Interplay between viroid-induced pathogenesis and RNA silencing pathways (original) (raw)

Plant-RNA viroid relationship: a complex host pathogen interaction

Viroids are non encapsidated small RNA plant pathogens unable to produce any protein. They are able to infect dramatically a broad range of plants including herbaceous and tree crops. The ways by which viroids are able to induce diseases are actually unknown. However, recent studies have shown that viroids are able to regulate the gene expression of their hosts, they can modify the host-protein phosphorylation sensibility and they interact with host-protein implicated RNA trafficking and protein phosphorylation. Moreover during their evolution plants have developed a mechanism able to regulate their gene expression and to degrade exogenous RNAs like viroids: the gene silencing. Unfortunately, this pathway seems, now, also highly implicated in the symptoms development. This review describes studies that are realized since a few years to increase the knowledge about the plant-viroid relationship.

Subviral pathogens of plants: Viroids and viroidlike satellite RNAs

The FASEB Journal

Contrary to earlier beliefs, viruses are not the smallest causative agents of infectious diseases. Single-stranded RNAs as small as 246 nucleotides exist in certain higher plants and cause more than a dozen crop diseases. These RNAs have been termed viroids. Despite their extremely limited information content, viroids replicate autonomously in susceptible cells--that is, they do not require helper functions from simultaneously replicating conventional viruses. Viroids are covalently closed circular molecules with a characteristic rodlike secondary structure in which short helical regions are interrupted by internal and bulge loops. Viroids are not translated; they are replicated by a host enzyme (or enzymes) (probably RNA polymerase II) via oligomeric RNA intermediates by a rolling circle mechanism. Viroidlike satellite RNAs resemble viroids in size and molecular structure, but are found within the capsids of specific helper viruses on which they depend for their own replication. Th...

Viroids: petite RNA pathogens with distinguished talents

Trends in plant science, 2004

Viroids are small, circular, single-stranded RNA molecules that cause several infectious plant diseases. Viroids do not encode any pathogen-specific peptides but nonetheless, the subviral pathogens replicate autonomously and spread in the plant by recruiting host proteins via functional motifs encoded in their RNA genome. During the past couple of years, considerable progress has been made towards comprehending how viroids interact with their hosts. Here, we summarize recent findings on the structure -function relationships of viroids, their strategies and mechanisms of replication and trafficking, and the identification and characterization of interacting host proteins. We also describe the impact of the RNA silencing machinery of plants on viroid RNAs and how this has started to influence our models of viroid replication and pathogenicity.

Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host mRNA as predicted by RNA silencing

The Plant Journal, 2012

How viroids, tiny non-protein-coding RNAs (250-400 nt), incite disease is unclear. One hypothesis is that viroid-derived small RNAs (vd-sRNAs; 21-24 nt) resulting from the host defensive response, via RNA silencing, may target for cleavage cell mRNAs and trigger a signal cascade, eventually leading to symptoms. Peach latent mosaic viroid (PLMVd), a chloroplast-replicating viroid, is particularly appropriate to tackle this question because it induces an albinism (peach calico, PC) strictly associated with variants containing a specific 12-14-nt hairpin insertion. By dissecting albino and green leaf sectors of Prunus persica (peach) seedlings inoculated with PLMVd natural and artificial variants, and cloning their progeny, we have established that the hairpin insertion sequence is involved in PC. Furthermore, using deep sequencing, semi-quantitative RT-PCR and RNA ligase-mediated rapid amplification of cDNA ends (RACE), we have determined that two PLMVd-sRNAs containing the PC-associated insertion (PC-sRNA8a and PC-sRNA8b) target for cleavage the mRNA encoding the chloroplastic heat-shock protein 90 (cHSP90), thus implicating RNA silencing in the modulation of host gene expression by a viroid. Chloroplast malformations previously reported in PC-expressing tissues are consistent with the downregulation of cHSP90, which participates in chloroplast biogenesis and plastid-tonucleus signal transduction in Arabidopsis. Besides PC-sRNA8a and PC-sRNA8b, both deriving from the lessabundant PLMVd ()) strand, we have identified other PLMVd-sRNAs potentially targeting peach mRNAs. These results also suggest that sRNAs derived from other PLMVd regions may downregulate additional peach genes, ultimately resulting in other symptoms or in a more favorable host environment for viroid infection.

review Viroids: an Ariadne's thread into the RNA labyrinth

Viroids are structurally, functionally and evolutionarily different from viruses. Despite their small, non-protein-encoding, singlestranded circular RNA genome, viroids can infect higher plants and cause certain diseases. Members of the two viroid families, Pospiviroidae and Avsunviroidae, have evolved to usurp the transcriptional machinery of their host nuclei and chloroplasts, respectively, in which replication proceeds through a rolling-circle mechanism involving RNA polymerization, cleavage and ligation. Remarkably, viroids subvert certain DNA-dependent RNA polymerases to transcribe RNA templates, and, in the family Avsunviroidae, post-transcriptional cleavage is catalysed by hammerhead ribozymes. Viroids are models for studying RNA evolution and for analysing RNA transport in plants, because they can move intracellularly, intercellularly through plasmodesmata and to distal parts of the plant through the vascular system. Viroids elicit RNA-silencing phenomena, which might mediate some of their biological properties, including pathogenesis. As some viroids behave as catalytic RNAs, they are regarded as remnants of the RNA world.

