12817

    Article  PubMed  PubMed Central  Google Scholar 

  • Daròs JA, Elena SF, Flores R (2006) Viroids: an Ariadne’s thread into the RNA labyrinth. EMBO Rep 7:593–598

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Daròs JA, Aragonés V, Cordero MT (2014) Recombinant RNA production. Patent EP14382177.5, PCT/EP2015/060912

    Google Scholar 

  • Davies JW, Kaesberg P, Diener TO (1974) Potato spindle tuber viroid XII. An investigation of viroid RNA as a messenger for protein synthesis. Virology 61:281–286

    Article  CAS  PubMed  Google Scholar 

  • Davies C, Sheldon CC, Symons RH (1991) Alternative hammerhead structures in the self-cleavage of avocado sunblotch viroid RNAs. Nucleic Acids Res 19:1893–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De la Peña M, Flores R (2002) Chrysanthemum chlorotic mottle viroid RNA: dissection of the pathogenicity determinant and comparative fitness of symptomatic and non-symptomatic variants. J Mol Biol 321:411–421

    Article  PubMed  CAS  Google Scholar 

  • De la Peña M, Gago S, Flores R (2003) Peripheral regions of natural hammerhead ribozymes greatly increase their self-cleavage activity. EMBO J 22:5561–5570

    Article  PubMed  PubMed Central  Google Scholar 

  • Delgado S, Martínez de Alba AE, Hernández 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 79:12934–12943. doi:10.1128/JVI.79.20.12934-12943.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Serio F, Daròs JA, Ragozzino A, Flores R (1997) A 451-nucleotide circular RNA from cherry with hammerhead ribozymes in its strands of both polarities. J Virol 71:6603–6610

    PubMed  PubMed Central  Google Scholar 

  • Di Serio F, Gisel A, Navarro B, Delgado S, Martínez de Alba AE, Donvito G, Flores R (2009) Deep sequencing of the small RNAs derived from two symptomatic variants of a chloroplastic viroid: implications for their genesis and for pathogenesis. PLoS One 4:e7539. doi:10.1371/journal.pone.0007539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Di Serio F, Martínez de Alba AE, Navarro B, Gisel A, Flores R (2010) RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. J Virol 84:2477–2489. doi:10.1128/JVI.02336-09

    Article  PubMed  CAS  Google Scholar 

  • Di Serio F, Flores R, Verhoeven JT, Li SF, Pallás V, Randles JW, Sano T, Vidalakis G, Owens RA (2014) Current status of viroid taxonomy. Arch Virol 159:3467–3478. doi:10.1007/s00705-014-2200-6

    Article  PubMed  CAS  Google Scholar 

  • Diener TO (1971a) Potato spindle tuber “virus” IV. A replicating, low molecular weight RNA. Virology 45:411–428

    Google Scholar 

  • Diener TO (1971b) Potato spindle tuber virus: a plant virus with properties of a free nucleic acid. III. Subcellular location of PSTV-RNA and the question of whether virions exist in extracts or in situ. Virology 43:75–89

    Google Scholar 

  • Diener TO (1972) Potato spindle tuber viroid VIII. Correlation of infectivity with a UV-absorbing component and thermal denaturation properties of the RNA. Virology 50:606–609

    Article  CAS  PubMed  Google Scholar 

  • Diener TO (1986) Viroid processing: a model involving the central conserved region and hairpin I. Proc Natl Acad Sci U S A 83:58–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diener TO (1989) Circular RNAs: relics of precellular evolution? Proc Natl Acad Sci U S A 86:9370–9374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diener TO (2003) Discovering viroids – a personal perspective. Nat Rev Microbiol 1:75–80. doi:10.1038/nrmicro736

    Article  CAS  PubMed  Google Scholar 

  • Diener TO, Raymer WB (1967) Potato spindle tuber virus: a plant virus with properties of a free nucleic acid. Science 158:378–381

    Article  CAS  PubMed  Google Scholar 

  • Diermann N, Matousek J, Junge M, Riesner D, Steger G (2010) Characterization of plant miRNAs and small RNAs derived from potato spindle tuber viroid (PSTVd) in infected tomato. Biol Chem 391:1379–1390. doi:10.1515/BC.2010.148

    Article  CAS  PubMed  Google Scholar 

  • Ding B (2009) The biology of viroid-host interactions. Annu Rev Phytopathol 47:105–131

    Article  CAS  PubMed  Google Scholar 

  • Ding SW (2010) RNA-based antiviral immunity. Nat Rev Immunol 10:632–644. doi:10.1038/nri2824

