Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families (original) (raw)
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On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites
Proceedings of the National Academy of Sciences, 2004
Viroids and most viral satellites have small, noncoding, and highly structured RNA genomes. How they cause disease symptoms without encoding proteins and why they have characteristic secondary structures are two longstanding questions. Recent studies have shown that both viroids and satellites are capable of inducing RNA silencing, suggesting a possible role of this mechanism in the pathology and evolution of these subviral RNAs. Here we show that preventing RNA silencing in tobacco, using a silencing suppressor, greatly reduces the symptoms caused by the Y satellite of cucumber mosaic virus. Furthermore, tomato plants expressing hairpin RNA, derived from potato spindle tuber viroid, developed symptoms similar to those of potato spindle tuber viroid infection. These results provide evidence suggesting that viroids and satellites cause disease symptoms by directing RNA silencing against physiologically important host genes. We also show that viroid and satellite RNAs are significantly resistant to RNA silencing-mediated degradation, suggesting that RNA silencing is an important selection pressure shaping the evolution of the secondary structures of these pathogens. Plant Transformation. Tobacco was transformed as described (11) by using 20 mg͞liter hygromycin (for pWBVec2-based plasmids),
Interplay between viroid-induced pathogenesis and RNA silencing pathways
Trends in Plant Science, 2009
Of all known plant pathogens, viroids have the lowest biological complexity. Their genome consists of a naked RNA without protein-encoding capacity. However, viroids contain sufficient genetic information to establish infection in susceptible hosts. The process by which this tiny RNA subverts the plant cell machinery by coercing the host to express symptoms of viroid infection is the 'Holy Grail' that has been searched for since the first viroid-induced disease was described. Recently, a large body of evidence has led to the emergent view that RNA silencing has a crucial role in viroid pathogenesis and evolution. Here, we chronologically analyse the relevant findings supporting this idea and propose a model to explain the possible interrelation between the transacting small interfering RNA (ta-siRNA) biogenesis pathway and viroid replication and pathogenesis.
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.
Journal of Virology, 2007
RNA silencing is a potent means of antiviral defense in plants and animals. A hallmark of this defense response is the production of 21-to 24-nucleotide viral small RNAs via mechanisms that remain to be fully understood. Many viruses encode suppressors of RNA silencing, and some viral RNAs function directly as silencing suppressors as counterdefense. The occurrence of viroid-specific small RNAs in infected plants suggests that viroids can trigger RNA silencing in a host, raising the question of how these noncoding and unencapsidated RNAs survive cellular RNA-silencing systems. We address this question by characterizing the production of small RNAs of Potato spindle tuber viroid (srPSTVds) and investigating how PSTVd responds to RNA silencing. Our molecular and biochemical studies provide evidence that srPSTVds were derived mostly from the secondary structure of viroid RNAs. Replication of PSTVd was resistant to RNA silencing, although the srPSTVds were biologically active in guiding RNA-induced silencing complex (RISC)-mediated cleavage, as shown with a sensor system. Further analyses showed that without possessing or triggering silencing suppressor activities, the PSTVd secondary structure played a critical role in resistance to RISC-mediated cleavage. These findings support the hypothesis that some infectious RNAs may have evolved specific secondary structures as an effective means to evade RNA silencing in addition to encoding silencing suppressor activities. Our results should have important implications in further studies on RNA-based mechanisms of host-pathogen interactions and the biological constraints that shape the evolution of infectious RNA structures.
Viroids: How to infect a host and cause disease without encoding proteins
Biochimie, 2012
Despite being composed by a single-stranded, circular, non-protein-coding RNA of just 246e401 nucleotides (nt), viroids can incite in their host plants symptoms similar to those caused by DNA and RNA viruses, which have genomes at least 20-fold bigger and encode proteins. On the other hand, certain non-protein-coding plant satellite RNAs display structural similarities with viroids but for replication and transmission they need to parasitize specific helper viruses (modifying concomitantly the symptoms they induce). While phenotypic alterations accompanying infection by viruses may partly result from expressing the proteins they code for, how the non-protein-coding viroids (and satellite RNAs) cause disease remains a conundrum. Initial ideas on viroid pathogenesis focused on a direct interaction of the genomic RNA with host proteins resulting in their malfunction. With the advent of RNA silencing, it was alternatively proposed that symptoms could be produced by viroid-derived small RNAs (vd-sRNAs) dgenerated by the host defensive machineryd targeting specific host mRNA or DNA sequences for posttranscriptional or transcriptional gene silencing, respectively, a hypothesis that could also explain pathogenesis of non-protein-coding satellite RNAs. Evidence sustaining this view has been circumstantial, but recent data provide support for it in two cases: i) the yellow symptoms associated with a specific satellite RNA result from a 22-nt small RNA (derived from the 24-nt fragment of the satellite genome harboring the pathogenic determinant), which is complementary to a segment of the mRNA of the chlorophyll biosynthetic gene CHLI and targets it for cleavage by the RNA silencing machinery, and ii) two 21-nt vd-sRNAS containing the pathogenic determinant of the albino phenotype induced by a chloroplast-replicating viroid target for cleavage the mRNA coding for the chloroplastic heat-shock protein 90 via RNA silencing too. This evidence, which is compelling for the satellite RNA, does not exclude alternative mechanisms.
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.
Cytopathic Effects Incited by Viroid RNAs and Putative Underlying Mechanisms
Frontiers in Plant Science, 2013
Viroids are infectious agents identified only in plants so far. In contrast to viruses, the genome of viroids is composed of a tiny circular RNA (250-400 nt) not coding for proteins, but containing in its compact structure all the information needed for parasitizing the transcriptional and RNA trafficking machineries of their hosts. Viroid infections are frequently accompanied by cellular and developmental disorders that ultimately result in macroscopic symptoms.The molecular events linking the structural domains of viroid RNAs with cellular and macroscopic alterations remain largely unexplored, although significant progress has been lately achieved in one specific viroid-host combination, highlighting the ability of viroids to strongly interfere with their host RNA regulatory networks. Cytopathic effects induced by nuclear-replicating viroids, which were investigated since early studies on viroids, consist in irregular proliferations of cell membranes (paramural bodies or plasmalemmasomes), cell wall distortions, and chloroplast malformations. Different alternatives have been proposed regarding how these cytological alterations may influence the onset of macroscopic symptoms. Recently, the cytopathology and histopathology incited by a chloroplast-replicating viroid have been investigated in depth, with defects in chloroplast development having been related to specific molecular events that involve RNA silencing and impairment of chloroplast ribosomal RNA maturation. On this basis, a tentative model connecting specific cytopathologic alterations with symptoms has been put forward. Here, early and more recent studies addressing this issue will be reviewed and reassessed in the light of recent advances in the regulatory roles of small RNAs.