Viroids: an Ariadne's thread into the RNA labyrinth

EMBO reports, 2006

Viroids are structurally, functionally and evolutionarily different from viruses. Despite their small, non-protein-encoding, singlestranded circular RNA genome, viroids can infect higher plants and cause certain diseases. Members of the two viroid families, Pospiviroidae and Avsunviroidae, have evolved to usurp the transcriptional machinery of their host nuclei and chloroplasts, respectively, in which replication proceeds through a rolling-circle mechanism involving RNA polymerization, cleavage and ligation. Remarkably, viroids subvert certain DNA-dependent RNA polymerases to transcribe RNA templates, and, in the family Avsunviroidae, post-transcriptional cleavage is catalysed by hammerhead ribozymes. Viroids are models for studying RNA evolution and for analysing RNA transport in plants, because they can move intracellularly, intercellularly through plasmodesmata and to distal parts of the plant through the vascular system. Viroids elicit RNA-silencing phenomena, which might mediate some of their biological properties, including pathogenesis. As some viroids behave as catalytic RNAs, they are regarded as remnants of the RNA world.

A naked plant-specific RNA ten-fold smaller than the smallest known viral RNA: the viroid

Comptes Rendus de l'Académie des Sciences - Series III - Sciences de la Vie, 2001

Viroids are subviral plant pathogens at the frontier of life. They are solely composed by a single-stranded circular RNA of 246-401 nt with a compact secondary structure. Viroids replicate autonomously when inoculated into their host plants and incite, in most of them, economically important diseases. In contrast to viruses, viroids do not code for any protein and depend on host enzymes for their replication, which in some viroids occurs in the nucleus and in others in the chloroplast, through a rollingcircle mechanism with three catalytic steps. Quite remarkably, however, one of the steps, cleavage of the oligomeric head-to-tail replicative intermediates to unit-length strands, is mediated in certain viroids by hammerhead ribozymes that can be formed by their strands of both polarities. Viroids induce disease by direct interaction with host factors, the nature of which is presently unknown. Some properties of viroids, particularly the presence of ribozymes, suggest that they might have appeared very early in evolution and could represent 'living fossils' of the precellular RNA world that presumably preceded our current world based on DNA and proteins. © 2001 Académie des sciences/Éditions scientifiques et médicales hammerhead ribozyme / viroid Résumé -Viroïde : un ARN nu, spécifique de plante, dix fois plus petit que le plus petit ARN viral connu. Les viroïdes sont des pathogènes subviraux des plantes à la frontière de la vie. Ils sont seulement composés d'un ARN circulaire monocaténaire de 246-401 nt ayant une structure secondaire compacte. Les viroïdes se repliquent de façon autonome quand ils sont inoculés à leurs plantes hôtes et induisent dans la plupart de cettes plantes des maladies d'importance économique. Au contraire des virus, les viroïdes ne codent pour aucune proteine et dépendent des enzymes de leur hôtes pour leur réplication., qui pour certains viroïdes a lieu dans le noyau et pour d'autres dans le chloroplaste, suivant un méchanisme de 'cercle roulant' avec trois étapes catalitiques. Cependant, de façon remarquable, une des ces étapes, la coupure des intermédiares réplicatifs oligomériques tête-queue en unités monomériques, est médiée chez certains viroïdes par des ribozymes de tête de marteau qui peuvent être formés par leurs chaînes de chaque polarité. Les viroïdes induisent les maladies par interactions directes avec des facteurs de l'hôte dont la nature n'est pas connue. Quelques proprietés des viroïdes, en particulier la présence des ribozymes, suggèrent qu'ils pourraient avoir apparu trés tôt lors de l'évolution et pourraient représenter des 'fossiles vivants' du monde précellulaire à ARN qui a probablement précédé notre monde actuel basé sur l'ADN et les protéines. © 2001 Académie des sciences/Éditions scientifiques et médicales ribozyme à tête de marteau / viroïde *Correspondence and reprints. E-mail address: rflores@ibmcp.upv.es (R. Flores).

Deep Sequencing of Viroid-Derived Small RNAs from Grapevine Provides New Insights on the Role of RNA Silencing in Plant-Viroid Interaction

2009

Background: Viroids are circular, highly structured, non-protein-coding RNAs that, usurping cellular enzymes and escaping host defense mechanisms, are able to replicate and move through infected plants. Similarly to viruses, viroid infections are associated with the accumulation of viroid-derived 21-24 nt small RNAs (vd-sRNAs) with the typical features of the small interfering RNAs characteristic of RNA silencing, a sequence-specific mechanism involved in defense against invading nucleic acids and in regulation of gene expression in most eukaryotic organisms.