    Article  CAS  PubMed  Google Scholar 

  • Ding B, Itaya A (2007) Viroid: a useful model for studying the basic principles of infection and RNA biology. Mol Plant Microbe Interact 20:7–20. doi:10.1094/MPMI-20-0007

    Article  CAS  PubMed  Google Scholar 

  • Ding B, Itaya A, Zhong X (2005) Viroid trafficking: a small RNA makes a big move. Curr Opin Plant Biol 8:606–612. doi:10.1016/j.pbi.2005.09.001

    Article  CAS  PubMed  Google Scholar 

  • Eamens AL, Smith NA, Dennis ES, Wassenegger M, Wang MB (2014) In Nicotiana species, an artificial microRNA corresponding to the virulence modulating region of Potato spindle tuber viroid directs RNA silencing of a soluble inorganic pyrophosphatase gene and the development of abnormal phenotypes. Virology 450–451:266–277. doi:10.1016/j.virol.2013.12.019

    Article  PubMed  CAS  Google Scholar 

  • Eiras M, Silva SR, Stuchi ES, Flores R, Daròs JA (2010) Viroid species associated with the bark-cracking phenotype of ‘Tahiti’ acid lime in the State of São Paulo, Brazil. Trop Plant Pathol 35:303–309

    Google Scholar 

  • Elena SF, Dopazo J, Flores R, Diener TO, Moya A (1991) Phylogeny of viroids, viroidlike satellite RNAs, and the viroidlike domain of hepatitis delta virus RNA. Proc Natl Acad Sci U S A 88:5631–5634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Englert M, Latz A, Becker D, Gimple O, Beier H, Akama K (2007) Plant pre-tRNA splicing enzymes are targeted to multiple cellular compartments. Biochimie 89:1351–1365

    Article  CAS  PubMed  Google Scholar 

  • Fadda Z, Daròs 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 77:6528–6532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flores R, Semancik JS (1982) Properties of a cell-free system for synthesis of citrus exocortis viroid. Proc Natl Acad Sci U S A 79:6285–6288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flores R, Daròs JA, Hernández C (2000) The Avsunviroidae family: viroids containing hammerhead ribozymes. AdvVirus Res 55:271–323

    CAS  Google Scholar 

  • Flores R, Hernández C, de la Peña M, Vera A, Daròs JA (2001) Hammerhead ribozyme structure and function in plant RNA replication. Methods Enzymol 341:540–552

    Article  CAS  PubMed  Google Scholar 

  • Flores R, Hernández C, Martínez de Alba AE, Daròs JA, Di Serio F (2005) Viroids and viroid-host interactions. Annu Rev Phytopathol 43:117–139

    Article  CAS  PubMed  Google Scholar 

  • Flores R, Ruiz-Ruiz S, Serra P (2012) Viroids and hepatitis delta virus. Semin Liver Dis 32:201–210. doi:10.1055/s-0032-1323624

    Article  CAS  PubMed  Google Scholar 

  • Flores R, Gago-Zachert S, Serra P, Sanjuán R, Elena SF (2014) Viroids: survivors from the RNA world? Annu Rev Microbiol 68:395–414. doi:10.1146/annurev-micro-091313-103416

    Article  CAS  PubMed  Google Scholar 

  • Flores R, Minoia S, Carbonell A, Gisel A, Delgado S, López-Carrasco A, Navarro B, Di Serio F (2015) Viroids, the simplest RNA replicons: How they manipulate their hosts for being propagated and how their hosts react for containing the infection. Virus Res. doi:10.1016/j.virusres.2015.02.027

    Google Scholar 

  • Forster AC, Davies C, Sheldon CC, Jeffries AC, Symons RH (1988) Self-cleaving viroid and newt RNAs may only be active as dimers. Nature 334:265–267

    Article  CAS  PubMed  Google Scholar 

  • Füssy Z, Patzak J, Stehlík J, Matoušek J (2013) Imbalance in expression of hop (Humulus lupulus) chalcone synthase H1 and its regulators during hop stunt viroid pathogenesis. J Plant Physiol 170:688–695. doi:10.1016/j.jplph.2012.12.006

