Viroids are infectious, nonprotein‐coding, highly structured small circular ribonucleic acids (RNAs) able to replicate autonomously and induce diseases in higher plants. Viroids and viruses differ in structure, function and evolutionary origin (with the former regarded as relics of a primitive RNA world). Viroids are classified into the families Pospiviroidae and Avsunviroidae, the members of which replicate in the nucleus and chloroplast, respectively, through an RNA‐based rolling circle mechanism with three steps catalysed by: (i) host deoxyribonucleic acid (DNA)‐dependent RNA polymerases redirected to accept RNA templates, (ii) processing enzymes or, in the family Avsunviroidae, hammerhead ribozymes and (iii) RNA ligases. When infecting a cell, the viroid RNA must travel to its replication organelle, with the resulting progeny moving cell‐to‐cell through plasmodesmata and reaching distal parts through the phloem. Pathogenesis could be triggered by the replicating viroid itself, or via RNA silencing. Viroids are detected by nucleic acid‐based approaches, some can be eliminated from infected plants by meristem tip culturing, and biotechnological approaches are being developed for their control.

Key Concepts:

  • Viroids are small nonprotein‐coding RNAs that infect, replicate and induce disease in higher plants.

  • Viroids differ from viruses in fundamental aspects that include structure, function and evolutionary origin.

  • Viroids are classified into the families Pospiviroidae (nuclear viroids) and Avsunviroidae (chloroplastic viroids).

  • Viroid RNAs adopt compact secondary structures additionally stabilised by elements of tertiary structure.

  • Viroids replicate through a rolling circle mechanism with only RNA intermediates and enzyme or ribozyme processing.

  • Different viroids have distinct host ranges and closely related viroids display cross‐protection effects when co‐infecting a common host.

  • Viroids move intracellularly, cell‐to‐cell through plasmodesmata, and long distance through the phloem.

  • Viroids may infect their host plants latently or induce different pathogenic alterations including death.

  • Viroids propagate in their hosts as a population of closely related variants (quasispecies).

  • Viroids are considered molecular fossils of the RNA world postulated to have preceded our present world dominated by DNA and proteins.

Keywords: small circular RNAs; viroid‐like satellite RNAs; catalytic RNAs; rolling circle replication; hammerhead ribozymes; RNA world

Figure 1.

Structural models for viroids. (a) Rod‐like secondary structure proposed for members of the family Pospiviroidae. The approximate locations of the five structural domains C (central), P (pathogenic), V (variable) and TL and TR (terminal left and right, respectively) are indicated. Nucleotide sequences of the TCH, TCR and CCR are shown within boxes, together with their occurrence in different viroids. Arrows represent flanking sequences that, along with the core nucleotides of the upper CCR strand, form imperfect inverted repeats. The inset shows loop E with an S‐shaped line connecting the nucleotides linked after ultraviolet irradiation; enlarged letters refer to nucleotides that are conserved in different RNAs containing this structural motif. N indicates nonconserved nucleotides. (b) Rod‐like and branched conformations proposed for the type members of genera Avsunviroid and Pelamoviroid, respectively. Broken lines in PLMVd represent a kissing‐loop interaction. Sequences strictly or highly conserved in natural hammerhead structures are shown within boxes with dark and white backgrounds for plus and minus polarities, respectively. The hammerhead structure of the PLMVd (+) strand is presented within the inset, with the arrowhead marking the self‐cleavage site. The tertiary interaction between loops I and II (in grey), which facilitates the catalytic activity at the low magnesium concentration existing in vivo is indicated by a rectangle. In both panels continuous lines and dots between nucleotides denote canonical and noncanonical base pairs, respectively. ASBVd, Avocado sunblotch viroid; ASSVd, Apple scar skin viroid; CbVd, Coleus blumei viroid; CCCVd, Coconut cadang–cadang viroid; HSVd, Hop stunt viroid; PLMVd, Peach latent mosaic viroid and PSTVd, Potato spindle tuber viroid.

Figure 2.

In situ hybridisation to Citrus exocortis viroid (CEVd) in tomato. Confocal micrograph of single mesophyll cell from CEVd‐infected tomato leaf material showing cell nucleus with viroid signal (red/orange) and cell structure by autofluorescence (green). Reproduced by permission from Bonfiglioli et al.. Copyright 1996 Blackwell Science Ltd.

Figure 3.

Rolling circle model for replication of viroids. (a) Asymmetric and (b) symmetric pathways with one and two rolling circles proposed to operate in the families Pospiviroidae and Avsunviroidae, respectively. Solid and open shapes refer to plus and minus polarities, respectively, and processing sites are denoted by short black arrows. The enzyme and ribozyme activities presumably involved in the replication steps are indicated; for the activities followed by a question mark the evidence is insufficient or controversial. NEP is an abbreviation for nuclear encoded polymerase.



Bernad L, Duran‐Vila N and Elena SF (2009) Effect of citrus hosts on the generation, maintenance and evolutionary fate of genetic variability of citrus exocortis viroid. Journal of General Virology 90: 2040–2049.

