Viroids

Abstract

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 (1) host deoxyribonucleic acid (DNA)‐dependent RNA polymerases redirected to accept RNA templates, (2) ribonucleases or, in the Avsunviroidae, hammerhead ribozymes and (3) RNA ligases, either DNA ligase 1 redirected to accept RNA substrates in the Pospiviroidae or a tRNA ligase in the Avsunviroidae. 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 replicate, infect and may 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 may be 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 denotes non‐conserved 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 of CEVd (Pospiviroidae) 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.
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Further Reading

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

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.

Hadidi A, Flores R, Randles J and Palukaitis P (eds) (2017) Viroids and Satellites, p 716. Academic Press: London, UK.

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Wang Y, Zirbel CL, Leontis NB and Ding B (2018) RNA 3‐dimensional structural motifs as a critical constraint of viroid RNA evolution. Public Library of Science Pathogens 14: e1006801.

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Flores, Ricardo, Daròs, José‐Antonio, Hernández, Carmen, Navarro, Beatriz, and Serio, Francesco Di(Aug 2020) Viroids. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029141]