    Article  PubMed  CAS  Google Scholar 

  • Gas ME, Hernández C, Flores R, Daròs JA (2007) Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Pathog 3:e182. doi:10.1371/journal.ppat.0030182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gas ME, Molina-Serrano D, Hernández C, Flores R, Daròs JA (2008) Monomeric linear RNA of Citrus exocortis viroid resulting from processing in vivo has 5′-phosphomonoester and 3′-hydroxyl termini: implications for the RNase and RNA ligase involved in replication. J Virol 82:10321–10325. doi:10.1128/JVI.01229-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giguère T, Adkar-Purushothama CR, Bolduc F, Perreault JP (2014a) Elucidation of the structures of all members of the Avsunviroidae family. Mol Plant Pathol 15:767–779

    Article  PubMed  CAS  Google Scholar 

  • Giguère T, Adkar-Purushothama CR, Perreault JP (2014b) Comprehensive secondary structure elucidation of four genera of the family Pospiviroidae. PLoS One 9:e98655. doi:10.1371/journal.pone.0098655

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gómez G, Pallás V (2001) Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol Plant Microbe Interact 14:910–913. doi:10.1094/MPMI.2001.14.7.910

    Article  PubMed  Google Scholar 

  • Gómez G, Pallás V (2004) A long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with Hop stunt viroid RNA. J Virol 78:10104–10110. doi:10.1128/JVI.78.18.10104-10110.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gómez G, Pallás V (2007) Mature monomeric forms of Hop stunt viroid resist RNA silencing in transgenic plants. Plant J 51:1041–1049. doi:10.1111/j.1365-313X.2007.03203.x

    Article  PubMed  CAS  Google Scholar 

  • Gómez G, Pallás V (2010) Noncoding RNA mediated traffic of foreign mRNA into chloroplasts reveals a novel signaling mechanism in plants. PLoS One 5:e12269. doi:10.1371/journal.pone.0012269

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gómez G, Pallás V (2012) Studies on subcellular compartmentalization of plant pathogenic noncoding RNAs give new insights into the intracellular RNA-traffic mechanisms. Plant Physiol 159:558–564. doi:10.1104/pp.112.195214

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grill LK, Semancik JS (1978) RNA sequences complementary to citrus exocortis viroid in nucleic acid preparations from infected Gynura aurantiaca. Proc Natl Acad Sci U S A 75:896–900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gross HJ, Domdey H, Lossow C, Jank P, Raba M, Alberty H, Sänger HL (1978) Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 273:203–208

    Article  CAS  PubMed  Google Scholar 

  • Hajizadeh M, Navarro B, Bashir NS, Torchetti EM, Di Serio F (2012) Development and validation of a multiplex RT-PCR method for the simultaneous detection of five grapevine viroids. J Virol Methods 179:62–69. doi:10.1016/j.jviromet.2011.09.022

    Article  CAS  PubMed  Google Scholar 

  • Hou WY, Li SF, Wu ZJ, Jiang DM, Sano T (2009a) Coleus blumei viroid 6: a new tentative member of the genus Coleviroid derived from natural genome shuffling. Arch Virol 154:993–997. doi:10.1007/s00705-009-0388-7

    Article  CAS  PubMed  Google Scholar 

  • Hou WY, Sano T, Li F, Wu ZJ, Li L, Li SF (2009b) Identification and characterization of a new coleviroid (CbVd-5). Arch Virol 154:315–320. doi:10.1007/s00705-008-0276-6

    Article  CAS  PubMed  Google Scholar 

  • Hu CC, Hsu YH, Lin NS (2009) Satellite RNAs and satellite viruses of plants. Viruses 1:1325–1350. doi:10.3390/v1031325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hutchins CJ, Rathjen PD, Forster AC, Symons RH (1986) Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res 14:3627–3640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itaya A, Folimonov A, Matsuda Y, Nelson RS, Ding B (2001) Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol Plant Microbe Interact 14:1332–1334. doi:10.1094/MPMI.2001.14.11.1332

    Article  CAS  PubMed  Google Scholar 

  • Itaya A, Matsuda Y, Gonzales RA, Nelson RS, Ding B (2002) Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Mol Plant Microbe Interact 15:990–999. doi:10.1094/MPMI.2002.15.10.990

    Article  CAS  PubMed  Google Scholar 

  • Itaya A, Zhong X, Bundschuh R, Qi Y, Wang Y, Takeda R, Harris AR, Molina C, Nelson RS, Ding B (2007) 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 81:2980–2994. doi:10.1128/JVI.02339-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito T, Suzaki K, Nakano M, Sato A (2013) Characterization of a new apscaviroid from American persimmon. Arch Virol 158:2629–2631. doi:10.1007/s00705-013-1772-x