Bonfiglioli RG, Webb DR and Symons RH (1996) Tissue and intra‐cellular distribution of coconut cadang‐cadang viroid and citrus exocortis viroid determined by in situ hybridization and confocal laser scanning and transmission electron microscopy. Plant Journal 9: 457–465.

Branch AD and Robertson HD (1984) A replication cycle for viroids and other small infectious RNAs. Science 223: 450–454.

Bussière F, Ouellet J, Côté F, Lévesque D and Perreault JP (2000) Mapping in solution shows the peach latent mosaic viroid to possess a new pseudoknot in a complex, branched secondary structure. Journal of Virology 74: 2647–2654.

Carbonell A, Flores R and Gago S (2011) Trans‐cleaving hammerhead ribozymes with tertiary stabilizing motifs: in vitro and in vivo activity against a structured viroid RNA. Nucleic Acids Research (in press). doi:10.1093/nar/gkq1051.

Daròs JA and Flores R (1995) Identification of a retroviroid‐like element from plants. Proceedings of the National Academy of Sciences of the USA 92: 6856–6860.

Daròs JA, Marcos JF, Hernández C and Flores R (1994) Replication of avocado sunblotch viroid: evidence for a symmetric pathway with two rolling circles and hammerhead ribozyme processing. Proceedings of the National Academy of Sciences of the USA 91: 12813–12817.

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

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 (1989) Circular RNAs: relics of precellular evolution? Proceedings of the National Academy of Sciences of the USA 86: 9370–9374.

Ding B, Kwon MO, Hammond R and Owens R (1997) Cell‐to‐cell movement of potato spindle tuber viroid. Plant Journal 12: 931–936.

Di Serio F, Martínez de Alba AE, Navarro B, Gisel A and Flores R (2010) RNA‐dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a nuclear‐replicating viroid. Journal of Virology 84: 2477–2489.

Gago S, de la Peña M and Flores R (2005) A kissing‐loop interaction in a hammerhead viroid RNA critical for its in vitro folding and in vivo viability. RNA 11: 1073–1083.

Gago S, Elena SF, Flores R and Sanjuán R (2009) Extremely high variability of a hammerhead viroid. Science 323: 1308.

Gas ME, Hernández C, Flores R and Daròs JA (2007) Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Pathogens 3: 1813–1826.

Gómez G and Pallás V (2004) A long‐distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with hop stunt viroid RNA. Journal of Virology 78: 10104–10110.

Grill LK and Semancik JS (1978) RNA sequences complementary to citrus exocortis viroid in nucleic acid preparations from infected Gynura aurantiaca. Proceedings of the National Academy of Sciences of the USA 75: 896–900.

Gross HJ, Domdey H, Lossow C et al. (1978) Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 273: 203–208.

Hadidi A and Yang X (1990) Detection of pome fruit viroids by enzymatic cDNA amplification. Journal of Virological Methods 30: 261–270.

Hammond R, Smith DR and Diener TO (1989) Nucleotide‐sequence and proposed secondary structure of columnea latent viroid: a natural mosaic of viroid sequences. Nucleic Acids Research 17: 10083–10094.

Haseloff J, Mohamed NA and Symons RH (1982) Viroid RNAs of cadang‐cadang disease of coconuts. Nature 299: 316–321.

Hernández C and Flores R (1992) Plus and minus RNAs of peach latent mosaic viroid self‐cleave in vitro via hammerhead structures. Proceedings of the National Academy of Sciences of the USA 89: 3711–3715.

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

Itaya A, Zhong X, Bundschuh R et al. (2007) A structured viroid RNA is substrate for Dicer‐like cleavage to produce biologically active small RNAs but is resistant to RISC‐mediated degradation. Journal of Virology 81: 2980–2994.

Kalantidis K, Denti MA, Tzortzakaki S et al. (2007) Virp1 is a host protein with a major role in potato spindle tuber viroid infection in Nicotiana plants. Journal of Virology 81: 12872–12880.

Keese P and Symons RH (1985) Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proceedings of the National Academy of Sciences of the USA 82: 4582–4586.

Martínez de Alba AE, Flores R and Hernández C (2002) Two chloroplastic viroids induce the accumulation of the small RNAs associated with post‐transcriptional gene silencing. Journal of Virology 76: 13094–13096.

Martínez de Alba AE, Sägesser R, Tabler M and Tsagris M (2003) A bromodomain‐containing protein from tomato specifically binds potato spindle tuber viroid RNA in vitro and in vivo. Journal of Virology 77: 9685–9694.

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

Navarro B and Flores R (1997) Chrysanthemum chlorotic mottle viroid: unusual structural properties of a subgroup of self‐cleaving viroids with hammerhead ribozymes. Proceedings of the National Academy of Sciences of the USA 94: 11262–11267.

Navarro JA and 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 Journal 19: 2662–2670.

Niblett CL, Dickson E, Fernow KH, Horst RK and Zaitlin M (1978) Cross‐protection among four viroids. Virology 91: 198–293.

