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Viroids: self‐replicating, mobile, and fast‐evolving noncoding regulatory RNAs

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Abstract Viroids are small, circular, and noncoding RNAs that infect plants. They replicate in the nucleus or chloroplast and then traffic from cell to cell and from organ to organ to establish systemic infection. Viroids achieve nearly all of the biological functions by directly interacting with host cellular factors. Viroid replication, together with replication of human hepatitis delta virus, demonstrates the biological novelty and significance of RNA‐dependent RNA polymerase activities of DNA‐dependent RNA polymerases. Viroid systemic infection uncovers a new biological principle—the role of three‐dimensional RNA structural motifs mediating RNA trafficking between specific cells. Viroid diseases are virtually the consequences of host gene regulation by noncoding RNAs. A viroid RNA has the highest in vivo mutation rate among all known nucleic acid replicons. The host range of many viroids is expanding, essentially as a result of continuing and fast evolution of noncoding sequences/structures to gain new biological functions. Here, I discuss recent progress in these areas, emphasizing the broad significance of viroid research to the discovery of fundamental biological principles. Copyright © 2010 John Wiley & Sons, Ltd. This article is categorized under: Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs RNA in Disease and Development > RNA in Disease RNA in Disease and Development > RNA in Development

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Secondary structures and functional motifs/domains of (A) ASBVd and (B) PSTVd, representing families Avsunviroidae and Pospiviroidae, respectively. The loops in PSTVd are numbered 1–27 from left to right. The flag and arrow indicate transcription initiation and cleavage sites, respectively. TL, left‐terminal domain; TR, right‐terminal domain. HPI, HPI″, HPII, and HPII″ indicate nucleotide sequences proposed to form the metastable hairpins I and II, respectively, as shown in (C). (D) Two‐dimensional representation of the three‐dimensional structure of loop E (loop 15), with specific non‐Watson–Crick hydrogen bonding between different base pairs indicated..

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Per‐site mutation rate for a viroid in comparison with other biological entities. (Reprinted with permission from Ref 2 Copyright 2009 from the American Association for the Advancement of Sciences).

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A mechanistic model of peach calico disease caused by PLMVd based on invasion of the plant shoot apical meristem (SAM), alteration of chloroplastic (plastid) development and changes in leaf structure. (Reprinted with permission from Ref 85 Copyright 2007 American Society for Plant Biologists).

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A genomic map of PSTVd motifs for systemic trafficking (T) in a whole plant or for replication (R) in single cells of N. benthamiana. (Reprinted, with modifications, with permission from Ref 31 Copyright 2008 American Society of Plant Biologists).

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Viroid RNA motif‐mediated trafficking across distinct cellular boundaries. (A) From an initially infected epidermal cell (Ep), a viroid replicates and traffics through palisade mesophyll (PM), spongy mesophyll (SM), and bundle sheath (BS) to finally enter the phloem (Ph) cells to start long‐distance movement. The red arrows illustrate this pathway. The viroid may also traffic from an epidermal cell into the phloem through a different route. The blue arrows indicate viroid trafficking between different cells. Xy, xylem. (B) Schematic drawings of a plasmodesma in longitudinal (upper) and transverse (bottom) views. A plasmodesma comprises the plasma membrane (PM) that spans across two neighboring cells, the cylindrical strand of endoplasmic reticulum (ER), and proteins embedded in these two membrane systems (solid circles). The space between the PM and ER forms microchannels (MC) for transport. (C) Scheme showing genomic positions of two PSTVd motifs required for trafficking between specific cells as indicated. (D) The 3D view of the U/C‐water inserted motif, showing superposition of a U/C water‐inserted helix on a canonical A/U helix with matching flanking base pairs. Water‐molecule (orange sphere) insertion opens up the U/C helix. The orange‐colored base pairs are G/C (top), U/C (middle), and C/G (bottom), with overall sequence GUC…GCC. The blue‐colored base pairs are G/C (top), A/U (middle), and C/G (bottom), with overall sequence GAC…GUC. (D is reprinted with permission from Ref 67 Copyright 2007 Nature Publishing Group).

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General models of intracellular localization and replication of viroids from families Pospiviroidae (A) and Avsunviroidae (B).

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Systemic infection of ASBVd and PSTVd that includes intracellular and cell‐to‐cell trafficking, replication, and long‐distance movement. (Modified with permission from Ref 5 Copyright 2007 the American Phytopathological Society).

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Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs
RNA in Disease and Development > RNA in Development
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