    Article  CAS  PubMed  Google Scholar 

  • Jiang D, Guo R, Wu Z, Wang H, Li S (2009) Molecular characterization of a member of a new species of grapevine viroid. Arch Virol 154:1563–1566. doi:10.1007/s00705-009-0454-1

    Article  CAS  PubMed  Google Scholar 

  • Kasai A, Sano T, Harada T (2013) Scion on a stock producing siRNAs of potato spindle tuber viroid (PSTVd) attenuates accumulation of the viroid. PLoS One 8:e57736. doi:10.1371/journal.pone.0057736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keese P, Symons RH (1985) Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc Natl Acad Sci U S A 82:4582–4586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khoury J, Singh RP, Boucher A, Coombs DH (1988) Concentration and distribution of mild and sever strains of potato spindle tuber viroid in cross-protected tomato plants. Phytopathology 78:1331–1336. doi:10.1094/Phyto-78-1331

    Article  Google Scholar 

  • Khvorova A, Lescoute A, Westhof E, Jayasena SD (2003) Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat Struct Biol 10:708–712

    Article  CAS  PubMed  Google Scholar 

  • Kolonko N, Bannach O, Aschermann K, Hu KH, Moors M, Schmitz M, Steger G, Riesner D (2006) Transcription of potato spindle tuber viroid by RNA polymerase II starts in the left terminal loop. Virology 347:392–404. doi:10.1016/j.virol.2005.11.039

    Article  CAS  PubMed  Google Scholar 

  • Li F, Ding SW (2006) Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol 60:503–531. doi:10.1146/annurev.micro.60.080805.142205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Baysal-Gurel F, Abdo Z, Miller SA, Ling KS (2015) Evaluation of disinfectants to prevent mechanical transmission of viruses and a viroid in greenhouse tomato production. Virology J 12:5. doi:10.1186/s12985-014-0237-5

    Article  CAS  Google Scholar 

  • Lima MI, Fonseca ME, Flores R, Kitajima EW (1994) Detection of avocado sunblotch viroid in chloroplasts of avocado leaves by in situ hybridization. Arch Virol 138:385–390

    Article  CAS  PubMed  Google Scholar 

  • Lin L, Li R, Mock R, Kinard G (2011) Development of a polyprobe to detect six viroids of pome and stone fruit trees. J Virol Methods 171:91–97. doi:10.1016/j.jviromet.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  • Lisón P, Tárraga S, López-Gresa P, Saurí A, Torres C, Campos L, Bellés JM, Conejero V, Rodrigo I (2013) A noncoding plant pathogen provokes both transcriptional and posttranscriptional alterations in tomato. Proteomics 13:833–844. doi:10.1002/pmic.201200286

    Article  PubMed  CAS  Google Scholar 

  • Malandraki I, Varveri C, Olmos A, Vassilakos N (2015) One-step multiplex quantitative RT-PCR for the simultaneous detection of viroids and phytoplasmas of pome fruit trees. J Virol Methods 213:12–17. doi:10.1016/j.jviromet.2014.11.010

    Article  CAS  PubMed  Google Scholar 

  • Malfitano M, Di Serio F, Covelli L, Ragozzino A, Hernández C, Flores R (2003) Peach latent mosaic viroid variants inducing peach calico (extreme chlorosis) contain a characteristic insertion that is responsible for this symptomatology. Virology 313:492–501

    Article  CAS  PubMed  Google Scholar 

  • Martín R, Arenas C, Daròs JA, Covarrubias A, Reyes JL, Chua NH (2007) Characterization of small RNAs derived from Citrus exocortis viroid (CEVd) in infected tomato plants. Virology 367:135–146. doi:10.1016/j.virol.2007.05.011

    Article  PubMed  CAS  Google Scholar 

  • Martínez de Alba AE, Flores R, Hernández C (2002) Two chloroplastic viroids induce the accumulation of small RNAs associated with posttranscriptional gene silencing. J Virol 76:13094–13096

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martínez G, Donaire L, Llave C, Pallás V, Gómez G (2010) High-throughput sequencing of Hop stunt viroid-derived small RNAs from cucumber leaves and phloem. Mol Plant Pathol 11:347–359. doi:10.1111/j.1364-3703.2009.00608.x

    Article  PubMed  Google Scholar 

  • Martinez G, Castellano M, Tortosa M, Pallas V, Gomez G (2014) A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucleic Acids Res 42:1553–1562. doi:10.1093/nar/gkt968