Owens RA and Diener TO (1981) Sensitive and rapid diagnosis of potato spindle tuber disease by nucleic acid hybridization. Science 213: 670–672.

Palukaitis P (1987) Potato spindle tuber viroid: investigation of the long‐distance, intra‐plant transport route. Virology 158: 239–241.

Papaefthimiou I, Hamilton AJ, Denti MA et al. (2001) Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post‐transcriptional gene silencing. Nucleic Acids Research 29: 2395–2400.

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

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

Qi YJ, Pelissier T, Itaya A et al. (2004) Direct role of a viroid RNA motif in mediating directional RNA trafficking across a specific cellular boundary. Plant Cell 16: 1741–1752.

Qu F, Heinrich C, Loss P et al. (1993) Multiple pathways of reversion in viroid conservation of structural domains. EMBO Journal 12: 2129–2139.

Rodio ME, Delgado S, De Stradis A et al. (2007) A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 19: 3610–3616.

Sano T, Candresse T, Hammond RW, Diener TO and Owens RA (1992) Identification of multiple structural domains regulating viroid pathogenicity. Proceedings of the National Academy of Sciences of the USA 89: 10104–10108.

Sano T, Nagayama A, Ogawa T, Ishida I and Okada Y (1997) Transgenic potato expressing a double‐stranded RNA‐specific ribonuclease is resistant to potato spindle tuber viroid. Nature Biotechnology 15: 1290–1294.

Schwind N, Zwiebel M, Itaya A et al. (2009) RNAi‐mediated resistance to potato spindle tuber viroid in transgenic tomato expressing a viroid hairpin RNA construct. Molecular Plant Pathology 10: 459–469.

Semancik JS, Szychowski JA, Rakowski AG and Symons RH (1993) Isolates of citrus exocortis viroid recovered by host and tissue selection. Journal of General Virology 74: 2427–2436.

Semancik JS and Szychowski JA (1994) Avocado sunblotch disease: a persistent viroid infection in which variants are associated with different symptoms. Journal of General Virology 75: 1543–1549.

Wang MB, Bian XY, Wu LM et al. (2004) On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proceedings of the National Academy of Sciences of the USA 101: 3275–3280.

Wassenegger M, Heimes S and Sänger HL (1994) An infectious viroid RNA replicon evolved from an in vitro‐generated non‐infectious viroid deletion mutant via a complementary deletion in vivo. EMBO Journal 13: 6172–6177.

Wassenegger M, Spieker RL, Thalmeir S et al. (1996) A single nucleotide substitution converts potato spindle tuber viroid (PSTVd) from a noninfectious to an infectious RNA for Nicotiana tabacum. Virology 226: 191–197.

Yang X, Yie Y, Zhu F et al. (1997) Ribozyme‐mediated high resistance against potato spindle tuber viroid in transgenic potatoes. Proceedings of the National Academy of Sciences of the USA 94: 4861–4865.

Zhong X, Archual AJ, Amin AA and Ding BA (2008) A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 20: 35–47.

Zhu Y, Green L, Woo YM, Owens R and Ding B (2001) Cellular basis of potato spindle tuber viroid systemic movement. Virology 279: 69–77.

Further Reading

Diener TO (ed.) (1987) The Viroids (The Viruses), p. 344. New York: Plenum Press.

Diener TO (1996) Origin and evolution of viroids and viroid‐like satellite RNAs. Virus Genes 11: 119–131.

Diener TO (2003) Discovering viroids – a personal perspective. Nature Reviews Microbiology 1: 75–80.

Ding B (2009) The biology of viroid‐host interactions. Annual Review of Phytopathology 47: 105–131.

Flores R, Daros JA and Hernández C (2000) The Avsunviroidae family: viroids with hammerhead ribozymes. Advances in Virus Research 55: 271–323.

Flores R, Hernández C, Martínez de Alba AE, Daros JA and Di Serio F (2005) Viroids and viroid–host interactions. Annual Review of Phytopathology 43: 117–139.

Flores R, Randles JW, Owens RA, Bar‐Joseph M and Diener TO (2005) Viroidae. In: Fauquet CM, Mayo MA and Maniloff J et al. (eds) Virus Taxonomy, Classification and Nomenclature. VIIII Report of the International Committee on Taxonomy of Viruses, pp. 1145–1159. London, UK: Elsevier/Academic Press.

Hadidi A, Flores R, Randles JW and Semancik JS (eds) (2003) Viroids, p. 370. Collingwood, Australia: CSIRO Publishing.

Symons RH (1997) Plant pathogenic RNAs and RNA catalysis. Nucleic Acids Research 20: 2683–2689.

Tsagris EM, Martínez de Alba AE, Gozmanova M and Kalantidis K (2008) Viroids. Cellular Microbiology 10: 2168–2179.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Flores, Ricardo, Daròs, José‐Antonio, Hernández, Carmen, and Di Serio, Francesco(Mar 2011) Viroids. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0000434.pub3]