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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abelson J, Trotta CR, Li H (1998) tRNA splicing. J Biol Chem 273:12685–12688
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
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
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
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
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
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
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
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
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
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
Branch AD, Robertson HD (1984) A replication cycle for viroids and other small infectious RNAs. Science 223:450–455
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
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
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
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
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
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
Dalakouras A, Dadami E, Wassenegger M (2013) Viroid-induced DNA methylation in plants. Biomol Concepts 4:557–565. doi:10.1515/bmc-2013-0030
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
Daròs JA, Flores R (1995) Identification of a retroviroid-like element from plants. Proc Natl Acad Sci U S A 92:6856–6860
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
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
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
Daròs JA, Elena SF, Flores R (2006) Viroids: an Ariadne’s thread into the RNA labyrinth. EMBO Rep 7:593–598
Daròs JA, Aragonés V, Cordero MT (2014) Recombinant RNA production. Patent EP14382177.5, PCT/EP2015/060912
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
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
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
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
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
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
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
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
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
Diener TO (1971a) Potato spindle tuber “virus” IV. A replicating, low molecular weight RNA. Virology 45:411–428
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
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
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
Diener TO (1989) Circular RNAs: relics of precellular evolution? Proc Natl Acad Sci U S A 86:9370–9374
Diener TO (2003) Discovering viroids – a personal perspective. Nat Rev Microbiol 1:75–80. doi:10.1038/nrmicro736
Diener TO, Raymer WB (1967) Potato spindle tuber virus: a plant virus with properties of a free nucleic acid. Science 158:378–381
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
Ding B (2009) The biology of viroid-host interactions. Annu Rev Phytopathol 47:105–131
Ding SW (2010) RNA-based antiviral immunity. Nat Rev Immunol 10:632–644. doi:10.1038/nri2824
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
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
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
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
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
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
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
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
Flores R, Daròs JA, Hernández C (2000) The Avsunviroidae family: viroids containing hammerhead ribozymes. AdvVirus Res 55:271–323
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Hu CC, Hsu YH, Lin NS (2009) Satellite RNAs and satellite viruses of plants. Viruses 1:1325–1350. doi:10.3390/v1031325
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nat Rev Genet 15:423–437. doi:10.1038/nrg3722
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
Mühlbach HP, Sänger HL (1979) Viroid replication is inhibited by α-amanitin. Nature 278:185–188
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
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
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
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
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
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
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
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
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
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
Niblett CL, Dickson E, Fernow KH, Horst RK, Zaitlin M (1978) Cross protection among four viroids. Virology 91:198–203
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
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
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
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
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
Palukaitis P (2014) What has been happening with viroids? Virus Genes 49:175–184. doi:10.1007/s11262-014-1110-8
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
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
Prody GA, Bakos JT, Buzayan JM, Schneider IR, Bruening G (1986) Autolytic processing of dimeric plant-virus satellite RNA. Science 231:1577–1580
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
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
Randles JW, Rodriguez MJ, Imperial JS (1988) Cadang-cadang disease of coconut palm. Microbiol Sci 5:18–22
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
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
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
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
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
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
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
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
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
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
Sogo JM, Koller T, Diener TO (1973) Potato spindle tuber viroid. X. Visualization and size determination by electron microscopy. Virology 55:70–80
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
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
Symons RH (1981) Avocado sunblotch viroid: primary sequence and proposed secondary structure. Nucleic Acids Res 9:6527–6537
Tabler M, Tsagris M (2004) Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci 9:339–348
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
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
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
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
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
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
Tsagris EM, Martínez de Alba AE, Gozmanova M, Kalantidis K (2008) Viroids. Cell Microbiol 10:2168–2179
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
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
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
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
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
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
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
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
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
Wassenegger M, Heimes S, Riedel L, Sänger HL (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76:567–576
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
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
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
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
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
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
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
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
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
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-3-319-32919-2_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-32917-8
Online ISBN: 978-3-319-32919-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)