    Article  CAS  PubMed  Google Scholar 

  • Matsuura S, Matsushita Y, Kozuka R, Shimizu S, Tsuda S (2010) Transmission of Tomato chlorotic dwarf viroid by bumblebees (Bombus ignitus) in tomato plants. Eur J Plant Pathol 126:111–115

    Article  Google Scholar 

  • Minoia S, Carbonell A, Di Serio F, Gisel A, Carrington JC, Navarro B, Flores R (2014a) Specific Argonautes selectively bind small RNAs derived from potato spindle tuber viroid and attenuate viroid accumulation in vivo. J Virol 88:11933–11945. doi:10.1128/JVI.01404-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Minoia S, Navarro B, Covelli L, Barone M, Garcia-Becedas MT, Ragozzino A, Alioto D, Flores R, Di Serio F (2014b) Viroid-like RNAs from cherry trees affected by leaf scorch disease: further data supporting their association with mycoviral double-stranded RNAs. Arch Virol 159:589–593

    Article  CAS  Google Scholar 

  • Minoia S, Navarro B, Delgado S, Di Serio F, Flores R (2015) Viroid RNA turnover: characterization of the subgenomic RNAs of potato spindle tuber viroid accumulating in infected tissues provides insights into decay pathways operating in vivo. Nucleic Acids Res 43:2313–2325. doi:10.1093/nar/gkv034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nat Rev Genet 15:423–437. doi:10.1038/nrg3722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Motard J, Bolduc F, Thompson D, Perreault JP (2008) The peach latent mosaic viroid replication initiation site is located at a universal position that appears to be defined by a conserved sequence. Virology 373:362–375. doi:10.1016/j.virol.2007.12.010

    Article  CAS  PubMed  Google Scholar 

  • Mühlbach HP, Sänger HL (1979) Viroid replication is inhibited by α-amanitin. Nature 278:185–188

    Article  PubMed  Google Scholar 

  • Murcia N, Serra P, Olmos A, Duran-Vila N (2009) A novel hybridization approach for detection of citrus viroids. Mol Cell Probes 23:95–102. doi:10.1016/j.mcp.2008.12.007

    Article  CAS  PubMed  Google Scholar 

  • Murcia N, Bernad L, Duran-Vila N, Serra P (2011) Two nucleotide positions in the Citrus exocortis viroid RNA associated with symptom expression in Etrog citron but not in experimental herbaceous hosts. Mol Plant Pathol 12:203–208. doi:10.1111/j.1364-3703.2010.00662.x

    Article  CAS  PubMed  Google Scholar 

  • Nakaune R, Nakano M (2008) Identification of a new Apscaviroid from Japanese persimmon. Arch Virol 153:969–972. doi:10.1007/s00705-008-0073-2

    Article  CAS  PubMed  Google Scholar 

  • Nam M, Kim JS, Lim S, Park CY, Kim JG, Choi HS, Lim HS, Moon JS, Lee SH (2014) Development of the large-scale oligonucleotide chip for the diagnosis of plant viruses and its practical use. Plant Pathol J 30:51–57. doi:10.5423/PPJ.OA.08.2013.0084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:2662–2670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navarro JA, Daròs JA, Flores R (1999) Complexes containing both polarity strands of avocado sunblotch viroid: identification in chloroplasts and characterization. Virology 253:77–85

    Article  CAS  PubMed  Google Scholar 

  • Navarro JA, Vera A, Flores R (2000) A chloroplastic RNA polymerase resistant to tagetitoxin is involved in replication of avocado sunblotch viroid. Virology 268:218–225

    Article  CAS  PubMed  Google Scholar 

  • Navarro B, Pantaleo V, Gisel A, Moxon S, Dalmay T, Bisztray G, Di Serio F, Burgyán J (2009) Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant-viroid interaction. PLoS One 4:e7686. doi:10.1371/journal.pone.0007686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F (2012a) 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. doi:10.1111/j.1365-313X.2012.04940.x

    Article  CAS  PubMed  Google Scholar 

  • Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F (2012b) Viroids: How to infect a host and cause disease without encoding proteins. Biochimie 94:1474–1480. doi:10.1016/j.biochi.2012.02.020

    Article  CAS  PubMed  Google Scholar 

  • Niblett CL, Dickson E, Fernow KH, Horst RK, Zaitlin M (1978) Cross protection among four viroids. Virology 91:198–203

    Article  CAS  PubMed  Google Scholar 

  • Nohales MA, Flores R, Daròs JA (2012a) Viroid RNA redirects host DNA ligase 1 to act as an RNA ligase. Proc Natl Acad Sci U S A 109:13805–13810. doi:10.1073/pnas.1206187109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nohales MA, Molina-Serrano D, Flores R, Daròs JA (2012b) Involvement of the chloroplastic isoform of tRNA ligase in the replication of viroids belonging to the family Avsunviroidae. J Virol 86:8269–8276. doi:10.1128/JVI.00629-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Owens RA, Blackburn M, Ding B (2001) Possible involvement of the phloem lectin in long-distance viroid movement. Mol Plant Microbe Interact 14:905–909. doi:10.1094/MPMI.2001.14.7.905

    Article  CAS  PubMed  Google Scholar 

  • Owens RA, Flores R, Di Serio F, Li SF, Pallás V, Randles JW, Sano T, Vidalakis G (2012a) Viroids. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, Academic Press, London, UK, pp 1221–1234

    Google Scholar 

  • Owens RA, Tech KB, Shao JY, Sano T, Baker CJ (2012b) Global analysis of tomato gene expression during Potato spindle tuber viroid infection reveals a complex array of changes affecting hormone signaling. Mol Plant Microbe Interact 25:582–598. doi:10.1094/MPMI-09-11-0258

    Article  CAS  PubMed  Google Scholar 

  • Palukaitis P (2014) What has been happening with viroids? Virus Genes 49:175–184. doi:10.1007/s11262-014-1110-8

    Article  CAS  PubMed  Google Scholar 

  • Papaefthimiou I, Hamilton A, Denti M, Baulcombe D, Tsagris M, Tabler M (2001) Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res 29:2395–2400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pelchat M, Côté F, Perreault JP (2001) Study of the polymerization step of the rolling circle replication of peach latent mosaic viroid. Arch Virol 146:1753–1763

    Article  CAS  PubMed  Google Scholar 

  • Prody GA, Bakos JT, Buzayan JM, Schneider IR, Bruening G (1986) Autolytic processing of dimeric plant-virus satellite RNA. Science 231:1577–1580

    Article  CAS  PubMed  Google Scholar 

  • Qi Y, Ding B (2003) Differential subnuclear localization of RNA strands of opposite polarity derived from an autonomously replicating viroid. Plant Cell 15:2566–2577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi Y, Pélissier T, Itaya A, Hunt E, Wassenegger M, Ding B (2004) Direct role of a viroid RNA motif in mediating directional RNA trafficking across a specific cellular boundary. Plant Cell 16:1741–1752. doi:10.1105/tpc.021980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Randles JW, Rodriguez MJ, Imperial JS (1988) Cadang-cadang disease of coconut palm. Microbiol Sci 5:18–22

    CAS  PubMed  Google Scholar 

  • Rao AL, Kalantidis K (2015) Virus-associated small satellite RNAs and viroids display similarities in their replication strategies. Virology 479–480C:627–636. doi:10.1016/j.virol.2015.02.018

    Google Scholar 

  • Rizza S, Conesa A, Juarez J, Catara A, Navarro L, Duran-Vila N, Ancillo G (2012) Microarray analysis of Etrog citron (Citrus medica L.) reveals changes in chloroplast, cell wall, peroxidase and symporter activities in response to viroid infection. Mol Plant Pathol 13:852–864. doi:10.1111/j.1364-3703.2012.00794.x

    Article  CAS  PubMed  Google Scholar 

  • Rocheleau L, Pelchat M (2006) The Subviral RNA Database: a toolbox for viroids, the hepatitis delta virus and satellite RNAs research. BMC Microbiol 6:24. doi:10.1186/1471-2180-6-24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sänger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK (1976) Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci U S A 73:3852–3856

    Article  PubMed  PubMed Central  Google Scholar 

  • Sano T, Barba M, Li SF, Hadidi A (2010) Viroids and RNA silencing: mechanism, role in viroid pathogenicity and development of viroid-resistant plants. GM Crops 1:80–86. doi:10.4161/gmcr.1.2.11871

    Article  PubMed  Google Scholar 

  • Schumacher J, Randles JW, Riesner D (1983) A two-dimensional electrophoretic technique for the detection of circular viroids and virusoids. Anal Biochem 135:288–295

    Article  CAS  PubMed  Google Scholar 

  • Semancik JS, Weathers LG (1972) Exocortis disease: evidence for a new species of “infectious” low molecular weight RNA in plants. Nat New Biol 237:242–244

    Article  CAS  PubMed  Google Scholar 

  • Serra P, Barbosa CJ, Daròs JA, Flores R, Duran-Vila N (2008) Citrus viroid V: molecular characterization and synergistic interactions with other members of the genus Apscaviroid. Virology 370:102–112

    Article  CAS  PubMed  Google Scholar 

  • Shimura H, Pantaleo V, Ishihara T, Myojo N, Inaba J, Sueda K, Burgyán J, Masuta C (2011) A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog 7:e1002021. doi:10.1371/journal.ppat.1002021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh RP, Dilworth AD, Ao XP, Singh M, Baranwal VK (2009) Citrus exocortis viroid transmission through commercially-distributed seeds of Impatiens and Verbena plants. Eur J Plant Pathol 124:691–694. doi:10.1007/s10658-009-9440-4

    Article  Google Scholar 

  • Sogo JM, Koller T, Diener TO (1973) Potato spindle tuber viroid. X. Visualization and size determination by electron microscopy. Virology 55:70–80

    Article  CAS  PubMed  Google Scholar 

  • Solovyev AG, Makarova SS, Remizowa MV, Lim HS, Hammond J, Owens RA, Kopertekh L, Schiemann J, Morozov SY (2013) Possible role of the Nt-4/1 protein in macromolecular transport in vascular tissue. Plant Signal Behav 8. doi:10.4161/psb 25784

    Google Scholar 

  • Spiesmacher E, Mühlbach HP, Schnölzer M, Haas B, Sänger HL (1983) Oligomeric forms of potato spindle tuber viroid (PSTV) and of its complementary RNA are present in nuclei isolated from viroid-infected potato cells. Biosci Rep 3:767–774

    Article  CAS  PubMed  Google Scholar 

  • Symons RH (1981) Avocado sunblotch viroid: primary sequence and proposed secondary structure. Nucleic Acids Res 9:6527–6537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tabler M, Tsagris M (2004) Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci 9:339–348

    Article  CAS  PubMed  Google Scholar 

  • Takeda R, Petrov AI, Leontis NB, Ding B (2011) A three-dimensional RNA motif in Potato spindle tuber viroid mediates trafficking from palisade mesophyll to spongy mesophyll in Nicotiana benthamiana. Plant Cell 23:258–272. doi:10.1105/tpc.110.081414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor JM (2014) Host RNA circles and the origin of hepatitis delta virus. World J Gastroenterol 20:2971–2978. doi:10.3748/wjg.v20.i11.2971

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 94:687–693. doi:10.1099/vir.0.048025-0

    Article  CAS  PubMed  Google Scholar 

  • Thanarajoo SS, Kong LL, Kadir J, Lau WH, Vadamalai G (2014) Detection of Coconut cadang-cadang viroid (CCCVd) in oil palm by reverse transcription loop-mediated isothermal amplification (RT-LAMP). J Virol Methods 202:19–23. doi:10.1016/j.jviromet.2014.02.024

    Article  CAS  PubMed  Google Scholar 

  • Torchetti EM, Navarro B, Di Serio F (2012) A single polyprobe for detecting simultaneously eight pospiviroids infecting ornamentals and vegetables. J Virol Methods 186:141–146. doi:10.1016/j.jviromet.2012.08.005

    Article  CAS  PubMed  Google Scholar 

  • Tsagris M, Tabler M, Sänger HL (1987) Oligomeric potato spindle tuber viroid (PSTV) RNA does not process autocatalytically under conditions where other RNAs do. Virology 157:227–231

    Article  CAS  PubMed  Google Scholar 

  • Tsagris EM, Martínez de Alba AE, Gozmanova M, Kalantidis K (2008) Viroids. Cell Microbiol 10:2168–2179

    Article  CAS  PubMed  Google Scholar 

  • Van Bogaert N, De Jonghe K, Van Damme EJ, Maes M, Smagghe G (2015) Quantitation and localization of pospiviroids in aphids. J Virol Methods 211:51–54. doi:10.1016/j.jviromet.2014.10.003

    Article  PubMed  CAS  Google Scholar 

  • Verhoeven JTJ, Jansen CCC, Roenhorst JW, Steyer S, Schwind N, Wassenegger M (2008) First report of Solanum jasminoides infected by Citrus exocortis viroid in Germany and the Netherlands and Tomato apical stunt viroid in Belgium and Germany. Plant Dis 92:973–973. doi:10.1094/pdis-92-6-0973a

    Article  Google Scholar 

  • Verhoeven JT, Jansen CC, Roenhorst JW, Flores R, de la Pena M (2009) Pepper chat fruit viroid: biological and molecular properties of a proposed new species of the genus Pospiviroid. Virus Res 144:209–214. doi:10.1016/j.virusres.2009.05.002

    Article  CAS  PubMed  Google Scholar 

  • 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 94:711–719. doi:10.1099/vir.0.048751-0

    Article  CAS  PubMed  Google Scholar 

  • Verhoeven JT, Roenhorst JW, Hooftman M, Meekes ET, Flores R, Serra P (2015) A pospiviroid from symptomless portulaca plants closely related to iresine viroid 1. Virus Res. doi:10.1016/j.virusres.2015.05.005

    PubMed  Google Scholar 

  • Visvader JE, Forster AC, Symons RH (1985) Infectivity and in vitro mutagenesis of monomeric cDNA clones of citrus exocortis viroid indicates the site of processing of viroid precursors. Nucleic Acids Res 13:5843–5856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt U, Pelissier T, Putz A, Razvi F, Fischer R, Wassenegger M (2004) Viroid-induced RNA silencing of GFP-viroid fusion transgenes does not induce extensive spreading of methylation or transitive silencing. Plant J 38:107–118. doi:10.1111/j.1365-313X.2004.02029.x

    Article  CAS  PubMed  Google Scholar 

  • Wang MB, Bian XY, Wu LM, Liu LX, Smith NA, Isenegger D, Wu RM, Masuta C, Vance VB, Watson JM, Rezaian A, Dennis ES, Waterhouse PM (2004) On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc Natl Acad Sci U S A 101:3275–3280. doi:10.1073/pnas.0400104101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warrilow D, Symons RH (1999) Citrus exocortis viroid RNA is associated with the largest subunit of RNA polymerase II in tomato in vivo. Arch Virol 144:2367–2375

    Article  CAS  PubMed  Google Scholar 

  • Wassenegger M, Heimes S, Riedel L, Sänger HL (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76:567–576

    Article  CAS  PubMed  Google Scholar 

  • Woo YM, Itaya A, Owens RA, Tang L, Hammond RW, Chou HC, Lai MMC, Ding B (1999) Characterization of nuclear import of potato spindle tuber viroid RNA in permeabilized protoplasts. Plant J 17:627–635. doi:10.1046/j.1365-313X.1999.00412.x

    Article  CAS  Google Scholar 

  • Wu Q, Wang Y, Cao M, Pantaleo V, Burgyan J, Li WX, Ding SW (2012) Homology-independent discovery of replicating pathogenic circular RNAs by deep sequencing and a new computational algorithm. Proc Natl Acad Sci U S A 109:3938–3943. doi:10.1073/pnas.1117815109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu YH, Cheong LC, Meon S, Lau WH, Kong LL, Joseph H, Vadamalai G (2013) Characterization of Coconut cadang-cadang viroid variants from oil palm affected by orange spotting disease in Malaysia. Arch Virol 158:1407–1410. doi:10.1007/s00705-013-1624-8

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Qi S, Tang N, Zhang X, Chen S, Zhu P, Ma L, Cheng J, Xu Y, Lu M, Wang H, Ding SW, Li S, Wu Q (2014) Discovery of replicating circular RNAs by RNA-seq and computational algorithms. PLoS Pathog 10:e1004553. doi:10.1371/journal.ppat.1004553

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Owens RA, Hammond RW (2001) 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 82:1491–1497

    Article  CAS  PubMed  Google Scholar 

  • Zhong X, Tao X, Stombaugh J, Leontis N, Ding B (2007) Tertiary structure and function of an RNA motif required for plant vascular entry to initiate systemic trafficking. EMBO J 26:3836–3846. doi:10.1038/sj.emboj.7601812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. doi:10.1105/tpc.107.056606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziebell H, Carr JP (2010) Cross-protection: a century of mystery. Adv Virus Res 76:211–264. doi:10.1016/S0065-3527(10)76006-1

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

This work was supported by grants AGL2013-49919-EXP and BIO2014-54269-R from Ministerio de Economía y Competitividad (MINECO, Spain).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José-Antonio Daròs .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Daròs, JA. (2016). Viroids: Small Noncoding Infectious RNAs with the Remarkable Ability of Autonomous Replication. In: Wang, A., Zhou, X. (eds) Current Research Topics in Plant Virology. Springer, Cham. https://doi.org/10.1007/978-3-319-32919-2_13

Download citation

Publish with us

Policies and ethics